The essential photoprotective role of proton gradient regulation 5 (PGR5)-dependent cyclic electron flow (CEF) has been reported in Arabidopsis, rice, and algae. However, its functional assessment has not been performed in tomato yet. In this study, we focused on elucidate the function of SlPGR5 and SlPGR5-like photosynthetic phenotype 1 (PGRL1) in tomato. We performed RNA interference and found that SlPGR5/SlPGRL1-suppressed transformants exhibited extremely low CO2 assimilation capacity, their photosystem I (PSI) and PSII were severely photoinhibited and chloroplasts were obviously damaged. The SlPGR5/SlPGRL1-suppressed plants almost completely inhibited CEF and Y(ND), and PSII photoinhibition may be directly related to the inability to produce sufficient proton motive force to induce NPQ. The transgenic plants overexpressing SlPGR5 and SlPGRL1 driven by 35S promoter capable alleviate photoinhibition of plants under low night temperature. The transcriptomic and proteomic analyses suggested that the nuclear gene transcription and turnover of chloroplast proteins, including the plastoglobule-related proteins, were closely related to SlPGR5/SlPGRL1 pathway dependent CEF. The bridge relationship between CEF and chloroplast quality maintenance was a novel report to our knowledge. In conclusion, these results revealed the regulatory mechanism of the SlPGR5/SlPGRL1 pathway in photoprotection and maintenance of chloroplast function in tomato, which is crucial for reduce yield loss, especially under adverse environmental conditions.

Melatonin is a direct free radical scavenger that has been demonstrated to increase plants’ resistance to a variety of stressors. Here, we sought to examine the effect of melatonin on tomato seedlings subjected to low night temperatures using an integrated physiological, transcriptomic, and proteomic approach. We found that a pretreatment with 100 μM melatonin increased photosynthetic and transpiration rates, stomatal apertures, and peroxidase activity, and reduced chloroplast damage of the tomato plant under a low night temperature. The melatonin pretreatment reduced the photoinhibition of photosystem I by regulating the balance of both donor- and acceptor-side restriction of PSI and by increasing electron transport. Furthermore, the melatonin pretreatment improved the photosynthetic performance of proton gradient regulation 5 (SlPGR5) and SlPGR5-like photosynthetic phenotype 1 (SlPGRL1)-suppressed transformants under a low night temperature stress. Transcriptomic and proteomic analyses found that the melatonin pretreatment resulted in the upregulation of genes and proteins related to transcription factors, signal transduction, environmental adaptation, and chloroplast integrity maintenance in low night temperature-stressed tomato plants. Collectively, our results suggest that melatonin can effectively improve the photosynthetic efficiency of tomato plants under a low night temperature and provide novel insights into the molecular mechanism of melatonin-mediated abiotic stress resistance.