Journal of Experimental Botany, Vol. 51, GMP Special Issue,
pp. 447–458, February 2000
Selectable traits to increase crop photosynthesis and
yield of grain crops
R.A. Richards1
CSIRO Plant Industry, PO Box 1600, Canberra, ACT 2601, Australia
Received 16 June 1999; Accepted 20 October 1999
Abstract
The grain yield of cereals has almost doubled this
century as a result of genetic manipulation by plant
breeding. Surprisingly, there has been no change in
the rate of photosynthesis per unit leaf area to accompany these increases. However, total photosynthesis
has increased as a result of an increase in leaf area,
daily duration of photosynthesis or leaf area duration.
There remain substantial opportunities to continue to
improve total photosynthesis and crop yield genetically
using conventional breeding practices. Selectable
traits are discussed here in the context of increasing
total above-ground biomass under favourable conditions. Opportunities exist to alter crop duration and
the timing of crop development to match it better to
radiation, temperature and vapour pressure during
crop growth, and to increase the rate of development
of early leaf area to achieve rapid canopy closure. The
importance of these traits will depend on the environment in which the crop is grown. Increases in crop
photosynthesis through breeding are also likely to
come via indirect means. Selection for a high and
sustained stomatal conductance during the period of
stem elongation is one way. Increasing assimilate
allocation to the reproductive primordia so as to establish a large potential sink should also indirectly
increase total crop photosynthesis. Evidence in the
major grain crops suggests that by anthesis the capacity for photosynthesis is high and that photosynthesis
is not limiting during grain filling. To use this surplus
capacity it is suggested that carbon and nitrogen partitioning to the reproductive meristem be increased so
as to establish a high potential grain number and the
potential for a large grain size. It is then expected that
additional photosynthesis will follow, either by a longer
daily duration of photosynthesis or by an extended leaf
area duration.
1 Fax: +61 2 6246 5399. E-mail: [email protected]
© Oxford University Press 2000
Key words: Genetic manipulation, cereals, yield, photosynthesis, selectable traits.
Introduction
The process of photosynthesis is pivotal to the production
of food and fibre as it provides the raw materials for all
plant products. The average global grain yield per unit
area of the major staple crops, wheat, rice and maize,
more than doubled in the period between 1940 and 1980
and this trend continues ( Evans, 1993). This doubling of
grain yield coincided with the period when the understanding of photosynthesis exploded. Advances in photosynthesis research continue with a new wave of excitement
brought on by the advances in molecular biology. There
are two rather surprising features of the yield increases.
Firstly, the greater understanding of photosynthesis has
not yet contributed to yield increases. Secondly, a genetic
increase in the rate of photosynthesis has not been
required to achieve the increased productivity. Increased
yields have been achieved by (i) increased or extended
photosynthesis per unit land area and (ii) increased
partitioning of crop biomass to the harvested product.
The first has mainly been achieved by irrigation schemes
and improved agronomic practices, in particular the use
of inorganic fertilizers, but also to elevated atmosphere
CO concentrations, whereas the second has largely been
2
due to plant breeding. Despite intense selection for
increased yield by plant breeders this century, selection
has not resulted in a genetic increase in photosynthesis
per unit leaf area. On the contrary, in many crops
photosynthesis per unit leaf area has declined with intensive breeding! Nevertheless, plant breeding has been successful in extending the duration of photosynthesis in
many crops although much of this has been assisted by
genetic improvements in disease resistance.
448 Richards
In this paper the changes in biomass and yield achieved
by plant breeding in several grain crops are briefly examined. The opportunities to increase biomass and yield
using a physiological breeding approach are then
explored. Finally, any photosynthetic processes that have
been associated with yield gains made by breeding will
be examined so as to identify the most likely targets for
future endeavours. The focus will primarily be on wheat
although results from other crops will also be drawn on
and the emphasis will be on crops grown under favourable
conditions. Crop production ha−1 are the units that will
be used to define yield and yield progress. Whereas these
are important in most regions, production ha−1 d−1 can
be more important in warmer climates where water is
available and where several crops can be grown each year.
Crop photosynthesis will be differentiated from leaf
photosynthesis. Crop photosynthesis will be used to
describe net carbon gain per unit ground area per unit of
time whereas leaf photosynthesis will refer to net photosynthesis (i.e. A ) per unit leaf area per unit of time.
max
Genetic improvements in yield potential
Increases in yield potential achieved by plant breeding
this century have been well documented for numerous
crops (Slafer, 1994). All studies show how successful
empirical breeding has been to increase grain yield in the
target environment. It is also interesting, and indeed
agriculturally important, that selection under favourable
conditions usually translate to higher yields in less favourable environments (Austin et al., 1980; Castleberry et al.,
1984; Russell, 1991). This is also evident in the spectacular
success of varieties bred at international centres such as
CIMMYT and IRRI and which are grown in other
regions with a lower yield potential. In wheat, most of
the increase in yield has been achieved by an increase in
harvest index and it is surprising that increases in aboveground biomass are not usually observed (Fig. 1),
although there is some evidence for an increased biomass
in the most favourable seasons (Austin et al., 1989). The
results shown in Fig. 1 are similar to other studies conducted in USA, Mexico, Argentina, Australia, and several
other countries for wheat (Slafer et al., 1994). Maize is
similar to wheat in that breeding has resulted in an
increase in yield ( Fig. 2). However, it contrasts with
wheat in that increases in biomass account for most of
the increase in grain yield (Fig. 2; Russell, 1991;
Tollenaar, 1991).
