Review
Tansley review
Opportunities for improving phosphorus-use
efficiency in crop plants
Author for correspondence:
Erik J. Veneklaas
Tel: +61 8 64883584
Email: [email protected]
Received: 22 December 2011
Accepted: 21 April 2012
Erik J. Veneklaas1,2, Hans Lambers1,2, Jason Bragg3, Patrick M. Finnegan1,2,
Catherine E. Lovelock4, William C. Plaxton5, Charles A. Price1, Wolf-Rüdiger
Scheible6, Michael W. Shane1, Philip J. White7 and John A. Raven1,8
1
School of Plant Biology, The University of Western Australia, Crawley, WA 6009, Australia; 2Institute of Agriculture, The
University of Western Australia, Crawley, WA 6009Australia; 3CSIRO Plant Industry, GPO Box 1600, Canberra, ACT 2601,
Australia; 4School of Biological Sciences, The University of Queensland, St Lucia, QLD 4072, Australia; 5Department of Biology
and Department of Biomedical and Molecular Sciences, Queen’s University, Kingston, Ontario, Canada K7L 3N6; 6Max-Planck
Institute of Molecular Plant Physiology, 14476 Potsdam, Germany; 7The James Hutton Institute, Invergowrie, Dundee DD2 5DA,
UK; 8Division of Plant Sciences, University of Dundee at the James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK
Contents
Summary
306
VIII.
Internal redistribution of P in a growing vegetative plant
313
I.
The need to use phosphorus efficiently
307
IX.
Allocation of P to reproductive structures
314
II.
P-use efficiency and P dynamics in a growing crop
307
X.
Constraints to P remobilisation
315
III.
P pools in plants
307
XI.
Do physiological or phylogenetic tradeoffs constrain traits that could improve PUE?
316
IV.
Phosphorus pools and growth rates
310
XII.
Identifying genetic loci associated with PUE
316
V.
Are crops different from other plants in their P concentration? 310
XIII.
Conclusions
317
VI.
Phosphorus use and photosynthesis
311
Acknowledgements
317
VII.
Crop development and canopy P distribution
312
References
317
Summary
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doi: 10.1111/j.1469-8137.2012.04190.x
Key words: crops, harvest index, phosphorus
(P) fractions, phosphorus-use efficiency,
photosynthesis, plant developmental phases,
remobilization.
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Limitation of grain crop productivity by phosphorus (P) is widespread and will probably increase
in the future. Enhanced P efficiency can be achieved by improved uptake of phosphate from
soil (P-acquisition efficiency) and by improved productivity per unit P taken up (P-use efficiency). This review focuses on improved P-use efficiency, which can be achieved by plants that
have overall lower P concentrations, and by optimal distribution and redistribution of P in the
plant allowing maximum growth and biomass allocation to harvestable plant parts. Significant
decreases in plant P pools may be possible, for example, through reductions of superfluous
ribosomal RNA and replacement of phospholipids by sulfolipids and galactolipids. Improvements in P distribution within the plant may be possible by increased remobilization from tissues
that no longer need it (e.g. senescing leaves) and reduced partitioning of P to developing
grains. Such changes would prolong and enhance the productive use of P in photosynthesis
and have nutritional and environmental benefits. Research considering physiological, metabolic, molecular biological, genetic and phylogenetic aspects of P-use efficiency is urgently
needed to allow significant progress to be made in our understanding of this complex trait.
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I. The need to use phosphorus efficiently
There is an increasing awareness that there are limits to global
rock phosphate reserves, and that increasing the efficiency with
which these reserves are used to produce crops is vital to maintain
current agricultural productivity, or to even increase it (Cordell
et al., 2009). Annual grain crops (cereals, oil seeds and pulses),
which are the focus of this review, provide 58% of the dietary
energy for the world’s growing population (FAO, 2010). Improving the efficiency of phosphorus (P) fertilizer use for crop growth
requires enhanced P acquisition by plants from the soil (P-acquisition efficiency) and enhanced use of P in processes that lead to
faster growth and greater allocation of biomass to the harvestable
parts (internal P-use efficiency (PUE), further defined below in
Section II). As only 15–30% of applied fertilizer P is taken up by
crops in the year of its application (Syers et al., 2008), potentially
large gains in efficiency can be made by improving P acquisition.
This aspect of P efficiency has received significant attention and
has been reviewed recently (White & Hammond, 2008;
Ramaekers et al., 2010; Wang et al., 2010; Richardson et al.,
2011), identifying promising opportunities for improved crop
traits and agronomic measures. By contrast, much less attention
has been paid to physiological PUE, and comparative studies of
PUE have often suffered from confounding effects of variation in
P-acquisition efficiency (Rose et al., 2011). Aiming at increasing
P uptake alone will benefit yields, but will also increase total
amounts of P exported from the field. Increased P exports can
cause considerable off-site environmental problems (Tiessen,
2008; Childers et al., 2011), and will need to be replaced with
additional fertilizer to avoid soil P depletion in the long term.
The most sustainable and productive agricultural systems will be
those where P exports are balanced by P inputs, and which have
high yields per unit P taken up, that is, they have high PUE. In
this review we identify plant traits, from the whole plant to the
biochemical level, that contribute to efficient use of internal P
after it has been acquired. We also assess how efficient crop plants
are in a wider context, and evaluate options for improvement.
II. P-use efficiency and P dynamics in a growing crop
PUE is the amount of total biomass, or yield, that is produced per
unit of P taken up (Hammond et al., 2009), distinguished when
relevant by subscripts, PUEt and PUEy, respectively. In the case of
biomass, measurements are often restricted to aboveground plant
parts. In grain crops, PUEy is the grain yield per unit of maximum
aboveground plant P. In vegetative plants, the productive use of a
unit of P taken up is determined by (a) the efficiency with which it is
used in metabolism and growth, and (b) the duration of its presence
in living parts of the plant where it contributes to these processes.
Following Berendse & Aerts (1987), who formalized this concept,
PUEt ¼ ðbiomass production per unit P per unit timeÞ
ðP residence timeÞ
Eqn 1
where P residence time represents the time that a unit of P
remains in living parts of the plant. Even from this simplified
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equation, which is most useful for steady-state vegetative growth,
it is clear that PUE encompasses a wide range of physiological,
structural and developmental traits as they determine tissue-level
use of P and allocation and reallocation of P among plant parts
with different functions and efficiencies. It is therefore useful to
first examine how P requirements change during the different
developmental stages of plants. Key aspects of PUE will then be
discussed in detail in the following sections.
Once seed P reserves are depleted, continued growth depends
upon P uptake by roots from the soil. This point in development
typically coincides with exponential growth in crop plants when
availability of soil P is likely to be highest, because fertilizers are
freshly applied and there is limited resource competition between
roots. Inevitably, crop relative growth rate (RGR) declines as a
result of self-shading, increasing respiratory costs, and senescence
of older plant tissues and organs, even if soil water and nutrients
are not depleted. At this stage, P uptake by roots continues, but
remobilization of P from senescing tissues can become a very significant internal source of P. At the time of reproductive growth,
remobilization of P from senescing vegetative tissues is typically
the main source of P for sink tissues, as P uptake by roots
decreases, as a result of declining root growth and depletion of
available soil P. In crops, a very large fraction of the P present in
vegetative parts is remobilized to the grain, and soil P availability
at this stage has a relatively small effect on grain yield (Römer &
Schilling, 1986; Rose et al., 2008).
