Photosynthesis is the foundation of all life on Earth, providing oxygen and energy. However, if not well regulated, it can also generate toxic reactive oxygen species (ROS), which can cause photodamage. Regulation of photosynthesis is highly dynamic, responding to both environmental and metabolic cues, and occurs at many levels, from light capture to energy storage and metabolic processes. One general mechanism of regulation involves the reversible oxidation and reduction of protein thiol groups, which can affect the activity of enzymes and the stability of proteins. Such redox regulation has been well studied in stromal enzymes, but more recently evidence has emerged of redox control of thylakoid lumenal enzymes. This review/hypothesis paper summarizes the latest research and discusses several open questions and challenges to achieving effective redox control in the lumen, focusing on the distinct environments and regulatory components of the thylakoid lumen, including the need to transport electrons across the thylakoid membrane, the effects of pH changes in the stromal and lumenal compartments, and the observed differences in redox states. These constraints suggest that activated oxygen species are likely to be major regulatory contributors to lumenal thiol redox regulation, with key components and processes yet to be discovered.

Triose-phosphate utilization (TPU) limits the maximum rate at which plants can photosynthesize. However, TPU is almost never found to be limiting photosynthesis under ambient conditions for plants. This, along with previous results showing adaptability of TPU at low temperature, suggest that TPU capacity is regulated to be just above the photosynthetic rate achievable under the prevailing conditions. A set of experiments were performed to study the adaptability of TPU capacity when plants are acclimated to elevated CO 2 concentrations. Plants held at 1500 ppm CO 2 were initially TPU limited. After 30 hours they no longer exhibited TPU limitations but they did not elevate their TPU capacity. Instead, the maximum rates of carboxylation and electron transport declined. A timecourse of regulatory responses was established. A step increase of CO 2 first caused PSI to be oxidized but after 40 s both PSI and PSII had excess electrons as a result of acceptor-side limitations. Electron flow to PSI slowed and the proton motive force increased. Eventually, non-photochemical quenching reduced electron flow sufficiently to balance the TPU limitation. Over several minutes rubisco deactivated contributing to regulation of metabolism to overcome the TPU limitation.

The work demonstrates the use of detailed, high-throughput phenotyping to generate and test mechanistic models to explain the genetic diversity of photosynthetic responses to abiotic stress. We assessed a population of recombinant inbred lines (RILs) of cowpea (Vigna unguiculata. (L.) Walp.) with significant differences in a range of photosynthetic responses to chilling. We found well-defined, colocalized (overlapping) QTL intervals for photosynthetic parameters, suggesting linkages among the redox states of QA, the thylakoid pmf, through effects on cyclic electron flow and photodamage to PSII. We propose that these genetic variations optimize photosynthesis in the tolerant lines under low temperatures, preventing recombination reactions within Photosystem II that can lead to deleterious 1O2 production. By contrast, we did not observe linkages to PSI redox state, PSI photodamage or ATP synthase activity, or nyctinastic (diurnally controlled) leaf movements, likely indicating that several proposed models likely do not contribute to the genetic control of photosynthesis at low temperature in our mapping panel. The identified QTL intervals include a range of potential causative genetic components, with direct applications to breeding of photosynthesis for more climate-resilient productivity.

Using a population of recombinant inbred lines (RILs) cowpea (Vigna unguiculata. L. Walp), we tested for co-linkages between lipid contents and chilling responses of photosynthesis. Under low temperature conditions (19°C/13°C, day/night), we observed co-linkages between quantitative trait loci (QTL) intervals for photosynthetic light reactions and specific fatty acids, most strikingly, the thylakoid-specific fatty acid 16:1Δ3trans found exclusively in phosphatidylglycerol (PG 16:1t). By contrast, we did not observe co-associations with bulk polyunsaturated fatty acids or high-melting-point-PG (sum of PG 16:0, PG 18:0 PG 16:1t) previously thought to be involved in chilling sensitivity. These results suggest that in cowpea, chilling sensitivity is modulated by specific lipid interactions rather than bulk properties. We were able to recapitulate the predicted impact of PG 16:1t levels on photosynthetic responses at low temperature using mutants and transgenic Arabidopsis lines. Because PG 16:1t synthesis requires the activity of peroxiredoxin-Q, which is activated by H2O2 and known to be involved in redox signaling, we hypothesize that the accumulation of PG 16:1t occurs as a result of upstream effects on photosynthesis that alter redox status and production of reactive oxygen species.

We explored the effects, on photosynthesis in cowpea (Vigna unguiculata), of high temperature and light — environmental stresses that often co-occur under field conditions. We observed contrasting responses in the light and carbon assimilatory reactions, whereby in high temperature, the light reactions were stimulated while CO2 assimilation was substantially reduced. There were two striking observations. First, the primary quinone acceptor (QA), a measure of the regulatory balance of the light reactions, became more oxidized with increasing temperature, suggesting increased electron sink capacity, despite the reduced CO2 fixation. Second, a strong, O2-dependent inactivation of assimilation capacity, consistent with down-regulation of rubisco under these conditions, a phenomenon that has not been previously reported. The dependence of these effects on CO2, O2 and light led us to conclude that both photorespiration and an alternative electron acceptor, supported increased electron flow, and thus provided photoprotection, under these conditions. Further experiments showed that the increased electron flow was maintained by rapid rates of PSII repair, particularly at combined high light and temperature. Overall, the results suggest that photodamage to the light reactions can be avoided under high light and temperatures by increasing electron sink strength, even when assimilation is strongly suppressed.