Update on Photosynthesis and Yield

Photosynthesis, Grain Yield, and Nitrogen Utilization in

Rice and Wheat1
Amane Makino*
Graduate School of Agricultural Science, Tohoku University, Sendai 9818555, Japan

Rice (Oryza sativa) and wheat (Triticum aestivum) are

the two most commercially important crops, accounting for more than 40% of global food production. They
were domesticated in different climates and differ
largely in their growth environments: Rice is tropically
cultivated in hot, wet climates, whereas wheat tends to
be grown in cooler temperate climates. However, both
crops have been bred in similar directions. For example, the introduction of semidwarf traits into rice and
wheat from Chinese and Japanese varieties in the
1960s made a great contribution to increasing yield in
both species (Evans, 1997). Since the semidwarf cultivars can use large inputs of nitrogen (N) fertilizer
without lodging, the introduction of dwarfing genes
allowed the production of varieties with high leaf N
content and enhanced sink capacity. Large inputs of
N fertilizer in turn have drawn much attention to
the environmental impact of N fertilization practices
(Cassman et al., 1998). Therefore, it is important for us
to increase the grain yield while limiting the environmental impact of agriculture. To achieve these conflicting goals, we must first consider the improvement
of both photosynthesis and grain yield for a given crop
N content. In this article, I will briefly review photosynthetic performance and yield in rice and wheat in
relation to N utilization.

LEAF PHOTOSYNTHESIS
Photosynthesis, Biomass, and Yield in Crops

More than 90% of crop biomass is derived from

photosynthetic products. Therefore, many crop scientists have believed that enhancing photosynthesis
at the level of the single leaf would increase yields.
When C4 photosynthesis was discovered in 1960s, this
expectation rose. For example, the high rates of C4
photosynthesis in maize (Zea mays) and sugarcane
(Saccharum officinarum) were always associated with
greater productivity than C3 crops. On the other hand,
a lack of correlation between photosynthesis and plant
1
This work was supported by a grant from the Ministry of
Agriculture, Forestry and Fisheries of Japan (Genomics for Agricultural Innovation; grant no. GPN0007) and Research in a Proposed
Research Area (Planned Research no. 21114006) from the Ministry of
Education, Culture, Sports, Science and Technology.
* E-mail makino@biochem.tohoku.ac.jp.
www.plantphysiol.org/cgi/doi/10.1104/pp.110.165076

yield has been frequently observed when different

genotypes of a crop are compared (for wheat, Evans
and Dunstone, 1970; for rice, Takano and Tsunoda,
1971). This is also true because modern cultivars have
been bred for various traits besides photosynthesis.
Since many recent studies on elevated [CO2] experiments show a close relationship between enhanced
photosynthesis, biomass, and yield, this suggests that
increasing photosynthesis increases yield when other
genetic factors are not altered (Long et al., 2006b). In
addition, Murata (1981) reviewed the relationship
between potential leaf photosynthesis and maximal
crop growth rate of many crops and found a highly
positive correlation between them. This also indicates
that photosynthesis at the single-leaf level can be an
important factor for potential biomass production. At
the same time, he found that rice and wheat had
higher photosynthesis than other C3 crops.
Difference in Rubisco Properties between Rice
and Wheat

Since photosynthetic capacity is closely related to

leaf N content, higher photosynthesis in rice and
wheat may be the result of breeding for cultivars
with higher leaf N content depending on heavy N
fertilization. When light-saturated photosynthesis in
air is plotted against leaf N content (both expressed
per unit of leaf area), however, a great deal of variation
exists among C3 species. Evans (1989) found that rice
and wheat show the highest rates of photosynthesis
per unit of leaf N content, up to 10 times higher than
some evergreen trees (Fig. 1). This variation is also
evident in the data when expressed on a dry weight
basis. Such higher rates of photosynthesis in both
crops may be caused by greater N allocation to
Rubisco (Makino et al., 1992) and higher mesophyll
conductance (von Caemmerer and Evans, 1991) compared to other plants. Rubisco is the primary CO2
fixation enzyme, and the amount and kinetic properties of this enzyme strongly affect the photosynthetic
rate. In addition, Rubisco has a low rate of catalysis,
and therefore a great deal of N is invested in Rubisco
protein. However, both the amount and properties of
Rubisco and the CO2 diffusion resistance differ greatly
between rice and wheat.
Rice allocates 25% to 30% of leaf N to Rubisco with
higher affinity for CO2 (20% lower Km for CO2) than

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125

Makino

Figure 1. Light-saturated rate of CO2 assimilation in air versus leaf N

content, both expressed per unit leaf area. :, Wheat; s, rice; black
and white squares, Raphanus raphanistrum; n, Death valley annuals;
h, Illinois annuals; d, Alocasia macrorrhiza; n, Lepechinia calycina;
), Californian evergreen trees and shrubs and rainforest trees; ,, South
Africa shrubs; , Prunus ilicifolia. Reprint from Evans (1989).

