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Redesigning rice photosynthesis to increase yieldREDESIGNING RICE PHOTOSYNTHESIS TO INCREASE YIELD Proceedings of a Workshop, 30 Nov.-3 Dec. 1999, Los Baños, Laguna, Philippines Edited by J. Sheehy, P. Mitchell, and B. Hardy The contribution of rice research to poverty alleviation David Dawe Rice is the dominant staple food of Asia, accounting for more than 70% of caloric intake in some countries. Furthermore, Asia is home to approximately 70% of the world's 1.3 billion poor, and the most severe malnutrition in the world occurs in South Asia. These considerations mean that rice research has a key role to play in global poverty alleviation. Rice research contributes to poverty alleviation through several pathways, and these contributions benefit both producers and consumers. The direct pathway leads to higher productivity and higher profits for farmers. The indirect pathway arises from the lower prices for consumers that are the inevitable result of higher farm productivity for any given level of demand. In the short run, lower prices for consumers reduce poverty because many poor people (the urban poor, the rural landless, and nonrice farmers) are net buyers of rice, and lower prices increase their effective incomes. In the long run, lower prices for consumers reduce the cost to employers of hiring workers (without sacrificing any welfare on the part of those workers). This stimulates job creation in the higher productivity industrial and service sectors of the economy, and eventually draws labor out of agriculture. This structural transformation of the economy is essential for long-term poverty alleviation. In fact, no country has ever become wealthy without removing a significant fraction of its labor force from the agricultural sector. After the initial success of the Green Revolution, rice yields have stagnated or grown slowly in many countries, and this slow growth retards the process of poverty alleviation. Creation of a C4 rice plant has the potential to generate substantially higher farm yields and make an important contribution to global poverty alleviation efforts. Future intensification of irrigated rice systems Achim Dobermann By 2020, average irrigated rice yields must rise by 30% to about 7 t ha- 1. This increase appears achievable, but requires that improved germplasm with a yield potential of 12 t ha-1 in the dry season and 8-9 t ha-1 in the wet season become available within the next 10 years. Moreover, significant improvements in soil and crop management are necessary, particularly nutrient and pest management, to lift average farm yields to about 70% of the yield potential. All this must be achieved in an environment where changes in crop management practices will occur, mainly triggered and driven by socioeconomic changes and competition for natural and human resources. Beyond 2020, further yield increases will probably require germplasm with greater radiation-use efficiency approaching that of plants with C4 photosynthesis. Gerald E. Edwards, Olavi Kiirats, Agu Laisk, and Thomas W. Okita CO2-concentrating mechanisms in photosynthetic organisms have in common a requirement for energy (ATP) and investment in proteins (enzymes/transporters). This investment can benefit the plant with a sufficient increase in the supply of CO2 to Rubisco under CO2-limited photosynthesis. The effectiveness of the CO2-concentrating mechanism in a C4 plant is discussed with respect to overcycling by the C4 pathway, the energetics of photorespiration, and CO2 diffusive resistance between Rubisco and phosphoenolpyruvate carboxylase. Comparisons of the minimum calculated quantum requirement for CO2 fixation at different intercellular levels of CO2 for a C4 plant (with variable overcycling and bundle sheath resistance) versus C3 photosynthesis illustrate when C4 photosynthesis may be of benefit as well as constraints in engineering C4 photosynthesis into C3 plants. Conditions in which photosynthesis is CO2-limited and conditions where rice may benefit from a CO2-concentrating mechanism are discussed. Would C4 rice produce more biomass than C3 rice? John R. Evans and Susanne von Caemmerer Evidence suggests that C4 plants produce greater amounts of biomass per unit of intercepted photosynthetically active radiation. This is due in large part to two factors. First, C4 plants have a greater quantum yield than C3 plants at 30 ° C (the C4 advantage diminishes at lower temperatures and as atmospheric CO2 partial pressures rise). Second, C4 