Temperature-driven changes in membrane fluidity differentially impact FILAMENTATION TEMPERATURE-SENSITIVE H2-mediated photosystem II repair.

Abstract

The Arabidopsis (Arabidopsis thaliana) yellow variegated2 (var2) mutant, lacking functional FILAMENTATION TEMPERATURE-SENSITIVE H2 (FtsH2), an ATP-dependent zinc metalloprotease, is a powerful tool for studying the photosystem II (PSII) repair process in plants. FtsH2, forming hetero-hexamers with FtsH1, FtsH5, and FtsH8, plays an indispensable role in PSII proteostasis. Although abiotic stresses like cold and heat increase chloroplast reactive oxygen species (ROS) and PSII damage, var2 mutants behave like wild-type plants under heat stress but collapse under cold stress. Our study on transgenic var2 lines expressing FtsH2 variants, defective in either substrate extraction or proteolysis, reveals that cold stress causes an increase in membrane viscosity, demanding more substrate extraction power than proteolysis by FtsH2. Overexpression of FtsH2 lacking substrate extraction activity does not rescue the cold-sensitive phenotype, while overexpression of FtsH2 lacking protease activity does in var2, with other FtsH isomers present. This indicates that FtsH2's substrate extraction activity is indispensable under cold stress when membranes become more viscous. As temperatures rise and membrane fluidity increases, substrate extraction activity from other isomers suffices, explaining the var2 mutant's heat stress resilience. These findings underscore the direct effect of membrane fluidity on the functionality of the thylakoid FtsH complex under stress. Future research should explore how membrane fluidity impacts proteostasis, potentially uncovering strategies to modulate thermosensitivity.