It is expected that grain yields will continue to increase
through both agronomic and genetic means. This is
because in most regions crop production is below the
potential for the region given water availability, light and
nutrients. Also, there is also little evidence that the genetic
yield potential has reached a plateau. Total crop photosynthesis and yield will increase as a result of agronomic
Fig. 1. The relation between grain yield, above-ground biomass, harvest
index and year of release of wheat cultivars released in the UK since
1820. (Data adapted from Austin et al., 1989.)
practices that improve water management, fertilizer use,
soil structure, and plant health. Genetic improvements in
the ratio of economic yield to above-ground crop biomass
(i.e. the harvest index) will continue, although, in intensively bred crops, the upper limit is being approached.
Current values for harvest index in high yielding wheats
are greater than 0.5 and the upper limit for wheat is
considered to be about 0.6 (Austin et al., 1980a). Further
Breeding for improved yield of cereals 449
close to the maximum value and any further increase may
only be counter-productive as it may also reduce biomass.
It is therefore appropriate to focus on ways to increase
biomass and thereby crop photosynthesis genetically.
Determinants of increased biomass
To identify selectable traits in a breeding programme to
improve crop photosynthesis it is helpful to consider the
components of biomass production. Assuming there is no
water limitation, biomass production is the product of
the solar radiation over the duration of the crop period
(Q), corrected for the amount intercepted by the crop
canopy (I ), and the conversion of this chemical energy
(E ) into plant dry matter. This can simply be expressed
as:
Fig. 2. Grain yield, above-ground biomass and harvest index of an
open-pollinated (OP) variety and hybrids of each 10 year era from
1930 to 1980. (Data adapted from Russell, 1985.)
increases in harvest index may come from a reduction in
the investment in leaves and other vegetative structures.
This in itself may compromise total biomass; it may also
require an increased rate or duration of photosynthesis
to compensate for the reduced photosynthetic area. In
maize it is considered that the harvest index is already
harvest
(1)
Biomass= ∑ Q×I×E
sowing
where the product of Q, I and E are summed over the
period between sowing and harvest.
From equation (1) it is seen that the ways to increase
total biomass are as follows: First, to increase the duration
of crop photosynthesis so that there is an increase in total
solar radiation received. The second term in equation (1),
the amount of light intercepted by the canopy, is the
component of biomass production that is perhaps most
amenable to genetic manipulation. Various aspects of this
term can be altered. For example, the rate of development
of leaf area can be manipulated genetically to achieve full
light interception more quickly. After full light interception by the canopy, usually at a leaf area index of about
3.5, then both canopy architecture and leaf area duration
offers opportunities for genetic manipulation. The final
term in the identity, the conversion of light energy to
plant dry matter, relates to the efficiency or rate of
photosynthesis and the ability of the crop to retain fixed
carbon. There is substantial evidence for genetic variation
in the rate of leaf photosynthesis, although, curiously,
this variation does not seem to have contributed to greater
biomass. Retention of fixed carbon relates to losses of
carbon by respiration or carbon exudation from the roots.
The duration of crop growth and the interception of
solar radiation are the two components of equation (1)
that have contributed most to increased biomass and
total photosynthesis of crops and thereby yield.
Conventional breeding and genetic manipulation and
agronomic practices together have contributed to this
increase. Advances in machinery and cropping practices
have contributed to more timely sowing and the genetic
manipulation of phenology in crops has further contributed to this timeliness. Management has also been important for increasing the interception of solar radiation with
the increased use of chemical fertilizers and improved
machinery to achieve the most efficient sowing densities
450 Richards
and sowing arrangements so as to maximize light interception. Both genetics and agronomy have been important
to maintain leaf area, with the use of genes giving
resistance to foliar diseases, changed rotations and the
use of prophylactic sprays. This interrelation between
breeding and crop husbandry has been important and
will remain so. It has been particularly evident in the
widespread adoption of dwarfing genes in wheat and rice
which have reduced crop lodging and allowed higher
rates of fertilizers to be applied.
Duration of crop photosynthesis
Extending crop duration is the simplest genetic way to
increase total photosynthesis, crop biomass and yield. A
longer crop duration simply increases the solar radiation
(Q) available during the crop growth period. For example,
in field-grown rice, biomass increased by 0.2 t ha−1 for
each day that growth duration was extended (Akita,
1989). Ample genetic variation is available in all crops to
alter the duration of the period between sowing and
anthesis. In temperate crops there are genes that are
sensitive/insensitive to vernalization and to photoperiod
as well as genes that influence the basic development rate
(Stelmakh, 1998). It is this variation that has extended
the boundaries of crop production away from their centres
of origin and sometimes to climatic extremes. Crops as
diverse as maize, soybean, wheat, and rice can now be
grown from the equator to 50° latitude and beyond. Thus,
for temperate crops such as wheat, manipulation of major
genes responsible for sensitivity/insensitivity to photoperiod and to vernalization enable wheat to be grown
over, say, an 11-month or a 3-month period.
