Redox regulation of the NOR transcription factor is involved in the regulation of fruit ripening in tomato

Abstract

Transcription factors (TFs) are important regulators of plant growth and development and responses to stresses. TFs themselves are also prone to multiple posttranslational modifications (PTMs). However, redox-mediated PTM of TFs in plants remains poorly understood. Here, we established that NON-RIPENING (NOR), a master TF regulating tomato (Solanum lycopersicum) fruit ripening, is a target of the Met sulfoxide reductases A and B, namely E4 and SlMsrB2, respectively, in tomato. Met oxidation in NOR, i.e. sulfoxidation, or mimicking sulfoxidation by mutating Met-138 to Gln, reduces its DNA-binding capacity and transcriptional regulatory activity in vitro. E4 and SlMsrB2 partially repair oxidized NOR and restore its DNA-binding capacity. Transgenic complementation of the nor mutant with NOR partially rescues the ripening defects. However, transformation of nor with NOR-M138Q, containing mimicked Met sulfoxidation, inhibits restoration of the fruit ripening phenotype, and this is associated with the decreased DNA-binding and transcriptional activation of a number of ripening-related genes. Taken together, these observations reveal a PTM mechanism by which Msr-mediated redox modification of NOR regulates the expression of ripening-related genes, thereby influencing tomato fruit ripening. Our report describes how sulfoxidation of TFs regulates developmental processes in plants.