Journal Of
of Experimental
Page
1 of
No.
242,
20122012
Experimental Botany,
Botany, Vol.
Vol. 63,
63,
13,pp.
pp.695–709,
4647–4670,
doi:10.1093/jxb/err313
doi:10.1093/jxb/ers124
2011
doi:10.1093/jxb/ers124 Advance
AdvanceAccess
Accesspublication
publication 425November,
June, 2012
This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details)
RESEARCH
DARWIN
REVIEW
PAPER
Non-structural
In
Posidonia oceanica
carbohydrate
cadmium
partitioning
induces changes
in grass stems:
in DNA
a
methylation
target to increase
and chromatin
yield stability,
patterning
stress tolerance, and
biofuel production
Maria Greco, Adriana Chiappetta, Leonardo Bruno and Maria Beatrice Bitonti*
DepartmentL.ofSlewinski*
Ecology, University of Calabria, Laboratory of Plant Cyto-physiology, Ponte Pietro Bucci, I-87036 Arcavacata di Rende,
Thomas
Cosenza, Italy
Department of Plant Biology, Cornell University, 262 Plant Science Building, Ithaca, NY 14853, USA
* To whom correspondence should be addressed. E-mail: [email protected]
* To whom correspondence should be addressed. E-mail: [email protected]
Received 29 May 2011; Revised 8 July 2011; Accepted 18 August 2011
Received 5 January 2012; Revised 30 March 2012; Accepted 4 April 2012
Abstract
Abstract
In mammals, cadmium is widely considered as a non-genotoxic carcinogen acting through a methylation-dependent
A
dramaticmechanism.
change in agricultural
crops is
in order
keep
with thepatten
demands
an increasing
human
epigenetic
Here, the effects
of needed
Cd treatment
onto
the
DNApace
methylation
are of
examined
together
with
population,
exponential
need
for
renewable
fuels,
and
uncertain
climatic
changes.
Grasses
make
up
the
vast
its effect on chromatin reconfiguration in Posidonia oceanica. DNA methylation level and pattern were analysed
in
majority
of
agricultural
commodities.
How
these
grasses
capture,
transport,
and
store
carbohydrates
underpins
all
actively growing organs, under short- (6 h) and long- (2 d or 4 d) term and low (10 mM) and high (50 mM) doses of Cd,
aspects
of Methylation-Sensitive
crop productivity. Sink–source
dynamics
within the
plant direct
much, where, and
when
through a
Amplification
Polymorphism
technique
and anhow
immunocytological
approach,
carbohydrates
are
allocated,
as
well
as
determine
the
harvestable
tissue.
Carbohydrate
partitioning
can
limit
the
respectively. The expression of one member of the CHROMOMETHYLASE (CMT) family, a DNA methyltransferase,
yield
capacity
of
these
plants,
thus
offering
a
potential
target
for
crop
improvement.
Grasses
have
the
ability
to
was also assessed by qRT-PCR. Nuclear chromatin ultrastructure was investigated by transmission electron
buffer
this
sink–source
interaction
by
transiently
storing
carbohydrates
in
stem
tissue
when
production
from
the
microscopy. Cd treatment induced a DNA hypermethylation, as well as an up-regulation of CMT, indicating that de
source
is greater than
whole-plant
These
reserves
improve
in grain
crops by providing an
novo methylation
did indeed
occur.demand.
Moreover,
a high
dose of
Cd ledyield
to a stability
progressive
heterochromatinization
of
alternative
source
when
photosynthetic
capacity
is
reduced
during
the
later
phases
of
grain
filling,
or during periods
interphase nuclei and apoptotic figures were also observed after long-term treatment. The data demonstrate
that Cd
of
environmental
biotic stresses.
grasses suchofasa sugarcane
and sweet sorghum
have
undergone
perturbs
the DNAand
methylation
statusDomesticated
through the involvement
specific methyltransferase.
Such
changes
are
selection
high accumulation
of stem carbohydrates,
which serve
as the
primary
of sugars for human
and
linked to for
nuclear
chromatin reconfiguration
likely to establish
a new
balance
of sources
expressed/repressed
chromatin.
animal
as ethanol
production
for fuel. With
the enormous
expectations
Overall,consumption,
the data showasanwell
epigenetic
basis
to the mechanism
underlying
Cd toxicity
in plants. placed on agricultural
production in the near future, research into carbohydrate partitioning in grasses is essential for maintaining and
increasing
in grass crops. This
review highlights
thechromatin
current reconfiguration,
knowledge ofCHROMOMETHYLASE,
non-structural carbohydrate
Key words: yields
5-Methylcytosine-antibody,
cadmium-stress
condition,
dynamics in grass
stems andSensitive
discusses
the impacts
of stem reserves
in essential
agronomic
grasses.
DNA-methylation,
MethylationAmplification
Polymorphism
(MSAP), Posidonia
oceanica
(L.) Delile.
Key words: Carbohydrate partitioning, grasses, non-structural carbohydrates, parenchyma cells, sink–source buffering, stem,
yield stability.
Introduction
In the Mediterranean coastal ecosystem, the endemic
seagrass Posidonia oceanica (L.) Delile plays a relevant role
Introduction
by ensuring primary production, water oxygenation and
provides
niches
for somewith
animals,
besides
Grasses have
co-evolved
humans
since counteracting
the dawn of
coastal
erosion
through
its
widespread
meadows
agriculture ;10 000 years ago. They represent(Ott,
the 1980;
most
Piazzi
et
al.,
1999;
Alcoverro
et
al.,
2001).
There
is also
productive and widely grown crop family and provide
evidence
P. oceanica
plants
are able to
aconsiderable
foundation for
humanthat
life across
the globe.
Grain-producing
absorb
and
accumulate
metals
from
sediments
grasses such as rice (Oryza spp.), maize (Zea mays), (Sanchiz
sorghum
et al., 1990; bicolor),
Pergent-Martini,
Masertiaestivum),
et al., 2005)barley
thus
(Sorghum
wheat 1998;
(Triticum
influencing
metal
bioavailability
in
the
marine
ecosystem.
(Hordeum vulgare), and oats (Avena sativa) provide the
For
this of
reason,
thisconsumed
seagrass by
is widely
considered (FAO,
to be
majority
calories
people worldwide
a2009).
metalSugarcane
bioindicator
species
(Maserti
et
al.,
1988;
Pergent
(Saccharum officinarum) and sweet sorghum
et al., 1995;
Lafabrie
et al., 2007).carbohydrates,
Cd is one ofmainly
most
produce
the bulk
of water-soluble
widespread
heavy
metals
in
both
terrestrial
and
marine
sucrose, for use in human and animal foods, along with
environments.
Although not essential for plant growth, in terrestrial
plants, Cd is readily absorbed by roots and translocated into
aerial organs while, in acquatic plants, it is directly taken up
by leaves.fermentable
In plants, Cdsubstrate
absorptionfor
induces
complex
changes
directly
ethanol
production
at
the
genetic,
biochemical
and
physiological
levels
which
(Waclawovsky et al., 2010). Forage grasses such as ryegrass
ultimately
account
for
its
toxicity
(Valle
and
Ulmer,
(Lolium perenne), switchgrass (Panicum virgatum), and1972;
misSanitz
Toppi and3giganeum)
Gabrielli, 1999;
Benavides
2005;
provide
much of et
theal.,
biomass
canthusdi(Miscanthus
Weber et by
al.,ruminant
2006; Liu
et al., 2008).
Thepastoral
most obvious
consumed
agricultural
and wild
animals
symptom
of
Cd
toxicity
is
a
reduction
in
plant
growth
due to
as well as lignocellulose feedstocks for second-generation
an
inhibition
of
photosynthesis,
respiration,
and
nitrogen
biofuel production (Mitchell et al., 2008; Somerville et al.,
metabolism, as well as a reduction in water and mineral
2010).
uptake
et al., 1997;
Perfus-Barbeoch
et al., 2000;
The (Ouzonidou
process by which
grasses
produce, transport,
and
Shukla
et
al.,
2003;
Sobkowiak
and
Deckert,
2003).
store carbohydrates underpins all aspects of yield traits.
At the our
genetic
level, knowledge
in both animals
plants, and
Cd
Despite
current
of theand
location
can induce chromosomal aberrations, abnormalities in
Abbreviations: NSC, non-structural carbohydrate; QTL, quantitative trait locus.
Abbreviations:
NSC, non-structural
carbohydrate;
QTL,
quantitative
trait
2011Author
The Author(s).
ª
The
[2012].
Published by Oxford
University
Press
[on behalf
of locus.
the Society for Experimental Biology]. All rights reserved.
© The
[2012].
Published
by Oxfordunder
University
Pressof
[onthe
behalf
of the
Society for
Experimental
Biology]. All rights
reserved.
For
Permissions,
please
e-mail:distributed
[email protected]
This
is Author
an Open
Access
article
the terms
Creative
Commons
Attribution
Non-Commercial
License
(http://creativecommons.org/licenses/byFor Permissions,
pleaseunrestricted
e-mail: [email protected]
nc/3.0),
which permits
non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
4648 2 of 24| Slewinski
| Slewinski
harvestable amount of these important carbohydrates, we
are only beginning to understand the molecular, genetic,
and physiological mechanisms that regulate their transport
and allocation preceding harvest. Expanding such knowledge is vital to creating and implementing rational strategies
to optimize whole-plant carbohydrate partitioning for
increased productivity.
For many of the grasses, rate of gain in yield potential
has been slowing while overall grain demands continue to
increase. Yields from primary crops such as maize, rice, and
wheat are predicted to decline over the next two decades in
semi-arid regions of the world due to climate change (Lobell
et al., 2008). In Africa, modern agricultural intensification
has not yet been achieved and per capita cereal production
has been declining since the 1960s (St.Clair and Lynch,
2010). Additionally, the merger of food and energy markets,
induced by increased demand for biofuels, now puts an
enormous strain on the supply and demand dynamics of
agricultural commodities—greatly impacting the availability
of grain-based foods worldwide (Oosterveer and Mol,
2010). When all of these factors are put into the same
equation to predict the critical variable in the future of
agricultural production, the physiology of the plant is the
factor that is under the most pressure to change and will
have the greatest impact compared with other agronomic
factors (Rosenzweig and Parry, 1994; Gregory and George,
2011). Most importantly, many of the targeted traits relate
directly to the physiology of sink–source dynamics and
whole-plant carbohydrate partitioning (Fischer and
Edmeades, 2010).
When we view carbohydrate partitioning on a whole-plant
level, we find something interesting about the grasses—their
stems. Many grasses, along with other monocots, such as
pineapple and agave, store excess carbohydrates in the form
of soluble sugars or sugar polymers within the vegetative
tissues (Antony et al., 2008; Davis et al., 2011). Grass stems
are capable of storing substantial amounts of soluble
carbohydrates in the storage parenchyma cells that surround
the vascular bundles located within internode tissues (Hoffmann-Thoma et al., 1996; Rae et al., 2005a).
The Green Revolution of the 1960s resulted in highyielding wheat and rice varieties with altered morphology
compared with the traditional land races, and resistance to
devastating pathogens such as wheat rust (Borlaug, 2007).
This dramatic increase in yield was largely due to a shift in
the way grasses partition structural carbohydrates in the stem
(Evenson and Gollin, 2003). Short statured, ‘semi-dwarf’,
genotypes were selected: these varieties redirected more
carbohydrates into harvestable grain and responded to
intensive fertilization without stem elongation and lodging.
The new green revolution must produce crops that have
higher yield stability in drier, hotter, and more saline
environments, while adapting to wetter environments with
reduced irradiance in others (Schmidhuber and Tubiello,
2007). Higher yields must also be achieved on lands that are
already under agricultural production, with fewer inputs such
as nitrogen, phosphorus, and fresh water (Fedoroff et al.,
2010). Another aim must be to decrease CO2 emissions
and aid in carbon sequestration by a reduction in tilling,
which would also protect top soil degradation and erosion
(Beddington, 2010). Manipulating stem non-structural carbohydrates (NSCs) provides one avenue to stabilize and
increase productivity in the face of rapidly changing demand
in the next century.
This review focuses on the roles of NSCs in grass stems
and their impacts on sink–source dynamics, overall productivity, and implications for future uses in agriculturally
and economically critical grass species. I will begin the
discussion with an overview of the roles of NSCs in grass
stems, then move to mechanistic models of radial transport,
current knowledge of stem NSCs in agricultural grasses,
and end with prospects and implications for stem NSC
research.
NSCs in grass stems
What are the roles of stem carbohydrates in the grasses?
The most widely accepted hypothesis is that grasses store
excess carbohydrates in stem tissues to buffer source–sink
interactions during different stages of growth and in varying
environmental conditions (Schnyder, 1993; Asseng and
Herwaarden, 2003; Slafer, 2003; Ruuska et al., 2006). This
represents long-term buffering, unlike the short-term buffering role for transient starch and sugar reserves in the
leaves, which vary on a diurnal basis. Stem storage
parenchyma cells, that encircle the vascular bundle, are
considered an in-route storage compartment, which theoretically could be a competing sink along the path to terminal
sinks such as the roots and seeds (Wardlaw, 1990; Sadras
and Denison, 2009). Such a dynamic has been suggested for
the internodes of sugarcane and sweet sorghum which retain
large amounts of carbohydrate after flowering (McBee and
Miller, 1982; Walsh et al., 2005; Garside and Bell, 2009).
However, in general, these stem storage carbohydrate pools
do not compete with other sink tissues in the plant; rather,
they store excess photosythate during periods of low sink
strength (Slafer, 2003). There are periods in the plant life
cycle where carbohydrate production in source tissues
exceeds the demands of sink tissues, and vice versa. This is
in agreement with a more integrative view of sink–source
interactions which emphasizes a co-limitation, rather than
strictly sink or source limitation (Slafer, 2003; Álvaro et al.,
2008; Acreche and Slafer, 2011). For example in wheat,
stem carbohydrates progressively accumulate in the stem
until the stage of rapid grain filling when stem carbohydrates reserves become mobile and partition to the developing grain (Ruuska et al., 2006). Additionally, buffering
confers an ability to tolerate catastrophes, such as pathogen
or herbivore attack, and rapidly re-grow after such events.
Buffering either directly or indirectly increases the
fecundity of the plant by increasing the ability to produce
viable seeds. Additionally, placing the buffering storage
pool away from the photosynthetic tissues may reduce
feedback inhibition of photosynthesis due to excessive
carbohydrate (Pollock et al., 2003). This phenomenon has
Non-structural
carbohydrate
partitioning
in grass
stems 4649
Non-structural
carbohydrate
partitioning
in grass
stems
| 3| of
24
been documented in sugarcane where cultivars and species
that do not accumulate high levels of sucrose in the stem
have higher photosynthetic rates than the high-sucroseaccumulating cultivars (Irvine, 1975). Thus, a robust buffering capacity of the stem may be one reason why grasses
seem to have considerable plasticity in sink–source dynamics, allowing them to be more readily modified for uses in
high-production agriculture.
The nature of the plant life cycle also has a dramatic
impact on whole-plant carbohydrate partitioning (Thompson
and Stewart, 1981). Most of the grain-producing grasses are
monocarpic annuals with only one chance at producing
offspring before the life cycle ends. Thus, carbohydrate
reserves buffer against extended periods of low light or
drought, allowing plants to produce some viable seed.
Perennials go one step further by storing carbohydrates in
stems and roots, which may include rhizomes, to fuel
re-growth of new tissues in the spring. Sugarcane is
a perennial grass that stores carbohydrate in the stems and
rhizomes (Matsuoka and Garcia, 2011). These reserves peak
at the end of the vegetative cycle, and are used during
flowering and seed production. After the sexual reproductive
phase is complete, remaining stem NSC reserves are mobilized to produce new vegetative structures. This is why
sugarcane is harvested before the reproductive phase begins
(Komor, 2000). One way in which breeders have increased
stem carbohydrate reserves is to delay reproduction and seed
set. Due to this strong selection, a majority of sugarcane
cultivars now are either sterile or the reproductive cycle has
been dramatically delayed, sometimes for years (Rae et al.,
2005a).
2010). Temperate C3 grasses, as well as rice, which grows in
hotter climates, convert imported sucrose into carbohydrate
polymers for sequestration, then convert them back into
sucrose for translocation out of the stem (Halford et al.,
2011). Thus, in these grasses, storage and remobilization is
dependent on both transport mechanisms and metabolic
processes within the stems.
The symplasmic path
A brief introduction to the models of transport between
storage parenchyma cells and the transport systems is
necessary for understanding carbohydrate partitioning processes in grass stems. Symplasmic transport is cell-to-cell
movement of molecules through plasmodesmata (Fig. 1A).
Radial transfer between the phloem and
stem storage parenchyma
Storage and remobilization strategies depend to a large
degree on the form in which carbohydrates are stored.
Depending on the species, stem carbohydrates can be stored
as soluble sugars, such as sucrose, fructans (soluble
polymers of fructose), or starch (insoluble polymers of
glucose) (Halford et al., 2011). The amount of stored
carbohydrate in the stem also varies with the species and
cultivar of grass and is dependent on the stage of
development and growing conditions. Some grasses that
have a central lacuna can also store carbohydrate in the
chloranchyma cells along the periphery of the stem.