Corresponding differences in biomass can be huge. For
example, sowing a winter wheat in south-eastern Australia
just one month earlier than the recommended sowing
date for a spring wheat, and with the same harvest time,
can result in an almost 2-fold difference in final biomass
(Gomez-Macpherson and Richards, 1995).
It is not just the duration of growth that can be
manipulated to increase biomass and yield, but also its
timing. For example, providing there are no other limiting
factors, full light interception should be achieved by the
time daily solar radiation is at its maximum. Manipulating
crop phenology so as to better match periods of high
radiation with critical growth stages can also be important. This is provided water availability and temperature
are also optimal. The period just before anthesis is a very
sensitive period in wheat and photothermal quotient
(radiation/temperature) has a major influence on grain
number and thereby yield (Fischer, 1985). A high photothermal quotient is favourable since high radiation results
in increased photosynthesis whereas low temperature
results in slower development during the critical period
of high radiation. Adjusting phenology by genetically
manipulating development times so that the pre-anthesis
period coincides with a high photothermal quotient is
therefore another way of increasing yield.
Timing may also be important to increase yield and
biomass in relation to water supply. If water is a major
limitation then maximizing growth when conditions are
cool and vapour pressure deficit is low will increase water
use efficiency and biomass production (Richards, 1991).
In the example given earlier of the 2-fold difference in
biomass (observed by Gomez-MacPherson and Richards,
1995), much of the difference was attributed to the greater
water use efficiency achieved by having full canopy cover
whilst vapour pressure deficit was low.
Interception of solar radiation
Early growth of leaf area
Agronomic practices associated with the use of chemical
fertilizers and sowing methods have resulted in major
increases in the interception of solar radiation and to
increased crop photosynthesis. However, genetic selection
has also been important, ever since the domestication of
crops about 10 000 years ago. Then, plants with the
largest seeds were probably selected giving larger seedlings
and thereby more vigorous, larger plants. Also, larger,
leafier young plants may also have been selected that
established more quickly and reduced weed competition.
Selection for both these features would result in more
competitive crops with greater early radiation interception
and faster crop growth rates. Evidence of selection for
these traits are the increase in leaf dimensions and seed
size of domesticated wheats compared with their progenitors ( Evans and Dunstone, 1970).
In the last three or four decades many of the competitive
features of the older, taller varieties have been lost from
breeding programmes as agriculture now relies on sowing
homogeneous shorter varieties at a high density with
adequate fertilizer, water and chemical weed control.
Although non-competitive homogeneous crops are appropriate for high-input agriculture, they are inappropriate
for environments where the crop life cycle is short, such
as where intercropping is practised, and where it is
important to maximize leaf area development to reduce
the loss of valuable soil water by evaporation from the
soil surface. Numerous opportunities exist to increase
light interception genetically during the early development
period of crops. A list of the most important traits to
increase light interception genetically as rapidly as possible in wheat is given in Table 1.
There are 2-fold differences in the early leaf area growth
between temperate cereals (López-Castañeda et al., 1995).
Surprisingly, variation in relative growth rates did not
contribute to these large differences. Similar results have
also been reported for wild and modern accessions of
Breeding for improved yield of cereals 451
Table 1. Traits that may improve establishment and early canopy
development of wheat (adapted from Richards et al., 1999)
Traits are arranged in a ‘loose’ priority order based on their likely
impact on early leaf area development and opportunities to manipulate
them genetically. An assessment of broad sense heritability for the trait
and the expected importance of genotype×environment (G×E ) are
given. Further discussion of these traits and references to them are
given in the text.
Trait
Heritability
G×E
Long coleoptiles
Broad seedling leaves
Embryo size
Specific leaf area
Large coleoptile tiller
Fast emergence
Fast leaf expansion rate
Large grains
Low temperature tolerance
Crown depth
Leaf area ratio
High
High
Intermediate
Intermediate
Intermediate
Low
Intermediate
High
Intermediate
Intermediate
Intermediate
Low
Low
Low
High
High
Low
Low
Low
Low
Intermediate
Low
wheat ( Evans and Dunstone, 1970) and maize (Duncan
and Hesketh, 1968). The most important factor contributing to the differences in leaf area among temperate cereals
was the size of the embryo. Specific leaf area (SLA, ratio
of leaf area to leaf weight) and the speed of germination
were also found to be important (López-Castañeda et al.,
1996). Other traits that contribute to an increased leaf
area in wheat are large grains ( Hadjichristodoulou et al.,
1977; Evans and Bhatt, 1977), a fast rate of leaf expansion
and a shallow crown depth (RA Richards, unpublished
results), the appearance of a coleoptile tiller (Liang and
Richards, 1994), and the absence of the major dwarfing
genes Rht-B1b (Rht1) and Rht-D1b (Rht2) (Richards,
1992b). Despite having a slower growth of leaf area,
wheat cultivars with the gibberellic acid (GA)-insensitive
dwarfing genes are now widespread globally because these
genes are easily identified and selected in breeding programmes and because they reduce lodging. The lodging
resistance allows cultivars with these genes to be grown
with more fertilizer if rainfall or irrigation water is
adequate and these higher inputs have resulted in substantially greater crop yields. The Rht1 and Rht2 genes also
increase the harvest index of wheat without reducing
above-ground biomass, thereby resulting in greater yields.