The whole-plant changes in P economy during crop development highlight the fact that, besides an efficient use of P in processes that lead to accumulation of biomass, optimal allocation
and efficient reallocation of P will also contribute to high PUE.
In this review we explore opportunities for improvement of PUE
by analysing the size and identity of P pools in plant tissues and
their functional importance, as well as their dynamics, including
re-use elsewhere in the plant.
III. P pools in plants
Phosphorus in plants exists either as the free inorganic orthophosphate form (Pi) or as organic phosphate esters. The Pi concentration of tissues generally reflects the Pi supply (White &
Hammond, 2008). This is true in crop plants, such as Brassica
napus and Cucurbita maxima (Pant et al., 2008), pasture plants,
such as Medicago truncatula (Branscheid et al., 2010), and undomesticated species, such as Hakea prostrata (Shane et al., 2004).
Tissue Pi is separated into two physiologically separate pools. The
metabolically active Pi pool, of the order of 0.1–0.8 mg P g)1 dry
weight (DW) (Bieleski, 1968; Rébeillé et al., 1983; Rouached
et al., 2011), is located in the cytoplasm and is kept within fairly
narrow limits (Bieleski, 1968; Mimura et al., 1996; Mimura,
1999). Cellular Pi in excess of current cytoplasmic need is stored
in the vacuole and is used to buffer the Pi demands of the cytoplasm, and is accordingly the most variable P fraction. For example, barley (Hordeum vulgare) grown in the absence of added Pi
had no detectable vacuolar P, as measured using 31P-NMR (Foyer
& Spencer, 1986). As Pi was withheld from barley, pre-grown in
nutrient solution containing 1.0 mM Pi, the vacuolar Pi
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concentration decreased sharply, while the cytosolic Pi concentration was less affected. Using protoplasts and vacuoles isolated
from intact barley leaves, it was shown that the vacuolar Pi concentration declined from 145 to 5 mM, when P supply declined
from 40 to 0 mM, whereas that of the cytoplasm (cytosol plus
mitochondria and plastids) declined from 35 to 26 mM (Mimura
et al., 1990). Similarly, for soybean (Glycine max) having just
reached full-flowering development, the vacuolar Pi concentration
decreased from 8.0 to < 0.05 mM as P supply declined, whereas
the cytosolic Pi concentration declined considerably less markedly, from 8.3 to 0.23 mM; the hexose monophosphate concentration declined less than that of Pi, from 7.7 to 0.54 mM (Lauer
et al., 1989). Pratt et al. (2009) reported that Pi concentrations in
the cytosol of sycamore (Acer pseudoplatanus) and Arabidopsis
suspension cells were much lower than those in the cytoplasm. In
summary, there is significant compartmentalization of Pi within
cells, and Pi concentrations are most variable in the vacuole, showing its buffering function. Differences in P uptake by plants result
in large variability of Pi concentration, making it a sensitive
indicator of plant P status (Bollons & Barraclough, 1999).
The main pools for esterified P are nucleic acids, phospholipids, phosphorylated water-soluble low relative molecular mass
(Mr) metabolites (commonly referred to as P-esters) and phosphorylated proteins. Phosphorylation of proteins serves a regulatory function, so phosphorylated proteins will not be considered
further. In the following sections, opportunities for increased P
efficiencies in the most significant P pools will be explored.
Fig. 1 summarizes available data on inorganic and organic P
fractions in photosynthetic tissue of a range of species. Observations of total P concentrations ([P]) > 5 mg g)1 DW are generally from plants growing at very high P supply. Optimal
concentrations for most crops are < 4 mg P g)1 DW (McLachlan
et al., 1987; Föhse et al., 1988; Rodrı́guez et al., 2000). For
wheat (Triticum aestivum), Bollons & Barraclough (1999)
reported critical concentrations for total P and Pi of approx. 3
and 0.6 mg g)1 DW, respectively. In order of size, and ignoring
stored (vacuolar) Pi, P pools are usually RNA > P-lipid > P-ester
> DNA > metabolically active Pi. Averaged for all cases where
total [P] < 4 mg g)1 DW (n = 21 species), and taking P-ester =
1, there are 1.3 units of lipid P, 2.0 units of nucleic acid P
(mainly RNA) and 1.4 units of inorganic P.
1. Nucleic acids – role and minimum requirements
The nucleic acid pool is typically the largest organic P pool in a
plant (Fig. 1), generally containing 40–60% of the P found in the
combined organic P pool (i.e. total P minus Pi). This equates to c.
0.3–2 mg P g)1 DW, depending on the species, tissue and P supply (Smillie & Krotkov, 1960; Bieleski, 1968; Tachibana, 1987).
The nucleic acid pool generally contains at least 85% RNA, with
the remainder being DNA (Bieleski, 1968; Tachibana, 1987).
Most RNA is ribosomal RNA (rRNA): Cucurbita ficifolia seedling
roots were found to contain c. 94% rRNA, 4% transfer RNA and
2% messenger RNA (Kanda et al., 1994).
There is generally a positive correlation between rRNA content,
and therefore ribosome number and protein synthesis capacity,
and growth rate over a range of taxa (Elser et al., 2000, 2010). As
leaves develop, rRNA levels increase to accommodate the rapid
synthesis of proteins, for example, Rubisco (Suzuki et al., 2010),
that are needed for photosynthesis. At full expansion or shortly
thereafter, net leaf protein synthesis ceases and RNA levels decrease
by up to 75% (Hensel et al., 1993; Suzuki et al., 2010). It is not
clear how much of the leaf RNA remains at the end of senescence.
The RNA pool generally adjusts in accordance with the growing
conditions, for example, RNA concentrations increased in trees in
which N concentration ([N]), [P] and growth rate were enhanced
through fertilization (Reef et al., 2010).
Opportunities for increasing the use efficiency of RNA and the
P it contains include optimizing the protein synthesis system
during plant development. The aim would be to deploy many
ribosomes, fully engaged in protein synthesis, when growth needs
to be rapid, but only enough ribosomes for maintenance processes when growth is complete, and no ribosomes upon senescent death. Presently, a fraction of the 40 S and 60 S ribosomal
subunits that are present at any given time is not actively
synthesizing protein (Mustroph et al., 2009). The role, and thus
15
Pi
P fractions concentration (mg g–1 DW)
Nucleic acids
Lipid P
Ester P
1
10
5
0
<1
1−2
2−4
4−8
>8
0
0
5
10
Sum of P fractions (mg g–1 DW)
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15
Fig. 1 Phosphorus (P) pools in photosynthetic tissues of
a wide range of plants grown at different P supply. Data
are from Bieleski (1968), Chapin & Bieleski (1982), Chapin
et al. (1982), Chapin et al. (1986), Tachibana (1987),
Chapin & Shaver (1988) and Marschner (2012). The inset
summarizes relative proportions of different P pools as
the total P concentration increases; the colours of the bars
correspond with the colours in the main figure.
