The development of tobacco plants that are genetically engineered to produce a more efficient form of Rubisco, an enzyme involved in photosynthesis, marks a step towards increasing crop yields. See Letter p.547
As the world's population increases, the spectre of severe food shortages is growing, with the United Nations predicting1 that food production will need to double by 2050. It has been proposed that cyanobacteria — which obtain their energy from a highly efficient form of photosynthesis — might hold the key to increasing the yield of our most important crops and vegetables. On page 547 of this issue, Lin et al.2 report a major step towards realizing this possibility, finding that cyanobacteria can be used to improve photosynthesis in the leaves of crops.
Photosynthesis harnesses sunlight to convert carbon dioxide into simple sugars. Rubisco, the key enzyme for CO2 fixation into sugar, is inefficient because it cannot easily discriminate between oxygen and CO2 and so wastes energy by fixing O2. The enzyme evolved at a time when O2 levels in the atmosphere were much lower than they are today, and there was therefore little evolutionary pressure to select for an ability to discriminate between the two molecules. Photosynthetic organisms have evolved to circumvent the problem of rising atmospheric O2 levels in two ways: first, by making more of a slower-acting version of Rubisco with an improved ability to discriminate; or second, by using various 'add-ons', called CO2-concentrating mechanisms (CCMs), to elevate CO2 levels in the vicinity of the enzyme.
Most crops have adopted the first strategy, making Rubisco possibly the most abundant enzyme on Earth. This approach, however, results in a 30% reduction in photosynthetic efficiency through the associated O2 fixation. That can be partly ameliorated by raising CO2 levels around the leaf3 in a manner conceptually similar to adding a CCM. There is currently increased focus on the second strategy — if a CCM could be introduced into crops, it might turbocharge photosynthetic CO2 fixation. CCMs have evolved independently in cyanobacteria, microalgae and some plants (mostly those regarded by us as weeds). Although several types of CCM are being considered for introduction into crops, Lin and colleagues' work focuses on the cyanobacterial CCM.
This CCM involves a series of membrane-based pumps for CO2 and bicarbonate (HCO3−), and special microcompartments called carboxysomes, which contain Rubisco4. HCO3− is pumped into the cell, then converted to CO2 in the carboxysomes by the enzyme carbonic anhydrase (Fig. 1). The resulting high local CO2 concentrations increase Rubisco efficiency, and so almost eliminate O2 fixation4. Furthermore, thanks to the CCM, cyanobacteria have retained an ancient form of Rubisco that is almost three times as efficient as that found in most crops5.
Lin et al. engineered tobacco plants to express a functional cyanobacterial form of Rubisco. This enzyme usually consists of a complex of eight large subunits and five to eight small subunits. The authors replaced DNA that encodes the large subunit of Rubisco in the tobacco plant with that encoding the cyanobacterial enzyme, ensuring that the photosynthesis and growth they observed occurred as a result of the introduced Rubisco, rather than the native version. This DNA is located in the cells' photosynthesizing factories, structures called chloroplasts.
Lin and colleagues' approach differs from those of earlier, unsuccessful efforts6 in several ways; most notably, the authors co-expressed the cyanobacterial Rubisco with proteins that are involved in the enzyme's assembly. They found that co-expression of cyanobacterial Rubisco with either the RbcX chaperone protein (which helps protein folding) or a carboxysomal protein called CcmM35 (a Rubisco-organizing protein) were equally effective at forming functional Rubisco. However, the latter approach produced large complexes of Rubisco, which seemed to be related to those that form during the assembly of pre-carboxysomes in cyanobacteria. This is because CcmM35 mimics three of Rubisco's small subunits and so is incorporated into Rubisco. But the protein also crosslinks to other Rubisco complexes, producing enzyme aggregates4.
The authors did not demonstrate whether the addition of CcmM35 or RbcX was the pivotal step in successfully expressing cyanobacterial Rubisco in tobacco, or whether other elements of the experimental design provided the crucial advantage. Earlier this year, the same group showed that co-expression of several carboxysomal shell proteins in chloroplasts can produce structures suggestive of carboxysome self-assembly7. Thus, prospects for building functional carboxysomes in tobacco-plant chloroplasts are now quite good. However, extending this to crops would be greatly aided by the development of technologies for altering the chloroplast genomes of key crop species.
In the past two years, the sequence of events required to build a cyanobacterial CCM in the chloroplast has been identified in detail8,9. Stand-alone addition of cyanobacterial Rubisco, or even of carboxysomes, to chloroplasts provides no obvious advantage. In fact, Lin et al. show that their modified plants survive only at high CO2 concentrations. To provide an advantage, both CO2 and HCO3− pumps are required, to elevate HCO3− levels in the chloroplast and so turbocharge CO2 levels in the carboxysomes. And even when these remaining steps have been achieved in model plants such as tobacco, improved crops are still some way off. However, this work is a milestone on the road to boosting plant efficiency. The advance can be likened to having a new engine block in place in a high-performance car engine — now we just need the turbocharger fitted and tuned.
Lin, M. T., Occhialini, A., Andralojc, P. J., Parry, M. A. J. & Hanson, M. R. Nature 513 547–550 (2014).
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Price, G., Howitt, S. Towards turbocharged photosynthesis. Nature 513, 497–498 (2014). https://doi.org/10.1038/nature13749
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