Similar results have also been found in rice. The slower
leaf area growth in wheat associated with these dwarfing
genes comes about from a delay in emergence (Bush and
Evans, 1988) and from the reduced cell size ( Keyes et al.,
1989). A major consequence of the latter is a short
coleoptile which can result in poor emergence if seeds are
sown deep, sown into stubble, or if pre-emergent herbicides are used (Rebetzke et al., 1998). Semi-dwarf,
GA-sensitive dwarfing genes are available to overcome
these features and these result in better emergence and
early leaf area growth (Rebetzke and Richards, 1999).
Genetic manipulation that results in differential parti-
tioning of assimilates between or within organs is another
way to increase early leaf area and thereby photosynthesis.
A high SLA is one way that barley achieves its early
growth advantage over wheat. Although a higher SLA
also results in a lower assimilation rate because of a likely
reduction in the amount of photosynthetic machinery per
unit leaf area associated with a higher SLA, the increase
in leaf area more than compensates for this reduction in
photosynthesis through greater light interception early in
crop development. Figure 3 shows the decline in net
assimilation rate (NAR) per unit leaf area as SLA
increases in a range of temperate cereal cultivars grown
under the same conditions (NAR=0.136–0.00174 SLA,
r2=−0.51, P<0.01). However, for the same investment
in leaf mass, as is likely, genotypes with a high SLA have
a substantially higher NAR (Fig. 3). Thus, for early
growth stages of cereals a high SLA results in a higher
NAR on a per unit leaf weight basis. In later growth
stages SLA declines in wheat thereby providing an important means for increased photosynthesis per unit leaf area
as canopy closure occurs (Rawson et al., 1987). The
root–shoot ratio (Gomez-Macpherson et al., 1998b) and
a shallow placement of the crown (RA Richards and AG
Condon, unpublished results) may also be amenable to
genetic manipulation to increase above-ground photosynthesis and biomass early in a crop’s development.
After canopy closure other traits become important to
increase photosynthesis and light interception. A high
SLA now becomes a hindrance to photosynthesis ( Fig. 3)
and a high root–shoot ratio may also penalize aboveground growth. A high SLA may not be a problem in
temperate cereals as there is a decline in SLA as the time
to anthesis approaches ( Rawson et al., 1987). Also, more
Fig. 3. The relation between specific leaf area and net assimilation rate
among cultivars of wheat, barley, oats and triticale (closed symbols,
NAR=0.136–0.00174 SLA, R2=−0.51, (C López-Castañeda and RA
Richards, unpublished data). Also shown is the corresponding increase
in net assimilation rate if data were expressed on a unit leaf weight
basis (open symbols).
452 Richards
assimilate may be available for root growth after there is
full light interception.
Canopy architecture also becomes very important once
the leaf area index exceeds 3, particularly in low latitude
environments or where maximum crop growth occurs
during peak summer. There is substantial genetic variation
in leaf posture in cereals and most of the highest yielding
cultivars of maize, rice and wheat already have very erect
leaf canopies late in development. Therefore, the limit for
maximum radiation interception throughout the leaf
canopy in these species may be close.
Duration of leaf photosynthesis
Maintaining green leaf area longer, particularly after
anthesis when there is usually a rapid decline in leaf area
index (LAI ), is another important means to increase total
crop photosynthesis and hence biomass production
through increased or extended light interception. Indeed
a longer duration of leaf photosynthetic activity has
contributed to increased yield in most of our major crops
( Evans, 1993). It has been of particular importance in
maize where genetic differences in photosynthetic duration
have been associated with a longer grain filling duration
and higher yields (Russell, 1991). However, it is difficult
to separate the effects of genetic increases in photosynthetic duration from those due to better nutrition, genetic
resistance to foliar diseases, and differences among genotypes in nitrogen allocation to seeds or increased demand
for photosynthates due to sink strength. An understanding of these relationships in relation to genetic variability
remains limited. Further discussion on genetic variation
in the maintenance of green leaves is given in this volume
( Thomas and Howarth, 2000).
Rate of photosynthesis
The finding that in most species there has been little
change in the rate of leaf photosynthesis per unit area to
accompany the substantial genetic increases in grain yield
is at first surprising. In fact in many species including
wheat, rice, sorghum, soybean, sugarcane, cotton,
Brassica, and sunflower, higher yields have been associated with a decline in the rate of photosynthesis per unit
leaf area relative to that of their progenitors. The absence
of any relationship between rate of leaf photosynthesis
and increases in grain yield is not because there is little
genetic variation in photosynthesis. On the contrary,
significant genetic differences in rates of photosynthesis
per unit leaf area among lines are often reported (for a
comprehensive list see Evans, 1993). Clearly, total crop
photosynthesis can be increased more readily than by
increasing the rate of leaf photosynthesis.