plants have greater rates of CO2 assimilation per unit leaf nitrogen (this benefit diminishes as leaf area index and/or canopy nitrogen content increases). The protein cost of C4 enzymes per unit chlorophyll is calculated and found to be similar to that of C3 photosynthesis. However, the rate of CO2 assimilation per unit nitrogen in C4 plants is greater than that of C3 plants because high CO2 partial pressure in the bundle sheath cells enables Rubisco to operate near its maximum catalytic rate and suppresses photorespiration. Rice leaf anatomy is examined with respect to locating the C4 metabolism. Chloroplasts in bundle sheath cells represent only a minute fraction of those present in the rice leaf. In addition, whereas mesophyll cells are immediately adjacent to bundle sheath cells in terrestrial C4 leaves, there are numerous mesophyll cells between adjacent veins in rice, which would diminish the efficiency of the C4 cycle. To engineer the C4 pathway into rice is therefore a formidable challenge. C4 photosynthesis in rice: some lessons from studies of C3 photosynthesis in field-grown rice Peter Horton and Erik H. Murchie The sites of limitations on photosynthesis in rice are reviewed for the purpose of developing a strategy to bring about an increase in yield. On the basis of measurements made on irrigated rice under tropical conditions, the sites of real and potential photosynthetic losses are identified. It was found that rice was not optimally adapted for photosynthesis under high irradiance, with light saturation of upper leaves and midmorning depressions of photosynthetic capacity. The limitation of photosynthetic capacity may occur because of the combined effects of developmental programming and incomplete acclimation to high irradiance. Some rice varieties appear to have Rubisco levels well in excess of those required to support measured photosynthetic rates, suggesting its role as a store of leaf N. The important interaction between photosynthetic capacity and the mobilization of Rubisco as a source of leaf N for grain development is discussed. These findings are considered in the context of the introduction of C4 photosynthesis into rice. In this regard, the implications of the increased ATP/NADPH requirement of C4 photosynthesis are also assessed in terms of electron transport. Strategies for increasing the yield potential of rice Gurdev S. Khush Rice is the most important food crop in the world. Major advances have occurred in rice production as a result of the wide-scale adoption of improved rice varieties. However, demand for rice in low-income countries continues to increase because of increases in the population of rice consumers and improvements in living standards. It is estimated that we will have to produce 50% more rice by 2025. To meet this challenge, we need rice varieties with higher yield potential. Several approaches are being employed for developing rice varieties with increased yield potential. These include population improvement, ideotype breeding, heterosis breeding, wide hybridization, genetic engineering, and molecular breeding. Photosynthetic performance of transgenic rice plants overexpressing maize C4 photosynthesis enzymes Maurice S.B. Ku, Dongha Cho, Ujwala Ranade, Tsui-Ping Hsu, Xia Li, De-Mao Jiao, Jim Ehleringer, Mitsue Miyao, and Makoto Matsuoka Transgenic rice plants overexpressing maize C4-specific phosphoenolpyruvate carboxylase (PEPC) exhibit a higher photosynthetic rate (up to 30%) and a more reduced O2 inhibition of photosynthesis than untransformed plants. There is a small increase in the amount of atmospheric CO2 being directly fixed by PEPC. Similarly, transgenic rice plants overexpressing the maize chloroplastic pyruvate, orthophosphate dikinase (PPDK), also have higher photosynthetic rates (up to 35%) than untransformed plants. This increased photosynthetic capacity is at least in part due to an enhanced stomatal conductance and a higher internal CO2 concentration. Using conventional hybridization, we have integrated maize PEPC and PPDK genes into the same transgenic rice plants. In the segregating population, the photosynthetic rates of plants with high levels of both maize enzymes are up to 35% higher than those of untransformed plants. Under full-sunlight conditions, the photosynthetic capacity of field-grown PEPC transgenic rice plants is twice as high as that of untransformed plants. PEPC transgenic plants consistently have a higher photosynthetic quantum yield by photosystem II and a higher capacity to dissipate