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the importance, of these subunits need to be evaluated so that the
pool size could be targeted for optimization. Moreover, Rubisco
large and small subunit mRNA levels can decline by > 90% in
fully expanded leaves, but cytosolic rRNA levels drop < 75%
during this period (Hensel et al., 1993; Suzuki et al., 2010). This
suggests an increased disjunction between the actual amount of
protein synthesis that takes place and the protein synthetic capacity that is available. However, ribosomes and tRNA are still
needed in mature leaves for protein turnover, including replacement of damaged protein, and for acclimation and programmed
cell death during senescence.
The costs of P, as RNA, of protein turnover and repair are
substantial (Raven, 2011, 2012). Quigg & Beardall (2003) compiled data from vascular land plants showing protein turnover at
0.04–0.42 d)1. For a relative growth rate of a crop plant of 0.2 g
g)1 d)1 this would mean an increase in RNA content relative to
what would be needed with no protein turnover of 20–210% in
an optimally allocating plant. With RNA representing 47% of the
organic P (Fig. 1, total [P] < 4 mg g)1), this would mean that an
increase of 9–99% in the organic P content of the plants is needed
to support protein turnover. Assuming that the protein turnover
estimates are accurate (the turnover rates are not easy to measure),
protein turnover would seem to be a target for saving on P. For
the specific cases of photodamage to the D1 protein of photosystem II and O2 damage to nitrogenase, it is, respectively, known
and probable that these proteins turn over significantly more
rapidly than most other proteins (Raven, 2011, 2012). D1 protein
is ubiquitous among oxygenic organisms, and the relatively small
additional P cost for ribosomes used in repairing photodamage in
an optimally allocating organism is already included in PUE estimates (Raven, 2011, 2012). The greater P costs of growth often
found for symbiotic and free-living diazotrophically growing
photosynthetic organisms than when they are growing on
combined nitrogen (Vitousek et al., 2002) might be explained, at
least in part, by the need for more ribosomes for synthesizing
nitrogenase to replace O2-damaged nitrogenase (Raven, 2011,
2012). This possibility needs further investigation.
The amount of P in the DNA pool is considerably smaller than
that in the RNA pool, and reductions of DNA content would
seem difficult and undesirable. However, there may be useful
long-term optimization strategies. A pivotal question here is
whether genome size and gene copy number can be optimized.
The answer will require a better understanding of the function of
the so-called ‘noncoding’ regions within genomes and of the ways
that genes are controlled, as well as the development of new technologies to change genome structure rationally. The common
occurrence of polyploidy in agricultural and invasive species
(Soltis & Soltis, 2000), suggesting competitive benefits in productive and disturbed environments, also requires further
research. A high copy number of rRNA genes (a few hundred to
several thousand rRNA genes per genome; Rogers & Bendich,
1987) is thought to help the plant meet the demands to produce
large amounts of rRNA to support protein synthesis and growth
(Elser et al., 2010). However, the actual number of rRNA genes
shows considerable variation between species, between individuals of the same species and even within individuals of some
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species (Rogers & Bendich, 1987). The question of genome size
and gene copy number applies to both nuclear and organellar
genomes. As an example, there can be > 10 000 copies of chloroplast DNA per cell, depending on species, tissue, developmental
stage and environmental conditions (Bendich, 1987). If such
high copy numbers reflect the demands for high levels of certain
transcripts, such as plastid rRNA or the transcripts for the large
subunit of Rubisco (Bendich, 1987), this is in stark contrast with
the low gene copy number for the small subunit of Rubisco in
the nuclear genome. In future, it may be possible to engineer
plant genomes in all three DNA-containing compartments to
optimize gene copy numbers for minimal P content while
maintaining gene function.
2. Other P pools – roles and requirements
Phospholipids are important in membranes. While it may not be
feasible to reduce the total area of membranes, there may be possible efficiency gains in their synthesis and composition. Thomas
& Sadras (2001) characterized the assembly process of thylakoid
membrane complexes as having large excess production and
subsequent breakdown of components which is energetically
inefficient but allows high responsiveness to changing internal
and external conditions. If the implied trade-off between
efficiency and responsiveness exists, tighter regulation of biosynthesis may be a trait worth investigating for increased resource
efficiency in predictable productive environments.
Sulfolipids and galactolipids, rather than phospholipids, are
the major lipids in the thylakoid membrane, and to a lesser extent
in the plastid envelope membranes. Phospholipids in other membranes can also be replaced by sulfolipids and ⁄ or galactolipids;
either constitutively or in response to P deficiency. Data (see Supporting Information Notes S1), particularly on cyanobacteria
and algae, show that this replacement can be almost complete
(Van Mooy et al., 2006, 2009), and that replacement can also
occur as a result of mutations. However, the information on the
functional consequences of such replacement is limited to the
tentative conclusion that there is no effect on proton permeability
(Notes S1, Table S1), but that there may be increased membrane
leakage of electrolytes which constrains chill tolerance (for
Arabidopsis, see Hurry et al., 2000).
Tissue P concentration may also be decreased by lowering the
content of low-Mr water-soluble Pi-esters, and the nonstorage,
metabolically active Pi. Notes S2 discusses three ways by which
this could be achieved for the photosynthetic CO2-assimilation
pathway involving Rubisco and the photosynthetic carbon reduction cycle (Rubisco–PCRC). The conclusion is that even the
most radical of the three proposed interventions, that is, replacing
the Rubisco–PCRC with some other pathway involving fewer
phosphorylated intermediates, is unlikely to decrease the content
of the low-Mr water-soluble Pi-esters by > 10%, with an overall
saving based on the allocations in Fig. 1 of 1.2%. It is important
to note that phloem is cytosolic and that any decrease in Pi-esters
and Pi in its metabolically active cytosol, plastid stroma, mitochondrial matrix and nucleoplasm might have impacts on P (and
N) transport in phloem which is particularly relevant for
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remobilization from senescing tissues. Notes S3 and Table S2
deal with the phloem in more detail, showing that it is unlikely
that P translocation out of senescing (or any) tissues is limited by
the availability of solutes to generate turgor for phloem transport
or other constraints on the composition of phloem sap.
IV. Phosphorus pools and growth rates
When plants are subjected to external P deprivation, shoot growth is
often rapidly inhibited, well before plant P status is reduced. For
example, in Spirodela oligorrhiza (Bieleski, 1968) shoot growth
declines within hours upon a shift to a medium lacking P, while
shoot Pi concentration is not greatly affected during this time.
Similarly, barley leaf growth is severely inhibited when the plants are
subjected to Pi deprivation, although leaf Pi concentrations remain
adequate (Mimura et al., 1996). Shoot growth also declines in
Arabidopsis plants grown with reduced Pi supply, despite adequate
concentrations of Pi in the leaf vacuoles (Rouached et al., 2011).
These observations indicate that plants start to economize on Pi, by
reducing shoot growth, well before the leaf vacuolar storage pool of
Pi is depleted. This was explored by Wareing’s group using a range
of species. They showed that a limiting supply of P caused a decline
in export of cytokinins from roots and in cytokinin concentrations
in roots and leaves (El-D et al., 1979; Horgan & Wareing, 1980).
Using Plantago major, Kuiper et al. (1989) showed that the decline
in shoot growth upon a decrease in nutrient supply could be restored
by supplying kinetin to the roots; this increased the endogenous
concentration of cytokinins. The effect of kinetin on shoot growth
was transient, as expected, but it does illustrate that roots sense that
nutrients (N or P) are limiting well before leaves experience
deficiency symptoms and that shoot growth is regulated in a
feed-forward manner (Lambers et al., 2008).