wheat, whereas wheat allocates 20% to 25% of leaf N to

Rubisco with greater kcat (50% higher Vmax for carboxylation) than rice (Makino et al., 1988). The CO2/O2
specificity for carboxylation and oxygenation does not
differ between the two species. The solubility of CO2 in
water decreases at higher temperatures. Coupled with
this, the present low atmospheric CO2 levels enhance
photorespiration at elevated temperatures. Therefore,
selection pressure for Rubisco with higher affinity for
CO2 may be imposed on rice that originates in warm
and hot regions. In contrast, since the CO2 solubility in
water increases at low temperatures, the Rubisco kcat
may be more important in wheat grown in cool environments. Thus, Rubiscos from both species may
have evolved to improve plant performance in their
typical habitats, respectively. Actually, light-saturated
photosynthesis measured at present CO2 levels is
higher in rice above 30C but higher in wheat below
25C when both species have similar leaf N concentrations (Nagai and Makino, 2009). Since the difference
in kcat between wheat and rice is greater than the difference in Km(CO2) and since Rubisco strongly limits
photosynthesis at cool temperatures (Makino and Sage,
2007), at cool temperatures the rate in wheat is considerably higher than in rice.
No variability in the kinetic properties of Rubisco
has been found among rice varieties, including old
and modern cultivars (Makino et al., 1987). Significant
126

higher kcat was observed only for a C-type genome

variety among Oryza species (Makino et al., 1987),
suggesting that Rubisco kinetic properties cannot be
targeted for conventional crossbreeding among cultivars. Similarly, in the Triticum genus, the variation in
the kcat for a main cultivar of wheat, T. aestivum, is not
significant, whereas there are some differences correlated with the genome constitution in the Triticum and
Aegilops species (Evans and Austin, 1986). Additionally, Evans and Austin (1986) found that Rubisco from
T. aestivum has a higher kcat than that from Triticum
monococcum. Higher kcat was associated with possession of the B-type cytoplasm genome, which encodes
the large subunit of Rubisco. Although the large
subunit is more conserved than the small subunit,
the results by Evans and Austin suggested that the
RbcL gene can be targeted for an improvement in
photosynthesis. Recent technology for plastid transformation, at least with tobacco (Nicotiana tabacum),
enables more precise manipulation and replacement of
Rubisco. For example, introduction of a gene into the
chloroplast linking both the large and small subunits
of Rubisco led to successful assembly of a novel
holoenzyme (Whitney et al., 2009). Such plastid transformation provides a transplastomic tobacco with a
foreign Rubisco with large and small subunits derived
from different higher plants. However, plastid transformation techniques have still not been developed for
the major crop species including rice and wheat.
Difference in CO2 Diffusion in a Leaf between Rice
and Wheat

Rice and wheat allocate different amounts of N to

Rubisco in response to an N supply (Evans, 1989;
Makino et al., 1992). With increasing N supply, rice
allocates an increasing proportion of N to Rubisco. By
contrast, wheat allocates a constant proportion of N to
Rubisco. To maintain the balance between the in vivo
capacities of Rubisco and other photosynthetic processes, a greater increase in Rubisco content in rice
may be required to offset changes in mesophyll conductance (Evans and Terashima, 1988). Mesophyll
conductance in leaves is estimated to decrease the
stromal CO2 partial pressure by 30% in general under
high irradiance conditions (von Caemmerer and
Evans, 1991). Furthermore, as a result of this resistance
to CO2 diffusion, the decrease in stromal CO2 partial
pressure becomes more severe with increasing leaf N
content. In wheat, an exponential increase in the
carbonic anhydrase activity was observed with increasing leaf N content (Makino et al., 1992). Although
there is little direct evidence for contribution of carbonic anhydrase to mesophyll conductance, these
differential responses of Rubisco and carbonic anhydrase between rice and wheat might be related to the
in vivo balance between Rubisco and other factors
limiting photosynthesis. Mesophyll conductance is
also affected by membrane permeability as a function
of aquaporin density (Hanba et al., 2004). Unfortu-

