Photosynthesis, grain yield and N utilization in rice and wheat Amane Makino

17 Pages·2010·0.18 MB·English

Plant Physiology Preview. Published on October 19, 2010, as DOI:10.1104/pp.110.165076
Photosynthesis, grain yield and N utilization in rice and wheat

Amane Makino

Corresponding author: Amane Makino
Graduate School of Agricultural Science, Tohoku University, 1-1
Tsutsumidori-Amamiyamachi, Aoba-ku, Sendai 981-8555, Japan
E-mail: [email protected]
Tel: [phone] / Fax: [phone]
Journal Research Area: Updates

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Copyright 2010 by the American Society of Plant Biologists
This work was supported by a grant from the Ministry of Agriculture, Forestry and
Fisheries of Japan (Genomics for Agricultural Innovation, GPN-0007) and Research in a
Proposed Research Area (Planned Research No. 21114006) from the Ministry of
Education, Culture, Sports, Science and Technology.
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Rice (Oryza sativa L.) and wheat (Triticum aestivum L.) 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 while wheat tends to be grown in cooler
temperate climates. However, both crops have been bred in similar directions. For
example, the introduction of semi-dwarf 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 semi-dwarf cultivars can use large inputs of 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 paper, 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 C photosynthesis was discovered in
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1960s, this expectation rose. For example, the high rates of C photosynthesis in maize
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and sugarcane were always associated with greater productivity than C crops. On the
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other hand, a lack of correlation between photosynthesis and plant yield has been
frequently observed when different genotypes of a crop are compared (for rice, Takano
and Tsunoda 1971; for wheat, Evans and Dunstone 1970). This is also true because
modern cultivars have been bred for various traits besides photosynthesis. Since many
recent studies on elevated [CO ] experiments show a close relationship between
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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 C crops.
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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 C species. Evans (1989) found that rice and wheat
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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 CO -fixation enzyme, and the amount and kinetic properties of
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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 CO diffusion resistance differ
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greatly between rice and wheat.
Rice allocates 25-30% of leaf N to Rubisco with higher affinity for CO (20%
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lower K for CO ) than wheat, whereas wheat allocates 20-25% of leaf N to Rubisco with
m 2
greater k (50% higher V for carboxylation) than rice (Makino et al. 1988). The
cat max
CO /O specificity for carboxylation and oxygenation does not differ between two species.
2 2
The solubility of CO in water decreases at higher temperatures. Coupled with this, the
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present low atmospheric CO levels enhance photorespiration at elevated temperatures.
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Therefore, selection pressure for Rubisco with higher affinity for CO may be imposed
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on rice which originates in warm and hot regions. In contrast, since the CO solubility in
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water increases at low temperatures, the Rubisco k may be more important in wheat
cat
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 CO levels is higher in rice above
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30ºC, but higher in wheat below 25ºC when both species have similar leaf N
concentrations (Nagai and Makino 2009). Since the difference in k between wheat and
cat
rice is greater than the difference in K (CO ) and since Rubisco strongly limits
m 2
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 higher
k was observed only for a CC-genome variety among Oryza species (Makino et al.
cat
1987), suggesting that Rubisco kinetic properties cannot be targeted for conventional
crossbreeding among cultivars. Similarly, in the Triticum genus, the variation in the k
cat
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 k than that from T. monococcum. Higher k was
cat cat
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, 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
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species including rice and wheat.

Difference in CO Diffusion in a Leaf between Rice and Wheat
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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 CO partial
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pressure by 30% in general under high irradiance conditions (von Caemmerer and
Evans 1991). Furthermore, as a result of this resistance to CO diffusion, the decrease
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in stromal CO partial pressure becomes more severe with increasing leaf-N content. In
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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 condictance is also affected by membrane permeability as a function of
aquaporin density (Hanba et al. 2004). Unfortunately, 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
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increase with increasing N application (Chonan 1970). Consistent with these
anatomical data, direct measurement of mesophyll conductance using carbon isotope
discrimination during CO uptake showed that rice had a greater conductance than
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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 CO diffusion into
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the stroma and the refixation of photorespired CO to thrive in hot environments where
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photorespiration is stimulated (Sage and Sage 2009).

Improvements in Photosynthesis
Improving photosynthesis is of greatest agronomic importance as the most
plausible route towards 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 wheat type photosynthetic system
could be expressed in rice, canopy carbon gain would be appreciably increased in cool
climates such as northern regions in Japan and 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,
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engineering C photosynthesis may not necessarily be suitable in some points. Rice has
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greater Rubisco content of the low K (CO )/low k form (Makino et al. 1988). In
m 2 cat
addition, rice mesophyll cells are specialized to effectively scavenge photorespired CO
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(Sage and Sage 2009). These characteristics are incompatible with engineering C
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photosynthesis. Another important adaptation will be to the steadily elevating
atmospheric CO concentration. Elevating CO may be more effective for wheat than for
2 2
rice because of wheat’s higher Km(CO )/high kcat form and lower N allocation to
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Rubisco. Some elevated CO experiments show that stimulation of photosynthesis is
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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 [CO ]
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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 CO
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concentrations shows higher rates of photosynthesis only under conditions of elevated
CO (Makino et al. 1997). This construction may be one of the model crops that perform
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better under low-N input conditions in near future high-CO environments.
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CROP YIELD
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
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number and size (Fisher 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 correlation between grain number and size is frequently observed (Fisher
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, 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 semi-dwarf indica rice genotypes than in japonica rice genotypes. Since semi-dwarf
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 semi-dwarf indica rice genotype increases grain number by more than 40% in a
japonica rice genotype. In addition, the introduction of semi-dwarf 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 semi-dwarf
genotypes may show a large increase in harvest index, defined as the ratio of grain mass
to total above ground 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
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(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 relationship in itself is mainly caused by light-use limitation due to an
excess leaf area which causes self-shading 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 today’s high-yielding cultivars.
Grain mass in the modern high-yielding rice and wheat has reached about 60%
of the total biomass above ground at harvest (Evans 1997, Long et al. 2006b, see Akita
63 in Fig. 2B and 2C). 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.

ACKNOWLEGDGEMENTS
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