Turning problems into opportunities: photorespiration for improved plant metabolism.

In the quest for more sustainable agriculture, improved crops with reduced photorespiration, a highly energy-consuming process, hold enormous potential. Researchers from the EU-funded Gain4Crops project have now succeeded in developing a solution that connects photorespiration and C4 metabolism, two of the main targets for improving crop yield. This first proof of concept opens the door to plants with enhanced productivity and reduced consumption of resources.

Schematic representation of the plants developed by GAIN4CROPS (on the right( compared to wild types (on the left).

In today’s plants, photorespiration dissipates a substantial fraction of the photosynthesis’s energy and releases CO2. It begins when the enzyme RuBisCO acts on oxygen instead of carbon dioxide creating toxic metabolites that require costly recycling reactions. The detoxification process releases previously fixed carbon and wastes energy, thus strongly limiting agricultural productivity.

Scientists generally pursue two approaches to minimize the harmful effects of photorespiration: mimicking the carbon concentrating mechanism of so-called C4 plants or introducing new metabolic pathways to bypass photorespiration.

Researchers led by Andreas Weber from Heinrich Heine University Düsseldorf and Tobias Erb from the Max Planck Institute for Terrestrial Microbiology have developed a solution that synergistically couples photorespiration and C4 plant metabolism, connecting two of the main targets in improving plant metabolism. Within the EU-funded project Gain4Crops, they have turned a novel photorespiration bypass route, the microbial BHAC pathway, into a carbon conserving mechanism in plants. The team has introduced enzymes from the BHAC pathway into the model plant Arabidposis thaliana, where they successfully convert the toxic product of photorespiration into a launchpad of a synthetic C4 cycle, without dissipating carbon, nitrogen, or energy.

Gas exchange measurements and metabolic profiling confirmed that the newly developed plants conserve nitrogen and accumulate signature metabolites of C4 plants. At the current stage, the prototype plants didn’t show any gain in the amount of CO2 assimilated via photosynthesis at the expense of the CO2 released by photorespiration. But, as the team pointed out, several bottlenecks still mask the full potential of the BHAC pathway, and they will be addressed in future research.

To fully appreciate the gain in carbon fixed and ultimately in yield, the pathway will be further improved, guided by kinetic and genome-scale metabolic models. Indeed, prototyping in model organisms, such as Arabidopsis, allows identifying shortcomings before moving to a target crop, thus speeding up the development process. To this end, the Gain4crops project will test the newly discovered pathway in a set of model organisms of increasing cellular and anatomical complexity before moving to its final target: the sunflower, an important oilseed crop in Europe.

Overall, this study represents the first proof of concept for carbon-concentrating mechanisms in crops dependent on photorespiration, coupling the solution with the problem, and creating opportunities for improved agricultural productivity. Furthermore, crops with increased photosynthetic efficiency might become valuable tools in the face of climate change thanks to their climate resilience and reduced consumption of resources.

Agriculture will have to keep pace with a growing population on a planet in short supply of resources and rapidly changing environmental conditions. “Improving sustainability is probably the biggest challenge of the 21st century, and, even if there is no single silver bullet, the combination of different solutions might bring an effective improvement,” says Andreas Weber. In the quest for more sustainable agriculture, land-sparing through improved crops with reduced photorespiration might be an essential part of the solution.

More information: Marc-Sven Roell et al, A synthetic C4 shuttle via the β-hydroxyaspartate cycle in C3 plants, Proceedings of the National Academy of Sciences (2021). DOI: 10.1073/pnas.2022307118

Journal information: Proceedings of the National Academy of Sciences