Growth analysis studies using transgenic tobacco plants
with antisense rbcS to decrease Rubisco are interesting
and demonstrate the buffering capacity of processes
important for photosynthesis. It has been shown that
Rubisco can be decreased to about one-half the wild-type
content before the rate of photosynthesis declines providing nitrogen levels are adequate (Quick et al, 1991). Even
when the rate of photosynthesis declines in transgenic
tobacco plants growth may not decline because SLA can
increase and can partly compensate for the decreased rate
of photosynthesis (Fichtner et al., 1993), although this
may vary with light intensity (Stitt et al., 1991).
It is important to consider whether selection for high
rates of leaf photosynthesis could be effective. Selection
in segregating populations is now feasible with portable
apparatus to measure photosynthesis. However, it is
difficult to advocate on a leaf basis because of the many
complications of its measurement and the pleiotropic
effects which may negate the selection progress. The
measurement of photosynthesis is plagued by the problems of integration over the life cycle. Spot measurements,
or even replicated measurements among genotypes may
vary with leaf age, position, leaf surface, time of day,
light intensity, and general plant health and development
stage. Pleiotropic effects include the associations between
photosynthesis, SLA, leaf nitrogen, and ‘sink strength’.
Indeed, selection for rate of leaf photosynthesis, given the
association between SLA and leaf nitrogen, may result in
selecting plants with a high rate of photosynthesis but
with small, thick leaves and a low LAI. Integrative
measurements of photosynthesis can be made using
carbon isotope discrimination of plant material. However,
this is unlikely to be satisfactory as carbon isotope
discrimination measures the relation between stomatal
conductance and photosynthetic capacity. This will be
discussed later. A further problem with the measurement
of photosynthesis is that it provides no information on
whether photosynthate is translocated to the actively
growing tissues.
If genetic increases in the rate of photosynthesis are
made there is no surety that total biomass would be
increased. Sinclair and Horie warn that because the
response curve between rate of photosynthesis and radiation use efficiency (crop biomass/radiant energy) flattens
at high rates of photosynthesis then substantial increases
in rates of photosynthesis would be required to achieve
even modest increases in biomass (Sinclair and Horie,
1989; Day and Chalabi, 1988).
In any consideration given to ways to increase photosynthesis genetically the potential to reduce respiration
and other losses of carbon cannot be ignored. The loss
of carbon by respiration may be as large as the net gain
in carbon by photosynthesis (Amthor, 1989), yet few
serious attempts have been made to reduce this loss. No
clear relationship between respiration and growth and/or
yield has been established. However, in the most comprehensive studies with ryegrass it has been shown that there
Breeding for improved yield of cereals 453
is important genetic variation in respiration rate and it is
highly heritable and related to growth ( Wilson, 1975;
Robson, 1982a). Very large differences in dark respiration
rates are also reported between rye, triticale and wheat
which were related to dry matter accumulation, but were
not associated with photosynthesis ( Winzeler et al., 1989).
There are also substantial losses of carbon from the roots
by sloughing and exudation (Martin and Kemp, 1986)
with some evidence of genetic variation in the proportion
of carbon lost from the roots into the rhizosphere (Martin
and Kemp, 1980). The potential to reduce these losses
deserves further attention.
That genetic changes in the rate of leaf photosynthesis
have not accompanied yield increases in major crops
suggests that either leaf photosynthesis does not limit
grain yield and that crops may have adequate photosynthetic capacity, or that other factors are limiting. A
reserve capacity in photosynthesis is suggested by crop
responses to favourable conditions and photosynthetic
responses to altered sources and sinks. This issue will be
discussed again later. However, a critical question remains
for wheat and many of our grain crops. That is: why has
there been little change in crop biomass production or
total photosynthesis to accompany the large yield
increases achieved through breeding? This question does
not only apply to the last century but to the last 10 000
years of domestication (Austin et al., 1986). The simplest
answer to this question is that in the selection process for
increased yields factors related to harvest index have been
genetically more variable, have had a higher heritability,
and have been more closely associated with yield than
have factors related to biomass. This increase in yield is
often achieved with some sacrifice in photosynthetic area
at anthesis. This highlights the suggestion that photosynthesis does not limit grain yield and that current crops
have sufficient surplus photosynthetic capacity to respond
to increases in yield potential.
To investigate this question more thoroughly it is
instructive to see whether any photosynthetic processes
have changed as yield has increased. Wheat and maize
will be examined as these differ in whether yield increases
are attributed to increases in harvest index or to biomass.
However, before considering these it is also worth considering whether management practices may have been a
substitute for genetic changes in photosynthesis.
Has nitrogen been a surrogate for genetic
increases in photosynthesis?
The lack of any increase in the rate of photosynthesis per
unit leaf area, despite intensive selection for increased
yield over the past century in a range of crops, is
interesting. A possible contributing factor may be that
increased nitrogen fertilizer has been a quick and relatively
inexpensive substitute for genetic increases in total photo-
synthesis. The application of nitrogen fertilizer results in
an increased leaf area, leaf area duration and leaf nitrogen
content, all of which increase photosynthesis per unit
ground area. If breeding trials are conducted under
favourable nutrient conditions, as they usually are, then
there may be little selection pressure for increased photosynthesis as a higher rate of photosynthesis is already
being achieved because of the favourable nutrient status
of the soil. Furthermore, leaf area would develop at its
maximum rate and crop growth rate would be maximized.