Sucrose is stored in the stems of the Andropogoneae tribe,
which includes C4 grasses such as maize, sorghum, and
sugarcane (Dillon et al., 2007; Glassop et al., 2010). In the
mature internodes, sucrose degradation and synthesis are
minimal. Since sucrose is also the only carbohydrate in the
phloem sap of these species, direct transport mechanisms
are hypothesized to be the primary driving forces for
storage and remobilization. However, the minimal sucrose
‘futile cycling’ may play important roles in sugar signalling,
sugar accumulation, and allocation of carbon to biological
processes that may regulate transport (Rossouw et al.,
Fig. 1. Putative models for radial transport in grass stems.
Pathways for carbohydrate import into stem storage parenchyma
cells are presented on the left. Pathways for re-mobilization and
phloem loading from storage parenchyma cells are on the right.
SE/CCC, sieve element–companion cell complex.
4650 4 of 24| Slewinski
| Slewinski
The driving forces behind symplasmic transport are mass
flow and diffusion, driven by pressure and chemical
gradients as well as respiration (Patrick, 1997; Slewinski
and Braun, 2010). Downhill gradients are generated by
metabolizing or converting sugars within the cell, or transporting them out of the cytosol into membrane-bound
compartments such as the vacuole (Patrick et al., 2001).
Initial phloem unloading into developing and elongating
grass internodes appears to be symplasmic, similar to the
unloading mechanism in most rapidly growing vegetative
sink tissues (Aoki et al., 2004). However, there is usually
a dramatic change in metabolic and transport reprogramming during the switch from utilization sink to storage sink
in the mature stem (Hoffmann-Thoma et al., 1996). At this
transition, when sucrose is no longer used for tissue
construction, some grasses may switch to an apoplasmic
transport mechanism (below) when high concentrations of
sucrose begin to accumulate (Tarpley and Vietor, 2007).
The main storage compartment for soluble sugars within
the storage parenchyma cells is the vacuole (Pollock and
Kingston-Smith, 1997; Rae et al., 2009). In most plants,
sucrose enters the vacuole and is cleaved by invertases,
producing glucose and fructose (Koch, 2004). However,
some grasses suppress invertase activity in the vacuolar
lumen, as well as sucrose synthase activity in the cytosol,
and store only sucrose in the vacuoles of the mature stem
storage parenchyma cells (Tarpley et al., 1996; Tarpley and
Vietor, 2007). Storage of sucrose in these cell types involves
active sucrose transporters embedded within the tonoplast
membrane (Rae et al., 2005a). For example, in rice,
H+–sucrose symport from the vacuole lumen to the cytosol
across the tonoplast membrane in most vegetative tissues
was recently found to be mediated by the SUCROSE
TRANSPORTER 2 protein (OsSUT2) (Eom et al., 2011).
Plants that are homozygous for a null mutation in the
OsSUT2 gene accumulate excessive sucrose in vacuoles and
are impaired in whole-plant carbohydrate partitioning.
Presumably the expression and function of OsSUT2 extends
to the stem storage parenchyma cells, but has yet to be
experimentally confirmed. Orthologues of the Arabidopsis
tonoplastic monosaccharide transporters, AtTMT1 and
AtTMT2, may mediate sucrose–H+ antiporter activity that
shuttles sucrose from the vacuole across the tonoplast
membrane into the cytosol (Schulz et al., 2011). More work
is needed to elucidate the functions of the tonoplastic sugar
transporters in grasses, which may perform different
functions in different species (Braun and Slewinski, 2009;
Slewinski and Braun, 2010).
The apoplasmic path
Cells that do not have sufficient plasmodesmatal connections, or have connections that are blocked, use apoplasmic
transport to shuttle carbohydrates from cell to cell (Fig. 1B)
(Rennie and Turgeon, 2009). Apoplasmic transfer between
cells is composed of both a linear efflux phase driven by
passive movement though a membrane into the surrounding
cell wall, and an energy-dependent transport component,
necessary for retrieval from the apoplast (Patrick, 1997).
The recently described SWEET family of passive sugar
effluxors is most probably responsible for the linear phase
of sucrose export from cells (Chen et al., 2011). The ‘active’
phase, governed by Michaelis–Menten kinetics, results from
energy-dependent transporters that span the membranes
(Patrick, 1997). Active transport of sucrose and monosaccharides is mediated by sucrose and monosaccharide/proton
symporters or antiporters. Apoplasmic transport, both the
passive linear component and the active component, are
presumed to function at most cell wall interfaces. However
there are some interfaces where cell walls are highly
suberized or lignified, and thus dramatically restrict apoplasmic movement (Rae et al., 2005a). Symplasmic transport though plasmodesmata would be the most likely path
of flux from cell to cell in this case.
Sequestration by polymer synthesis
Some grasses store NSCs in the form of polymers in the
storage parenchyma cells, either as starch or as fructans
(Fig. 1C) (Morvan-Bertrand et al., 2001; Xue et al., 2008).
Most tissues that produce carbohydrate polymers have high
symplasmic connectivity to surrounding cells. Polymerizing
carbohydrates within the cells reduces the osmotic strength
of the sugars, thus plants are able to store more reduced
carbon per unit volume (Spoolen and Nelson, 1988). Polymer synthesis, which is mostly restricted to plastids or
vacuoles, also produces a chemical gradient necessary to
drive passive flux in the direction of the storage cell when
polymers are formed, or in the direction of export when
polymers are degraded and converted back to sucrose
(Schnyder et al., 1988; Patrick, 1997).
Grass species that are indigenous to temperate climates
and that regularly experience periods of drought and frost
typically utilize fructans as a carbohydrate storage pool
(Halford et al., 2011). Fructans are synthesized in the
vacuolar lumen from imported sucrose (Pollock et al.,
2003). Either sucrose:sucrose 1-fructosyltransferase (1-SST)
or sucrose:fructan 6-fructosyltransferase (6-SFT) adds
a fructose moiety to the fructose on a sucrose molecule to
initiate fructan synthesis. 6-SFT then adds consecutive
fructose moieties to the previously attached fructose moiety
to produce an elongating fructose polymer anchored on
a sucrose base (Chalmers et al., 2005). The length and
branching of the fructan polymer vary widely between
tissues, species, and environmental conditions. Usually
a higher concentration of fructans is associated with a higher
degree of polymerization (Ruuska et al., 2006, 2008). When
reserves are mobilized, fructans are hydrolysed in the
vacuole by fructan exohydrolases and invertases into free
fructose. Fructose is then exported from the vacuole, resynthesized into sucrose in the cytosol, and exported into
the phloem by the apoplasmic mechanism (Berthier et al.,
2009). (For further discussion and review of fructan
metabolism, see Pollock and Cairns, 1991; Cairns, 1992;
Non-structural
carbohydrate
partitioning
in grass
stems 4651
Non-structural
carbohydrate
partitioning
in grass
stems
| 5| of
24
Mechanisms of partitioning and impacts in
the agricultural grasses
Maize
Sucrose in the maize stem is considered to be the major
component of the ‘buffering system’ in the sink–source
relationship (Daynard et al., 1969). Indeed, one hypothesis
to explain the origins and domestication of maize is that
teosinte, the ancestor of maize, was originally cultivated for
the soluble sugars in the stems (Willaman et al., 1924;
Singleton, 1948; Smalley and Blake, 2003). Stem sucrose
was most probably extracted by chewing or sucking the
stalks, then fermenting the extract into a ‘stem sugar beer’.
Subsequent development as a grain crop may have occurred
when favourable mutations made the teosintie seeds more
palatable and abundant, and thus more amenable for
human consumption. Subsequently, seeds, not stem sugar,
were selected.
Stem sugar in maize is now considered a secondary trait
and has received minimal attention in the last few decades,
mainly due to the focus on primary traits such as yield,
lodging resistance, drought tolerance, and nutritional content. However, with the revitalization of liquid biofuels,
maize stem sugar has, again, become a central target for
breeding and biotechnology as a source for renewable
energy (White et al., 2011). Previous interest in the production of ethanol from maize stems peaked in the late
1970s and early 1980s, when oil prices rose and prompted
interest in alternative energy sources, in a trend similar to
that of recent years (Widstrom et al., 1987).
Sucrose intercellular transport in maize stems is presumed
to be apoplasmic (Setter and Flannigan, 1986). In the
storage parenchyma cells, sucrose is transported in, stored,
and effluxed unaltered. Reducing sugars and starch contribute minimally to total stem carbohydrate reserves. Hexoses
usually do not fluctuate with change in overall stem dry
matter accumulation/depletion or by alterations in the
overall source–sink balance of the plant (Sayre et al., 1931;
Setter and Flannigan, 1986). Thus partitioning in the stem
is presumably due to the activity of sucrose transporters
located in the plasma membranes of the companion cell–
sieve element complex and the adjacent parenchyma cells,
as well as in the membranes of the tonoplasts. To date, only
one member of the sucrose transporter family of maize,
ZmSUT1, has been characterized. ZmSUT1 is expressed in
photosynthetic leaves and functions in phloem loading in
source leaves (Slewinski et al., 2009, 2010). The mechanism
of re-mobilization and phloem loading in the stem remains
unclear. It is possible that phloem loading also occurs via
an apoplasmic mechanism that involves ZmSUT1, which
has the possibility of mediating both phloem loading and
unloading depending on both the chemical and electrochemical gradients that are present (Carpaneto et al., 2005).
Characterization of the remaining family members will
hopefully reveal which sucrose transporters are involved in
stem carbohydrate partitioning (Braun and Slewinski,
2009). It will be interesting to see if the sucrose transporter
transcript level or protein abundance in both the vascular
and storage parenchyma cells is correlated with increased
phloem unloading and storage capacity in stems, thus
providing a target to manipulate stem NSC reserves in
maize.
Sink–source manipulations also provide some insight into
the buffering capacity of the maize stem. For example,
when leaves above and below the ear are removed at the
time of silking, plants accumulate less sucrose in the stems
compared with unaltered control plants (Jones and Simmons, 1983). When ears are removed, sucrose accumulates
to a much higher concentration relative to the defoliated
and control plants (Fig. 2) (Van Reen and Singleton, 1952;
Hume and Campbell, 1972). Major contributions of the
stem NSC reserves can also be seen when plants in the mid
to late stages of grain filling are defoliated by herbicides
(Donaghy et al., 2008). When photosynthesis is compromised, maize stems enhance re-mobilization of stem NSCs,
while accelerating the kernel filling and maturation process
(Allison and Watson, 1966; Rajcan and Tollenaar, 1999).
This suggests that leveraging stem reserves may be one way
to increase yield stability in environments where either
photosynthesis, or the photosynthetic structures, are damaged in the later phase of kernel maturation.
Dry matter partitioning in Maize
Dry Matter
Schnyder, 1993; Vijn and Smeekens, 1999; Van den Ende
et al., 2004; Chalmers et al., 2005).
Only a few grasses use starch as a primary reserve in the
stems (discussed below). Unlike fructans, starch is formed
in the plastids/amyloplasts by metabolic events both in the
plastid and in the cytosol. Remobilization requires the
breakdown of starch in the plastids, then sucrose resynthesis in the cytosol before export from the cell. For
further discussions on starch metabolism, see Zeeman et al.
(2010) and Weise et al. (2011).
Ear pollination
Seedling
(Time)
Harvest
Fig. 2. Dry matter partitioning in the vegetative tissues and the ear
of maize over the life of the plant. Adapted from Sayre et al.
[Journal of the American Society of Agronomy 23, 751–753 (1931),
with permission, copyright American Society of Agronomy]; Allison
JCS and Watson DJ. 1996. The production and distribution of dry
matter in maize after flowering. Annals of Botany 30, 365–381,
with permission from Oxford University Press; and Hume and
Campell (1972) with permission from the author.
4652 6 of 24| Slewinski
| Slewinski
This conclusion is further supported by studies using
radioactive carbon tracers that show that stem NSC
reserves contribute little to final grain fill under normal field
conditions (Cliquet et al., 1990), but play a significant role
under suboptimal conditions (Jurgens et al., 1978; Setter
et al., 2001). For example, when 14C-labelled sucrose is
injected into the apoplast of the stems of leafless explants of
maize, 30% of the radioactivity is recovered in the kernels 2
d later (Setter and Meller, 1984). This suggests that
although stem carbohydrates do not directly increase yield
potential in maize under high input agricultural practices,
they greatly contribute to yield stability when plants are
challenged by environmental and biotic stressors, or are
grown on marginal and rain-fed lands.
Photosynthesis in maize leaves is at a maximum during
silking, then steadily declines during the phase of rapid
grain filling (Ying et al., 2000). Stem sucrose, along with
declining current photosynthate, provides the steady stream
of carbohydrates needed for efficient grain filling. Under
normal field conditions, stem carbohydrates accumulate
until the mid-phase of grain filling, when concentrations
begin to plummet (Fig. 2) (Sayre et al., 1931; Hume and
Campbell, 1972). This coincides with the start of rapid
starch storage in the endosperm (Setter and Flannigan,
1989). High-grain-yielding varieties tend to have low
amounts of stem carbohydrate that steadily decrease over
time. In contrast, lower yielding varieties tend to have high
concentrations of stem sugars that gradually increase during
the grain-filling period (Van Reen and Singleton, 1952).
Interestingly, when the ears of either the high- or lowyielding varieties are removed, stem carbohydrates reach
equivalent amounts in both varieties (Daynard et al., 1969).
This suggests there are no differences in the transport or
storage capacities in the two varieties; it is utilization by the
developing ear that impacts stem carbohydrate reserves.
Stem NSC reserves may also be essential to stabilize
carbohydrate availability during the early phases of ear
development when sink strength capacity of the grain is
determined (Borrás et al., 2004). The number and size of
cells in the endosperm, which regulates the entire carbohydrate storage capacity by determining the total number of
starch grains, are established before the phase of rapid
biomass accumulation (Borrás and Westgate, 2006; Gambin
et al., 2007). These early events determine the final yield
potential for the kernel. Disruptions in water or carbohydrate availability during this time greatly reduce the sink
potential of the kernel, leading to smaller kernels even if
excess carbohydrate is available during the later phase of
rapid grain fill (Borrás et al., 2004). Additionally, disruptions in water and carbohydrate supply can lead to floret
abortion in the ear, which dramatically decreases the yield
capacity of the plant (Setter and Flannigan, 2001; Wang
et al., 2002; Yu and Setter, 2003). However, some of these
detrimental effects can be reduced by injecting sucrose
directly into the stems of stressed plants, reducing floret
abortion and maintaining grain filling (Hiyane et al., 2010).
Standability is a critically important trait for mass
production agriculture (Betrán et al., 2003; Flint-Garcia
et al., 2003). Plants must remain erect for harvesting, and to
ensure proper grain quality by keeping grains away from
the soil surface. Unfortunately, many hybrids with high
yield potential suffer from lodging susceptibility due to
weak stem architecture or late season stem rot (Mortimore
and Ward, 1964). However, it was noticed early in hybrid
development that concentrations of stem soluble sugars
have a positive correlation with standability in maize
(Campbell, 1963; Mortimore and Ward, 1964). Cultivars
and hybrids that have high concentrations of stem carbohydrates have greater standabilty. How are stem sugars and
lodging resistance connected? One possibility is that high
sugar concentrations within the stem may keep the cells
alive longer, presumably due to the active component of
carbohydrate remobilization (Campbell, 1963). This may
prevent degradation from opportunistic necrotrophs which
degrade dead tissues and compromise the structural integrity of the stalk before the grain is harvested. Stem sugar
storage may be an essential component of the ’ functional
staygreen’ trait, the delay of senescence at the end of the
season or during periods of environmental stress (Thomas
and Howarth, 2000), providing an alternative transient sink
for photosynthate, while also prolonging standability and
photosynthesis for grain fill.
The diversity of maize genetic resources along with the
tools currently available for breeding suggests that leveraging stem NSC buffering capacity is an achievable objective
over the short term. Carbohydrate concentrations and
volumes of maize stems appear to have high heritabilities
(Widstrom et al., 1984). Additionally, maize displays a vast
range of phenotypic and genetic variably for the trait
(Daynard et al., 1969; White et al., 2011). Thus, there is
considerable potential to breed high-yielding maize lines
for direct stem sucrose production, as well as to breed it as
a secondary trait to increase standability, drought tolerance, and yield stability. Several lines of high sugar ‘Sweet
Maize’ have already been developed and marketed as
forage crops. These include the Cargill High-Sugar 50 line
(Marten and Westerberg, 1972) and the Connecticut 103
inbred line (Singleton, 1948; Van Reen and Singleton,
1952). The strategy behind the Cargill High-Sugar 50 line
is to prevent or delay the production of fertile ears,
therefore saturating the stem with sucrose that would have
been partitioned to the grain. Unfortunately, storage in the
stem cannot fully compensate for the loss of storage in the
grains, resulting in a net reduction of carbohydrate
accumulation in this line compared with normal grain
maize when used as silage. Many farmers prefer to grow
normal grain maize, giving them the option to use it for
grain or forage, rather than only having a forage crop
(Marten and Westerberg, 1972). In the case of the
Connecticut 103 inbred line, internodes were found to
have significantly more vascular bundles, little to no pith,
and high juice volumes when compared with other inbred
lines (Singleton, 1948). The stem anatomy and physiology
of Connecticut 103 resembles more those of high-yielding
cultivars of sugarcane and sweet sorghum, rather than
those of traditional maize stems.