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Photosynthesis and Yield

nately, there is no available data on the response of this

factor to leaf N content.
Mesophyll conductance is closely related to the
surface area of chloroplasts exposed to the intercellular air spaces (Evans and Loreto, 2000; Terashima et al.,
2006). Chloroplast surface area is strongly dependent
on the total mesophyll cell area, and both of these are
higher in rice than in wheat. For example, chloroplasts
including stromules cover more than 95% of the mesophyll cell periphery in rice (Sage and Sage, 2009)
whereas the exposed surface area of the chloroplast in
wheat was estimated to be 76% (Evans and Loreto,
2000). The ratio of total surface area of mesophyll cell
to leaf area in rice ranges from 23 to 44, while the
values in wheat are between 8 and 24 (von Caemmerer
and Evans, 1991). In rice, both this area ratio and
intercellular air spaces increase with increasing N
application (Chonan, 1970). Consistent with these anatomical data, direct measurement of mesophyll conductance using carbon isotope discrimination during
CO2 uptake showed that rice had a greater conductance
than wheat, which increased with increasing leaf N
content (von Caemmerer and Evans, 1991). Additionally, mitochondria and peroxisomes are confined to the
interior regions of the cytoplasm and encapsulated by
the chloroplasts and stromules in rice, whereas they are
pressed against the cell periphery by the large vacuole
in wheat (Sage and Sage, 2009). Thus, rice mesophyll
cells are specialized to maximize both the CO2 diffusion into the stroma and the refixation of photorespired
CO2 to thrive in hot environments where photorespiration is stimulated (Sage and Sage, 2009).

China. The replacement of wheat Rubisco with a high

kcat form may be effective. As described above, since
the photosynthetic system of rice may have evolved to
adapt to warm and hot environments, engineering C4
photosynthesis may not necessarily be suitable in
some points. Rice has greater Rubisco content of the
low Km(CO2)/low kcat form (Makino et al., 1988). In
addition, rice mesophyll cells are specialized to effectively scavenge photorespired CO2 (Sage and Sage,
2009). These characteristics are incompatible with engineering C4 photosynthesis. Another important adaptation will be to the steadily elevating atmospheric
CO2 concentration. Elevating CO2 may be more effective for wheat than for rice because of wheats higher
Km(CO2)/high kcat form and lower N allocation to
Rubisco. Some elevated CO2 experiments show that
stimulation of photosynthesis is greater in wheat than
in rice (Long et al., 2006a). Furthermore, Rubisco
content in both species exceeds the level necessary
for maximal photosynthesis in elevated [CO2] environments (for rice, Makino et al., 1997; for wheat,
Theobald et al., 1998). Since large amounts of N are
invested in Rubisco, an attempt to decrease N allocation
to Rubisco may lead to the improvement in photosynthesis per unit of leaf N content. In fact, antisense RBCS
rice with theoretically optimal Rubisco content at elevated CO2 concentrations shows higher rates of photosynthesis only under conditions of elevated CO2
(Makino et al., 1997). This construction may be one of
the model crops that perform better under low N input
conditions in near future high CO2 environments.
CROP YIELD

Improvements in Photosynthesis

Improving photosynthesis is of greatest agronomic

importance as the most plausible route toward enhanced biomass production. Although no genetic differences in Rubisco properties are evident, a great deal
of apparently genetically controlled variation in stomatal conductance has been recently observed for a
given leaf N content or for a given rate of photosynthesis in rice cultivars (Hirasawa et al., 2010). Such
variation may provide a starting point for breeding
approaches to improve photosynthesis. Improving
photosynthetic adaptation to environmental conditions is also another agronomic goal. For example,
the success of the northwards extension of rice cultivation was the result of breeding for cool tolerance
(Nishiyama, 1993) and the loss of photoperiod sensitivity (Izawa, 2007). No attempt has been made to
adapt potential photosynthesis to cool environments.
Photosynthetic efficiency and biomass productivity in
rice largely decreased at cool temperatures (Nagai and
Makino, 2009), and rice yield in northern regions of
Japan is limited by low biomass accumulation in cool
climates between spring and early summer. If a wheattype photosynthetic system could be expressed in rice,
canopy carbon gain would be appreciably increased in
cool climates such as northern regions in Japan and

Historical increases in cereal yield have depended

on large inputs of N fertilizer. Cereal yield is determined by grain numbers per unit land area, grain
weight, and the proportion of grains that fill. In rice,
since single grain weight is genetically constant irrespective of N application and growth environments
(Yoshida, 1981), yield is simply determined by the
product of the two elements: grain number and the
ratio of filled grains, both of which are affected by N
application. Although a negative correlation between
them is frequently observed when the yield target is
high (Matsushima, 1993), in many cases rice yield is
limited by the grain number (Yoshida, 1981; Yoshida
et al., 2006). Therefore, the important issue for achieving a high yield in rice is enhancing the grain number
with a high proportion of ripened grains. In wheat,
however, since single grain weight varies depending
on growth conditions, yield is affected by both the
grain number and size (Fisher et al., 1977; Jamieson
et al., 1995). Thus, the targets for a high yield may be
more complicated in wheat than in rice.
Grain number in both crops is linearly correlated
with total plant N content. This is because N is an
important resource, both limiting yield and contributing to the determination of grain number (Sinclair and
Jamieson, 2006). In wheat, however, since a negative

