How can Photosynthetic Carbon Assimilation be Improved?

One of the Grand Challenges of the 21st century

The problem with Rubisco and photorespiration. Many crop plants have an inefficient pathway of CO₂ assimilation. This pathway is termed C₃ photosynthesis and is found in staple crops, such as wheat, barley, rice, soybean and potatoes. All plants rely upon an enzyme for fixing CO₂ called Rubisco. Rubisco evolved in the very first photosynthetic bacteria some 3.5 billion years ago, but it evolved in an atmosphere that was CO₂-rich and in the absence of O₂. Subsequently, the CO₂ concentration in the atmosphere has declined drastically. Moreover, the evolution of O₂-evolving photosynthesis in the cyanobacteria 2.5 billion years ago and the subsequent evolution of land plants 550 million years ago have vastly increased amounts of O₂ in the atmosphere. The problem with Rubisco is that it not only fixes CO₂ but also fixes O₂, in a side reaction that is an inevitable consequence of its reaction mechanism.

The oxygenation reaction of Rubisco leads to a product, glycollate, which cannot be further metabolised by the reactions of C₃ photosynthesis. The salvage of this glycollate occurs in a process called photorespiration that involves the light-dependent loss of CO₂ from leaves (i.e. the opposite of photosynthesis). Photorespiration is therefore a major drain on a plant’s carbon. At ambient atmospheric CO₂ concentrations at 25°C, the loss of carbon is about 25% of that recently fixed, but can be considerably higher under warmer, tropical conditions.

How can the deficiencies in Rubisco be overcome? It would be surprising if billions of years of evolution had not ironed out some of the problems with Rubisco. It is undoubtedly a better enzyme at fixing CO₂ in the present atmosphere than its bacterial precursor (especially in some algae, notably in thermophilic red algae). Nevertheless, the fact that reaction with O₂ is an inevitable consequence of its reaction mechanism means that Rubisco will never be ideal and that oxygenation is a reaction that cannot be eliminated by genetic engineering. It is also a very slow enzyme, so that plants need a lot of it, resulting in a large investment of valuable nitrogen in Rubisco protein (it is the world’s most abundant protein).  One strategy to improve Rubisco in crop plants is to substitute it with better Rubisco from algae, but that in itself is a difficult task since the assembly of Rubisco in plants is a particularly complex process. Another solution that has been adopted by many algae and some land plants is to increase the CO₂ concentration around Rubisco, outcompeting the oxygenase reaction. This can be achieved in aquatic organisms by active uptake of inorganic carbon to concentrate CO₂ around Rubisco in specialised structures, such carboxysomes or pyrenoids in algae or, in terrestrial plants, by concentrating CO₂ around Rubisco in the cells surrounding the vasculature, termed bundle sheath (Kranz) cells. This is the process that occurs in C₄ plants.

In C₄ plants, the first product of CO₂ fixation is a four carbon (C₄) acid, contrasting with glycerate 3-P (three carbons) in C₃ plants. Although flowering plant species that have C₄ photosynthesis comprise only about 3% of the total, about 50% of all grasses are C₄, many in warm climates. Thus the majority of grasses in savannas (about 15% of Earth’s vegetated surface) are C₄ and are responsible for about 20% of global photosynthesis. C₄ plants are responsible for 40% of the world's grain harvest and include some of world’s most important crop species, such as maize, sugar cane and millet.

If photorespiration could be reduced in current C₃ crops, or if they could be converted to use C₄ photosynthesis, large economic and environmental benefits would ensue both because of their increased productivity and the reduced inputs per unit yield associated with the C₄ pathway. C₄ photosynthesis results in improved rates of carbon fixation, improved nitrogen use efficiency (because less investment of nitrogen in Rubisco protein is needed) and improved water use efficiency (because less CO₂ is required for photosynthesis and hence stomata can remain more closed). Efficient C₄ photosynthesis is associated with alterations to leaf development, cell biology and biochemistry and so transferring these traits into C₃ crops is a long-term undertaking. Despite its complexity, C₄ photosynthesis has evolved independently over 66 times and this argues strongly for it being a tractable system to understand and manipulate. It is important to note that the huge advances in agricultural production associated with the Green Revolution were not associated with increases in photosynthesis, and so its manipulation remains an unexplored target for crop improvement both for food and biomass. Even partial long-term success would have significant economic and environmental benefits.