Non-structural
carbohydrate
partitioning
in grass
stems 4653
Non-structural
carbohydrate
partitioning
in grass
stems
| 7| of
24
Can breeders develop maize that has both high stem
sucrose and grain yields? Is it possible to overlay the grain
productivity of the temperate grain maize-producing
regions with the productivity of sugarcane fields of the
tropics? Sweet corn production could provide a model for
such a system (Willaman et al., 1924). Sweet corn is
harvested when plants are still photosynthetically active.
The ear has been filled to the desired capacity of carbohydrates and removed for human consumption, but the plant
is programmed to continue production and allocation of
carbohydrates until the genetic termination point has been
reached. The green stalks, left standing without the strong
sink of the ear, fill with sugars derived from residual
photosynthesis in the leaves. These stalks have reached the
peak of sugar storage capacity and can be harvested and
treated in the same way as a sweet sorghum crop for
processing (Singleton, 1948). The next challenge for such
a maize plant, as well as high-grain-yielding sweet sorghum
varieties, will be to extract the grain and sucrose-rich stem
juice during harvest in the field, while leaving the vegetative
biomass to replenish the soil organic matter.
There is considerable potential to exploit stem NSCs in
maize. Controlling NSC reserves in maize stems has been
proposed as one way to mitigate the deleterious effects of
seasonal instability on maize yields in environmentally
unpredictable regions (Shiferaw et al., 2011). For example,
leveraging the stem NSC buffering system may be crucial in
new varieties produced for developing countries, such as
sub-Saharan Africa, Asia, and Latin America, where maize
is grown as a rain-fed crop, and thus more prone to
experience dramatic shifts in water availability. To be most
effective in maize, NSC reserves must be balanced with
remobilization to ensure the highest obtainable yields,
without yield penalties caused by excessive sucrose storage
in the stem (Monneveux et al., 2008).
Sorghum
Although sorghum only plays a modest role in highly
industrialized agriculture, it has been, and will continue to
be, an essential crop for many subsistence farmers in
developing countries. Due to sorghum’s drought tolerance,
it has become an important staple food for humans and
animals in many arid regions of the world (Garrity et al.,
2010). Sweet sorghum varieties are also gaining prominence
as a temperate substitute for tropical sugarcane to produce
sucrose for food and ethanol production. Thus, there is
considerable interest in developing sweet sorghum varieties
to fuel next-generation biofuels in non-tropical and marginal areas.
Sorghum presents an interesting model to study stem
NSC partitioning and its effects on other agronomic traits
due to the diverse varieties that are widely grown. The main
classes of sorghum are fibre, forage, grain, and sweet
(Dolciotti et al., 1998). The two most commonly grown
types are grain sorghum, grown for seed, and sweet
sorghum which is grown for the sucrose-filled stalks similar
to sugarcane. The primary difference between the two lines
is that one partitions carbohydrate mostly to one sink, the
grains, and the other to two sinks (grains plus stem). In the
case of sweet sorghum, stem storage parenchyma cells have
been bred to be terminal sucrose sinks, rather than transient
storage compartments. Thus selection has produced a dominant stem sink that appears to have higher priority for
sucrose storage than growing vegetative tissues or reproductive structures (McBee and Miller, 1982). Grain sorghums
usually contain less carbohydrate in the upper internodes
compared with sweet sorghum varieties, presumable due to
increased partitioning to the grains in the apical panicle.
Sorghum is similar to maize in that it employs the
apoplasmic mechanism of importing, storing, and remobilizing sucrose in mature internodes of the stem (Tarpley and
Vietor, 2007). Sucrose is neither converted to other substrates nor metabolized in the process. For example, when
internode tissues are infused with sucrose carrying a tritium
label on the fructose moiety, 81% of the sucrose is recovered
unchanged 1 d after infusion, suggesting that most of the
sucrose translocated into the stem storage parenchyma is
not hydrolysed or re-synthesized. In addition, sucrose
synthase and sucrose phosphate synthase activities are not
correlated with sucrose carbohydrate accumulation within
the internode (Hoffmann-Thoma et al., 1996). Thus, the
majority of sucrose transport is most probably mediated by
the sugar transporter proteins, for which expression patterns and functions remain unknown (Braun and Slewinski,
2009).
Sugar accumulation in internodes rapidly increases once
internode elongation has ceased (Hoffmann-Thoma et al.,
1996). It is still unclear when the internodes switch from
being symplasmic utilization sinks to apoplasmic storage
sinks. A decline in sucrose cleavage, presumably by reducing the activities of sucrose synthase and invertase
activity, has been associated with this possible transition
point (Tarpley et al., 1994, 1996). There are however,
notable exceptions. Some sorghum cultivars such as ‘Tracy’
have been bred to store hexoses at concentrations similar to
those of sucrose in the stem tissues. This line is particularly
useful in producing commercial syrups (Hoffmann-Thoma
et al., 1996). Increased hexose concentration could not be
attributed to elevated or prolonged invertase activity;
therefore, it is still unknown how these lines accumulate
high levels of hexoses.
Quantitative trait locus (QTL) analyses on populations
generated from crosses between grain and sweet sorghum
varieties reveal that the there are few large-effect loci that
condition the ‘pithy’ stalks of grain sorghum or ‘juicy’
stalks of sweet sorghum (Ritter et al., 2008; Murray et al.,
2009). ‘Pithy’ stems are characterized by an abundance of
dead-air-filled cells in the centre of the stem with vascular
bundles concentrated around the periphery of the stem
(Fig. 3). ‘Juicy’ stems have little to no dead-air-filled cells,
and usually have abundant vascular bundles across the
diameter of the stem. One QTL on chromosome 3 has been
shown in three independent analyses to control between
18% and 25% of the phenotypic variation for these traits
(Natoli et al., 2002; Ritter et al., 2008; Murray et al., 2009).
4654 8 of 24| Slewinski
| Slewinski
Sucrose-yield QTLs in sweet sorghum varieties are usually
pleiotropic and co-localize with other traits such as stem
diameter, plant height, flowering time, and tillering. Sucrose
yield per unit area is usually highly correlated with stem
density in the field (Vietor et al., 1990). In contrast, the
sucrose concentration trait in the stem appears to be
quantitative, resulting from many small-effect QTLs widely
distributed across the genome (Shiringani et al., 2010). Stem
sugar concentration is an additive trait, but is not noticeably increased in hybrids. Presumably, this lack of heterosis
for the trait is due to repeated selection for high juice
sucrose concentrations, which may now be at a physiological
ceiling for sucrose concentration (Pfeiffer et al., 2010). If
sugar yields per plant are to increase rapidly, breeders may
need to select for juice volume, a trait that is correlated with
stem volume and overall plant biomass. Storage of soluble
carbohydrates in the stem may be similar to storage
capacity of starch in the endosperm, which is determined
by the number of starch grains. The number of vacuoles,
determined by the number of storage parenchyma cells in
the internode, thus becomes a general indicator of sink
capacity in sorghum stems.
Light interception and the staygreen trait greatly affect
the concentrations of carbohydrates in the internodes
(Cook and Evans, 1983). An increase in sucrose yields in
sweet sorghum varieties may be achieved by genetic
adjustment of leaf angles to optimize light interception.
Additionally, staygreen varieties of sweet sorghum usually
have higher stem sugar concentrations than senescing lines
Fig. 3. Grain sorghum cultivar showing thin (A) and pithy (C) stem.
Sweet sorghum cultivar with a thick (B) and juicy (D) stem. Stem
tissue is composed of vascular bundles with surrounding parenchyma cells and also dead-air-filled parenchyma cells (white
arrowheads) which are more prevalent in C than in D. The white
dashed line in A and C represents the regions where sections in
C and D were taken. Bar, 5 mm.
(Borrell and Hammer, 2000). This may be due to the
reduced need for re-mobilizing stem sucrose in addition to
prolonged photosynthetic capacity (Duncan et al., 1981).
Thus the staygreen trait could be a significant trait in sweet
sorghum varieties in which stem sugar concentrations have
not reached the physiological maximum.
In warmer climates, sorghum fields can be ratooned (Byrt
et al., 2011); that is, harvested multiple times from one
initial planting. The effectiveness of ratooning depends on
which cultivars of sorghum are selected and how much of
the vegetative tissue is left for the regenerative process to
occur. When the plants are harvested, sugars in the stem
stubble left on the base are mobilized and transported to
new tillers (Fig. 4). Thus the root systems have already been
‘paid for’ in the carbon economy of the first cropping cycle.
Now the plants can more rapidly regenerate vegetatively.
This works well with highly tillered cultivars of either sweet
or grain-type sorghums that produce many stalks. The
rotation speed and quality of the ratoon crop may depend
on the carbohydrates left in the stubble after harvest which
can support initial growth before photosynthetic capacity is
regained (Dohleman and Long, 2009; Turgeon, 2010).
Ratooning also depends on the precise timing of senescence
of the floral structures to ensure proper dry-down of the
grains, the last step in seed maturation, while initiating new
vegetative growth at the base of the plant. Much more work
is needed to determine the impact these carbohydrates have
on the ratooned harvest and the development of agronomic
practices which would optimize the successive harvests.
Many grain sorghum varieties also have the ability to
remain highly productive during drought stress (Massacci
et al., 1996). Although the mechanisms that underlie this
trait are currently unknown, it is reasonable to hypothesize
that soluble carbohydrates within the vegetative structures
play a role. Soluble sugars in sorghum stems may be
Fig. 4. Sorghum tiller re-growth after the stem has been
harvested.
Non-structural
carbohydrate
partitioning
in grass
stems 4655
Non-structural
carbohydrate
partitioning
in grass
stems
| 9| of
24
functionally similar to those recently described for trees
(Q. Fu et al., 2011). It was proposed that in trees, high
concentrations of soluble sugars, and other osmotically
active compounds in the leaves, help to draw water into the
canopy to offset low hydrolytic conductance values of the
xylem transport stream. Thus, soluble sugars in the
vegetative tissues function in whole-plant water relations,
as well as in water stress tolerance.
Sugarcane
Almost 70% of commercially produced sucrose is derived
from sugarcane stems (Carson and Botha, 2002). Additionally, sugarcane has become a primary feedstock for the
production of ethanol in tropical countries such as Brazil,
supplying a large portion of liquid fuel. For the rest of the
world, it is estimated that by 2030 oil demand will be 50–
60% higher than current production. Reserves of easily
extractable crude oil [or better referred to as a ‘one-time,
incredibly concentrated reserve of solar energy’ (Pelletier,
2010)] are arguably declining. Therefore alternative, liquid,
renewable fuels such as sugarcane ethanol will become even
more critical for sustaining energy demands in the near
future while advanced generation biofuels are brought
online at practical, ecologically and economically feasible
scales (Hotta et al., 2010; Buckeridge et al., 2011).
Sugarcane accumulates large amounts of highly concentrated sucrose in the stem storage parenchyma cells. Sucrose
concentrations within stems can reach up to 0.7 M (;Brix
of 20) or ;50% of the stem dry weight (Moore, 1995;
Inman-Bamber et al., 2009). Unlike maize and sorghum,
sugarcane appears to employ a symplasmic transport
mechanism of phloem unloading into the storage parenchyma cells (Fig. 1) (Welbaum et al., 1992; Walsh et al.,
2005). Suberization and lignification of the cell walls that
surround the phloem block most, if not all, apoplasmic
sucrose movement from cell to cell. Additionally, asymmetrically labelled sucrose fed into the internodes remains
intact, suggesting there is little breakdown and re-synthesis
in the mature internode. This correlates with earlier studies
that suggest that futile cycling of carbohydrates also
decreases as the internode matures (Uys et al., 2007).
Therefore, sucrose influx to the storage parenchyma is
primarily conducted through the abundant plasmodesmata
that provide cytosolic continuity between cells which are
divided by highly suberized and lignified walls.
Presumably, the primary mechanism for sucrose storage
and mobilization is derived from the activity of sucrose
transporters on the tonoplast membranes of the storage
parenchyma cells (Rae et al., 2009). Recent evidence from
modelling studies further supports the idea that sucrose
movement into the vacuole is against a concentration
gradient, driven by an active transport mechanism (Moore,
2005). The turgor and sink strength in the storage parenchyma cells may also be balanced by increasing the sucrose
concentration in the apoplast that surrounds these cells
(Walsh et al., 2005). The highly suberized and lignified
barrier limits the spread of the sucrose to non-storage cells,
which prevents sucrose from leaking into the xylem stream.
This also prevents water movement into the concentrated
apoplasmic sucrose pool (Jacobsen et al., 1992; Welbaum
et al., 1992). It has been proposed that ShSUT1, a plasma
membrane-localized sucrose transporter expressed in the
storage parenchyma cells, most probably functions to
retrieve sucrose from the apoplasmic space, indirectly
regulating sucrose flux into the parenchyma cell (Rae et al.,
2005b). Interestingly, there is significant expression of
hexose transporters in the storage parenchyma tissues, but
their roles are still unclear (Casu et al., 2003). It is likely
that orthologues of AtSUC4, AtTMT1, and AtTMT2 in
sugarcane also mediate sugar flux across the tonoplast
membrane, regulated by both sucrose and hexose concentrations in the cells (Schulz et al., 2011).
Evidence suggests that once these cells have been filled to
capacity, plasmodesmata in the storage parenchyma cells
become blocked, which serves to prevent backflow (Rae
et al., 2005a). Due to the lignified and suberized cell walls
surrounding the storage parenchyma cells, export to the
vascular parenchyma cells during the re-mobilization process also appears to be symplasmic, driven by osmotic
potential between storage parenchyma cells and the phloem
when plasmodesmata are re-opened for transport (Rae
et al., 2005a). However, it is still unclear whether phloem
loading in the stems is apoplasmic or symplasmic during remobilization. It is possible that once sucrose reaches the
vascular parenchyma cells, it is effluxed into the apoplast
directly adjacent to the sieve elements and companion cells,
and retrieved by sucrose transporters. Extracellular invertase activity could also play a role in the reversal of sucrose
accumulation to export remobilization as suggested by the
expression of hexose transporter in the stem phloem tissue
(Casu et al., 2003). However, more work to support such
a mechanism is needed.
Improvement of yields in sugarcane by conventional
breeding is reaching a plateau, mostly due to the narrow
gene pool available in the commercial hybrid genetic stock
(Grof and Campbell, 2001). It is also possible that
sugarcane has reached a physiological limit with sucrose
concentrations at ;17–20% (w/v) (Jackson, 2005). Integration of other secondary traits such as disease resistance,
cold tolerance, and ratoon performance may have slowed
the direct improvement of sugar concentration in the stems.
Similarly to sweet sorghum, higher yields of sugar have
been obtained by breeding for stem volume and stem juice
yield, while maintaining high sucrose concentrations. The
final volume of the internode space capable of storing
sucrose is determined during the phase of internode
elongation, well before sucrose accumulation begins
(Glassop et al., 2007). Once cell volume is established, dry
matter, mostly sucrose, progressively replaces the water
until maximum physiological concentrations are reached.
Thus further sucrose yields attained from breeding may
come from morphological, not physiological, selection.
Sucrose concentration is greatly affected by agronomic
practices such as planting density. Higher stalk density
increases sucrose partitioning to the stems in sugarcane. In
| Slewinski
4656 10 of 24
| Slewinski
contrast, wider spacing increases assimilate supply in the
source leaves, but results in decreased partitioning to stored
sucrose in the stem, thus lowering yields (Pammenter and
Allison, 2002). However, shading leaves of more widely
spaced plants results in increased partitioning of sucrose to
the stem, even though overall biomass accumulation is lower.
A similar trend was reported for sucrose concentrations in
maize stems (Hume and Campbell, 1972). These data imply
that shading impacts partitioning within grass stems, suggesting signalling mechanisms that operate through assimilates
themselves, or hormones associated with shade avoidance or
vegetative development. Cooler temperatures are also known
to induce higher sucrose accumulation in sugarcane stems,
presumably due to decreased growth in vegetative structures,
which are competing sinks for sucrose (Lingle et al., 2009;
van Heerden et al., 2010). Interestingly, when sugarcane is
grown under high CO2 conditions, the amount of stem juice
produced per plant increases, but the concentration of sugars
remains the same (Vu and Allen, 2009).