Genetic variation in leaf area growth, leaf area duration
or leaf photosynthesis, that may be important for less
optimal conditions, may be masked under these conditions and therefore not selected.
That favourable soil nutrient conditions, particularly
nitrogen, may not expose important variation in rate of
photosynthesis raises several interesting questions. Firstly,
if selection for yield was made under conditions of lower
fertility, would this have exposed important genetic variation and increased photosynthesis? Secondly, since the
nutrient status of growers’ fields are usually less favourable than experimental trials, could there be important
genetic variation in the rate of photosynthesis per unit
leaf area that has not been incorporated into current
varieties?
Traits associated with genetic increases in yield in
wheat and maize
Breeding has been very successful in raising the genetic
yield potential of both wheat and maize. Interestingly,
the increase in wheat has come from an increase in harvest
index whereas above-ground biomass has largely been
associated with the increase in maize ( Figs 1, 2). Several
recent studies have investigated traits associated with the
yield increases achieved with breeding and some photosynthetic processes have been important. It was found
that for wheats bred at CIMMYT Mexico, kernel number,
stomatal conductance, maximum photosynthesis rate, and
carbon isotope discrimination (13C/12C ) were all associated with yield progress ( Fischer et al., 1998). 18O/16O
has also been found to be associated with yield in a
historic set of wheats bred at CIMMYT (Barbour et al.,
2000). Among the photosynthetic characteristics, the correlation with leaf conductance was strongest (Fig. 4). A
similar positive association between yield and carbon
isotope discrimination was also reported (Condon et al.,
1987) in a random group of wheat lines grown in eastern
Australia. However, in the above study (Condon et al.,
1987) the increase in yield per unit increase in discrimination was greater than expected suggesting that genetic
differences in stomatal conductance as well as in leaf area
index were responsible for the variation in yield. The high
13C in leaf tissue results from the high CO concentration
2
in the intercellular spaces of photosynthetic tissue. This
454 Richards
Fig. 4. Relationship between mean grain yield over six years to mean
stomatal conductance (abaxial+adaxial ) over nine measurement
periods in three years for eight wheat cultivars in Mexico. (Data derived
from Sayre et al., 1997; Fischer et al., 1998.)
contrasts with the negative relationship between 13C discrimination and transpiration efficiency ( Farquhar and
Richards, 1984).
It is interesting that a positive relationship between
13C/12C discrimination and yield of grain or biomass
among lines is commonly observed under favourable
conditions. This can arise if the highest yielding genotypes
have a lower assimilation capacity per unit area than the
lowest yielding lines with low discrimination or that lines
with a higher stomatal conductance have the highest
yields. The latter is the favoured interpretation. The
underlying causes of the relationship between stomatal
traits and yield was not determined (study by Fischer
et al., 1998). However, decreased stomatal sensitivity to
vapour pressure deficit or to subtle water stress between
irrigation events, extra cooling particularly at warmer
temperatures, or increased sink strength in newer cultivars
were proposed as possibly contributing to the relationship
between stomatal conductance and yield.
In maize, the greater biomass of newer hybrids compared with older ones is only apparent from the middle
of grain filling. Associated with the biomass increase in
the newer hybrids is a delayed leaf senescence and therefore a longer duration of photosynthesis, continued nitrogen uptake and increased kernel number and kernel
weight (Moll et al., 1994; Rajcan and Tollenaar, 1999a,
b). No differences between the hybrids in their rates of
photosynthesis were found.
Results from data sets comparing varieties released
over different eras have consistently shown that increased
yields are more closely associated with an increased grain
number than an increased grain weight. Similar results
have also been observed among near-isogenic lines
differing in yield (Richards, 1992a; Ortelli et al., 1996a).
There is also a substantial body of evidence showing the
plasticity of photosynthetic processes in crops in response
to source/sink manipulations. This plasticity typically
reflects the tight co-ordination between supply (photosynthesis) and demand (sink size). In general, photosynthetic
rate declines when sinks are reduced, but increases when
sinks are increased (ie demand increases). These responses
can be sustained over long time intervals and at different
times of development. For example, near-isogenic wheat
lines differing in flowering time had an identical relative
growth rate up to heading despite a very different leaf
area index (LAI ). The lines with the lowest LAI compensated by having a high net assimilation rate (rate of
biomass increase per unit leaf area) in two very contrasting
environments (Gomez-Macpherson et al., 1998a, b)
Similar compensations for a reduced leaf area are also
evident after anthesis. In experiments conducted with
both pot and field-grown wheats a substantial response
in photosynthetic activity was noted (measured by
stomatal conductance and 13C/12C of the grain) when leaf
area was manipulated. 13C/12C was measured since it
provides an integrated measure of the balance between
stomatal conductance and photosynthetic capacity during
the grain filling period. When the leaf area of well-watered
plants was halved 5 d after anthesis no reduction in grain
number (expected ) and no reduction in grain weight
(unexpected) was found (Richards, 1996). However, the
13C/12C of grain showed that 13C discrimination increased
by 2‰ compared to control plants, indicating that
stomatal conductance increased substantially relative to
photosynthetic capacity. An increased duration of
stomatal opening could also contribute to this increase.
