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.

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.