SPINDLY interacts with EIN2 to facilitate ethylene signalling‐mediated fruit ripening in tomato

Abstract

The post-translational modification of proteins enables cells to respond promptly to dynamic stimuli by controlling protein functions. In higher plants, SPINDLY (SPY) and SECRET AGENT (SEC) are two prominent O-glycosylation enzymes that have both unique and overlapping roles; however, the effects of their O-glycosylation on fruit ripening and the underlying mechanisms remain largely unknown. Here we report that SlSPY affects tomato fruit ripening. Using slspy mutants and two SlSPY-OE lines, we provide biological evidence for the positive role of SlSPY in fruit ripening. We demonstrate that SlSPY regulates fruit ripening by changing the ethylene response in tomato. To further investigate the underlying mechanism, we identify a central regulator of ethylene signalling ETHYLENE INSENSITIVE 2 (EIN2) as a SlSPY interacting protein. SlSPY promotes the stability and nuclear accumulation of SlEIN2. Mass spectrometry analysis further identified that SlEIN2 has two potential sites Ser771 and Thr821 of O-glycans modifications. Further study shows that SlEIN2 is essential for SlSPY in regulating fruit ripening in tomatoes. Collectively, our findings reveal a novel regulatory function of SlSPY in fruit and provide novel insights into the role of the SlSPY-SlEIN2 module in tomato fruit ripening.

SPINDLY mediates O-fucosylation of hundreds of proteins and sugar-dependent growth in Arabidopsis

“…Fifteen TOR-regulated phosphoproteins are both O -fucosylated and O -GlcNAcylated ( Fig. 4A ; Supplemental Dataset S8 ), including EIN2, a key component of the ethylene signaling pathway recently reported to be a substrate of TOR ( Fu et al 2021 ) and to interact with SPY in tomato ( Solanum lycopersicum ) ( Xu et al 2022 ). Almost half of the O -GlcNAcylated proteins (128 of 262) are O -fucosylated.…”

Role of Ethylene in the Regulation of Plant Developmental Processes

“…Studies have shown that posttranslational modifications also play a role in fruit ripening. For instance, a recent report observed SPINDLY (O-glycosylation enzymes) collaborated with EIN2 to enhance the process of ET signaling, which in turn promoted the ripening of fruits in S. lycopersicum plants [103]. Histone modifiers, like histone deacetylases, are enlisted by AP2/ERFs to regulate fruit ripening.…”