Nitric Oxide Regulates Protein Methylation during Stress Responses in Plants

Abstract

Methylation and nitric oxide (NO)-based S-nitrosylation are highly conserved protein posttranslational modifications that regulate diverse biological processes. In higher eukaryotes, PRMT5 catalyzes Arg symmetric dimethylation, including key components of the spliceosome. The Arabidopsis prmt5 mutant shows severe developmental defects and impaired stress responses. However, little is known about the mechanisms regulating the PRMT5 activity. Here, we report that NO positively regulates the PRMT5 activity through S-nitrosylation at Cys-125 during stress responses. In prmt5-1 plants, a PRMT5 transgene, carrying a non-nitrosylatable mutation at Cys-125, fully rescues the developmental defects, but not the stress hypersensitive phenotype and the responsiveness to NO during stress responses. Moreover, the salt-induced Arg symmetric dimethylation is abolished in PRMT5/prmt5-1 plants, correlated to aberrant splicing of pre-mRNA derived from a stress-related gene. These findings define a mechanism by which plants transduce stress-triggered NO signal to protein methylation machinery through S-nitrosylation of PRMT5 in response to environmental alterations.

Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants

“…S-nitrosylation mediated by NO represents a key process in plant growth and development, as well as responses to environmental changes (Hess et al, 2005;Kovacs & Lindermayr, 2013;Hu et al, 2017;Zhan et al, 2018)…”

Protein S‐Nitrosylation in plants: Current progresses and challenges

“…However, the PRMT5 C125S transgenic plants are hypersensitive to NaCl and ABA, but insensitive to NO that enhances resistance to stress, indicating that S ‐nitrosylation at Cys‐125 is essential for the PRMT5‐regulated stress responses. Moreover, salt stress‐induced arginine symmetric demethylation is also abolished in PRMT5 C125S transgenic plants, correlated to aberrant pre‐mRNA splicing of stress‐related genes (Hu et al ). This study illustrates the importance of the crosstalk between S ‐nitrosylation and arginine methylation in modulating stress responses.…”

Present knowledge and controversies, deficiencies, and misconceptions on nitric oxide synthesis, sensing, and signaling in plants

“…It has been reported that plants transduce NO signal through S‐nitrosylation of protein arginine methyl transferase 5 involved in protein methylation machinery and the subsequent epigenetic regulation of pre‐mRNA splicing, DNA damage repair, and mRNA translation (Blanc & Richard, ) in response to environmental alterations (Hu et al, ). It is worth mentioning that the polycomb repressive complex 2 subunit VERNALIZATION 2 is regulated, like ERFVIIs, in an O 2 ‐ and NO‐dependent manner involving the Cys–Arg branch of the N‐end rule proteolytic pathway (Gibbs et al, ), thus representing an additional support for a functional link between NO signaling and epigenetic regulation.…”