Salicylic acid regulates two photosystem II protection pathways in tomato under chilling stress mediated by ETHYLENE INSENSITIVE 3-like proteins.

Chilling stress seriously impairs photosynthesis and activates a series of molecular responses in plants. Previous studies have shown that ETHYLENE INSENSITIVE 3 (EIN3) and EIN3-like (SlEIL) proteins mediate ethylene signaling and reduce plant tolerance to freezing in tomato (Solanum lycopersicum). However, the specific molecular mechanisms underlying an EIN3/EILs-mediated photoprotection pathway under chilling stress are unclear. Here, we discovered that salicylic acid (SA) participates in photosystem II (PSII) protection via SlEIL2 and SlEIL7. Under chilling stress, the phenylalanine ammonia-lyase gene SlPAL5 plays an important role in the production of SA, which also induces WHIRLY1 (SlWHY1) transcription. The resulting accumulation of SlWHY1 activates SlEIL7 expression under chilling stress. SlEIL7 then binds to and blocks the repression domain of the heat shock factor SlHSFB-2B, releasing its inhibition of HEAT SHOCK PROTEIN 21 (HSP21) expression to maintain PSII stability. In addition, SlWHY1 indirectly represses SlEIL2 expression, allowing the expression of l-GALACTOSE-1-PHOSPHATE PHOSPHATASE3 (SlGPP3). The ensuing higher SlGPP3 abundance promotes the accumulation of ascorbic acid (AsA), which scavenges reactive oxygen species produced upon chilling stress and thus protects PSII. Our study demonstrates that SlEIL2 and SlEIL7 protect PSII under chilling stress via two different SA response mechanisms: one involving the antioxidant AsA and the other involving the photoprotective chaperone protein HSP21.