Plant evolution: The inevitability of C4 photosynthesis

Although atmospheric carbon dioxide (CO₂) levels are currently rising, the last 30 million years witnessed great declines in CO₂, which has limited the efficiency of photosynthesis. Rubisco, the critical photosynthetic enzyme that catalyses the fixation of CO₂ into carbohydrate, also reacts with oxygen when CO₂ levels are low and temperatures are high. When this occurs, plants activate a process known as photorespiration, an energetically expensive set of reactions that release one molecule of CO₂.

C4 photosynthesis is a clever solution to the problem of low atmospheric CO₂. It is an internal plant carbon-concentrating mechanism that largely eliminates photorespiration: a ‘fuel-injection’ system for the photosynthetic engine. C4 plants differ from plants with the more typical ‘C3’ photosynthesis because they restrict Rubisco activity to an inner compartment, typically the bundle sheath, with atmospheric CO₂ being fixed into a 4-carbon acid in the outer mesophyll. This molecule then travels to the bundle sheath, where it is broken down again, bathing Rubisco in CO₂ and limiting the costly process of photorespiration.

The evolution of the C4 pathway requires many changes. These include the recruitment of multiple enzymes into new biochemical functions, massive shifts in the spatial distribution of proteins and organelles, and a set of anatomical modifications to cell size and structure. It is complex, and it is also highly effective: C4 plants include many of our most important and productive crops (maize, sorghum, sugarcane, millet) and are responsible for around 25% of global terrestrial photosynthesis. A new paper in eLife examines how this process may have evolved, first to correct an intercellular nitrogen imbalance, and only later evolved a central role in carbon fixation.