As reduced shoot growth is a major concern for agricultural
systems, it would be desirable to maintain maximal shoot growth
as long as possible under P-limiting conditions, that is, until
vacuolar Pi contents are almost depleted, which would ultimately
reduce the amount of fertilizer needed for these managed systems.
The uncoupling of P limitation from its effect on growth is in
fact possible, as demonstrated in a recent study (Rouached et al.,
2011). The Arabidopsis PHOSPHATE1 (AtPHO1) gene has
previously been shown to be necessary for Pi transport from root
to shoot (Poirier et al., 1991; Hamburger et al., 2002). The
shoots of Atpho1 mutants grown under Pi-sufficient conditions
have all the typical symptoms of P deficiency, including severely
reduced shoot growth and expression of Pi-starvation inducible
(PSI) genes (Morcuende et al., 2007). By contrast, reduction of
AtPHO1 expression by co-suppression, or expression of the rice
(Oryza sativa) PHO1 orthologue (OsPHO1;2; Secco et al., 2010)
in an Arabidopsis Atpho1 null mutant resulted in shoot growth,
fresh weight, seed yield and lipid profiles under high Pi supply
that were more similar to those of wild-type plants than to those
of Atpho1 null mutants, despite the depleted shoot vacuolar Pi in
the transgenics (Rouached et al., 2011). Moreover, the AtPHO1
suppressed and OsPHO1;2 expressor lines also largely lacked the
Pi-starvation response typical of pho1 mutants (i.e. the expression
of a large set of PSI gene transcripts). Notably, the same
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conclusion was reached when PHO1 under-expressors and
wild-type plants with similar root-to-shoot Pi-transport rates
were compared (Rouached et al., 2011). While the shoot fresh
weight of the transgenics remained high with low vacuolar Pi
content, the shoot fresh weight of the wild-type decreased to
almost half, despite a much higher vacuolar Pi concentration than
in the PHO1 under-expressor. Importantly, the size of the leaf
cytoplasmic Pi pool was similar for all the plants. These data
illustrate that the reduction of growth, changes in lipid profiles
or changes in gene expression that are associated with the
Pi-deprivation response are not a direct consequence of low shoot
P status, but the result of signalling events that can be genetically
controlled. This gives hope that uncoupling growth from Pi
status will eventually also be feasible in crop species, and will
potentially become an important approach to ensure biomass
production at lower Pi input.
V. Are crops different from other plants in their P
concentration?
Crops have high tissue concentrations of P and N, as expected for
fast-growing plants (Poorter & Bergkotte, 1992). In a global
compilation of leaf traits known to be associated with the fast
growth–slow growth continuum in plants (Reich et al., 1999;
Wright et al., 2004), crop species form a very nonrandom subset of
plants as a whole (Fig. 2a). The high concentrations of both leaf N
and P may result from one of two processes: (1) preferential
selection of fast-growing species for our crops, or (2) artificial
selection shifting trait values within crop species towards the fast
end of the continuum. Of course these processes are not mutually
exclusive. The first process is probably the dominant factor for
N and P concentrations, as it is not uncommon to find lower
concentrations in modern crops than in their wild progenitors
(Evans, 1993).
In plants with higher concentrations of N and P, the ratio N :
P is lower (Elser et al., 2010); however, crops have relatively high
N : P compared with noncrops at this end of the spectrum
(Fig. 2a), partly as a result of the predominance of legume crops,
which tend to have high N concentrations. N : P ratios are
related to the cellular content of (N-rich) protein relative to the
content of (P-rich) RNA (Elser et al., 2010). Crops tend to have
lower and less variable protein : RNA ratios (i.e. a greater investment in RNA relative to protein), compared with tree species
(Fig. 2b). Woody species generally have much longer leaf
life-spans and invest more in lignified tissue to resist mechanical
damage. Crops have more similar protein : RNA ratios to algae
and microbes than to woody species (e.g. Loladze & Elser
(2011)). Protein : RNA and N : P ratios are sensitive to nutrient
availability (e.g. Close & Beadle (2004)) and thus the observed
ratio of c. 15 in crop plants (Fig. 2b) may reflect the nutrient-replete conditions generally found in agricultural systems, or
is the signature of selection for growth in high-nutrient soils (or
both). Sadras (2005) showed that N : P variation in crops is
better explained by differences in P concentration than in N concentration, and suggested that closer regulation of [N] and more
variable remobilization of P may contribute to this pattern. The
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Log mass based nitrogen concentration
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2
1.5
1
Herbaceous noncrop species
Woody noncrop species
Crop species
N:P=15
0.5
200
Protein : RNA
determinant of crop PUE. Photosynthetic phosphorus-use efficiency (PPUEmax) is defined as the instantaneous light-saturated
rate of leaf photosynthesis expressed per unit leaf P. Photosynthetic capacities (Amax, mass-based) of crop species are found at
the high end of the leaf trait spectrum, associated with fast growth
and low leaf mass per area (LMA) (Lambers & Poorter, 1992). As
a result of similar increases of Amax and P concentrations with
decreasing LMA, however, PPUE is not strongly correlated with
LMA (Fig. 3), so fast-growing species, which tend to have low
LMA, do not necessarily have a high PPUE. For example, thin
leaves of barley have a similarly high PPUE to the sclerophylls of
the genus Banksia (Lambers et al., 2011). Barley achieves this with
a high [P], whereas Banksia has very low [P], but barley apparently
uses P sparingly in structural tissue and very efficiently in photosynthetic machinery (Lambers et al., 2011). Interestingly, PPUE
varies by an order of magnitude at any LMA, and part of this variation can be attributed to leaf N concentration (cf. Reich
et al.(2009): mean PPUE is 59 nmol g)1 s)1 for leaves with N :
P < 15, whereas PPUE is 129 nmol g)1 s)1 for leaves with N : P
> 15 (n = 74 and 138, Glopnet data set; Wright et al., 2004). In
the Glopnet data set, high N : P is associated with low [P] rather
than high [N] (cf. Fig. 2a), and low [P] is clearly not conducive to
high rates of photosynthesis (Fig. 3b). Crops generally have low
LMA but not particularly high N : P (12.3 for the 17 grain crops
included in Fig. 2a), suggesting that a closer look at variation in
PPUE among and within crop species may be worthwhile and
may give insights into factors underlying high PPUE.
It is important to note that the above data refer to maximum
photosynthetic rates, rather than actual photosynthesis of leaves
during growth. In dense canopies, only a small proportion of
leaves operate at full photosynthetic capacity, for part of the day.
Nevertheless, it is fair to assume that mean daily rates of actual
photosynthesis, and even night-time respiration, scale with photosynthetic capacity, as has been shown for several species in a
number of environments (Zotz & Winter, 1993; Reich et al.,
2009).