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Makino

correlation between grain number and size is frequently observed (Fisher et al., 1977), the correlation
between grain number and total N accumulation in
crop may differ among varieties and growth conditions. On the other hand, the correlation between grain
number and total N in rice has been observed to be
independent of variety and growth conditions (Wada
and Matsushima, 1962; see Fig. 2A). In the study by
Wada and Matsushima (1962), N uptake by the plants
depending on growth conditions until the time of
heading determined the grain number, irrespective of
variety. However, since these results were based on
japonica rice cultivars and a limited variety of growth
conditions, some attention has been paid to investigate
whether genotypic differences in the grain number
exist for a given N accumulation (Horie et al., 1997).
Recently, Yoshida et al. (2006) reported that the grain
number per unit of plant N content is clearly higher in
semidwarf indica rice genotypes than in japonica rice
genotypes. Since semidwarf indica rice genotypes preferentially tend to differentiate grains on secondary
and tertiary rachis branches (Yoshida et al., 2006),
these traits may be governed by the indica Gn1 allele
that increases grain number (Ashikari et al., 2005). The
Gn1 allele from a semidwarf indica rice genotype
increases grain number by more than 40% in a japonica
rice genotype. In addition, the introduction of semidwarf traits into indica rice genotypes has led to a
typical success for high yielding. In genotypes with a
large grain sink, the introduction of the dwarfing gene
means that assimilates formerly needed for stem
growth are effectively used in grain development.
Therefore, such semidwarf genotypes may show a
large increase in harvest index, defined as the ratio of
grain mass to total aboveground biomass at harvest
(Evans, 1997; Sinclair, 1998).
For japonica rice genotypes, a new type of high-yielding and large-grain cultivar, Akita 63 has been released
(Mae et al., 2006). While the grain number of this cultivar
did not differ from the common japonica cultivars at any
given plant N content (Fig. 2A; as pointed out by Wada
and Matsushima, 1962), the single grain weight was
about 35% larger. Since single grain weight is genetically
constant in rice, such a large grain size without reducing
the grain number directly enhances the sink capacity,
and the amount of N required for achieving a sink
capacity necessary for a high yield was less than in the
common cultivar. Consequently, this cultivar showed
high yield for a given crop N content (Fig. 2B).
For these high-yielding cultivars, however, a decline
in the ratio of filled grains is frequently observed when
grown with heavy N application (Matsushima, 1993;
Mae et al., 2006). This may be because source capacity
has not been improved whereas the grain sink has been
successfully enlarged with N application. For example,
when the relationships between grain number, biomass,
and crop N content at harvest are examined, the grain
number increases linearly with increasing total crop N
content passing through the origin whereas total biomass increases curvilinearly (Fig. 2). The curvilinear
128

Figure 2. Grain numbers, yield (rough rice), and total biomass aboveground versus total crop N content per unit of land area at harvest
in japonica rice cultivars. Red circles, Akita 63 in 2000; red triangles,
in 2001; red squares, in 2009; blue squares, Yukigesyou in 2000;
blue triangles, Toyonishiki in 2001; purple diamonds, Akitakomachi in
2000; green circles, Akita 39 in 2009. The single grain weight of Akita
63 was 35% larger than that of other cultivars. Therefore, Akita 63
showed higher yield for a given crop N content. Some data are reproduced from Mae et al. (2006).

relationship in itself is mainly caused by light use

limitation due to an excess leaf area that causes selfshading under conditions of high N application. However, the results in Figure 2 indicate that source capacity
limits the yield potential of current high-yielding cultivars when the yield target is high. This means that
further improvement in sink capacity is no longer effective and improving photosynthesis and biomass production is the only remaining target for any further increase
in the yield potential of todays high-yielding cultivars.
Grain mass in the modern high-yielding rice and
wheat has reached about 60% of the total biomass

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Photosynthesis and Yield

aboveground at harvest (Evans, 1997; Long et al.,

2006b; see Akita 63 in Fig. 2, B and C). This is the
highest in all cereal crops. Although it is not apparent
whether further increase in the harvest index is feasible (Miura et al., 2010), to substantially enhance yield
in both crops will be difficult unless source capacity
including photosynthesis is improved by genetic engineering. In addition, since improving source capacity could lead to a decrease in the amount of N
required for a high yield, it will reduce the environmental impact of agriculture.
ACKNOWLEDGMENTS
I thank Drs. Tadahiko Mae, Thomas R. Sinclair, and Louis Irving for
valuable discussion and comments on the manuscript.
Received August 31, 2010; accepted October 17, 2010; published October
19, 2010.

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