Abscisic acid (ABA) plays a key role in promoting the growth and development of plants, as well as mediating the responses of plants to adverse environmental conditions. Here, we measured the photosynthetic capacity of wild-type RR, mutant sitiens (sit), and ABA-pretreated sit tomato seedlings following exposure to low-temperature (LT) stress. We found that the net photosynthetic rate, intercellular carbon dioxide concentration, transpiration rate, and stomatal conductance of sit seedlings were lower than those of RR seedlings under LT stress. The chloroplast width, area, and number of osmiophilic granules were significantly larger in sit seedlings than in RR seedlings, while the chloroplast length/width ratio was significantly lower in sit seedlings than in RR seedlings. The photochemical activity of sit seedlings was lower, and the expression of photosynthesis-related genes in sit seedlings was altered following exposure to LT stress. ABA pretreatment significantly alleviated the above phenomenon. We also conducted an RNA sequencing analysis and characterized the expression patterns of genes in tomato seedlings following exposure to LT stress. We constructed 15 cDNA libraries and identified several differentially expressed genes involved in photosynthesis, plant hormone signaling transduction, and primary and secondary metabolism. Additional analyses of genes encoding transcription factors and proteins involved in photosynthesis-related processes showed pronounced changes in expression under LT stress. Luciferase reporter assay and electrophoretic mobility shift assay revealed that WRKY22 regulates the expression of PsbA. The PSII of WRKY22 and PsbA-silenced plants was inhibited. Our findings indicate that ABA plays a role in regulating the process of photosynthesis and protecting PSII in tomato under LT stress through the WRKY22–PsbA complex.

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.