Highest PPUE tends to be achieved by leaves with high rates
of photosynthesis, high P concentration and low LMA, but such
traits are associated with short leaf life-spans (Wright et al.,
2004), implying a trade-off that will reduce the C return per unit
P over the life of a leaf (PPUEleaf,life). For an appraisal of
PPUEleaf,life it is also important to consider that a large fraction
(a)
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Fig. 2 (a) Leaf nitrogen (N) vs leaf phosphorus (P) (log of concentration in
mg g)1 DW) among 700+ plant species, distinguishing woody and herbaceous species. Crop plants (c. 50 species) are found exclusively at the high
leaf N and P concentration end of the continuum, consistent with
fast-growing, thin, cheaply constructed leaves. Data are from the Glopnet
global compilation (Wright et al., 2004) and are supplemented by crop
and pasture data from Reuter et al. (1997), Pederson et al. (2002) and
Schultz & French (1978). (b) Ratio of protein concentration to RNA
concentration in photosynthetic tissue of algae (n = 11), crops (n = 3) and
trees (n = 8; an outlying value of 364 is not shown).
variation in protein : RNA ratios in trees and even among crops
(Fig. 2b) may indicate the potential for selection to reduce investment in RNA relative to protein in order to increase PUE.
VI. Phosphorus use and photosynthesis
Plant productivity relies on photosynthesis, and the photosynthetic process relies on P-containing compounds. Thus, an efficient use of P in photosynthesis is a potentially important
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Log Amax (nmol g–1 s–1)
Fig. 3 (a) Photosynthetic phosphorus-use efficiency
(PPUE) for leaves of 171 species (Glopnet data set;
Wright et al., 2004), plotted against leaf mass per area
(LMA), differentiating leaves that have N : P ratios below
(red circles) or above (blue) 15. PPUE is defined as the
light-saturated rate of photosynthesis expressed per unit
leaf P. (b) Maximum photosynthetic rate (Amax) plotted
against leaf phosphorus concentration (N : P ratios below
(red circles) or above (blue) 15). Lines are standard major
axis regressions.
Log PPUE (µmol g–1 s–1)
3
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m–2)
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Log P (mg g–1)
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of P in leaves is remobilized during senescence and re-used elsewhere in the plant (cf. Small, 1972; Aerts & Chapin, 2000). A
simple model of PPUEleaf,life taking into account the mentioned
factors is given by
(a)
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PPUEleaf ;life ¼ ðAmax b LL CCÞ=ðð1 rP Þ ½PÞ Eqn 2
VII. Crop development and canopy P distribution
The general pattern of P accumulation is remarkably similar
among monocarpic crops (Figs 4, 5a). Early growth of a seedling
depends to a large extent on P reserves in the seed, that is, remobilization of stored P (Bolland & Baker, 1988; Thomson et al.,
1991; White & Veneklaas, 2012). Duration of seed P reserve
dependence during early growth varies with seed mass, seed [P],
soil P availability and seedling P requirement, but is unlikely to
last longer than a few weeks. In crop plants, P concentrations of
seeds and seedlings are quite similar (e.g. 2.4–6.4 mg g)1 in seeds
and 2.9–4.5 mg g)1 in young plants of eight crops including
cereals, legumes and oil seeds (Schultz & French, 1978)), so
growth beyond the seedling stage is soon dependent on P uptake
from the soil. Maize (Zea mays) seedlings started taking up significant amounts of 32P from soil c. 5 d after sowing, but continued
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40
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160
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Plant P content (mg)
where Amax is the maximum mass-based photosynthetic rate
(nmol g)1 s)1), b converts Amax to a daily total C exchange rate,
LL is the life-span of a leaf (d), CC is the carbon cost for leaf
structure (g g)1, taking into account any C remobilization during
senescence), rP is the fraction of P remobilized during senescence,
and [P] is the concentration of P in the mature leaf (g g)1). In
crops that have a high relative growth rate (growth rate per mass
present), it is reasonable to assume that the carbon cost (CC) of a
leaf represents a minor fraction of its lifetime carbon gain (Amax ·
b · LL) (Poorter et al., 1991). The extent of variation in b is
poorly known, but the proportionality between photosynthetic
capacity and daily net C assimilation (Zotz & Winter, 1993;
Koyama & Kikuzawa, 2009; Reich et al., 2009) indicates that
such variation is low among species in the same environment.
Global leaf trait relationships (Wright et al., 2004) show that
Amax is approximately inversely proportional to LL, which makes
it likely, according to Eqn 2, that high PPUEleaf,life in nature is
mostly achieved by leaves with low concentrations of P and high
remobilization of P upon senescence. Such traits are to be
expected in high-LMA leaves with long life-spans and low photosynthetic capacities. In conclusion, the near-proportionality of
Amax and leaf [P] and the inverse proportionality of these traits
with leaf life-span lead to the absence of general trends in C
return per unit P along the leaf economics spectrum. This is in
contrast to the instantaneous PPUEmax. It is important to note,
however, that there is considerable variation between species in
both indices, indicating that other leaf traits influence the efficiency of P use in photosynthesis, such as shown for leaf N. Zhu
et al. (2010) argue that future increases in crop yield potential
will come from increased photosynthetic capacity. It will be
important to achieve this along with increased PPUE.
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canola
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(e)
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sunflower
100
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Time after sowing (d)
Fig. 4 Phosphorus (P) accumulation in the whole plant (blue) and
vegetative plant (red) of five crops: (a) rice (Oryza sativa) (Rose et al.,
2010), (b) wheat (Triticum aestivum) (Rose et al., 2007), (c) lupin (Lupinus
albus) (Hocking & Pate, 1978), (d) canola (Brassica napus) (Rose et al.,
2008) and (e) sunflower (Helianthus annuus) (Hocking & Steer, 1983).
to use seed P reserves for c. 2 wk (Nadeem et al., 2011). While P
derived from seeds may be a minor component of whole-plant P
at maturity, it does have a lasting influence on plant development
(Bolland & Baker, 1988), especially if early vigour provides better access to potentially growth-limiting resources such as soil
moisture, nutrients and light, in the absolute sense or relative to
competitors.
As crop canopies develop and leaf area indices increase, photosynthetic rates of the lower shaded leaves decrease. Plants redistribute N from older shaded leaves to younger well-lit leaves in a
pattern that approaches an optimal distribution of total canopy
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Seed to vegetative plant
Soil to vegetative plant
Vegetative plant to grain
Soil to grain
3.5
Net P flux (mg d–1)
P content (mg)
3
Fig. 5 Schematic time course of (a) the phosphorus (P)
content of a monocarpic crop plant from germination to
maturity; (b) net P fluxes from seed and soil to vegetative
plant and grain, as well as net remobilization from
vegetative plant to grain. Approximate values based on
studies of growth and P accumulation shown in Fig. 4.
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N (Field, 1983; Hirose & Werger, 1987; Franklin & Ågren,
2002). Redistribution of P for optimal plant C gain has been
little studied, but the same principles are expected to apply as for
N. Adequate concentrations of P are important to maintain high
rates of photosynthesis (Rychter & Rao, 2005), and rates of P
remobilization from senescing leaves are at least as high as those
for N (Aerts, 1996). With near-optimal nutrition, shoot [N] and
[P] decrease in a similar way as plants grow (Greenwood et al.,
2008), suggesting similar patterns in uptake and redistribution of
N and P under such conditions; however, when one of these
elements is limiting, shifts in the N : P ratio may occur as a result
of reduced uptake of N or P which cannot be fully compensated
by internal redistribution. The N : P ratio of shoots of six cereal
and oilseed crops changed only slightly from approx. 11 to 9
between the early vegetative and mid-flowering stages, while
concentrations of both elements decreased by > 60% (Schultz &
French, 1978).