excess energy photochemically and nonphotochemically. Preliminary data from field tests show that the grain yield is about 10-30% higher in PEPC and 30-35% higher in PPDK transgenic rice plants relative to untransformed plants. Taken together, these results suggest that introduction of C4 photosynthesis enzymes into rice has a good potential for enhancing the crop's photosynthetic capacity and yield. Overcoming barriers: CO2-concentrating mechanisms and C4 metabolism in relation to transport Richard C. Leegood The essential features of CO2-concentrating mechanisms in C4 plants, algae, and cyanobacteria; in the single cell CO2-concentrating mechanism found in the aquatic macrophyte Hydrilla verticillata; and in the simplest CO2-salvaging mechanism found in C3-C4 intermediates are discussed. Some of the key structural and metabolic aspects that appear to be essential for the operation of C4 photosynthesis or that are very specialized features in C4 plants are discussed, including anatomical constraints and the role of plasmodesmata, the regulatory consequences of intercellular metabolite transport, the specialization of metabolite transporters, electron transport pathways, and mitochondrial function, and the mechanisms and functions of the regulation of enzyme activity in C3 and C4 plants. Most of these are intimately connected with intra- and intercellular communication. I consider how this communication is achieved at the structural level and how metabolic cross-talk between the two cell types involved in photosynthesis enables integration of function at a metabolic level and draw attention to some of the limitations that may arise if attempts are made to introduce C4-like characteristics, either at the single cell level or at the level of the mesophyll and bundle sheath, into C3 plants such as rice. How to express some C4 photosynthesis genes at high levels in rice Makoto Matsuoka, Hiroshi Fukayama, Hiroko Tsuchida, Mika Nomura, Sakae Agarie, Maurice S.B. Ku, and Mitsue Miyao To investigate the difference between Pdk genes that encode pyruvate, orthophosphate dikinase (PPDK), a Pdk gene homologous to the maize C4-type Pdk gene was isolated from a C3 plant, rice, and compared with the maize gene. The primary structures of the genes are essentially the same, except that the rice gene has two additional introns. A transient expression assay of Pdk promoters using maize mesophyll protoplasts showed that the mode of expression of the maize and rice genes differs only in the expression activity of the promoter for the chloroplast-type PPDK: the maize gene was expressed fourfold higher than the rice gene. It was also found that a chimeric gene containing the maize Pdk promoter and a reporter gene led to high expression of the reporter gene in transgenic rice. Based on the above observations, the intact genes from maize encoding enzymes for C4 photosynthesis were introduced into rice to increase the activity of the C4 enzymes. As expected, the introduction of the maize gene led to high expression of C4 enzymes in transgenic rice. The activities of phospoenolpyruvate carboxylase (PEPC) and PPDK increased up to 110- and 40-fold more, respectively, than those of nontransgenic rice. High expression of C4 enzymes did not result solely from the high expression activity of the maize gene, since the introduction of a maize PPDK cDNA fused to the maize Pdk promoter or rice Cab promoter did not lead to high expression of PPDK. In some transgenic rice plants carrying the intact maize gene, the level of PPDK protein amounted to 35% of total leaf-soluble protein. The high expression of each C4 enzyme altered metabolism slightly but did not seem to increase the photosynthetic efficiency of transgenic rice leaves. Performance of a potential C4 rice: overview from quantum yield to grain yield P.L. Mitchell and J.E. Sheehy The primary determinant of yield in relation to solar radiation and photosynthesis is the radiation conversion factor (RCF, so-called radiation-use efficiency): the amount of aboveground dry matter produced from each megajoule of photosynthetically active radiation (PAR) intercepted by the crop. The RCF of rice (2.2 g MJ- 1) is lower than that of wheat (2.7 g MJ- 1) or maize (3.3 g MJ- 1). If genetic engineering could produce rice with C4 photosynthesis that possessed the RCF of maize, a 50% increase in yield would be conceivable. Analysis of losses of potential fixed carbon when scaling up from quantum yield to RCF identifies the differences between C3 and C4 plants. The