A metabolic bypass increases crop productivity

By Konstantinos Vavitsas

Carbon fixation is a notoriously inefficient process in land plants. The key enzyme of carbon fixation, ribulose-1,5-bisphosphate carboxylase-oxygenase (RuBisCO), can also react with oxygen, generating 2-phosphoglycolate. This molecule is toxic and has to be remediated by photorespiration, a costly metabolic route and result in a net loss of energy and of carbon to CO2, which could otherwise have been assimilated into biomass. In a recent work, researchers from the University of Illinois, Urbana, inserted into tobacco plants a synthetic metabolic pathway that bypasses photorespiration. They showed that the transformed plants display increased photosynthetic capacity and biomass yield in field trials.

Out of every 1000 kJ of solar energy that reach a leaf, only 46 kJ can be assimilated into plant biomass. This number represents a theoretical maximum, lowering the value to about 3% or less for crop plants growing in the field. One of the processes that account for a big energy loss is photorespiration. As ribulose-1,5-bisphosphate carboxylase-oxygenase (RuBisCO) can accept both CO2 and oxygen, photorespiration recycles the oxygen reaction’s toxic byproduct within the central carbon metabolism (Figure 1).

Figure 1: Simplified reaction scheme of photorespiratory pathways. RuBisCO can accept CO2 and ribulose bisphosphate (RuBP) as substrate, producing two molecules of 3-phosphoglycerate (Calvin cycle reactions). When RuBP reacts with oxygen, it converts to 2-phospoglycolate, which is recycled via the photorespiration reactions (depicted in red) that span across three organelles. South and his co-workers introduced a synthetic metabolic bypass (depicted in blue) that releases CO2 in the proximity or RuBisCO. Transportation of molecules across organelles is depicted in dashed arrows.

As photorespiration accounts for about 20% of drop in photosynthetic efficiency, it is often the target of genetic modifications for rational increase in plant productivity. It is an essential process that intertwines with many reactions of the primary metabolism, therefore it is not feasible to disrupt it by knocking it out. The idea of inserting metabolic bypasses with more efficient recycling of 2-phosphoglycolate has been implemented and resulted in increased growth in the model plant Arabidopsis thaliana and the oilseed crop Camelina sativa.

In a recent work, Paul South and his co-workers employed a synthetic biology approach to bypass photorespiration in tobacco plants. The researchers introduced a two-step heterologous pathway into the plastid genome that converts glycolate – the first intermediate of photorespiration – to malate (Figure 1). They used a modular golden gate approach and tested their novel synthetic route and the previously described bypasses in Nicotiana tabacum. As an extra improvement, they decided to decrease (but not completely disrupt) the endogenous photorespiration activity. Using RNAi, they supressed the expression of the transporter PLGG1 by 80% – the protein that facilitates the transportation of glycolate to the peroxisome and of glycerate to the chloroplast (Figure 1).

The transformed plants grow healthy and have higher photosynthetic efficiency by 20%. One of the most important outcomes of this study is the result of the field experiments, which assessed tobacco productivity in realistic out-of-the laboratory conditions. The transgenic plants accumulated 40% more biomass and 12% more starch than the control plants.

The results are fascinating and provide a good example of synthetic biology in action, with direct commercial and basic research applications. The study displays how former results can be enriched with new knowledge and formulate better designs. The transgenic plants can provide invaluable insights for the importance of photorespiration besides carbon recycling (e.g. during oxidative stress). Finally, it would be interesting to see how this approach performs in other crop plants or in combination with other photosynthetic enhancement techniques.

I would like to thank Jenna Gallegos for her feedback.