Genetics and genomics in sugarcane are difficult due to
the size, complexity, and instability of the genome. Sugarcane contains between 10 and 13 homo(eo)logous copies of
most loci (Mudge et al., 2009), making QTL analyses for
sugar-related traits complex (Ming et al., 2002). Very few
large-effect QTLs have been identified in sugarcane, each
only explaining 5–7% of the whole variation for yield traits
in one study (Hoarau et al., 2002), and between 3% and 6%
in another (Aitken et al., 2006). Each QTL effect may be the
result of specific combinations and ratios of expression of
alleles at each locus, making accurate marker-assisted
selection almost impossible (Mudge et al., 2009). Fortunately, sorghum and maize are closely related to sugarcane,
diverging ;5 million years ago (Vermerris, 2011). Thus,
there is much co-linearity between the genomes (Wang
et al., 2010). Progress gained in sorghum and maize may be
translatable into sugarcane for traits such as height, stem
thickness, disease resistance, tillering, ratooning ability, and
time to maturity (Guimaraes et al., 1997). The practice of
ratooning in sugarcane is similar to that of sorghum, with
the exception that sugarcane fuels much of its re-growth
using carbohydrates stored in underground rhizomes, along
with sugars left in the stubble (Matsuoka and Garcia, 2011).
It will be interesting to see how sugar storage traits compare
between species because of their divergent mechanisms of
sucrose transport and stem anatomy. Further investigations
are needed to elucidate finer details on the developmental
control and physiology that underpin sucrose storage ability
in sugarcane, sorghum, and maize so that genetic and
genomic data can be accurately translated between species.
It is estimated that ;80% of the genome of high-sugar
cultivars of sugarcane is from Saccharum officinarum,
a species that naturally accumulates large amounts of
sucrose, rarely flowers, and has few tillers (Hoarau et al.,
2002). The other 10% of the genome is from Saccharum
spontaneum, a species that does not accumulate sucrose,
flowers profusely, and is highly tillered. Hybrids made from
S. spontaneum are now used for the production of ‘energy
cane’ cultivars that are utilized for cellulosic biomass, rather
than sucrose production (Waclawovsky et al., 2010).
However, breeding strategies for sugar-producing grasses
are not limited to intraspecies crosses. For example,
sugarcane will produce viable offspring when crossed to
Miscanthus, Erianthus, Narenga, and Sclerostachya
(Glassop et al., 2010). These grasses are known as the
saccharum complex, and are currently being utilized to
produce intergenic hybrids that maximize favourable traits
of two species and broaden the climatic zones where cane
sugar and biomass can be produced. Saccharum crosses
with Miscanthus produce cold-tolerant hybrids for sugar
and biomass production in subtropical regions.
Wide crosses to sugarcane are not limited to the
saccharum complex. The reproductive barrier between
sugarcane and sorghum has recently been defeated, allowing the production of an F1 hybrid between the two genera
(Hodnett et al., 2010). It will be interesting to investigate the
mechanism that these hybrids use to transport and store
sucrose in the internodes, given that each parent uses
a different mechanism.
Raising the concentration of sucrose alone in sugarcane
stems by the use of biotechnology has been difficult. Only
a handful of the specific transporters, enzymes, or other
proteins that regulate sucrose accumulation are currently
known (Casu et al., 2005). Sugarcane is also prone to
transgene silencing, which limits the successes of many
transgenic approaches (Mudge et al., 2009). Microarray
analysis on sugarcane genotypes that vary in sucrose content
revealed that many of the genes associated with high sucrose
content show overlap with drought data sets, but appear to
be mostly independent from abscisic acid signalling (PapiniTerzi et al., 2009). In spite of the difficulty, there have been
reports of transgenic sugarcane plants that show increased
sucrose accumulation. Down-regulation of pyrophosphatefructose-6-phosphate 1-phosphotransferase activity leads to
a 3- to 6-fold increase in sucrose in immature stems,
presumably by limiting the conversion of hexose phosphates
to triose phosphates (van der Merwe et al., 2010). Additionally, down-regulation of neutral invertase results in an
increased sucrose to hexose ratio by decreasing respiration
and sucrose cycling in the mature stems (Rossouw et al.,
2010).
Is the plateau in sucrose accumulation due to osmotic
limitations? Production of sucrose isomers in sugarcane
suggests not. Transgenic sugarcane plants expressing a vacuolar-localized sucrose isomerase that produces the
disaccharide isomaltose accumulate double the amount of
soluble carbon in the stem storage parenchyma (Wu and
Birch, 2007). Isomaltose is biologically active in plant cells,
but may not trigger the same sugar signalling mechanism as
sucrose or hexoses. In the transgenic lines that produced
high concentrations of isomaltose there was also an increase
in photosynthetic rates in the leaves. This suggests that the
plants are capable of producing and storing more carbohydrates, but may be limited by a feedback mechanism linked
to sucrose or hexose concentrations and not total osmotic
potential. These data also correlate to physiological evidence that suggest a more sink-limiting model in sugarcane,
Non-structural
carbohydrate
partitioning
in grass
stems 4657
Non-structural
carbohydrate
partitioning
in grass
stems
| 11| of
24
suggesting that photosynthetic rates in the leaves are
regulated by the downstream capacity of storage in the
stems (McCormick et al., 2008a, b, c). As seen with the
production of isomaltose, the source tissues will adapt to
changes in the metabolism and compartmentalization in
sink tissues.
Symplasmic transport through the storage parenchyma
cells has been suggested to be a control point for sucrose
flux into the storage cells (Walsh et al., 2005). Thus
manipulation of plasmodesmata may be one method to
alter sucrose partitioning within the stem. Flux through
plasmodesmata is altered by the presences of viral movement proteins, thereby facilitating cell-to-cell trafficking of
viruses (Ueki and Citovsky, 2011). Strategic expression of
these proteins in stem storage parenchyma cells has been
proposed as one avenue to manipulate symplasmic flux and
sucrose accumulation rates in sugarcane.
The reduced-growth phenomenon documented in sugarcane is presumably caused by feedback inhibition when
stem sucrose becomes elevated, which also increases foliar
carbohydrate concentrations (van Heerden et al., 2010).
Foliar hexose pools, especially glucose, have been suggested
to inhibit photosynthesis as a mechanism of feedback
regulation in sugarcane (McCormick et al., 2008c). The
majority of the sugar signalling mechanisms, such as the
hexokinase-dependent mechanism, are located in the cytosol
(Granot, 2008; Slewinski, 2011). One way to defeat such
feedback inhibition would be to overexpress the tonoplastlocalized glucose/sucrose transporters to reduce the cytosolic pool of glucose, regardless of the sink strength of the
stalk (Wingenter et al., 2010). Proof of concept for this
mechanism was recently shown in Arabidopsis where increased activity of AtTMT1 apparently ‘hides’ glucose from
cytosol-localized sensing mechanisms without disrupting the
carbohydrate dynamics of the plant (Wingenter et al., 2010;
Slewinski, 2011). Overexpression of AtTMT1 in Arabidopsis
also leads to an increased rate of photosynthesis, carbohydrate partitioning, and reduced whole-plant respiration.
Perhaps the same process of overexpressing TMTs could be
engineered into sugarcane to reduce feedback inhibition and
mitigate the reduced growth phenomenon.
Rice
Rice is the most important crop on the earth, providing
35–60% of the calories consumed by almost half of
humanity (Fageria et al., 2003). It is estimated that 30–40%
of the grain mass can be comprised of previously stored
stem reserves when plants are grown under normal conditions (Yoshida, 1981). Carbohydrate partitioning in rice
plants is also interesting because plants store carbohydrate
reserves as sucrose in the leaves and both starch and sucrose
in the stems—a pattern that diverges from many of the
grasses (Scofield et al., 2009).
Phloem unloading into stem storage parenchyma cells is
presumably symplasmic (Scofield et al., 2007). Chemical
and osmotic gradients necessary for influx into the cells are
generated by rapid conversion of sucrose to starch which is
stored in the amyloplasts (Patrick, 1997). It is unclear how
sucrose is exported from the stem storage parenchyma cells
back to the phloem during the re-mobilization process. It is
possible that during export, cells block plasmodesmata and
switch to an apoplasmic mechanism which utilizes sucrose
transporters, such as OsSUT1, to pump sucrose actively
against a concentration gradient into the phloem (Scofield
et al., 2007)
Crop management practices can also have a dramatic
effect on carbohydrate partitioning in rice (Fageria et al.,
2003). One of the largest concerns is the use of fresh water
for rice production. Taking into consideration that rice
production consumes almost 80% of the fresh water in
Asia, practices that reduce water consumption, such as
partial drying during the crop cycle, may become more
common as the abundance of fresh water declines (Yang
and Zhang, 2010a). Fortuitously, partial drying of the soil
enhances the mobilization of carbohydrates from the stems
and expedites the grain filling process, leading to high
grain yield and harvest index. However, this only works if
the drying is controlled in a manner that does not severely
impact current photosynthesis and induce a drought response. For a more in-depth discussion of water management practices and rice yields, I refer readers to Yang and
Zhang (2010a).
Quantifying NSCs in stems at harvest is one way to
detect sink–source imbalances in grain-producing grasses.
A recent survey of major domestic cultivars of rice grown
under normal agricultural conditions in Japan found that
all varieties have significant NSC left in the straw (Park
et al., 2011). Other reports indicate that if too much
nitrogen is applied to fields, or plants express the staygreen
condition longer than is needed for grain fill, stems become
saturated with starch (Pan et al., 2011). This starch is then
disposed of in the chaff during harvest, which decreases the
harvest index. Interestingly, hybrid rice varieties also have
reduced harvest index, presumably due to the same
phenomenon. These data suggest that rice exhibits more
sink than source limitation imposed by constraints in the
transport or grain-filling processes.
This raises some important questions. Will increasing
carbohydrate source strength be enough to increase yield?
Does increased and sustained photosynthesis correlate
with increased grain fill and harvest index? Carbohydrate
partitioning involves not only the production, storage, and
utilization of carbohydrates, but is also critically dependent on transport. Transport is determined by both the
physiology and vascular architecture of the transport
system (Dinant and Lemoine, 2010). Rice panicles that
produce more spikelets per panicle, so-called ‘Super Rice’,
have problems filling grains produced on the inferior
spikelets (Yang and Zhang, 2010b). These plants become
more ‘source limited’ as spikelet density increases, but the
grain-filling problem may result from inadequate vascular
connections to the inferior spikelet. This results in normal
grain filling in the superior spikelet, but reduced in the
inferior spikelets, throughout the panicle (Yang et al.,
2002). Such morphogenetic constraints in the vascular
| Slewinski
4658 12 of 24
| Slewinski
system can confound investigations into sink–source dynamics (Watson and Casper, 1984). Furthermore, grass
inflorescences do not function as a homogeneous sink
tissue, but function sectorially based on architecture (Cook
and Evans, 1983). This raises great concern about increasing the productivity of rice, as well as other grain
crops by increasing photosynthetic capacity, carbon storage, or spikelet density. Research is now directed towards
installing the high capacity C4 photosynthetic system into
rice (Sage and Zhu, 2011). Such questions need to be
addressed in the near future to optimize the efficacy of
such strategies. New limiting factors to yield enhancement
appear as other factors become non-limiting. Increasing
productivity will most probably require an extensive
redesign of the plant, including the physical architecture
of the vascular system and buffering capabilities in the
stem, not simply the introduction of the C4 photosynthetic
syndrome.
It is also important to understand that, as noted above
for maize, NSCs in the stems during the pre-anthesis stages
of development may dramatically affect final sink strength
by increasing spikelet survival during the exceptionally
sensitive early development phase of the spike. Higher
reserves of NSCs may also impact cell size and starch
granule number in the spiklets early in development, which
are the primary indicators of sink potential during grain fill
(J. Fu et al., 2011). Total above-ground biomass has
a positive correlation with sink strength in varieties that are
proportionally higher in inferior spikelet density.
In climates that have extended growing seasons, rice can
also be ratooned (Turner and Jund, 1993). The second
harvest only yields about one-third of the first harvest
(Harrell et al., 2009). However, increasing the total yield
from one planting without significant inputs can drastically
improve grain production on a per-land and fertilizer basis
(Santos et al., 2003). The speed of vegetative re-growth,
flowering, and grain filling depends on the initial reserves
that remain after the first harvest. For rice, this is correlated
with the size of the stem tissue that remains (Jones, 1993).
Starch in the remaining stem is quickly hydrolysed and
transported to new tillers at the base. Alternatively, if the
stem is long enough, carbohydrates will be partitioned to
nodes on the stem to produce new floral structures
immediately. Regeneration of floral structures is usually
more rapid than in the first crop. Grain set and filling are
also significantly accelerated (Harrell et al., 2009). As with
most plants, the early investment in photosynthetic organs
has the most impact on overall plant growth and development (Turgeon, 2010).
Is it possible to optimize the sugar transport stream
further in order to convert more of the NSCs in the stem
into grain mass? As the data highlighted above suggest,
there is still much that remains unknown about carbohydrate partitioning in rice, and how entire life cycle dynamics
impact yield. Even though many aspects of carbohydrate
partitioning remain elusive, there is potential for improvement in the way currently grown cultivars convert carbohydrate stores into harvested grains.
Wheat, barley, and oat
Wheat, barley, and oat collectively provide most of the grain
calories in the temperate and cooler regions of the world. The
roles and mechanisms of storing and remobilizing stem
carbohydrates in wheat have been more intensely studied
than in other grain-bearing grasses (Schnyder, 1993; Blum
et al., 1994; Wardlaw and Willenbrink, 2000). This is because
early researchers discovered a direct correlation between
carbohydrate storage in the stems and the ability of the
plants to maintain high yield stability under drought or other
environmentally deleterious conditions (Bindinger et al.,
1977; Asseng and Herwaarden, 2003). Mobilized reserves
from the stem tissues can contribute ;20–40% of the final
grain weight under normal non-stressed growing conditions
(Dreccer et al., 2009). The greater contribution of stem
reserves comes into play under stressful conditions during
grain fill, such as end-of-season drought, when stem carbohydrates can contribute to >70% of the final grain mass
(Goggin and Setter, 2004; Ehdaie et al., 2006; Rebetzke et al.,
2008). High NSC wheat genotypes are usually shorter,
produce fewer but more fertile tillers, and flower earlier.
Overall biomass of the high NSC lines is low, but a higher
proportion is partitioned to the grain, leading to a higher
harvest index (Rebetzke et al., 2008).
During the grain-filling process, current photosynthesis
usually provides more than enough carbohydrates for the
developing grains (Slafer and Andrade, 1991). Only when
current photosynthesis drops below the maximum fill rate
of the kernel does mobilization from the stem begin. These
data imply that grain filling is a rate-limiting process that is
driven at maximum capacity during the entire filling process
(Bingham et al., 2007). In barley, carbohydrates derived
from stem reserves may be preferred to prolonged photosynthesis during the later phases of grain fill. Cultivars with
high NSCs in the stems usually produce grains with higher
dry mass. However, there does seem to be a trade-off in
grain number. Low NSC lines usually produce more grain
per unit area, but produce grains with lower individual mass
(Rebetzke et al., 2008). Increased grain mass in the high
NSC lines appears to compensate for the lower grain
number because these lines are overall higher yielding and
produce higher quality grain.
Increases in wheat yields over the past few decades were
due to producing more grains per unit area rather than
increasing individual grain mass (Sadras, 2007; Sadras and
Egli, 2008). Thus, reducing yield losses from floret abortion
and sterility, due to carbohydrate starvation, are still critical
targets for cultivar improvement (González et al., 2011).
However, grain filling in wheat may be similar to that in
rice in that the vascular system itself is insufficient to
transport needed sugars to the developing spike. For
example, the distal florets are connected to the primary
vascular bundles in the spike stem through the subvascular
system—a transport route that lacks direct connections to
the primary phloem (Hanif and Langer, 1972). This raises
major concerns for yield improvement in wheat and barley
by increasing spikelet number per panicle. As breeders and
Non-structural
carbohydrate
partitioning
in grass
stems 4659
Non-structural
carbohydrate
partitioning
in grass
stems
| 13| of
24
basic scientists raise both source and sink potentials, the
physical architecture of the vascular system itself may
become the new limiting factor in the carbon economy of
the plant (Asli and Houshmandfar, 2011). Buffering the
supply with stem carbohydrate reserves may be one way to
maximize transport through a constrained vascular route.
However, eventually the vascular system itself will have to
be altered to accommodate the high rates of transport to the
developing florets and grains. More research is needed in
this area to identify substantial bottlenecks in transport and
grain-filling processes.
Presumably, influx into storage parenchyma cells of these
grasses is symplasmic, as it is in many tissues that
accumulate sugar polymers (Aoki et al., 2004). Stem NSC
in wheat, barley, and oat is mostly in the form of fructans
stored in the vacuoles of the stem storage parenchyma cells.
Other major carbohydrates do not significantly contribute
to the NSC reserves, or show little variance between high
and low stem NSC lines (Bancal and Triboı̈, 1993; Ruuska
et al., 2006). Starch is present in the stem and leaves of
wheat, but has been suggested to function as a source for
vegetative growth rather than for mobilization to the grain
(Scofield et al., 2009). Fructan synthesis may depend more
on sucrose availability, as seen when fructans become
rapidly labelled when [14C]sucrose is injected into wheat
stems (Hogan and Hendrix, 1986). However, fructan
concentrations in wheat are not directly correlated with
fructosyltranserase activity (Goggin and Setter, 2004).
