Strawberry COP9 signalosome FvCSN5 regulates plant development and fruit ripening by facilitating polyamine oxidase FvPAO5 degradation to control polyamine and H2O2homeostasis

Abstract

AbstractPolyamines (PAs), including putrescine, spermidine, and spermine, are essential for plant growth and development. However, the post-translational regulation of PA metabolism remains elusive. Here, we report the COP9 signalosome subunit 5A (FvCSN5A)-mediated degradation of the PA oxidase FvPAO5 which catalyzes polyamines to produce H2O2. FvCSN5A was identified through a yeast two-hybrid screen using FvPAO5 as the bait. FvCSN5A localized in both the cytoplasm and nucleus, and its interaction with FvPAO5 occurred in the cytoplasm.FvCSN5Aexpression was ubiquitous in strawberries and peaked during fruit ripening. We utilized two independent RNAi lines, RNAi -1 and RNAi -2, in whichFvCSN5Aexpression was downregulated by 8-fold and 46-fold, respectively, to demonstrate the pleiotropic roles of FvCSN5A. FvCSN5A positively regulated plant development, fertility, and fruit ripening by maintaining PA homeostasis, and promotes ubiquitination degradation of FvPAO5 through the interaction with cullin 1 (FvCUL1). The accumulation of FvPAO5 in the partial loss-of-function of FvCSN5A transgenic plants resulted from the inhibition of polyubiquitination modification of FvPAO5. Finally, we propose a post-translational regulatory mechanism involving the FvCSN5A-FvCUL1-FvPAO5 axis underlying PA and H2O2homeostasis, providing novel insights into the regulation of plant growth by integrating the COP9 signalosome-mediated ubiquitination system into PA metabolism.