scaling-up progresses from photochemistry in the cell (nanoseconds) through leaf and canopy photosynthesis (seconds to hours) to crop growth (weeks to months). Rice and maize differ in several respects. Rice has losses from photorespiration but maize has a lower theoretical quantum yield because of the energy costs of the C4 pathway. In the hierarchy of scale, there are losses at the cell level from inactive absorption of PAR and these are smaller in maize than in rice. The loss at the transition between leaf and canopy photosynthesis is also smaller in maize. Scaling up from leaf to canopy includes changing from leaf photosynthesis unsaturated for PAR (in which each additional unit of absorbed PAR produces the same additional amount of fixed carbon) to photosynthesis by the canopy with leaves at varying saturation depending on PAR incident on the leaf and on leaf age and photosynthetic capability. The analysis shows that a C4 rice with improved RCF, approaching that of maize, must have higher quantum yield and higher rates of leaf photosynthesis. Suppression of photorespiration will increase quantum yield provided that the energy costs of the C4 pathway, including leakage of carbon dioxide from the bundle sheath, are not much above the minimum observed in C4 plants. Higher rates of leaf photosynthesis, arising from increased concentration of carbon dioxide around Rubisco, increase canopy photosynthesis and make it less prone to saturation by PAR. Many features of C4 photosynthesis must be introduced into a C4 rice, and must operate with high efficiency and coordination, if RCF and yield are to be improved significantly. Mitsuru Osaki A root-shoot interaction model is proposed to explain the high productivity of high-yielding varieties of several crops, based on high-yielding trials. In the high-yielding varieties, nitrogen is always actively absorbed during maturation (the ripening stage of growth). Thus, the photosynthetic rate (dry matter increase) and root activity (nutrient absorption) remained constant during maturation in the high-yielding varieties because a high photosynthetic rate maintains a high root activity by supplying a sufficient amount of photosynthates to the roots, a phenomenon referred to as root-shoot interaction for high productivity. On the other hand, in the varieties with standard yield, hereafter referred to as standard or old or low-yielding varieties, the photosynthetic rate decreased, followed by a decrease in root activity because of the reduced carbohydrate supply; nitrogen incorporated into leaves and stems before maturation was retranslocated during maturation. Two carbon-nitrogen (C-N) interaction models are developed. One is DMt = DM0 exp(CNI × Nt) for cereals and the other is DMt = DM0 + CNI¢ × Nt for legumes, where DMt is the dry weight of a plant at a given time, Nt is the amount of N accumulated in the plant at a given time, DM0 is the initial dry weight, and CNI and CNI¢ are the C-N indices. Moreover, the productivity per unit amount of N accumulated in legumes is quite low compared with that in cereals during the vegetative growth stage. This is caused by the low growth efficiencies [accumulated dry matter / (accumulated dry matter + respiration)] of whole plants regardless of nitrogen concentration, indicating that the concept of growth and maintenance respiration is not valid. The fate of photosynthesized 14CO2 was quite different between rice and soya bean. In soya bean, a large amount of photosynthesized 14CO2 is respired in the light compared with that in the dark, but in rice the amount of 14C retained in the leaves is similar regardless of light conditions. This high respiratory loss of current photosynthates in soya bean in the light can be explained partly by the high rate of photorespiration in the leaves. A large portion of photosynthetically fixed 14CO2 in soya bean in the light was distributed into organic acids, amino acids, and protein compared with that in rice, where metabolism of newly fixed carbon is mainly regulated by the activity of sucrose phosphate synthase (SPS) and especially phosphoenolpyruvate carboxylase (PEPC). Thus, it is assumed that the carbon-nitrogen balance of the whole plant is regulated by (1) whether current photosynthates distribute into the tricarboxylic acid (TCA) cycle or sucrose metabolism in the light, which is regulated by PEPC or SPS, respectively, and (2) whether photorespiratory activity is high or not. This information will help to improve crop productivity through regulation of carbon-nitrogen