In densely planted, fast-growing crops, the transition from
young leaves to senescing leaves happens rapidly (Niinemets,
2007), and such leaves do not reach their potential life-span. This
may cause a reduction in PPUEleaf,life but enhances growth and
whole-plant PUE if the proportional gain in whole-plant photosynthesis is greater than the proportional loss of P as a result of
leaf senescence. Thomas & Sadras (2001), however, point out
that leaves are often retained when they have long ceased to make
a positive contribution to plant C balance. These authors argued
that these ‘unproductive’ leaves may act as storage organs for C
and N needed at a later stage for reproductive growth. The
importance of such storage and its effect on whole-plant C
balance depend on developmental stage and nutrient availability.
In dense stands of Xanthium canadense, leaf retention at high N
availability was longer than expected based on optimal allocation
for whole-plant C gain (Oikawa et al., 2008). The selective
pressure for retention of N and P in unproductive tissue may be
primarily related to allocation of these reserves to reproductive
output in nature, or to yield in crops; constraints on the N : P
ratio in sieve tube sap are considered in Notes S3. There is only
limited research into the effect of N or P redistribution on C
balance in the reproductive stage, but Schieving et al. (1992)
showed that leaf shedding and associated remobilization of N in
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flowering Solidago altissima helped maintain high rates of canopy
photosynthesis. In contrast to the ‘parasitic’ old leaves described
by Thomas & Sadras (2001) for species at high nutrient availability, Reich et al. (2009) found that leaves of ten evergreen woody
species still had a positive C balance when they reached their
average life-span. Enhancing PUE of crops will require a better
understanding of the distribution and redistribution of P among
leaves in the canopy and its effect on C gain.
VIII. Internal redistribution of P in a growing
vegetative plant
As plants tend to remobilize at least 50% of P from senescing
leaves, and often much more (Aerts, 1996), redistributed P is a
quantitatively important P source for growth, especially at later
stages of plant development and in situations where soil P availability is low. In vegetative plants in the exponential growth
phase, amounts of senescing tissues are much smaller than
amounts of growing tissue, such that the potential P benefit from
remobilization is very small, probably only a fraction of the total
P required (Fig. 6). At this stage, P uptake by roots is by far the
most important P source, and roots would indeed be expected to
be exploring the most P-rich soil. As growth rates decline, usually
when the older foliage experiences lower light conditions and
starts senescing, and expansion and P uptake by root systems
decrease, remobilization can provide significant amounts of P to
new growth. This shift from uptake-dominated P supply to
remobilization-dominated P supply probably happens in the
late vegetative or early reproductive stage (Fig. 5). Remobilized
P is also particularly important in P-deficient plants. Under P
starvation, plants display several transcriptional and posttranscriptional adaptive responses (Plaxton & Tran, 2011;
Notes S4). P deficiency accelerates senescence in some but not all
cases (Crafts-Brandner, 1992; Lynch & Brown, 2006), but
suppression of new growth in P-deficient plants is always likely to
be larger than any effect on senescence, such that the relative
contribution of remobilized P for growth becomes greater.
Between early and late vegetative stages, crop growth is faster
than P uptake, causing a considerable decrease of shoot [P]
(Fig. 7); however, remobilization of P from senescing tissues
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P concentration (mg g−1)
Potential % of P from remobilization
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Grain
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Relative growth rate (g g−1 d−1)
Fig. 6 Potential importance of phosphorus (P) remobilized from senescing
tissues as a source of P for plants growing at different relative growth rates
and tissue longevities. Calculations are based on the assumptions of
constant relative growth rate (RGR; dry mass increase per unit dry mass
present per unit time), constant plant P concentration, and 100%
remobilization of P when tissue reaches the end of its life-span. The
fraction of P derived from remobilization is estimated as Premob ⁄ Pplant =
P0 Æ eRGRÆ (t ) LL) ⁄ (P0 Æ eRGRÆt) = e)RGRÆLL where t is time (d), P0 is plant P
content at t = 0 (germination) and LL is the life-span of the tissue. Relative
growth rates of crop plants in the exponential growth phase are typically
0.05–0.1 g g)1 d)1. Leaf life-spans of annual herbaceous species are
typically 20–60 d (Kikuzawa & Lechowicz, 2006). Red, lifespan 30 d; blue,
lifespan 60 d; green, lifespan 90 d.
helps maintain high [P] in young leaves which fuels this growth.
The importance of P remobilization during vegetative growth is
expected to be greatest in crops that have long growing seasons
and short leaf life-spans, and grow in dense stands.
IX. Allocation of P to reproductive structures
Large changes occur in monocarpic plants, such as annual grain
crops, when they enter into the reproductive phase. The massive
translocation of C and mineral nutrients into seeds during this last
phase of the life cycle enhances resource availability for rapid early
growth of the next generation (Sklensky & Davies, 1993). Domestication and breeding of crops for high yields has achieved further
increases in the proportion of dry mass allocated to seeds (harvest
index (HI); Sinclair, 1998), and the allocation of P and N has
increased similarly. High grain N concentrations are favoured
because of the nutritional value of protein; however, high P
concentrations are not necessarily desirable (Batten, 1986; Raboy,
2009). First, most P in cereal grains and legume seeds is in the
form of phytate, which is not assimilated by humans or monogastric livestock and restricts the bioavailability of iron and zinc in
their diets (White & Broadley, 2009). Secondly, most P contained
in produce that is exported from crop land is released to the environment in the form of waste streams (e.g. manure and sewage)
and needs to be replaced with new P-fertilizer to maintain soil P
status (Raboy, 2009). There are therefore nutritional as well as
environmental reasons for reducing the allocation of P to grain
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0
Barley
Oats
Wheat
Linseed
Rape
Safflower
Lupin
Pea
Tillering
Straw
Flowering
Maturity
Fig. 7 Change in phosphorus (P) concentration in eight crops during
development, Barley (Hordeum vulgare); Oats (Avena sativa); Wheat
(Triticum aestivum); Linseed (Linum usitatissimum); Rape (Brassica
napus); Safflower (Carthamus tinctorius); Lupin (Lupinus angustifolius)
and Pea (Pisum sativum). Data are from Schultz & French (1978). Between
flowering and maturity, P accumulates in seeds (solid lines) at the cost of P
in straw (dashed lines).
(the phosphorus harvest index (PHI)) while maintaining or
increasing HI. However, mutants with reduced seed phytate
concentrations often, although not always, have reduced vigour
(Raboy, 2007). Crop management options may be able to deal
with this by separate production of seeds under higher P fertilization rates, and ⁄ or by ensuring high P availability for seedling
growth through seed coating technology or fertilizer placement
(Pariasca-Tanaka et al., 2009; Burns et al., 2010; Sekiya & Yano,
2010). But is it feasible to decrease grain P while increasing yield?
Before this is discussed, it is important to examine the processes
that determine grain yield and its P content.
