Mankind urgently has to find ways to use solar energy more effectively, more extensively and more efficiently. This includes increasing plant and algal photosynthesis for food, fuel and other products (fibre, chemical feedstocks etc). When considering the food crops of the developing world, in my opinion there are only two ways to do this. The first is to optimise photosynthesis for crop yield. Studies have clearly show that maximum photosynthetic potential is never realised, particularly under field conditions [1,2]. The reasons for this are many and varied, but there are two major influences – firstly, the direct limitation imposed by environmental stresses (shortage of water or soil nutrients, high or low temperatures); and secondly, the presence in the plant’s genotype of regulatory processes which reduce photosynthetic activity. The latter are particularly intriguing, and they arise because of the “conservative” nature of most plant species. Put simply, stability and survival in the natural environment are the driving forces of evolution, not necessarily high growth rate or high grain yield. Man’s demand for high agricultural yield is in conflict with key features of plant biology. Plants record, memorise and predict their environments, to ensure that they always have enough energy storage (completely from photosynthesis) to power their growth and development. For example, plants have to determine the size of their reproductive sinks (i.e. grain capacity) in advance, predicting what the photosynthetic rate will be to give maximum grain filling. Over-estimation of future photosynthesis results in poor grain filling and/or poor quality grain. Under-estimation of future photosynthesis results in a decrease in the efficiency of solar energy use and losses of potential productivity.

Another specific example relates to the “down regulation” of photosynthetic efficiency during periods when the sun light intensity is in excess of that which can be used in photosynthesis – this occurs not just when intensities of solar radiation are maximum but also at lower intensities when other environmental factors are sub-optimal for photosynthesis. During such periods of excess light, absorbed energy is dissipated harmlessly as heat to protect the leaves from photo-damage, a process, known as nonphotochemical quenching, NPQ [3,4]. Because NPQ decreases the efficiency of light energy storage (because some absorbed light energy is dissipated), there is a decrease in photosynthetic efficiency when the sunlight intensity decreases. Thus, in fluctuating conditions, common in nature, potential photosynthetic activity is lost. Calculations show that 30% increases in yield could occur if the rate of relaxation of NPQ was increased [5]. Optimisation of NPQ depends on balancing the photosynthetic losses incurred because of the finite rate of NPQ relaxation with the demonstrated benefits arising from the photoprotection afforded by this process [6].

There are many other examples that could be discussed, since nearly every aspect of a plant’s development hinges upon its energy metabolism [7]. Altering such optimisation in favour of higher yield may not be that complicated – a small number of proteins are involved in many of these regulatory mechanisms. Other alterations may be more difficult in part because of the unexpected effects of various compensatory responses to genetic alterations [8] and, in many cases, there are significant gaps in our knowledge of the molecular mechanisms involved. However, it is clear that optimisation points are subject to genetic variation – for example, a South American survey of 24 commercial varieties and accessions of common bean revealed that those which are stress tolerant have a low growth rate under favourable conditions, whereas others have high yield under favourable condition but suffer badly when grown under stress [9] This shows that the optimisation points of these accessions are different. Thus, I suggest that significant benefits will come from understanding at the molecular and genetic levels such trade-offs between stress tolerance and yield potential, and manipulating them to suit specific agricultural scenarios.

Probably, the main reason why the photosynthetic rate of crops such as rice does not reach maximum capacity is the inefficiency of the primary process of C02 fixation. In the majority of plants, including rice, CO2 is first fixed into a compound with three carbons (C3) by the enzyme ribulose bisphosphate carboxylase oxygenase (Rubisco) – this is known as C3 photosynthesis. Rubisco is inherently inefficient because it can also react with oxygen in the air giving a wasteful process known as photorespiration. At temperatures in excess of 20°C, O2 begins to out-compete CO2 and dramatic reductions in photosynthetic efficiency result. Thus, in the hot tropics where most rice is grown, photosynthesis becomes very inefficient. How could this inherent inefficiency be overcome? Theoretically the answer is increase the competitive advantage of C02 over O2, most simply by increasing the concentration of CO2 and/or reducing the concentration of O2. Nature has given us a way to achieve this – in a range of photosynthetic organisms, but not in rice, specific CO2 concentrating mechanisms have been found. Most significantly some of the most productive crops known such a maize, sorghum and sugar cane concentrate CO2 using the C4 pathways of CO2 fixation. Thus, introduction of the C4 pathway into crops such as rice would eliminate photorespiration, increase photosynthetic rate and boost the amount of energy storage in the plant [10]. Yield increases are bound to result. Although this is an ambitious undertaking, the fact that the C4 pathway has evolved independently many times gives cause for optimism.

These two routes to improving photosynthetic efficiency are not mutually exclusive. The most desirable outcome would be the design of specific crop varieties, all carrying out C4 photosynthesis, and in which other parts of the photosynthesis process have been differentially optimised for the highest yield in a number of different agronomic situations. Furthermore, the same research tools, such as screening of wild rice accessions and mutant populations, would be used in the pursuit of both goals.

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References

For a Tansley review of this topic, see Murchie EH, Pinto M, Horton P (2009) Agriculture and the new challenges for photosynthesis research. New Phytologist 181: xx-xx. For a comprehensive account of the issues surrounding C4 rice, see Sheehy JE, Mitchell , Hardy P. eds, (2008) Charting new pathways to C4 rice, World Scientific Publishing Co. USA (ISBN 978-981-270-951-6).

1. Horton P (2000) Prospects for crop improvement through the genetic manipulation of photosynthesis: morphological and biochemical aspects of light capture. Journal of Experimental Botany 51: 475-485
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9. Lizana C, Wentworth M, Martinez JP, Villegas D, Meneses R, Murchie EH, Pastenes C, Lercari B, Vernieri P, Horton P, Pinto M. (2006) Differential adaptation of two varieties of common bean to abiotic stress. I. Effects of drought on yield and photosynthesis. Journal of Experimental Botany 57: 685-697
10. Hibberd JM, Sheehy JE, Langdale JA (2008) Using C-4 photosynthesis to increase the yield of rice - rationale and feasibility. Current Opinion in Plant Biology 11: 228-231