Sub-optimal temperature leads to tighter coupling between photosynthetic electron transport and CO ₂ assimilation under fluctuating light in maize

The C ₄ carbon concentrating pathway promotes high CO ₂ assimilation rates. To keep C ₄ photosynthesis energetically efficient, electron transport reactions and downstream biochemistry need to be carefully balanced. Here we use a combination of non-invasive measurements and metabolic profiling to study the efficiency of C ₄ photosynthesis in maize under two conditions that can lead to decoupling between electron transport and carbon assimilation: fluctuating light and suboptimal temperature. Measurements were performed for three fluctuating light regimes and three temperatures, providing the most detailed study to date of the interaction between fluctuating light and suboptimal temperature on the photosynthetic performance of maize, an important global crop. At room temperature, CO ₂ assimilation rates were decoupled from photosynthetic electron transport under fluctuating light regimes, in contrast to tight coordination observed under constant light. This decoupling was underpinned by metabolic flexibility and buffering by large pools of C ₄ transfer metabolites. Surprisingly, at sub-optimal temperatures, CO ₂ assimilation rates became more tightly coupled to photosynthetic electron transport rates under fluctuating light regimes. This appeared to be caused by strong feedback downregulation of electron transport and a stronger degree of light-saturation of CO ₂ assimilation at low temperature. Low temperature impacted carbon assimilation rates more strongly than metabolite pools or intercellular metabolite distribution, which could reflect negative effects on diffusional metabolite transfer through plasmodesmata. Altogether, these results show that maize is able to maintain energetic efficiency by buffering light transitions under room temperature, as well as avoid oxidative damage by strongly downregulating electron transfer under short-term exposure to low temperature.