The average degree of fructan polymerization in leaves
varies depending on cultivar, stage of plant growth, and
environmental conditions (Wardlaw and Willenbrink,
1994). NSC accumulation usually occurs between anthesis
and completion of endosperm cell division (Wardlaw and
Porter, 1967). There also appears to be minimal costs to
storing carbohydrates in the wheat stem as there is minimal
energy lost to respiration. Thus, the storage and remobilization process appears to be metabolically efficient (Bell and
Incoll, 1990; Gebbing and Schnyder, 1999; Xue et al., 2008).
In barley, the most promising potential to increase
radiation use efficiency may come from alterations in sink–
source dynamics (Bingham et al., 2007; Newton et al.,
2011). Barley appears to be much more sink than source
limited. Presumably, the low sink capacity of barley leads to
a reduction in photosynthetic productivity due to feedback
inhibition. In most genotypes and environments, stem
carbohydrate reserves build up and are not remobilized to
the grain, resulting in a decreased harvest index. Improved
partitioning to the ear when the spikelets are forming
during the stem elongation phase may help to increase
spikelet survival, leading to more grains per plant, thus
increasing sink strength and yields (Borràs-Gelonch et al.,
2010). For such a scenario to be feasible, stem elongation
will have to start earlier in the plant life cycle and near
completion before spikelet development progresses, all
without disrupting the time to anthesis (Borràs et al., 2009).
Because oat employs the same mechanism of fructan
storage in stems, progress made in wheat and barley may
be transferred into oat (Livingston et al., 1993, 1994).
Improving stress tolerance in wheat by manipulating
NSCs in stems has already been put into practice in areas
where environmental conditions are suboptimal (Ehdaie
et al., 2006). Such is the case in Australia where severe and
terminal droughts are common (Bell et al., 2010). Wheat
cultivars that have high NSCs in stems show improved
floret fertility, grain filling, and yield stability when grown
under rain-fed or drought conditions. When these lines are
grown under irrigated and non-stress conditions, yields
from high stem NSC lines are comparable with those of
low NSC lines, suggesting there are no yield penalties
associated with high NSCs if the plant does not experience
stress (Foulkes et al., 2007).
One QTL study for stem NSCs in wheat identified two
regions located on chromosomes 1b and 2A (Foulkes et al.,
2001). In another QTL study it was proposed that there are
between eight and 16 QTLs for stem NSC concentration, and
between four and eight QTLs for total NSC yield (Rebetzke
et al., 2008). Many of the genes that encode enzymes that
function in fructan degradation and remobilization, such as
fructan exohydrolase, also co-localize with QTLs for stem
NSC concentration, grain-filling rate, and grain weight
(Yang et al., 2004). Similar to the grasses mentioned above,
the NSC trait in wheat is linked to morphological characteristics. Because stem length, diameter, and solidness all have
high heritability values ranging between 0.42 and 0.84
(Ehdaie et al., 2006), breeding programmes could be highly
effective at optimizing and combining the traits to increase
stem NSCs in wheat varieties designed for more arid and
drought-prone areas. There is also high variability in stem
elongation rates in wheat and barley. Therefore, the ability to
modify the timing of spikelet development and onset of NSC
accumulation genetically also shows potential (Slafer and
Araus, 2007).
Modulating the transcription of fructan-synthesizing and
degradation genes could also be employed for controlling
NSC partitioning in wheat and barley stems. Recently, the
wheat transcription factor TaMYB13 was found to be
a transcriptional activator of Ta1-SST and Ta6SFT,
suggesting that TaMYB13 and its orthologues are involved
in the regulation of the fructan synthetic pathway (Xue
et al., 2011). Perhaps similar MYB-type transcription
factors also control carbohydrate partitioning genes in
other grasses. Manipulation of such transcriptional modifiers, through either introgression of natural variants or
transgenic approaches, could offer a new route to control
carbohydrate distribution in grasses.
Forage and energy grasses
Mixed-pasture grasslands cover almost a quarter of the
total ice-free land area on earth—roughly 30 million km2
(Monfreda et al., 2008; Lee et al., 2010). Most of these
grasslands are essential for livestock feed, which dramatically impacts global food production and economies, and
supports the indigenous wildlife that inhabits those areas
(Lee et al., 2010). Knowledge of the growth and re-growth
cycles of grassland species is critical for determining the
| Slewinski
4660 14 of 24
| Slewinski
stocking density of the pasture and overall grazing management practices (McNaughton, 1979; Lemaire et al., 2009).
Overgrazing can lead to pasture collapse, and undergrazing
can lead to unproductive land use and deterioration of
nutrient value of the fodder. In addition, the stage of regrowth at which the grasses are consumed is important for
animal nutrition. Such vast grasslands also act as a carbon
sink which can buffer the effects of increased CO2 emissions.
Unfortunately, improper management practices along with
recent environmental insatiability have severely degraded
large portions of essential pastures and grasslands, thus
exacerbating the effects of climate change, CO2 sequestration, and pasture-based food production (FAO, 2009).
Most of the economically important forage and energy
grasses are perennials, which store moderate levels of
carbon reserves in stems and roots to fuel re-growth from
year to year, and also after grazing or cropping (reviewed in
Fulkerson and Donaghy, 2001). Grasses in pasture lands
lose much of their photosynthetic leaf area during grazing;
therefore, subsequent photosynthetic capacity is not sufficient to drive re-growth of the photosynthetic tissues
(Turner et al., 2006; Lee et al., 2010). Mobilized reserves
from stems, pedicels, and roots are utilized until leaves are
about three-quarters their final size—the stage when leaves
transition into productive source tissues. Presumably,
grasses that have evolved in areas where grazing is common
have a reduced specific leaf weight, thereby reducing
construction costs of a new photosynthetic area after
defoliation (Cullen et al., 2006).
In Lolium prenne (ryegrass), fructans in the stem and leaf
sheath are used for both energy storage and stress protection (Griffith, 1992; Hisano et al., 2004). After repetitive
carbon depletions, photosynthetic and fructan synthesis
genes become up-regulated while fructan degradation genes
are down-regulated (Lee et al., 2010). This ensures that
long-term stores are recovered before the next defoliation
event. Fructans also play an important role in freezing
tolerance in Lolium. Lolium perenne plants that express both
6-SFT and 1-SST under the 35S promoter have increased
tolerance to freezing. Presumably, high levels of fructans
help to stabilize membranes under cold stress and support
winter hardiness (Hisano et al., 2004). Re-mobilization of
carbohydrate reserves in Lolium uses the apoplasmic
mechanism. Expression of LpSUT1 is strongly induced in
the lamina within 24 h of blade detachment, suggesting that
fructans stored in the cells are converted into sucrose and
pumped into the phloem against a concentration gradient
(Berthier et al., 2009).
Energy grasses, such as miscanthus or switchgrass, are
grown for their cellulose-rich stems and leaves. Along with
stem carbohydrates, these grasses also utilize underground
rhizomes to store energy for the subsequent year’s growth
(Glowacka, 2011). Switchgrass is similar to rice in that the
main store of NSCs in the stems is starch (Smith, 1975).
Starch accumulation peaks at the beginning and end of the
growing season, before and after flushes of rapid growth.
Upon defoliation, starch levels plummet, then rapidly rise
once a new photosynthetic area has been produced. Switch-
grass plants that overexpress the Corgrass/miR156 transcript,
which alters the developmental progression from juvenile to
reproductive phase, hyperaccumulate starch in the internode
tissue (Chuck et al., 2011). These lines also show a dramatic
increase in tillering and biomass accumulation when compared with controls. The hyperaccumulation of starch is
presumably due to the absence of flowering in the transgenic
lines which partitions more carbon into vegetative storage,
similar to the sucrose accumulation patterns in maize and
sugarcane cultivars that have a delayed or suppressed
reproductive phase. Starch hyperaccumulation in grass
biofuels feedstocks may be favourable because starch can be
stored as dry matter for long periods. Thus, starch in stems
may be easier and more cost-effective to convert into ethanol
when compared with soluble sugar or pure cellulosic feedstocks (Chuck et al., 2011).
Miscanthus offers the most efficient model for carbon
allocation in next-generation biofuel crops. Miscanthus
appears to be most similar to sugarcane in that it stores
NSCs as sucrose in the stems, although the mechanism for
radial sucrose transport into the storage parenchyma cells
remains to be elucidated (Burner et al., 2009). The aboveground biomass of miscanthus is harvested after the plant
has fully senesced (Glowacka, 2011). Thus, any remaining
NSCs, minerals, and high molecular weight compounds that
are not incorporated into structural tissues are mobilized
and partitioned to rhizomes to increase winter survival and
fuel the next year’s growth. Unlike annual grasses, excess
NSCs in the stems at the end of the season remains part of
the productive carbon economy of the plant. As mentioned
above, crosses with sugarcane will potentially result in new
high-yielding hybrids that produce both cellulosic biomass
and sucrose in more temperate regions of the world.
Prospects for NSC partitioning in grass
stems
One of the most disturbing trends in agriculture is the
increasing yield gap in the grass crops (Godfray et al.,
2010). Yield potentials in many of the crops are already
high, but actual yields rarely reach the upper limits. The
yield gap results from the accumulation of unfavourable
events during the life cycle that lead to a decrease of
carbohydrate production or partitioning to the harvested
tissue, in most cases the grains (Willenbrink et al., 1998).
Closing the yield gap will require drastic exploitation of the
sink–source relationship in the grass crops. However, most
sink or source components that directly affect yield appear
to be negatively correlated with each other (Slafer et al.,
1996). The nature of these negative relationships remains
unknown. Therefore, new descriptive models are needed
that diverge from simple sink- or source-limited systems, to
whole-plant entire life cycle systems to understand these
relationships fully. This will require deeper investigations
into the underlying physiological phenomenon at the ‘crop
level of organization’ (Slafer and Savin, 1994; Boote et al.,
Non-structural
carbohydrate
partitioning
in grass
stems 4661
Non-structural
carbohydrate
partitioning
in grass
stems
| 15| of
24
2001; Slafer, 2003) which incorporates the buffering capacity of the stems.
Much of the temperature and water stress in grain crops
does, and will continue to occur during the grain-filling
periods of the life cycle, near the end of growing seasons.
Rising global temperatures between 1981 and 2002 have
already decreased yields in major cereal grains, resulting in
US$5 billion in losses per year due to such stresses (Lobell
et al., 2008, 2011). Stem NSC reserves may be able to
mitigate some of the loss due to decreased photosynthetic
rates, uncoupling the on-demand assimilate supply that
drives yield increases in current grain cultivars. Non-irrigated
agriculture stands to gain the most from the leveraging of
NSCs in stems because most rain-fed crops experience at
least some degree of drought-like conditions during the
growing season. High soluble sugar concentrations in the
stems may also be an adaptive trait in grasses that have low
optimal hydraulic conductance, in order to pull water from
the soil into the vegetative parts of the plants, such as the
mechanisms proposed in trees (Q. Fu et al., 2011). However,
more work is needed to confirm this hypothesis in the
grasses.
Can larger stem NSC reserves increase radiation use
efficiency in the grasses (Reynolds et al., 2011)? It has been
suggested that in barley, one of the most promising ways to
increase radiation use efficiency is to increase sink strength
and storage capacity (Newton et al., 2011), which includes
NSC reserves in the stems. Climate change will result in areas
of the world that are hotter and more prone to drought,
while also creating wetter areas elsewhere, resulting in
a decrease in irradiance (Stanhill and Cohen, 2001). In the
wetter areas of increased cloud cover, excess moisture will
increase the prevalence of pathogen and insect damage to
photosynthetically productive leaf area (Garrett et al., 2006).
Grass stems, especially sugarcane, hold promise as
a sustainable commercial platform to produce sugar-derived
biomaterials. Single-gene transgenic lines of sugarcane that
constitutively express either isomaltose synthase or trehalose synthase efficiently convert the majority of the sucrose
in the storage parenchyma vacuoles into the respective
isomer (Wu and Birch, 2007; Hamerli and Birch, 2011).
Isomaltose and trehalulose have high commercial value as
non-carcinogenic and low-glycaemic food additives
(Basnayake et al., 2011). There is also potential to use
sugarcane and other grasses for the production of sugar
derivatives, sucrose-derived polymers, bioplastics, waxes,
and other compounds (reviewed in Verpoorte et al., 1999;
Birch, 2007). It may also be possible to install one of the
polymer synthesis mechanisms, such as fructan or starch
synthesis, into sugarcane stem storage parenchyma cells in
order to increase carbohydrate density, thus increasing the
sink strength and storage ability of the cane. Similar to
production of sucrose isomers, polymer synthesis may
bypass the native sugar signalling mechanisms which would
allow for hyperaccumulation of carbon reserves within the
cells (Basnayake et al., 2011). Theoretically, installing
fructan synthesis into sugarcane or sweet sorghum may be
relatively simple because of the few proteins that are needed
to synthesize fructans, as wells as the entire process being
confined to the vacuole (Pollock and Kingston-Smith, 1997;
Cairns, 2003; Rae et al., 2009).
Ratooning can be used as an already existing agricultural
model of how to develop and manage perennial grain and
biomass crops (DeHaan et al., 2005). More in-depth investigations into current successes and pitfalls will help breeders
and biotechnologists select and design essential traits early in
development of the perennial counterparts to our current
annual crops (Wagoner and Schaeffer, 1990; Cox et al.,
2006). Important traits for the perennial conditions will most
probably involve vegetative carbohydrate storage organs
such as stems, roots, and tubers that fuel rapid re-growth for
successive croppings or seasons as well as prolonged resistance to disease and insects (Glover et al., 2010). Prospects
to reduce tilling and inputs in such perennial systems are
substantial. One of the major problems with prolonged or
permanent cropping systems is the infestation of weeds,
which consume resources and compete with the crops
(Clements and Ditommaso, 2011). Aggressive weeds can
destroy up to 100% of a harvest in some annual crops. If
such devastation is possible in annual crops, what will
happen in the perennial cropping system where weeds will
have more opportunities to establish larger reserves of seed
banks in the soils, as well as underground structures that will
re-fuel their own re-growth year after year? One strategy to
help control weed devastation is to increase the growth rate
of the crop, thus outcompeting the weeds. As seen with the
difference in growth rates between miscanthus and maize
(Dohleman and Long, 2009), initial investments into productive photosynthetic area dramatically alters the plant’s
ability to produce biomass and compete with other plants.
Proper management of stem carbohydrate reserves, by
strategic harvesting practices to maximize reserves that
remain in the vegetative structures, may increase the resistance to weed damage in ratooned and perennial crops.
Thus, utilizing ratooned crops as a model to optimize and
troubleshoot potential problems is essential for the early
developmental stages of perennial cropping systems.
New strategies for complex genetic traits
Although there is great potential for the applications of
stem NSC buffering, phenotyping stem carbohydrates is
usually destructive and time consuming. This makes it
difficult for conventional breeding practices, or for agricultural biotechnology companies, to produce products in an
inexpensive and timely manner. Indirect phenotyping, by
measuring the dry matter content of the stem, is used as an
indicator of NSC in wheat stems (Ford et al., 1979; Xue
et al., 2009; Saint Pierre et al., 2010). This bypasses the need
to extract and quantify fructans and soluble sugars.
Methodologies used for sugarcane and sweet sorghum rely
on brix, the refractive index of juice that gives an estimate
of soluble contents in a liquid, to phenotype stems sugars
rapidly (Ritter et al., 2008). New methods of stem nearinfrared reflectance spectroscopy are now being developed
| Slewinski
4662 16 of 24
| Slewinski
to measure sugar concentration in vivo, eliminating the need
for destructive sampling (Wang et al., 2011).
Stem carbohydrate concentrations and total yields appear
to be complex genetic traits in the grasses. Very few largeeffect QTLs that account for significant variation have been
found, or are effective in increasing carbohydrates when
introgressed into elite lines (Aitken et al., 2006). Thus stem
carbohydrates must be approached using quantitative trait
methodologies, similar to grain yield, which result from the
additive effects of many small-effect genes dispersed
throughout the genome. Many secondary traits that control
NSCs in stems also display transgressive phenotypic variance, meaning offspring display phenotypes that are beyond
the range of the parents (Ming et al., 2002; Rebetzke et al.,
2008). Therefore, hybrids that leverage heterosis are theoretically possible. A wide variation of stem carbohydrate
traits already exists within the germplasm used for hybrid
production (Ruuska et al., 2006). Trait-based physiological
breeding has already been implemented in wheat in
Australia, and CIMMYT includes higher transpiration
efficiency, reduced tillering, and dehydration avoidance
(Foulkes et al., 2011). Similar approaches can be used for
many stem NSC traits in many of the grass species.
Although standard QTL identification and introgression
may not be a possibility for stem carbohydrate traits, these
traits are excellent candidates for genomic selection which
can rapidly compile additive small-effect loci into individual
plants. For crops such as sugarcane, genomic selection may
be one of the only methods that could be employed to
improve sugar traits rapidly due to the genomic complexity,
long reproductive cycle, and heterogeneity of the breeding
stock. Elite sugarcane parents still have many untapped
small- to moderate-effect QTLs that, when collectively
utilized on a whole-genome scale, could lead to steady
incremental increases in volume and concentration of
sucrose (Aitken et al., 2006). Genomic selection was developed to enhance quickly and cheaply the breeding of
genetically complex traits such as stem NSC partitioning
(Rutkoski et al., 2011). Genomic selection can predict the
breeding value of the individual based on the genomic
similarly to another individual that has been phenotyped
and genotyped. These methods also reduce the necessity for
large-scale destructive measurements within every round of
selections (Heffner et al., 2009). The main input costs are in
genotyping individuals, which has become a relatively cheap
and high-throughput method (Heffner et al., 2010)..