Patterns of P accumulation and partitioning in a number of
crop species (Figs 4, 5) reveal that most of the increase in seed P
content is synchronous with a decrease in the P of senescing
leaves and stems, although there can still be some increase in
whole-plant P content (i.e. net P uptake) during early reproductive growth, particularly in indeterminate crops. As P concentrations are typically much higher in grain than in vegetative
material at maturity, the proportion of total plant P that is found
in grains (PHI) is higher than the proportion of dry mass (HI)
(Fig. 8a). Breeding for high yield in the past has increased HI in
all crops (Sinclair, 1998), but PHI has not increased to the same
extent, which means that a decrease in P concentrations in the
grain has occurred. Batten (1986) reported a decrease of c. 27%
in grain [P] from diploid to hexaploid wheat grown in pots with
adequate P fertilization, while HI more than doubled and PHI
increased by only 15%. This trend was also shown in a field study
by Calderini et al. (1995) for wheat cultivars released between
1920 and 1990, but a pot study of cultivars released between
1840 and 1983 showed increased HI but not decreased grain [P]
(Jones et al., 1989). In 37 varieties of rice, with high average HI
and PHI, correlations between grain [P] and these allocation
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indices were weak (Rose et al., 2010). P fertilization causing a
six-fold increase in wheat grain yield did not affect PHI and HI
significantly (Fig. 8b; Jones et al., 1989).
The above indicates that modern crop varieties use P more efficiently than older varieties (higher PUEy), as a result mainly of
improvements in HI which are related to plant structural and
C-allocation traits. How much further can these traits be
improved? Can key physiological traits such as high photosynthetic rates (enabling a small plant to produce a large amount of
photosynthates to fill grain) and efficient translocation of carbohydrates to growing seeds be maintained in crops that have low leaf
[P]? The breeding goals for efficient use of P are quite similar to
those for N, with the important exception that high grain [N] can
be a positive trait and high grain [P] is not. As shown above, efficient use of N and P requires both elements to be present at high
concentrations. Similarly, high percentage remobilization from senescing to young vegetative tissue is also favourable for both N and
P. Therefore, the key question for P is whether mobilization of P
into grains can be reduced without reducing grain growth or grain
[N]. Does grain-filling require high [P]? Are the fluxes of carbohydrates, N and P into grain functionally linked? Aspects of phloem
function that relate to these issues are discussed in Notes S3.
Marshall & Wardlaw (1973) observed a close correspondence
between transport of P and that of sugars from source leaves to
grain in wheat and concluded that the movement of P from leaves
is largely determined by the movement and demand for carbohydrate within the plant and not by the P requirement of the sink.
Similarly, Pugnaire & Chapin (1992) found that P and N remobilization from leaves to ears in barley increased in plants with high
sink strength, but also those with low source activity. Peng & Li
(2005) confirmed this in wheat. Batten & Wardlaw (1987) found
no positive effect on grain growth after adding P to P-deficient
wheat ears. Movement of P into developing wheat grains is faster
than that of carbohydrates, and apparently regulated independently (Batten & Wardlaw, 1987; Rodriguez & Goudriaan, 1995;
Peng & Li, 2005). P arriving in the grain tissue is quickly converted to phytate to keep Pi concentrations low. High Pi concentrations would inhibit starch formation (Smidansky et al., 2002,
2003). Genetic transformation of the key regulatory enzyme of
starch biosynthesis, ADP-glucose pyrophosphorylase, to reduce its
allosteric inhibition by Pi leads to greater yield in rice and wheat,
not by improving allocation of C into seeds (improved HI), but by
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Fig. 8 (a) Harvest index (HI) and phosphorus harvest
index (PHI) for a number of crops (Schultz & French,
1978; Jones et al., 1989; Araújo et al., 2007; Parentoni
et al., 2010; Rose et al., 2010). (b) HI and PHI for 23
wheat cultivars grown in pots at low and adequate P
availability, 2 and 40 kg ha)1 (Jones et al., 1989).
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Adequate P
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enhancing sink strength which indirectly increases plant growth
(Smidansky et al., 2002, 2003). As P import in early grain growth
seems more than adequate, even under P deficiency, it would seem
worth exploring ways to reduce P allocation to grain.
The N : P ratio in grain is lower than that in the vegetative
plant. Greenwood et al. (2008) modelled the decrease of N : P
with development in horticultural crops as a transition from
growth-related tissue with an N : P ratio of approx. 12 to storage-related tissue with an N : P of approx. 6. Sadras (2005)
found that adequately fertilized cereal and oilseed crops attaining
maximum yields had N : P ratios at final harvest between 4 and
6. In wheat, grain N : P was unchanged from old to modern
wheat cultivars and averaged approx. 6 (Calderini et al., 1995). It
appears that N : P ratios are quite conserved in productive, adequately fertilized crops. In noncrop species, seed N : P ratios are
also lower than whole-plant N : P ratios (Güsewell, 2004). The
larger allocation of P than N to seeds agrees with the greater
degree of remobilization of P from leaves (e.g. 22% more remobilization of P than N in graminoids; Aerts, 1996). Greater remobilization of P than N from senescing tissue may partly explain
low seed N : P, but there may also have been stronger selection
for high seed P, perhaps because acquiring poorly mobile P is
more challenging than acquiring N for small root systems.
X. Constraints to P remobilization
Remobilization of P from senescing leaves is more variable than
that of N. P-resorption efficiency (PRE; the percentage of mature
leaf P that has been exported before death) can reach values as
high as 90% (Aerts & Chapin, 2000). In wild plants PRE is not
significantly different among plant groups; for example, woody
species and forbs have similar means and variability (Aerts &
Chapin, 2000). Nevertheless, there is evidence that PRE is under
selection, giving rise to ‘ecotypes’ that have higher PRE in Plimited sites (e.g. Güsewell, 2005; Lovelock et al., 2007), suggesting that selective breeding for high PRE in crops could be
successful. The high variability in P remobilization is determined
by its sensitivity to a range of environmental factors, including
nutrient availability, water availability, and sink strength
(Pugnaire & Chapin, 1992; Güsewell, 2005; Fife et al., 2008).
When conditions favour remobilization, little P is left behind in
senesced tissue (Fig. 6; Schultz & French, 1978). Güsewell
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(2005) suggests that higher PRE is achieved by lengthening of
the senescent phase of leaf life times and by increasing the sink
strength for P (e.g. underground storage organs, or seeds). Plant
breeding has so far focused mainly on lengthening or shortening
leaf life time before senescence rather than on modifying the
duration of the senescent phase (Gregersen et al., 2008), yet this
may be a trait that if altered could improve PRE in crops. The
possibility that PRE may be related to the relative sizes of the different P pools has not been explored in crops or other plants.
It was shown earlier that low leaf [P] and high PRE are important
factors for PPUEleaf,life, in a global leaf trait data set where leaf longevity and photosynthesis are inversely proportional. Aerts &
Chapin (2000) came to a similar conclusion for forbs and graminoids, from which many crops are derived. This seems to offer little
hope for increased crop PUE, as low [P] and high PRE are not common in fast-growing plants with high levels of metabolic activity.
However, this does not mean that no improvement is possible.
There is significant variation among and within species in these
traits, and it is important to assess which traits can be improved
without secondary undesirable effects (Lambers et al., 2011).