This capacity for stomatal regulation of photosynthesis
is not inconsistent with the frequent finding of midday
closure of stomates in otherwise well-watered crops and
peak assimilation rates being achieved by midday and a
decline thereafter (Dunin et al. 1989). These results
suggest that in the highest yielding wheats (i) there is
substantial reserve capacity for photosynthesis, (ii) that
crops may be operating below their potential, and (iii)
that crops may have a capacity to respond to the increased
demands of larger sinks.
Further evidence for (iii) above is the increased yield
of irrigated crops grown at high fertility when grain
number is increased. For example, grain number of wheat
was increased by various crowding treatments in field
experiments conducted over three years ( Fischer et al.,
1977). Crowding began at ear peep when there was full
light interception so that no additional light energy was
available. Since irrigated crops rely mostly on postanthesis photosynthesis for grain dry matter, any increase
in yield must come principally from increased photosynthesis. Figure 5 shows the relationship between grain
number and yield as a result of the crowding treatments.
It is evident that crops were able to increase their photosynthesis to match the increased demand by the greater
Breeding for improved yield of cereals 455
Fig. 5. The relation between grain number and grain yield of wheat
where crowding was used to increase grain number. Open symbols
show crowded treatments where leaf area was substantially reduced.
The cluster of points around 15–20×103 grains m−2 are adjacent
control plots managed to maximize grain yield. The regression equation
does not include the treatments to reduce leaf area. See text for further
explanation. (Data adapted from Fischer et al., 1977.)
grain number, although extra photosynthate also came
from stored resources as crowded crops had less soluble
sugars in the stems at maturity. Also shown are two
crowding treatments (open circles) where leaf area was
reduced either by removing the distal half of all leaves or
all leaves below the penultimate leaf. These treatments
show that high yields can still be achieved despite a
substantial reduction in photosynthetic area.
Results from shading and CO fertilization experiments
2
also indicate the importance of ‘sink strength’ of wheat
crops. At Obregon, Mexico, irrigated spring wheat crops
shaded from anthesis through to maturity reduced radiation by 50%; however, yield was only reduced by 10%
(Fischer, 1975). In CO fertilization experiments con2
ducted over three years field crops were exposed to CO 2
enriched air for a 1 month period at either early tillering,
late tillering, stem elongation/spike growth, or grain filling
(Fischer and Aguilar, 1976). Apart from the one month
period of enriched CO crops grew at ambient CO
2
2
concentrations. The largest yield increase came from CO
2
fertilization treatments imposed during late tillering or
the stem elongation period. These treatments also resulted
in the largest increases in grain number. In almost all
treatments grain yield was increased with little reduction
in kernel weight indicating that crop photosynthesis after
flowering, at ambient CO concentrations, responded to
2
the increased demand for carbon by the increased grain
number.
Thus it seems that wheat, at least, is very plastic or
even conservative in its crop photosynthesis as it has
substantial capacity to increase its photosynthesis when
required. It is therefore not surprising that there has been
little change in the rate of leaf photosynthesis to accompany the substantial yield increases. Photosynthesis is
more easily regulated through the control of leaf area
and leaf senescence and through the daily duration and
extent of stomatal opening. These provide a crop with
substantial flexibility. Certainly from an evolutionary
point of view it is sensible for plants to have this spare
capacity for photosynthesis as protection against leaf
herbivory or leaf pathogens. This spare capacity must be
matched with some spare capacity in nitrogen storage or
uptake, particularly if protein storage in the seed is
important. Recent maize hybrids have this ability as they
continue to accumulate N during grain filling (Pan et al.,
1995). There is little information for wheat, although a
genetic association has been shown between increased
root activity and yield mediated through gas exchange
(Ortelli et al., 1996b).
If crop photosynthesis is responsive to increased
demand by the growing grains, via an increased stomatal
conductance as appears evident in wheat and by the
abundant examples in the literature, then this raises
several possibilities to genetically increase yields. Stomatal
traits could be used as an indirect selection criteria for
yield ( Fischer et al., 1998). There is substantial appeal in
this as traits such as canopy temperature and stomatal
conductance can be measured quickly whereas 13C/12C
or 18O/16O, which can also be measured relatively quickly,
can be valuable because they integrate stomatal traits
over time. Stomatal traits are also likely to be useful in
more arid environments where there is irrigation, since
they may have a more direct influence on yield through
both increased leaf photosynthesis as a result of more
open stomata as well as reduced canopy temperature.
Cooler canopies during sensitive reproductive stages in
hot and dry regions may have a significant effect on both
grain set and yield (Amani et al., 1996).