metabolism. The distribution of 14CO2 to chemical compounds was studied in transgenic rice plants that showed high expression of the maize PEPC gene. The C/N ratio decreased in transgenic plants compared with controls because of high 14C distribution to organic acids and amino acids. As the transgenic plant could exudate much organic acid from the roots, this plant showed a high tolerance for aluminum in low pH solution and high phosphorus use in soil low in phosphorus. Single-leaf and canopy photosynthesis of rice Shaobing Peng Rice single-leaf photosynthesis has been studied intensively in the 1960s and '70s. However, these studies did not contribute significantly to rice crop improvement because of poor correlation between single-leaf photosynthetic rate and grain yield. Canopy photosynthesis has received more attention since then. There is little doubt that canopy net photosynthesis rate correlates with biomass production. Yield enhancement by conventional breeding has mainly resulted from improvement in plant type, which has increased canopy net photosynthesis, especially during the grain-filling period. It is argued that further improvement in canopy net photosynthesis by fine-tuning plant type is difficult because most high-yielding cultivars are close to the optimum canopy architecture. This suggests that increasing single-leaf photosynthesis could be the only way to substantially enhance rice yield potential. With a better understanding of limiting processes in photosynthesis, advances in measurement methodology, and the advent of biotechnology, which enables the modification of content or activity of individual enzymes, the possibility of enhancing biomass production by improving single-leaf photosynthesis should be reexamined. In this chapter, I review the characteristics of rice photosynthesis at the single-leaf and canopy levels by summarizing the external and internal factors that control single-leaf and canopy photosynthetic rates. I also discuss the scenario of increasing rice yield potential by improving single-leaf photosynthesis. C3 versus C4 photosynthesis in rice: ecophysiological perspectives Rowan F. Sage C4 photosynthesis confers substantial benefits upon herbaceous plants in tropical environments, most notably in high-light habitats with frequent drought, heat, and salinity stress. In flooded situations, it is less beneficial, for reasons that are not clear. Conditions in wetlands may not enhance CO2 assimilation rates of C4 plants to the degree needed to suppress C3 competitors; alternatively, wetland C3 plants may be well adapted for marshy environments for reasons unrelated to photosynthetic pathway. If the wetland condition prevents C4 dominance because C3 photosynthetic performance is relatively strong in flooded soils, then the development of C4 rice would probably be of significant benefit in upland situations only, particularly those that experience drought. Alternatively, if C4 plants are less well adapted to flooded conditions than C3 plants for reasons unrelated to photosynthetic pathway, then substantial benefits may result from introducing C4 rice plants into flooded soils. In either case, these considerations must be evaluated in the context of future levels of atmospheric CO2. Elevated CO2 will enhance photosynthetic efficiency and yield of C3 rice plants, perhaps more than might be obtained with C4 rice. Existing rice varieties may not be adapted to fully exploit the increased productive potential that high CO2 represents, and thus engineering C3 rice for a CO2-enriched environment may be an important way to enhance yield. For example, current varieties of rice plants grown at high CO2 contain too much Rubisco, and reduction of Rubisco content by antisense technology can further enhance yield and resource-use efficiency. Because the high CO2 levels favoring C3 over C4 photosynthesis may not appear for many decades, however, the C4 strategy may be the best approach for increasing rice production in the next half-century. Will increased photosynthetic efficiency lead to increased yield in rice? Thomas D. Sharkey, Marianne M. Laporte, and Eric L. Kruger Plant mass is primarily derived from photosynthesis and so it is surprising that final plant mass (yield) and photosynthetic rate of leaves are often not well correlated. The rate of plant respiration and loss of plant matter through detachment also influence yield. The lack of correlation also reflects the fact that photosynthate availability is just one of many signals that affect