Update on Chloroplast Bicarbonate Pumps The Prospect of Using Cyanobacterial Bicarbonate Transporters to Improve Leaf Photosynthesis in C 3 Crop Plants [W] G. Dean Price*, Murray R. Badger, and Susanne von Caemmerer Molecular Plant Physiology Cluster, Research School of Biology, Australian National University, Canberra, Australian Capital Territory 0200, Australia The photosynthetic CO 2 -fixing enzyme Rubisco arose some 3.5 billion years ago, in an environment when CO 2 was high and oxygen (O 2 ) was low. Under these conditions, it was CO 2 saturated and presumably performed well (Badger et al., 1998). However, since the advent of oxygenic photosynthesis, the levels of O 2 have risen dramatically and CO 2 has fallen to very low levels. This has gradually created conditions where CO 2 has become limiting for Rubisco and allowed O 2 to act as an alternative inhibitory substrate for the enzyme. To cope with these dramatic environmental changes, two major strategies have evolved to help Rubisco maximize its carboxylation rate at ambient levels of limiting CO 2 . First, the enzyme has evolved better kinetic properties, where the K m (CO 2 ) has de- creased and the ability to distinguish against O 2 has increased at the expense of catalytic rate (Badger et al., 1998). Alternatively, many photosynthetic organisms, ranging from cyanobacteria to algae to land plants, have developed active CO 2 -concentrating mechanisms (CCMs) to turbo-charge Rubisco’s CO 2 supply at a minor metabolic cost (Badger et al., 1998). Most nota- bly, among plants this has led to the development of C 4 photosynthesis (Sage, 2004). Most of the important grain crops (rice [Oryza sativa], wheat [Triticum aestivum], barley [Hordeum vulgare], canola [Brassica napus], soybean [Glycine max]), tuber crops, and vegetable crops are C 3 species and have applied the first strategy and lack any form of CCM at the leaf or chloroplast level. Much of the inherent inefficiency in C 3 photosynthesis revolves around the need to gain CO 2 through passive diffusion through the leaf pores (stomata), across cell walls and cytoplasm, and eventually through to the chloroplasts. Diffusive resistance to CO 2 passage results in a draw- down of the effective CO 2 concentration in the chlo- roplast, and C 3 plants have adopted strategies to maximize the diffusive conductivity for CO 2 by ap- pressing chloroplasts against the intracellular airspaces and having large chloroplast surface area-to-leaf area ratios (Evans and von Caemmerer, 1996). Low chloro- plast CO 2 concentrations exacerbate the CO 2 limita- tions and increase the wasteful Rubisco oxygenation reaction of ribulose 1,5-bisphosphate (RuBP) to pro- duce phosphoglycolate, which must be recycled back to RuBP through a complex set of reactions known as the photorespiratory cycle. This is worsened by in- creased temperature, with the affinity for CO 2 drop- ping and the oxygenase reaction being relatively enhanced (Kubien and Sage, 2008). To achieve accept- able high rates of photosynthetic CO 2 fixation, typical C 3 species invest up to 30% of soluble protein and some 25% of leaf nitrogen into Rubisco protein. Evo- lution of the CCM in C 4 plants effectively circum- vented a number of the inefficiencies, creating the present-day impetus for attempting to introduce C 4 CCMs into important C 3 crops such as rice (Hibberd et al., 2008). However, while the C 4 CCM is one approach to elevating CO 2 around Rubisco, drawing from our knowledge of single-cell CCMs in cyanobacteria (Price et al., 2008), there are also opportunities to elevate CO 2 around Rubisco at the individual leaf chloroplast level. These prospects are expanded upon below, but in brief we consider two scenarios. The first, and simplest, approach is to consider the transplantation of cyanobacterial bicarbonate transporters to the C 3 chloroplasts to provide marginal but significant im- provement in photosynthetic performance. The sec- ond, more elaborate, longer term objective would be to engineer a more functional cyanobacterial CCM in the chloroplast. THE CYANOBACTERIAL CCM Cyanobacteria have evolved an extremely efficient CCM (Fig. 1; see below), being able to concentrate CO 2 around Rubisco by a factor of up to 1,000-fold. As a result, cyanobacterial CO 2 fixation has been able to retain a Rubisco with a relatively high carboxylation rate, although lower selectivity between CO 2 and O 2 , compared with the Rubisco in C 3 plants (Badger et al., 1998). Cyanobacterial cells also have high nitrogen use efficiency, as less nitrogen is devoted to Rubisco than in a C 3 plant (Badger et al., 1998). In addition, Rubisco within a cyanobacterium operates at near CO 2 satura- tion due to the action of the CCM, such that wasteful photorespiration is largely eliminated. * Corresponding author; e-mail dean.price@anu.edu.au. [W] The online version of this article contains Web-only data. www.plantphysiol.org/cgi/doi/10.1104/pp.110.164681 20 Plant Physiology Ò , January 2011, Vol. 155, pp. 20–26, www.plantphysiol.org Ó 2010 American Society of Plant Biologists Downloaded from https://academic.oup.com/plphys/article/155/1/20/6111524 by guest on 26 June 2022