The evidence that crops have surplus capacity for
additional photosynthesis comes principally during the
period of grain filling when grain number has been
established. That is, during grain filling crops are limited
by sink size rather than source. However, evidence from
CO fertilization experiments also suggest that crops are
2
source limited, particularly at the beginning of the stem
elongation phase ( Fischer and Aguilar, 1976; Mulholland
et al., 1997). This phase corresponds to the time when
there is a substantial increase in crop growth rate (Green
et al., 1983) and when stems, leaves, ears, and roots are
all actively growing. Presumably insufficient assimilate is
available to match the demand for growth during this
time. Selection for a high and a sustained stomatal
conductance into the late afternoon during this period
may provide a simple means to select genotypes with a
high rate of leaf photosynthesis and a high yield potential
during this critical period. Indeed, a significant association
was found between stomatal conductance at this stage
and yield in a group of high yielding spring wheats
( Fischer et al., 1998).
456 Richards
It has been argued elsewhere that stomatal traits are
likely to reflect the consequences of an increased sink size
and may not be the causative factors (Richards, 1996).
Nonetheless they may be useful in identifying those
breeding lines with a larger sink size and the greatest
capacity for growth. But in order to target the fundamental process, understanding the determinants of sink
strength should lead to a more focused target for genetic
manipulation to increase both biomass and yield than
will selection for photosynthetic characteristics per se.
Devising ways to increase assimilate supply to meristems
and to selected actively growing tissues deserve attention.
There are several ways this may be achieved. One way is
to divert assimilates away from competing sinks of lesser
importance. A good example which has resulted in
increased yields of many cereals, has been to divert
assimilate used for growing long stems to growing the
grain bearing ears. This has been achieved by the introduction of dwarfing genes. Another example that offers
potential is genetically to inhibit wasteful tillers in cereals.
This diversion of assimilates results in substantially larger
stems and ears in wheat (Atsmon and Jacobs, 1977;
Richards, 1988) and perhaps also contributes to the
success of maize. A second way to increase assimilate
supply to selected organs is to increase their duration of
growth. If the total crop duration cannot be changed this
may need to be at the expense of other less important
organs. An example in wheat is to increase the duration
of the spike growth period to allow more assimilate
supply to the growing florets to reduce the very high rate
of floret abortion just before anthesis (Miralles and
Richards, 1999). There are a number of other economies
where genetic manipulation could reduce investment in
leaf, stem or ear structure which could also free up
assimilate for growth of reproductive organs in cereals.
Other areas of research that may provide opportunities
to capitalize on the apparent plasticity of photosynthesis
are as follows. To investigate what causes grain maturation since if the duration of grain growth could be
extended then grain weight and grain yield should be
increased. The endosperm cell number just after fertilization appears to be important in determining kernel weight
(Brocklehurst, 1977) so that manipulating endosperm cell
number may provide further sink capacity. There is
evidence that the nitrogen content of the spike at anthesis
is an important determinant of grain number (Abbate
et al., 1995; van Herwaarden, 1995) and may be a
determinant of floret survival. There is little understanding
of the cause of senescence of photosynthetic tissue.
Maintenance of this tissue and maintenance of root
activity after anthesis to allow continued nitrogen uptake
would extend the carbon and nitrogen supply period as
well as overcoming the trade-off between nitrogen remobilization and senescence.
The above characteristics can be genetically manip-
ulated using conventional approaches, although screening
methods may not yet be available. Molecular biology will
also offer further insights and new opportunities.
Molecular approaches to regulating the metabolism and
transport of sugar and nitrogen and the regulation of
meristematic regions offer exciting opportunities to
increase growth of the reproductive organs. If this can be
achieved it is expected that increased photosynthesis and
yield will follow.
Conclusions
Evidence from our most intensively bred crops such as
wheat and maize suggests that, except for a period just
before anthesis, photosynthate production is not limiting
and crops have a reserve capacity for photosynthesis
under favourable conditions. This may account for the
near doubling of the genetic yield potential during this
century without any change in the rate of photosynthesis
per unit leaf area. It is proposed that significant opportunities remain to improve total photosynthesis. The most
likely way, apart from an increased crop duration, is by
achieving canopy closure more quickly through increasing
vigour at the beginning of the season. Then, to increase
partitioning of carbon and nitrogen to reproductive meristems to establish a high number of fertile florets with a
potential for a large grain size. There is evidence that
there is a shortage of photosynthate during stem elongation and selection for a high and sustained stomatal
conductance offers potential to reduce this shortage
through breeding. Once past this bottleneck it is expected
that more crop photosynthesis will follow either by a
longer daily duration of photosynthesis or by an extension
of the leaf area duration during the grain filling period.
In the search for the underlying means through which
yield can be increased, the importance of direct selection
for yield (or biomass) should not be neglected. Direct
selection has been responsible for the spectacular genetic
gains that have been achieved in most crops (in many
crops it has been about 1% per year). There is no strong
evidence to suggest that yields are plateauing so it is likely
that direct selection for yield will continue to be successful
and remain the cornerstone of crop improvement.
However, a search for underlying mechanisms that may
be responsible for variation in yield must continue as the
knowledge gained will provide opportunities for achieving
faster genetic gains. Also, the identification of limiting
factors, and then direct selection to reduce them, may
result in the incorporation of new and important genetic
variation into breeding programmes. This may have the
added advantage that the traits may be less prone to
genotype×environment interactions, and have a higher
heritability than yield itself; it may also be possible to
select for the traits out of season, in earlier generations,
and more easily, so that yield grains will be hastened.
Breeding for improved yield of cereals 457
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