plant growth and development. Plants grown in elevated carbon dioxide normally have increased yield, which tells us that increasing the availability of photosynthate is likely to increase yield, though perhaps not as much as might be expected. In redesigning photosynthesis for increased yield, we can focus on the inputs, fundamental mechanisms, or outputs. Given the importance of the relationship between photosynthesis and plant growth, this chapter focuses on the outputs of photosynthesis and their immediate use, especially the enzyme sucrose-phosphate synthase (SPS). Plants that are transformed to express more sucrose-phosphate synthase sometimes have higher yields than untransformed plants. Two hypotheses were tested to explain this variability in response: (1) Does expression of the gene in nonphotosynthetic tissue affect yield? (2) Is there an optimum level of SPS that should be sought? It was found that expression in nonphotosynthetic tissue was not important but that there was an optimum level of SPS activity. Too much or too little of this enzyme results in lowered yield and it may be that most plants have a level appropriate to the preindustrial atmospheric carbon dioxide concentration or a level that results in a more conservative strategy than is required for crop plants. Limits to yield for C3 and C4 rice: an agronomist's view John E. Sheehy The conversion of solar energy into grain involves several processes: photosynthesis, respiration, allocation of assimilates to different plant organs, storage, cycling of nitrogen, turnover of short-lived parts, losses of matter owing to biotic and abiotic factors, floret abortion, and sterility. In a growing season of fixed duration, it is inevitable that increased rates of resource capture and retention are required for higher-yielding crops. In this chapter, I assume that mass accumulation is translated into the crop structural and architectural properties required to sustain maximum rates of resource capture. The components of yield and of solar radiation conversion into biomass have been explored using simple theory. I conclude that the upper yield limit of rice crops with conventional photosynthetic pathways will only take us halfway to IRRI's stated goal of a 50% increase in yield. Future increases in production have to be achieved with less land, less water, less labor, and less pollution. A C4 rice plant may satisfy all of those requirements and improve yields. Indeed, its greatest impact may be in areas of low rainfall and poor soil conditions. However, the potential yield of such a crop in irrigated systems could be limited by the intrinsically low N content characteristic of C4 crops. C4 rice: What are the lessons from developmental and molecular studies? William C. Taylor The unique features of C4 leaf anatomy contribute to the photosynthetic and physiological properties of C4 plants. Our current state of knowledge of the developmental program of C4 leaves is reviewed. Adding C4 morphological features to rice leaves will depend on the isolation of genes controlling these traits. Strategies for isolating genes controlling C4 leaf anatomy, the differentiation of the two photosynthetic cell types, and cell-specific gene expression are discussed. Genes encoding C4 enzymes are regulated by a diverse set of mechanisms. Although several C4 genes have been expressed at high levels in transgenic C3 plants, including rice, at least one C4 gene is not expressed in C3 plants. |
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The contribution of rice research to poverty alleviation Future intensification of irrigated rice systems Would C4 rice produce more biomass than C3 rice? C4 photosynthesis in rice: some lessons from studies of C3 photosynthesis in field-grown rice Strategies for increasing the yield potential of rice Photosynthetic performance of transgenic rice plants overexpressing maize C4 photosynthesis enzymes Overcoming barriers: CO2-concentrating mechanisms and C4 metabolism in relation to transport How to express some C4 photosynthesis genes at high levels in rice Performance of a potential C4 rice: overview from quantum yield to grain yield Single-leaf and canopy photosynthesis of rice C3 versus C4 photosynthesis in rice: ecophysiological perspectives Will increased photosynthetic efficiency lead to increased yield in rice? Limits to yield for C3 and C4 rice: an agronomist’s view C4 rice: What are the lessons from developmental and molecular studies? |
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