Concluding thoughts
The mechanisms and agricultural applications of NSC
partitioning in grass stems are diverse to say the least. This
presents many challenges for this trait because there are no
simple models that fit every system. Thus, there is still a long
road ahead for physiologists, breeders, and plant scientists.
The modification of crops must keep pace with human,
ecological, and economic demands. Darwin’s pioneering
work on evolution and breeding must now be approached
with the methods of an engineer—accelerating the plant
evolutionary processes to an unprecedented rate in order to
provide food, fuel, and fibre for future generations of people
on earth. Previously, constant high selection pressures have
produced plants that have drastically changed in sink–source
dynamics when compared with their wild relatives. That
same pressure is now on the already high-yielding crops to
produce the same increases as seen in the last few thousand
years, in only a few decades. Improving our understanding
and further optimizing whole-plant sink–source dynamics of
the grass species that cover a vast portion of the earth’s
surface will have profound impacts in the near future. It
cannot be understated that there has been no other time in
human history when the study of the fundamentals of plant
evolution and physiology has become so critical.
Acknowledgements
I would like to thank Tim Setter, Robert Turgeon, Diane
Wang, Andre Jagendorf, Cherith Wissmann, and three
anonymous reviewers for their critical reviews which greatly
improved this manuscript. Any mentions of specific cultivars or varieties in this article are for academic purposes
only and do not reflect an endorsement or opposition of
those varieties, individual developers, or their affiliated
companies. No conflict of interest declared. This work is
supported by the United States Department of AgricultureNational Institute of Food and Agriculture Fellowship
Grant #2011-67012-30774 to TLS.
References
Acreche MM, Slafer GA. 2011. Lodging yield penalties as affected
by breeding in Mediterranean wheats. Field Crops Research 122,
40–48.
Aitken K, Jackson P, McIntyre C. 2006. Quantitative trait loci
identified for sugar related traits in a sugarcane (Saccharum spp.)
cultivar 3 Saccharum officinarum population. Theoretical and Applied
Genetics 112, 1306–1317.
Allison JCS, Watson DJ. 1966. The production and distribution of
dry matter in maize after flowering. Annals of Botany 30, 365–381.
Álvaro F, Royo C, Garcı́a del Moral LF, Villegas D. 2008. Grain
filling and dry matter translocation responses to source–sink
modifications in a historical series of durum wheat. Crop Science 48,
1523–1531.
Antony E, Taybi T, Courbot M, Mugford ST, Smith JAC,
Borland AM. 2008. Cloning, localization and expression analysis of
vacuolar sugar transporters in the CAM plant Ananas comosus
(pineapple). Journal of Experimental Botany 59, 1895–1908.
Aoki N, Scofield GN, Wang X-D, Patrick JW, Offler CE,
Furbank RT. 2004. Expression and localisation analysis of the wheat
sucrose transporter TaSUT1 in vegetative tissues. Planta 219, 76–184.
Asli DE, Houshmandfar A. 2011. An anatomical study of vascular
system of spikelet supplying transocates to differentially growing grains
of wheat. Advances in Environmental Biology 5, 1597–1601.
Non-structural
carbohydrate
partitioning
in grass
stems 4663
Non-structural
carbohydrate
partitioning
in grass
stems
| 17| of
24
Asseng S. Herwaarden AFv. 2003. Analysis of the benefits to wheat
yield from assimilates stored prior to grain filling in a range of
environments. Plant and Soil 256, 217–229.
Borrás L, Slafer GA, Otegui ME. 2004. Seed dry weight response to
source–sink manipulations in wheat, maize and soybean:
a quantitative reappraisal. Field Crops Research 86, 131–146.
Bancal P, Triboı̈ E. 1993. Temperature effect on fructan oligomer
contents and fructan-related enzyme activities in stems of wheat
(Triticum aestivum L.) during grain filling. New Phytologist
123, 247–253.
Borrás L, Westgate ME. 2006. Predicting maize kernel sink capacity
early in development. Field Crops Research 95, 223–233.
Basnayake SWV, Morgan TC, Wu L, Birch RG. 2011. Field
performance of transgenic sugarcane expressing isomaltulose
synthase. Plant Biotechnology Journal 10, 217–225.
Braun DM, Slewinski TL. 2009. Genetic control of carbon
partitioning in grasses: roles of sucrose transporters and tie-dyed loci
in phloem loading. Plant Physiology 149, 71–81.
Beddington J. 2010. Food security: contributions from science to
a new and greener revolution. Philosophical Transactions of the Royal
Society B: Biological Sciences 365, 61–71.
Buckeridge MS, De Souza AP, Arundale RA, AndersonTeixeira KJ, DeLucia E. 2011. Ethanol from sugarcane in Brazil:
a ‘midway’ strategy for increasing ethanol production while maximizing
environmental benefits. GCB Bioenergy 4, 119–126.
Bell CJ, Incoll LD. 1990. The redistribution of assimilate in fieldgrown winter wheat. Journal of Experimental Botany 41, 949–960.
Bell LW, Wade LJ, Ewing MA. 2010. Perennial wheat: a review of
environmental and agronomic prospects for development in Australia.
Crop and Pasture Science 61, 679–690.
Berthier A, Desclos M, Amiard V, Morvan-Bertrand A, DemmigAdams B, Adams WW lll, Turgeon R, Prud’homme M-P,
Noiraud-Romy N. 2009. Activation of sucrose transport in defoliated
Lolium perenne L.: an example of apoplastic phloem loading plasticity.
Plant and Cell Physiology 50, 1329–1344.
Betrán FJ, Beck D, Bänziger M, Edmeades GO. 2003. Secondary
traits in parental inbreds and hybrids under stress and non-stress
environments in tropical maize. Field Crops Research 83, 51–65.
Bindinger F, Musgrave RB, Fischer RA. 1977. Contribution of
stored pre-anthesis assimilate to grain yield in wheat and barley.
Nature 270, 431–433.
Bingham IJ, Blake J, Foulkes MJ, Spink J. 2007. Is barley yield in
the UK sink limited? I. Post-anthesis radiation interception, radiationuse efficiency and source–sink balance. Field Crops Research
101, 198–211.
Birch R. 2007. In: Verpoorte R, Alfermann AW, Johnson TS, eds.
Metabolic engineering in sugarcane: assisting the transition to a biobased economy applications of plant metabolic engineering
Applications of plant metabolic engineering. Dordrecht: Springer,
249–281.
Blum A, Sinmena B, Mayer J, Golan G, Shpiler L. 1994. Stem
reserve mobilization supports wheat-grain filling under heat stress.
Functional Plant Biology 21, 771–781.
Boote KJ, Kropff MJ, Bindraban PS. 2001. Physiology and
modelling of traits in crop plants: implications for genetic improvement.
Agricultural Systems 70, 395–420.
Borlaug N. 2007. Sixty-two years of fighting hunger: personal
recollections. Euphytica 157, 287–297.
Borràs G, Romagosa I, van Eeuwijk F, Slafer GA. 2009. Genetic
variability in duration of pre-heading phases and relationships with leaf
appearance and tillering dynamics in a barley population. Field Crops
Research 113, 95–104.
Borràs-Gelonch G, Slafer GA, Casas AM, van Eeuwijk F,
Romagosa I. 2010. Genetic control of pre-heading phases and other
traits related to development in a double-haploid barley (Hordeum
vulgare L.) population. Field Crops Research 119, 36–47.
Borrell AK, Hammer GL. 2000. Nitrogen dynamics and the physiological
basis of stay-green in sorghum. Crop Science 40, 1295–1307.
Burner DM, Tew TL, Harvey JJ, Belesky DP. 2009. Dry matter
partitioning and quality of Miscanthus, Panicum, and Saccharum
genotypes in Arkansas, USA. Biomass and Bioenergy 33, 610–619.
Byrt CS, Grof CPL, Furbank RT. 2011. C4 plants as biofuel feedstocks:
optimising biomass production and feedstock quality from a lignocellulosic
perspective. Journal of Integrative Plant Biology 53, 120–135.
Cairns AJ. 1992. Fructan biosynthesis in excised leaves of Lolium
temulentum L. V. De novo synthesis of large fructans from sucrose.
New Phytologist 122, 253–259.
Cairns AJ. 2003. Fructan biosynthesis in transgenic plants. Journal of
Experimental Botany 54, 549–567.
Campbell CM. 1963. Influence of seed formation of corn on
accumulation of vegetative dry matter and stalk strength. Crop
Science 4, 31–34.
Carpaneto A, Geiger D, Bamberg E, Sauer N, Fromm J,
Hedrich R. 2005. Phloem-localized, proton-coupled sucrose carrier
ZmSUT1 mediates sucrose efflux under the control of the sucrose
gradient and the proton motive force. Journal of Biological Chemistry
280, 21437–21443.
Carson DC, Botha FB. 2002. Genes expressed in sugarcane
maturing internodal tissue. Plant Cell Reports 20, 1075–1081.
Casu R, Grof C, Rae A, McIntyre C, Dimmock C, Manners J.
2003. Identification of a novel sugar transporter homologue strongly
expressed in maturing stem vascular tissues of sugarcane by
expressed sequence tag and microarray analysis. Plant Molecular
Biology 52, 371–386.
Casu RE, Manners JM, Bonnett GD, Jackson PA, McIntyre CL,
Dunne R, Chapman SC, Rae AL, Grof CPL. 2005. Genomics
approaches for the identification of genes determining important traits
in sugarcane. Field Crops Research 92, 137–147.
Chalmers J, Lidgett A, Cummings N, Cao Y, Forster J,
Spangenberg G. 2005. Molecular genetics of fructan metabolism in
perennial ryegrass. Plant Biotechnology Journal 3, 459–474.
Chen L-Q, Qu X-Q, Hou B-H, Sosso D, Osorio S, Fernie AR,
Frommer WB. 2011. Sucrose efflux mediated by SWEET proteins as
a key step for phloem transport. Science 335, 207–211.
Chuck GS, Tobias C, Sun L, et al. 2011. Overexpression of the
maize Corngrass1 microRNA prevents flowering, improves digestibility,
and increases starch content of switchgrass. Proceedings of the
National Academy of Sciences, USA 108, 17550–17555.
| Slewinski
4664 18 of 24
| Slewinski
Clements DR, Ditommaso A. 2011. Climate change and weed
adaptation: can evolution of invasive plants lead to greater range
expansion than forecasted? Weed Research 51, 227–240.
Cliquet J-B, Deléens E, Mariotti A. 1990. C and N mobilization from
stalk and leaves during kernel filling by 13C and 15N tracing in Zea
mays L. Plant Physiology 94, 1547–1553.
Cook M, Evans L. 1983. The roles of sink size and location in the
partitioning of assimilates in wheat ears. Functional Plant Biology
10, 313–327.
Cox TS, Glover JD, Van Tassel DL, Cox CM, DeHaan LR. 2006.
Prospects for developing perennial grain crops. BioScience 56, 649–659.
Cullen BR, Chapman DF, Quigley PE. 2006. Comparative
defoliation tolerance of temperate perennial grasses. Grass and
Forage Science 61, 405–412.
Davis SC, Dohleman FG, Long SP. 2011. The global potential for
Agave as a biofuel feedstock. GCB Bioenergy 3, 68–78.
Daynard TB, Tanner JW, Hume DJ. 1969. Contribution of stalk
soluble carbohydrates to grain yield in corn (Zea mays L.). Crop
Science 9, 831–834.
DeHaan LR, Van Tassel DL, Cox TS. 2005. Perennial grain crops:
a synthesis of ecology and plant breeding. Renewable Agriculture and
Food Systems 20, 5–14.
Dillon SL, Shapter FM, Henry RJ, Cordeiro G, Izquierdo L,
Lee LS. 2007. Domestication to crop improvement: genetic resources
for sorghum and saccharum (Andropogoneae). Annals of Botany
100, 975–989.
Dinant S, Lemoine R. 2010. The phloem pathway: new issues and
old debates. Comptes Rendus Biologies 333, 307–319.
Dohleman FG, Long SP. 2009. More productive than maize in the
midwest: how does miscanthus do it? Plant Physiology
150, 2104–2115.
Dolciotti I, Mambelli S, Grandi S, Venturi G. 1998. Comparison of
two sorghum genotypes for sugar and fiber production. Industrial
Crops and Products 7, 265–272.
Donaghy DJ, Turner LR, Adamczewski KA. 2008. Effect of
defoliation management on water-soluble carbohydrate energy
reserves, dry matter yields, and herbage quality of tall fescue.
Agronomy Journal 100, 122–127.
Dreccer MF, van Herwaarden AF, Chapman SC. 2009. Grain
number and grain weight in wheat lines contrasting for stem water
soluble carbohydrate concentration. Field Crops Research 112, 43–54.
Fageria NK, Slaton NA, Baligar VC. 2003. Nutrient management for
improving lowland rice productivity and sustainability. In: Sparkes DL,
ed. Advances in agronomy, Vol. 80. New York: Academic Press,
63–152.
FAO. 2009. Statistics Division 2009. ResourceSTAT, Rome: Italy,
www.faostat.fao.org.
Fedoroff NV, Battisti DS, Beachy RN, et al. 2010. Radically
rethinking agriculture in the 21st century. Science 327, 883–884.
Fischer RA, Edmeades GO. 2010. Breeding and cereal yield
progress. Crop Science 50, S-85–S-98.
Flint-Garcia SA, Jampatong C, Darrah LL, McMullen MD. 2003.
Quantitative trait locus analysis of stalk strength in four maize
populations. Crop Science 43, 13–22.
Ford MA, Blackwell RD, Parker ML, Austin RB. 1979.
Associations between stem solidity, soluble carbohydrate
accumulation and other characters in wheat. Annals of Botany
44, 731–738.
Foulkes MJ, Slafer GA, Davies WJ, Berry PM, SylvesterBradley R, Martre P, Calderini DF, Griffiths S, Reynolds MP.
2011. Raising yield potential of wheat. III. Optimizing partitioning to
grain while maintaining lodging resistance. Journal of Experimental
Botany 62, 469–486.
Foulkes MJ, Sylvester-Bradley R, Weightman R, Snape JW.
2007. Identifying physiological traits associated with improved drought
resistance in winter wheat. Field Crops Research 103, 11–24.
Fu J, Huang Z, Wang Z, Yang J, Zhang J. 2011. Pre-anthesis nonstructural carbohydrate reserve in the stem enhances the sink strength
of inferior spikelets during grain filling of rice. Field Crops Research
123, 170–182.
Fu Q, Cheng L, Guo Y, Turgeon R. 2011. Phloem loading strategies
and water relations in trees and herbaceous plants. Plant Physiology
157, 1518–1527.
Fulkerson WJ, Donaghy DJ. 2001. Plant-soluble carbohydrate
reserves and senescence—key criteria for developing an effective
grazing management system for ryegrass-based pasture: a review.
Australian Journal of Experimental Agriculture 41, 261–275.
Gambin BL, Borras L, Otegui ME. 2007. Is maize kernel size limited
by its capacity to expand? Maydica 52, 431–441.
Garrett KA, Dendy SP, Frank EE, Rouse MN, Travers SE. 2006.
Climate change effects on plant disease: genomes to ecosystems.
Annual Review of Phytopathology 44, 489–509.
Duncan RR, Bockholt AJ, Miller FR. 1981. Descriptive comparison
of senescent and nonsenescent sorghum genotypes. Agronomy
Journal 73, 849–853.
Garrity D, Akinnifesi F, Ajayi O, Weldesemayat S, Mowo J,
Kalinganire A, Larwanou M, Bayala J. 2010. Evergreen agriculture:
a robust approach to sustainable food security in Africa. Food Security
2, 197–214.
Ehdaie B, Alloush GA, Madore MA, Waines JG. 2006. Genotypic
variation for stem reserves and mobilization in wheat. Crop Science
46, 2093–2103.
Garside AL, Bell MJ. 2009. Row spacing and planting density effects
on the growth and yield of sugarcane. 3. Responses with different
cultivars. Crop and Pasture Science 60, 555–565.
Eom J-S, Cho J-I, Reinders A, et al. 2011. Impaired function of the
tonoplast-localized sucrose transporter in rice (Oryza sativa), OsSUT2,
limits the transport of vacuolar reserve sucrose and affects plant
growth. Plant Physiology 157, 109–119.
Gebbing T, Schnyder H. 1999. Pre-anthesis reserve utilization for
protein and carbohydrate synthesis in grains of wheat. Plant
Physiology 121, 871–878.
Evenson RE, Gollin D. 2003. Assessing the impact of the green
revolution, 1960 to 2000. Science 300, 758–762.
Glassop D, Roessner U, Bacic A, Bonnett GD. 2007. Changes in
the sugarcane metabolome with stem development. Are they related
to sucrose accumulation? Plant and Cell Physiology 48, 573–584.