Insight into the key enzymes and transporters involved in the
breakdown of P compounds, their export from senescing tissue and
transport to growing tissue is increasing (Notes S4). Considering
the large pool of nucleic acid P in cells, it is not surprising that
RNases become more abundant during senescence, as well as under
P deprivation (Taylor et al., 1993; Bariola et al., 1999; Morcuende
et al., 2007). Similarly, purple acid phosphatases (PAPs) play an
important role in the hydrolysis of Pi from a wide range of organic
P compounds including mononucleotides derived from nucleic
acid breakdown (Plaxton & Tran, 2011). Transcription of the
phosphatase genes AtPAP17 and AtPAP26 is greatly increased in
senescing Arabidopsis leaves (Gepstein et al., 2003), suggesting an
important role for the encoded enzymes in Pi scavenging during
senescence. Long-distance transport of nutrients from senescing
leaves to the seeds or other parts of the plant requires Pi transporters. Reports are now emerging of individual Pi transporter genes
that are up-regulated at the transcript level in senescent tissues; this
suggests that they have a role in Pi remobilization from old source
to new sink tissues and are linked to ethylene signalling (Chapin &
Jones, 2009; Nagarajan et al., 2011). Further research on the
molecular physiology of P remobilization may provide valuable
insights leading to enhanced P re-use in crop plants.
XI. Do physiological or phylogenetic trade-offs
constrain traits that could improve PUE?
Correlations among traits of diverse land plants provide valuable
insights into trade-offs in the use and allocation of P. In some cases
it might be desirable to breed crop plants that have combinations
of traits that are rarely observed in nature. It would therefore be
useful to know whether the observed correlations among species
are imposed by physical or genetic constraints, or if they are the
result of natural selection in which certain trait combinations are
disadvantageous, but not impossible. A recent analysis (Donovan
et al., 2011) suggests that strong correlations among species in leaf
traits (photosynthesis, N concentration, leaf mass per unit area
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and leaf life-span) are the result of natural selection, rather than
being attributable to unavoidable physical or genetic constraints.
This was shown by compiling information from studies of quantitative genetic variation in leaf traits. Specifically, it was observed
that individuals from the same species typically exhibit little
genetic correlation in leaf traits (e.g. LMA and photosynthesis per
area), suggesting that only a small proportion of variation in trait
values (mean heritability values < 0.3; Donovan et al. (2011) can
be attributed to genetic similarity. In the future, it might be informative to apply similar analyses to measures of intra-specific variation in P-use traits. This could help us understand mechanisms
behind the evolution of inter-specific correlations between P use
and other traits (e.g. the relationship between leaf P and N
concentrations; Fig. 2), and provide insights into the potential to
decouple these correlations through artificial selection.
XII. Identifying genetic loci associated with PUE
There is substantial genetic variation in traits associated with PUE
within the crop plants that have been examined (see references in
White et al. (2012) and within Arabidopsis, see Prinzenberg et al.
(2010)). Analysis of this variation has led to the identification of
numerous genetic loci that influence PUE. The ability to identify
these quantitative trait loci (QTL) suggests that improvements in
PUE may be gained through conventional or marker-assisted
breeding programmes, directed gene identification and genetic
engineering, or a combination of these approaches.
Nearly all QTL mapping has focused on traits associated with
efficient P acquisition rather than efficient internal use of P (see
references in White et al. (2012)). These traits include high total
plant P content, large root systems, improved root architecture
(increased lateral root production, improved topsoil foraging,
greater root surface to volume ratio, greater root hair production,
and greater root:shoot ratio), and the exudation of phosphatases
and organic acids into the rhizosphere. Nevertheless, QTL that
have the potential to influence internal PUE have been found in
several crop species (see references in Vance (2010); Rose et al.
(2011); White et al. (2012)). However, internal PUE is generally
lower in plants with high P-acquisition efficiency as a result of
higher tissue P concentrations, making it difficult to disentangle
QTL that affect agronomic PUE generally from QTL that may
specifically influence internal PUE (Rose et al., 2011). Rose et al.
(2011) proposed that identifying QTL for internal PUE requires
studies where P acquisition is equal and metabolically nonsaturating
among cultivars. As an alternative, explicit quantification of
tissue P pools would allow a more specific evaluation of genotypes and identification of QTL that are related to the efficiency
of P use in nucleic acids, phospholipids and P-esters. As shown in
Fig. 1, plants with high P concentrations store large amounts of
Pi in vacuoles. This large Pi pool does not contribute to metabolism and growth and therefore has a net negative effect on
internal PUE. Calculation of PUE indices based on the main
metabolically active P pools (i.e. growth or photosynthesis
expressed per unit of nucleic acid, phospholipid, or P-ester),
might yield better insights into the efficiency with which P is used
at a cell physiological level. This approach might also help us to
2012 The Authors
New Phytologist 2012 New Phytologist Trust
New
Phytologist
understand the processes that lead to accumulation of Pi in existing tissues rather than its incorporation in metabolically active P
of new tissues. The P-pool-specific PUE indices are likely to be
better suited to QTL mapping studies, and should be targeted if
the goal is to identify QTL and genes related specifically to
internal PUE.
There is much scope for future mapping of QTL that influence
internal PUE. Advanced methods of genetic analysis have not yet
been used extensively in the area of plant P relations. Approaches
such as genome-wide expression (transcriptome) QTL analyses
(Hammond et al., 2011) and genome-wide association studies
(Zhao et al., 2007; George et al., 2011) supported by such
emergent technologies as next generation sequencing hold
much promise to identify loci related to and controlling plant P
relations, including internal PUE (Vance, 2010; Morrell et al.,
2012).
XIII. Conclusions
A greater effort to enhance the efficiency of P use for crop
production will reduce environmental impacts associated with P
fertilizers and P waste, increase the nutritional value of grains,
and improve farm economies. We have identified developmental
and physiological aspects of PUE, underpinned by genetics and
molecular biology, which suggest that significant improvement in
internal PUE is possible. The magnitude of PUE gains that may
be obtained through different mechanisms, and their variation
associated with genetic and environmental factors, should be
quantified through targeted research. More efficient use of P
within the plant adds to the gains that can be made by improving
P-acquisition efficiency, but also reduces P fluxes on crop land
and in the environment. The largest yield benefits of improved
PUE are expected for crops growing in soils that have very low P
content and where little or no P fertilizer is applied. The largest
savings in P fertilizer are expected on productive land where
conditions for crop growth are near optimal.
Acknowledgements
This paper is a result of the workshop ‘Phosphorus, the inside
story’, held at the School of Plant Biology, The University of
Western Australia. Funding contributions from the School of
Plant Biology, the Faculty of Natural and Agricultural Sciences,
the Pro Vice-Chancellor (Research) and the Institute of Agriculture of The University of Western Australia are gratefully
acknowledged. The University of Dundee is a registered Scottish
charity, No SC10596. Constructive comments from three
reviewers are gratefully acknowledged.
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Supporting Information
Additional supporting information may be found in the online
version of this article.
Notes S1 Possibilities of replacement of phosphorus by other
elements – phospholipids.
Notes S2 Possibility of decreasing the low-molecular-mass
water-soluble P esters.
Notes S3 N and P removal from senescing structures in relation
to phloem function.
Notes S4 Molecular constraints of Pi remobilization from
senescing leaves.
Table S1 Proton permeability (PH+) as a function of membrane
lipid composition
Table S2 Nitrogen and phosphorus in phloem sap
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