Metabolite profiling reveals slow and uncoordinated adjustment of C4 photosynthesis to sudden changes in irradiance

In the field, plants continually experience changes in irradiance. Research in C3 species has revealed that while the Calvin-Benson cycle (CBC) adjusts rapidly to changing irradiance, there is substantial loss of photosynthetic efficiency due to slow adjustment of energy dissipation and stomatal conductance. Less is known about the impact of changing irradiance on photosynthetic efficiency in C4 species. We subjected maize (Zea mays) to a sudden increase or decrease of irradiance in the nonsaturating range and performed time-resolved measurement of photosynthetic rate and profiling of metabolites from the CBC, the CO2-concentrating mechanism (CCM), the energy shuttle, photorespiration, and end-product biosynthesis. After a decrease in irradiance, photosynthesis is transiently buffered by energy delivered from transformations in the large metabolite pools in the energy shuttle and CCM. During the subsequent decline in photosynthesis, metabolism transitions to a suboptimal state for photosynthesis in low irradiance, from which it takes several minutes to recover. One reason is that end-product synthesis depletes the metabolite pools that drive intercellular shuttles and time is required to replenish these pools. After an increase in irradiance, there is an initial rapid rise of photosynthesis linked to build-up of CBC intermediates and, probably, activation of enzymes in the CBC and the CCM. This is followed by a further slow rise of photosynthesis linked to gradual accumulation of the large metabolite pools that drive intercellular shuttles. In addition, in both transitions, transient imbalances between pumping and utilization of CO2 lead to further losses in photosynthetic efficiency.