Non-structural
carbohydrate
partitioning
in grass
stems 4665
Non-structural
carbohydrate
partitioning
in grass
stems
| 19| of
24
Glassop D, Ryan LP, Bonnett GD, Rae AL. 2010. The complement
of soluble sugars in the Saccharum complex. Tropical Plant Biology
3, 110–122.
Hiyane R, Hiyane S, Tang AC, Boyer JS. 2010. Sucrose feeding
reverses shade-induced kernel losses in maize. Annals of Botany 106,
395–403.
Glover JD, Reganold JP, Bell LW, et al. 2010. Increased food and
ecosystem security via perennial grains. Science 328, 1638–1639.
Hoarau JYH, Grivet LG, Offmann BO, Raboin LMR, Diorflar JPD,
Payet JP, Hellmann MH, D’Hont ADH, Glaszmann JCG. 2002.
Genetic dissection of a modern sugarcane cultivar (Saccharum spp.). II.
Detection of QTLs for yield components. Theoretical and Applied
Genetics 105, 1027–1037.
Glowacka K. 2011. A review of the genetic study of the energy crop
Miscanthus. Biomass and Bioenergy 35, 2445–2454.
Godfray HCJ, Crute IR, Haddad L, Lawrence D, Muir JF,
Nisbett N, Pretty J, Robinson S, Toulmin C, Whiteley R. 2010.
The future of the global food system. Philosophical Transactions
of the Royal Society Series B: Biological Sciences 365,
2769–2777.
Hodnett GL, Hale AL, Packer DJ, Stelly DM, da Silva J,
Rooney WL. 2010. Elimination of a reproductive barrier facilitates
intergeneric hybridization of Sorghum bicolor and. Saccharum. Crop
Science 50, 1188–1195.
Goggin DE, Setter TL. 2004. Fructosyltransferase activity and fructan
accumulation during development in wheat exposed to terminal
drought. Functional Plant Biology 31, 11–21.
Hoffmann-Thoma G, Hinkel K, Nicolay P, Willenbrink J. 1996.
Sucrose accumulation in sweet sorghum stem internodes in relation to
growth. Physiologia Plantarum 97, 277–284.
González FG, Miralles DJ, Slafer GA. 2011. Wheat floret survival as
related to pre-anthesis spike growth. Journal of Experimental Botany
62, 4889–4901.
Hogan ME, Hendrix JE. 1986. Labeling of fructans in winter wheat
stems. Plant Physiology 80, 1048–1050.
Granot D. 2008. Putting plant hexokinases in their proper place.
Phytochemistry 69, 2649–2654.
Hotta C, Lembke C, Domingues D, et al. 2010. The
biotechnology roadmap for sugarcane improvement. Tropical Plant
Biology 3, 75–87.
Gregory PJ, George TS. 2011. Feeding nine billion: the challenge to
sustainable crop production. Journal of Experimental Botany
62, 5233–5239.
Hume DJ, Campbell CM. 1972. Accumulation and translocation of
soluble solids in corn stalks. Canadian Journal of Plant Science
52, 363–368.
Griffith SM. 1992. Changes in post-anthesis assimilates in stem and
spike components of Italian ryegrass (Lolium multiflorum Lam.). I.
Water soluble carbohydrates. Annals of Botany 69, 243–248.
Inman-Bamber NG, Bonnett GD, Spillman MF, Hewitt ML, Xu J.
2009. Source–sink differences in genotypes and water regimes
influencing sucrose accumulation in sugarcane stalks. Crop and
Pasture Science 60, 316–327.
Grof CPL, Campbell JA. 2001. Sugarcane sucrose metabolism,
scope for molecular manipulation. Functional Plant Biology 28, 1–12.
Guimaraes C, Sills G, Sobral B. 1997. Comparative mapping of
Andropogoneae: Saccharum L. (sugarcane) and its relation to
sorghum and maize. Proceedings of the National Academy of
Sciences, USA 94, 14261–14266.
Halford NG, Curtis TY, Muttucumaru N, Postles J, Mottram DS.
2011. Sugars in crop plants. Annals of Applied Biology 158, 1–25.
Hamerli D, Birch RG. 2011. Transgenic expression of trehalulose
synthase results in high concentrations of the sucrose isomer
trehalulose in mature stems of field-grown sugarcane. Plant
Biotechnology Journal 9, 32–37.
Hanif M, Langer RHM. 1972. The vascular system of the spikelet in
wheat (Triticum aestivum). Annals of Botany 36, 721–727.
Harrell DL, Bond JA, Blanche S. 2009. Evaluation of main-crop
stubble height on ratoon rice growth and development. Field Crops
Research 114, 396–403.
Heffner EL, Lorenz AJ, Jannink J-L, Sorrells ME. 2010. Plant
breeding with genomic selection: gain per unit time and cost. Crop
Science 50, 1681–1690.
Heffner EL, Sorrells ME, Jannink J- L. 2009. Genomic selection for
crop improvement. Crop Science 49, 1–12.
Hisano H, Kanazawa A, Kawakami A, Yoshida M, Shimamoto Y,
Yamada T. 2004. Transgenic perennial ryegrass plants expressing
wheat fructosyltransferase genes accumulate increased amounts of
fructan and acquire increased tolerance on a cellular level to freezing.
Plant Science 167, 861–868.
Irvine JE. 1975. Relations of photosynthetic rates and leaf and
canopy characters to sugarcane yield. Crop Science 15, 671–676.
Jackson PA. 2005. Breeding for improved sugar content in
sugarcane. Field Crops Research 92, 277–290.
Jacobsen KR, Fisher DG, Maretzki A, Moore PH. 1992.
Developmental changes in the anatomy of the sugarcane stem in
relation to phloem unloading and sucrose storage relation. Botanica
Acta 105, 70–80.
Jones DB. 1993. Rice ratoon response to main crop harvest cutting
height. Agronomy Journal 85, 1139–1142.
Jones RJ, Simmons SR. 1983. Effect of altered source–sink ratio on
growth of maize kernels. Crop Science 23, 129–134.
Jurgens SK, Johnson RR, Boyer JS. 1978. Dry matter production
and translocation in maize subjected to drought during grain fill.
Agronomy Journal 70, 678–682.
Koch K. 2004. Sucrose metabolism: regulatory mechanisms and
pivotal roles in sugar sensing and plant development. Current Opinion
in Plant Biology 7, 235–246.
Komor E. 2000. The physiology of sucrose storage in sugarcane.
In: Gupta AM, Kaur N, eds. Carbohydrate reserves in
plants—synthesis and regulation. Elsevier, 35–53.
Lee JM, Sathish P, Donaghy DJ, Roche JR. 2010. Plants modify
biological processes to ensure survival following carbon depletion:
a Lolium perenne model. PLoS ONE 5, e12306.
Lemaire G, Da Silva SC, Agnusdei M, Wade M, Hodgson J. 2009.
Interactions between leaf lifespan and defoliation frequency in
| Slewinski
4666 20 of 24
| Slewinski
temperate and tropical pastures: a review. Grass and Forage Science
64, 341–353.
Lingle SE, Viator RP, Johnson RM, Tew TL, Boykin DL. 2009.
Recurrent selection for sucrose content has altered growth and sugar
accumulation in sugarcane. Field Crops Research 113, 306–311.
Livingston DP, Chatterton NJ, Harrison PA. 1993. Structure and
quantity of fructan oligomers in oat (Avena spp.). New Phytologist
123, 725–734.
Livingston DP, Knievel DP, Gildow FE. 1994. Fructan synthesis in
oat. New Phytologist 127, 27–36.
Lobell DB, Burke MB, Tebaldi C, Mastrandrea MD, Falcon WP,
Naylor RL. 2008. Prioritizing climate change adaptation needs for
food security in 2030. Science 319, 607–610.
Lobell DB, Schlenker W, Costa-Roberts J. 2011. Climate trends
and global crop production since 1980. Science 333, 616–620.
Marten GC, Westerberg PM. 1972. Maize fodder—influence of
barrenness on yield and quality. Crop Science 12, 367–369.
Massacci A, Battistelli A, Loreto F. 1996. Effect of drought stress
on photosynthetic characteristics, growth and sugar accumulation of
field-grown sweet sorghum. Functional Plant Biology 23, 331–340.
Matsuoka S, Garcia AAF. 2011. Sugarcane underground organs:
going deep for sustainable production. Tropical Plant Biology 4, 22–30.
McBee GG, Miller FR. 1982. Carbohydrates in sorghum culms as
influenced by cultivars, spacing, and maturity over a diurnal period.
Crop Science 22, 381–385.
McCormick AJ, Cramer MD, Watt DA. 2008a. Changes in
photosynthetic rates and gene expression of leaves during a source–
sink perturbation in sugarcane. Annals of Botany 101, 89–102.
McCormick AJ, Cramer MD, Watt DA. 2008b. Culm sucrose
accumulation promotes physiological decline of mature leaves in
ripening sugarcane. Field Crops Research 108, 250–258.
McCormick AJ, Cramer MD, Watt DA. 2008c. Regulation of
photosynthesis by sugars in sugarcane leaves. Journal of Plant
Physiology 165, 1817–1829.
McNaughton SJ. 1979. Grazing as an optimization process: grass–
ungulate relationships in the Serengeti. American Naturalist 113, 691–703.
Moore PH. 2005. Integration of sucrose accumulation processes
across hierarchical scales: towards developing an understanding
of the gene-to-crop continuum. Field Crops Research
92, 119–135.
Mortimore CG, Ward GM. 1964. Root and stalk rot of corn in
southwestern Ontario. Canadian Journal of Plant Science
44, 451–457.
Morvan-Bertrand A, Boucaud J, Le Saos Jl, Prud’homme M- P.
2001. Roles of the fructans from leaf sheaths and from the elongating
leaf bases in the regrowth following defoliation of Lolium perenne L.
Planta 213, 109–120.
Mudge S, Osabe K, Casu R, Bonnett G, Manners J, Birch R.
2009. Efficient silencing of reporter transgenes coupled to known
functional promoters in sugarcane, a highly polyploid crop species.
Planta 229, 549–558.
Murray SC, Rooney WL, Hamblin MT, Mitchell SE, Kresovich S.
2009. Sweet sorghum genetic diversity and association mapping for
brix and height. Plant Genome 2, 48–62.
Natoli A, Gorni C, Chegdani F, Marsan PA, Colombi C,
Lorenzoni C, Morocco A. 2002. Identification of QTLs associated
with sweet sorghum quaility. Maydica 47, 311–322.
Newton A, Flavell A, George T, et al. 2011. Crops that feed the
world 4. Barley: a resilient crop? Strengths and weaknesses in the
context of food security. Food Security 3, 141–178.
Oosterveer P, Mol APJ. 2010. Biofuels, trade and sustainability:
a review of perspectives for developing countries. Biofuels,
Bioproducts and Biorefining 4, 66–76.
Pammenter NW, Allison JCS. 2002. Effects of treatments potentially
influencing the supply of assimilate on its partitioning in sugarcane.
Journal of Experimental Botany 53, 123–129.
Pan J, Cui K, Wei D, Huang J, Xiang J, Nie L. 2011. Relationships
of non-structural carbohydrate accumulation and translocation with
yield formation in rice recombinant inbred lines under two nitrogen
levels. Physiologia Plantarum 141, 321–331.
Papini-Terzi F, Rocha F, Vêncio R, et al. 2009. Sugarcane genes
associated with sucrose content. BMC Genomics 10, 120.
Ming RM, Wang YW, Draye XD, Moore PM, Irvine JI,
Paterson AP. 2002. Molecular dissection of complex traits in
autopolyploids: mapping QTLs affecting sugar yield and related traits
in sugarcane. Theoretical and Applied Genetics 105, 332–345.
Park J-y, Kanda E, Fukushima A, Motobayashi K, Nagata K,
Kondo M, Ohshita Y, Morita S, Tokuyasu K. 2011. Contents of
various sources of glucose and fructose in rice straw, a potential
feedstock for ethanol production in Japan. Biomass and Bioenergy
35, 3733–3735.
Mitchell R, Vogel KP, Sarath G. 2008. Managing and enhancing
switchgrass as a bioenergy feedstock. Biofuels, Bioproducts and
Biorefining 2, 530–539.
Patrick JW. 1997. Phloem unloading: sieve element unloading and
post-sieve element transport. Annual Review of Plant Physiology and
Plant Molecular Biology 48, 191–222.
Monfreda C, Ramankutty N, Foley JA. 2008. Farming the planet:
2. Geographic distribution of crop areas, yields, physiological types,
and net primary production in the year 2000. Global Biogeochemical
Cycles 22, GB1022.
Patrick JW, Zhang W, Tyerman SD, Offler CE, Walker NA. 2001.
Role of membrane transport in phloem translocation of assimilates and
water. Functional Plant Biology 28, 697–709.
Monneveux P, Sanchez C, Tiessen A. 2008. Future progress in
drought tolerance in maize needs new secondary traits and cross
combinations. Journal of Agricultural Science 146, 287–300.
Pelletier N. 2010. Of laws and limits: an ecological economic
perspective on redressing the failure of contemporary global
environmental governance. Global Environmental Change 20,
220–228.
Moore P. 1995. Temporal and spatial regulation of sucrose
accumulation in the sugarcane stem. Australian Journal of Plant
Physiology 22, 661.
Pfeiffer TW, Bitzer MJ, Toy JJ, Pedersen JF. 2010. Heterosis in
sweet sorghum and selection of a new sweet sorghum hybrid for use
in syrup production in appalachia. Crop Science 50, 1788–1794.
Non-structural
carbohydrate
partitioning
in grass
stems 4667
Non-structural
carbohydrate
partitioning
in grass
stems
| 21| of
24
Pollock CJ, Cairns AJ. 1991. Fructan metabolism in grasses and
cereals. Annual Review of Plant Physiology and Plant Molecular
Biology 42, 77–101.
Pollock C, Farrar J, Tomos D, Gallagher J, Lu C, Koroleva O.
2003. Balancing supply and demand: the spatial regulation of carbon
metabolism in grass and cereal leaves. Journal of Experimental Botany
54, 489–494.
Pollock CJ, Kingston-Smith AH. 1997. The vacoule and
carbohydrate metabolism. In: Leigh RA, Sanders D, eds. Advances in
Botanical Research, Vol. 25. London: Academic Press, 195–215.
Rae A, Grof C, Casu R, Bonnett G. 2005a. Sucrose accumulation in
the sugarcane stem: pathways and control points for transport and
compartmentation. Field Crops Research 92, 159–168.
Rae AL, Jackson MA, Nguyen CH, Bonnett GD. 2009. Functional
specialization of vacuoles in sugarcane leaf and stem. Tropical Plant
Biology 2, 13–22.
Ruuska SA, Rebetzke GJ, van Herwaarden AF, Richards RA,
Fettell NA, Tabe L, Jenkins CLD. 2006. Genotypic variation in
water-soluble carbohydrate accumulation in wheat. Functional Plant
Biology 33, 799–809.
Sadras VO. 2007. Evolutionary aspects of the trade-off between seed
size and number in crops. Field Crops Research 100, 125–138.
Sadras VO, Denison RF. 2009. Do plant parts compete for
resources? An evolutionary viewpoint. New Phytologist 183, 565–574.
Sadras VO, Egli DB. 2008. Seed size variation in grain crops:
allometric relationships between rate and duration of seed growth.
Crop Science 48, 408–416.
Sage RF, Zhu X- G. 2011. Exploiting the engine of C4
photosynthesis. Journal of Experimental Botany 62, 2989–3000.
Saint Pierre C, Trethowan R, Reynolds M. 2010. Stem solidness
and its relationship to water-soluble carbohydrates: association with
wheat yield under water deficit. Functional Plant Biology
37, 166–174.
Rae A, Perroux J, Grof C. 2005b. Sucrose partitioning between
vascular bundles and storage parenchyma in the sugarcane stem:
a potential role for the ShSUT1 sucrose transporter. Planta
220, 817–825.
Santos AB, Fageria NK, Prabhu AS. 2003. Rice ratooning
management practices for higher yields. Communications in Soil
Science and Plant Analysis 34, 881–918.
Rajcan I, Tollenaar M. 1999. Source:sink ratio and leaf senescence
in maize: I. Dry matter accumulation and partitioning during grain filling.
Field Crops Research 60, 245–253.
Sayre JD, Morris VH, Richey FD. 1931. The effects of preventing
fruiting and of reducing leaf area on the accumulation of sugars in the
corn stem. Journal of the American Society of Agronomy 23, 751–753.
Rebetzke GJ, van Herwaarden AF, Jenkins C, Weiss M,
Lewis D, Ruuska S, Tabe L, Fettell NA, Richards RA. 2008.
Quantitative trait loci for water-soluble carbohydrates and associations
with agronomic traits in wheat. Australian Journal of Agricultural
Research 59, 891–905.
Rennie EA, Turgeon R. 2009. A comprehensive picture of phloem
loading strategies. Proceedings of the National Academy of Sciences,
USA 106, 14162–14167.
Reynolds M, Bonnett D, Chapman SC, Furbank RT, Manès Y,
Mather DE, Parry MAJ. 2011. Raising yield potential of wheat. I.
Overview of a consortium approach and breeding strategies. Journal
of Experimental Botany 62, 439–452.
Ritter K, Jordan D, Chapman S, Godwin I, Mace E, Lynne
McIntyre C. 2008. Identification of QTL for sugar-related traits in
a sweet 3 grain sorghum (Sorghum bicolor L. Moench) recombinant
inbred population. Molecular Breeding 22, 367–384.
Rosenzweig C, Parry ML. 1994. Potential impact of climate change
on world food supply. Nature 367, 133–138.
Rossouw D, Kossmann J, Botha FC, Groenewald J. 2010.
Reduced neutral invertase activity in the culm tissues of transgenic
sugarcane plants results in a decrease in respiration and sucrose
cycling and an increase in the sucrose to hexose ratio. Functional
Plant Biology 37, 22–31.
Rutkoski J, Heffner E, Sorrells M. 2011. Genomic selection for
durable stem rust resistance in wheat. Euphytica 179, 161–173.
Ruuska S, Lewis D, Kennedy G, Furbank R, Jenkins C, Tabe L.
2008. Large scale transcriptome analysis of the effects of
nitrogen nutrition on accumulation of stem carbohydrate
reserves in reproductive stage wheat. Plant Molecular Biology
66, 15–32.
Schmidhuber J, Tubiello FN. 2007. Global food security under
climate change. Proceedings of the National Academy of Sciences,
USA 104, 19703–19708.
Schnyder H. 1993. The role of carbohydrate storage and
redistribution in the source–sink relations of wheat and barley during
grain filling—a review. New Phytologist 123, 233–245.
Schnyder H, Nelson C, Spollen W. 1988. Diurnal growth of tall
fescue leaf blades. II. Dry matter partitioning and carbohydrate
metabolism in the elongation zone and adjacent expanding tissue.
Plant Physiology 86, 1077–1083.
Schulz A, Beyhl D, Marten I, Wormit A, Neuhaus E, Poschet G,
Büttner M, Schneider S, Sauer N, Hedrich R. 2011. Proton-driven
sucrose symport and antiport are provided by the vacuolar
transporters SUC4 and TMT1/2. The Plant Journal 68, 129–136.
Scofield GN, Hirose T, Aoki N, Furbank RT. 2007. Involvement of
the sucrose transporter, OsSUT1, in the long-distance pathway for
assimilate transport in rice. Journal of Experimental Botany
58, 3155–3169.
Scofield GN, Ruuska SA, Aoki N, Lewis DC, Tabe LM,
Jenkins CLD. 2009. Starch storage in the stems of wheat plants:
localization and temporal changes. Annals of Botany 103, 859–868.
Setter TL, Flannigan BA. 1986. Sugar and starch redistribution in
maize in response to shade and ear temperature treatment. Crop
Science 26, 575–579.
Setter TL, Flannigan BA. 1989. Relationship between photosynthate
supply and endosperm development in maize. Annals of Botany
64, 481–487.
Setter TL, Flannigan BA. 2001. Water deficit inhibits cell division and
expression of transcripts involved in cell proliferation and
endoreduplication in maize endosperm. Journal of Experimental
Botany 52, 1401–1408.
| Slewinski
4668 22 of 24
| Slewinski
Setter TL, Flannigan BA, Melkonian J. 2001. Loss of kernel set due
to water deficit and shade in maize: carbohydrate supplies, abscisic
acid, and cytokinins. Crop Science 41, 1530–1540.
St. Clair S, Lynch J. 2010. The opening of Pandora’s Box: climate
change impacts on soil fertility and crop nutrition in developing
countries. Plant and Soil 335, 101–115.
Setter TL, Meller VH. 1984. Reserve carbohydrate in maize stem:
[14C]glucose and [14C]sucrose uptake characteristics. Plant
Physiology 75, 617–622.
Stanhill G, Cohen S. 2001. Global dimming: a review of the
evidence for a widespread and significant reduction in global
radiation with discussion of its probable causes and possible
agricultural consequences. Agricultural and Forest Meteorology 107,
255–278.
Shiferaw B, Prasanna B, Hellin J, Bänziger M. 2011. Crops that
feed the world 6. Past successes and future challenges to the role
played by maize in global food security. Food Security 3, 307–327.
Shiringani A, Frisch M, Friedt W. 2010. Genetic mapping of QTLs
for sugar-related traits in a RIL population of Sorghum bicolor L.
Moench. Theoretical and Applied Genetics 121, 323–336.
Singleton WR. 1948. Sucrose in the stalks of maize inbreds. Science
107, 174.
Slafer GA. 2003. Genetic basis of yield as viewed from a crop
physiologist’s perspective. Annals of Applied Biology 142, 117–128.
Slafer GA, Andrade FH. 1991. Changes in physiological attributes of
the dry matter economy of bread wheat (Triticum aestivum) through
genetic improvement of grain yield potential at different regions of the
world. Euphytica 58, 37–49.
Slafer GA, Araus JL. 2007. Physiological traits for improving wheat
yeild under a wide range of conditions. In: Spiertz JHJ, Struik PC,
Van Laar HH, eds. Scale and complexity in plant systems research:
gene–plant–crop relations.. Dordrecht, The Netherlands: Springer,
147–156.
Slafer GA, Calderini DF, Miralles DJ. 1996. Yield components and
compensation in wheat: opportunities for further increasing yield
potential. In: Reynolds MP, Rajaram S, McNab A, eds. Increasing yield
potential in wheat: breaking the barriers. D.F. Mexico: CIMMYT,
101–134.
Slafer GA, Savin R. 1994. Source–sink relationships and grain mass
at different positions within the spike in wheat. Field Crops Research
37, 39–49.
Slewinski TL. 2011. Diverse functional roles of monosaccharide
transporters and their homologs in vascular plants: a physiological
perspective. Molecular Plant 4, 641–662.
Slewinski TL, Braun DM. 2010. Current perspectives on the
regulation of whole-plant carbohydrate partitioning. Plant Science 178,
341–349.
Slewinski TL, Garg A, Johal GS, Braun DM. 2010. Maize SUT1
functions in phloem loading. Plant Signaling and Behavior 5, 687–690.
Slewinski TL, Meeley R, Braun DM. 2009. Sucrose transporter1
functions in phloem loading in maize leaves. Journal of Experimental
Botany 60, 881–892.
Smalley J, Blake M. 2003. Sweet beginings: stalk sugar and the
domesticaion of maize. Current Anthropology 44, 675–709.
Tarpley L, Lingle S, Vietor D, Andrews D, Miller F. 1994.
Enzymatic control of nonstructural carbohydrate concentrations
in stems and panicles of sorghum. Crop Science 34, 446–452.
Tarpley L, Vietor D. 2007. Compartmentation of sucrose during
radial transfer in mature sorghum culm. BMC Plant Biology 7, 33.
Tarpley L, Vietor D, Miller F. 1996. Metabolism of sucrose during
storage in intact sorghum stalk. International Journal of Plant Sciences
157, 159–163.
Thomas H, Howarth CJ. 2000. Five ways to stay green. Journal of
Experimental Botany 51, 329–337.
Thompson K, Stewart AJA. 1981. The measurement and
meaning of reproductive effort in plants. American Naturalist 117,
205–211.
Turgeon R. 2010. The role of phloem loading reconsidered. Plant
Physiology 152, 1817–1823.
Turner FT, Jund MF. 1993. Rice ratoon crop linked to main crop
stem carbohydrates. Crop Science 33, 150–153.
Turner LR, Donaghy DJ, Lane PA, Rawnsley RP. 2006.
Effect of defoliation management, based on leaf stage, on
perennial ryegrass (Lolium perenne L.), prairie grass (Bromus
willdenowii Kunth.) and cocksfoot (Dactylis glomerata L.) under dryland
conditions. Regrowth, tillering and water-soluble carbohydrate
concentration. Grass and Forage Science 61, 164–174.
Ueki S, Citovsky V. 2011. To gate, or not to gate: regulatory
mechanisms for intercellular protein transport and virus movement in
plants. Molecular Plant 4, 782–793.
Uys L, Botha FC, Hofmeyr J-HS, Rohwer JM. 2007. Kinetic model
of sucrose accumulation in maturing sugarcane culm tissue.
Phytochemistry 68, 2375–2392.
Van den Ende W, De Coninck B, Van Laere A. 2004. Plant fructan
exohydrolases: a role in signaling and defense? Trends in Plant
Science 9, 523.
van der Merwe M, Groenewald J-H, Stitt M, Kossmann J,
Botha F. 2010. Downregulation of pyrophosphate-fructose-6phosphate 1-phosphotransferase activity in sugarcane culms
enhances sucrose accumulation due to elevated hexose-phosphate
levels. Planta 231, 595–608.
Smith D. 1975. Trends of nonstructural carbohydrates in the stem
base of switchgrass. Journal of Range Management 28, 389–391.
van Heerden PDR, Donaldson RA, Watt DA, Singels A. 2010.
Biomass accumulation in sugarcane: unravelling the factors
underpinning reduced growth phenomena. Journal of Experimental
Botany 61, 2877–2887.
Somerville C, Youngs H, Taylor C, Davis SC, Long SP. 2010.
Feedstocks for lignocellulosic biofuels. Science 329, 790–792.
Van Reen R, Singleton WR. 1952. Sucrose content in the stalks of
maize inbreds. Agronomy Journal 44, 610–614.
Spoolen WG, Nelson CJ. 1988. Characterization of fructan from
mature leaf blades and elongation zones of developing leaf blades of
wheat, tall fescue, and timothy. Plant Physiology 88, 1349–1353.
Vermerris W. 2011. Survey of genomics approaches to improve
bioenergy traits in maize, sorghum and sugarcane. Journal of
Integrative Plant Biology 53, 105–119.
Non-structural
carbohydrate
partitioning
in grass
stems 4669
Non-structural
carbohydrate
partitioning
in grass
stems
| 23| of
24
Verpoorte R, van der Heijden R, ten Hoopen HJG, Memelink J.
1999. Metabolic engineering of plant secondary metabolite pathways for
the production of fine chemicals. Biotechnology Letters 21, 467–479.
Vietor D, Miller F, Cralle H. 1990. Nonstructural carbohydrates in
axillary branches and main stem of senescent and nonsenescent
sorghum types. Crop Science 30, 97–100.
Vijn I, Smeekens S. 1999. Fructan: more than a reserve
carbohydrate? Plant Physiology 120, 351–360.
Vu JCV, Allen LHJ. 2009. Stem juice production of the C4 sugarcane
(Saccharum officinarum) is enhanced by growth at double-ambient CO2
and high temperature. Journal of Plant Physiology 166, 1141–1151.
Waclawovsky AJ, Sato PM, Lembke CG, Moore PH, Souza GM.
2010. Sugarcane for bioenergy production: an assessment of yield
and regulation of sucrose content. Plant Biotechnology Journal 8,
263–276.
Wagoner P, Schaeffer JR. 1990. Perennial grain development: past
efforts and potential for the future. Critical Reviews in Plant Sciences 9,
381–408.
Walsh KB, Sky RC, Brown SM. 2005. The anatomy of the pathway
of sucrose unloading within the sugarcane stalk. Functional Plant
Biology 32, 367–374.
Wang J, Roe B, Macmil S, et al. 2010. Microcollinearity between
autopolyploid sugarcane and diploid sorghum genomes. BMC
Genomics 11, 261.
Wang Z, Liu X, Li R, Chang X, Jing R. 2011. Development of nearinfrared reflectance spectroscopy models for quantitative
determination of water-soluble carbohydrate in wheat stem and glum.
Analytical Letters 44, 2478–2490.
Wang Z, Mambelli S, Setter TL. 2002. Abscisic acid catabolism in
maize kernels in response to water deficit at early endosperm
development. Annals of Botany 90, 623–630.
Wardlaw IF. 1990. Tansley Review No. 27. The control of carbon
partitioning in plants. New Phytologist 116, 341–381.
Wardlaw I, Porter H. 1967. The redistribution of stem sugars in
wheat during grain development. Australian Journal of Biological
Sciences 20, 309–318.
Wardlaw I, Willenbrink J. 1994. Carbohydrate storage and
mobilisation by the culm of wheat between heading and grain maturity:
the relation to sucrose synthase and sucrose-phosphate synthase.
Functional Plant Biology 21, 255–271.
Wardlaw IF, Willenbrink J. 2000. Mobilization of fructan reserves
and changes in enzyme activities in wheat stems correlate with water
stress during kernel filling. New Phytologist 148, 413–422.
Watson MA, Casper BB. 1984. Morphogenetic constraints on
patterns of carbon distribution in plants. Annual Review of Ecology and
Systematics 15, 233–258.
Weise SE, van Wijk KJ, Sharkey TD. 2011. The role of transitory
starch in C3, CAM, and C4 metabolism and opportunities for
engineering leaf starch accumulation. Journal of Experimental Botany
62, 3109–3118.
Welbaum G, Meinzer F, Grayson R, Thornham K. 1992. Evidence
for the consequences of a barrier to solute diffusion between the
apoplast and vascular bundles in sugarcane stalk tissue. Australian
Journal of Plant Physiology 19, 611–623.
White WG, Moose SP, Weil CF, McCann MC, Carpita NC,
Below FE. 2011. Tropical maize: exploiting maize genetic diversity to
develop a novel annual crop for lignocellulosic biomass and sugar
production. In: Buckeridge MS, Goldman GH, eds. Routes to cellulosic
ethanol. New York: Springer, 167–179.
Widstrom NW, Bagby MO, Palmer DM, Black LT, Carr ME. 1984.
Relative stalk sugar yields among maize populations, cultivars, and
hybrids. Crop Science 24, 913–915.
Widstrom NW, Carr ME, Bagby MO, Black LT. 1987. Harvest
methods for estimated ethanol yields from relative fermentable
carbohydrate accumulation in maize hybrids. Agronomy Journal 79,
758–760.
Willaman JJ, Burr GO, Davidson FR. 1924. Cornstalk syrup
investigations. Industrial and Engineering Chemistry 16, 734–739.
Willenbrink J, Bonnett GD, Willenbrink S, Wardlaw IF. 1998.
Changes of enzyme activities associated with the mobilization of
carbohydrate reserves (fructans) from the stem of wheat during kernel
filling. New Phytologist 139, 471–478.
Wingenter K, Schulz A, Wormit A, Wic S, Trentmann O,
Hoermiller II, Heyer AG, Marten I, Hedrich R, Neuhaus HE.
2010. Increased activity of the vacuolar monosaccharide transporter
TMT1 alters cellular sugar partitioning, sugar signaling, and seed yield
in Arabidopsis. Plant Physiology 154, 665–677.
Wu L, Birch RG. 2007. Doubled sugar content in sugarcane plants
modified to produce a sucrose isomer. Plant Biotechnology Journal 5,
109–117.
Xue G-P, Kooiker M, Drenth J, Mclntyre CL. 2011. TaMYB13 is
a transcriptional activator of fructosyltransferase genes involved in
beta-2,6-linked fructan synthesis in wheat. The Plant Journal 68,
857–870.
Xue G-P, McIntyre CL, Jenkins CLD, Glassop D, van
Herwaarden AF, Shorter R. 2008. Molecular dissection of variation
in carbohydrate metabolism related to water-soluble carbohydrate
accumulation in stems of wheat. Plant Physiology 146, 441–454.
Xue G, McIntyre CL, Rattey AR, van Herwaarden AF, Shorter R.
2009. Use of dry matter content as a rapid and low-cost estimate for
ranking genotypic differences in water-soluble carbohydrate
concentrations in the stem and leaf sheath of Triticum aestivum. Crop
and Pasture Science 60, 51–59.
Yang J, Peng S, Zhang Z, Wang Z, Visperas RM, Zhu Q. 2002.
Grain and dry matter yields and partitioning of assimilates in Japonica/
Indica hybrid rice. Crop Science 42, 766–772.
Yang J, Zhang J. 2010a. Crop management techniques to enhance
harvest index in rice. Journal of Experimental Botany 61, 3177–3189.
Yang J, Zhang J. 2010b. Grain-filling problem in ‘super’ rice. Journal
of Experimental Botany 61, 1–5.
Yang J, Zhang J, Wang Z, Xu G, Zhu Q. 2004. Activities of key
enzymes in sucrose-to-starch conversion in wheat grains subjected to
water deficit during grain filling. Plant Physiology 135, 1621–1629.
Ying J, Lee EA, Tollenaar M. 2000. Response of maize leaf
photosynthesis to low temperature during the grain-filling period. Field
Crops Research 68, 87–96.
Yoshida S. ed. 1981. International Rice Research Institute.
Fundamentals of rice crop science
| Slewinski
4670 24 of 24
| Slewinski
Yu L-X, Setter TL. 2003. Comparative transcriptional profiling of
placenta and endosperm in developing maize kernels in response to
water deficit. Plant Physiology 131, 568–582.
Zeeman SC, Kossmann J, Smith AM. 2010. Starch: its metabolism,
evolution, and biotechnological modification in plants. Annual Review
of Plant Biology 61, 209–234.