Phytochrome B enhances seed germination tolerance to high temperature by reducing S‐nitrosylation of HFR1

Abstract

Light and ambient high temperature (HT) have opposite effects on seed germination. Light induces seed germination through activating the photoreceptor phytochrome B (phyB), resulting in the stabilization of the transcription factor HFR1, which in turn sequesters the suppressor PIF1. HT suppresses seed germination and triggers protein S‐nitrosylation. Here, we find that HT suppresses seed germination by inducing the S‐nitrosylation of HFR1 at C164, resulting in its degradation, the release of PIF1, and the activation of PIF1‐targeted SOMNUS (SOM) expression to alter gibberellin (GA) and abscisic acid (ABA) metabolism. Active phyB (phyBY276H) antagonizes HFR1 S‐nitrosylation and degradation by increasing S‐nitrosoglutathione reductase (GSNOR) activity. In line with this, substituting cysteine‐164 of HFR1 with serine (HFR1C164S) abolishes the S‐nitrosylation of HFR1 and decreases the HT‐induced degradation of HFR1. Taken together, our study suggests that HT and phyB antagonistically modulate the S‐nitrosylation level of HFR1 to coordinate seed germination, and provides the possibility to enhance seed thermotolerance through gene‐editing of HFR1.

Recent progress in molecular genetics and omics-driven research in seed biology

“…Thus 80 Snitrosylated proteins were identified, including glyceraldehyde 3-phosphate dehydrogenase, indicating that S-nitrosylation of this enzyme may accelerate cell death and seed deterioration during aging; similar results were obtained for Arabidopsis seeds [231]. It has been recently reported that elevated temperature (32 °C) inhibits Arabidopsis seed germination and triggers protein S-nitrosylation [232]. Under this temperature, the bHLH transcription factor LONG HYPOCOTYL IN FAR-RED1 (HFR1) is S-nitrosylated at Cyt164, resulting in its degradation and breakdown PIF1-HFR1 heterodimer to release PHYTOCHROME INTERACTING FACTOR 1 (PIF1) activity.…”

“…Ainsi, 80 protéines Snitrosylées ont été identifiées, dont la glycéraldéhyde 3-phosphate déshydrogénase, indiquant que la Snitrosylation de cette enzyme peut accélérer la mort cellulaire et la détérioration des graines au cours du vieillissement ; des résultats similaires ont été obtenus pour les graines d'Arabidopsis [231]. Il a été récemment signalé qu'une température élevée (32 °C) inhibe la germination des graines d'Arabidopsis et déclenche la S-nitrosylation des protéines [232]. Sous cette température, le facteur de transcription bHLH LONG HYPOCOTYL IN FAR-RED1 (HFR1) est Snitrosylé à Cyt164, entraînant sa dégradation et la rupture de l'hétérodimère PIF1-HFR1 pour libérer l'activité du PHYTOCHROME INTERACTING FAC-TOR 1 (PIF1).…”

Cysteine thiol-based post-translational modification: What do we know about transcription factors?

“…Light and high temperature have opposite effects on seed germination, while light induces, heat suppresses seed germination. Recently, S-nitrosation of LONG HYPOCOTYL IN FAR-RED1 (HFR1) offered a mechanistic link between light-and heat-controlled seed germination [86]. Light stabilizes HFR1 that forms a heterodimeric complex with PIF1 and inhibits its DNA binding activity, thereby promoting seed germination under light.…”

“…Light stabilizes HFR1 that forms a heterodimeric complex with PIF1 and inhibits its DNA binding activity, thereby promoting seed germination under light. However, high temperature induces S-nitrosation of HFR1 Cys164, resulting in its degradation and release of PIF1 that activates expression of the CCCH-type zinc finger protein SOMNUS which can alter GA and ABA metabolism and finally suppress seed germination [86].…”

Functions of nitric oxide-mediated post-translational modifications under abiotic stress

“…NO mechanisms during plant acclimation to HS include activation of cellular responses through the S -nitrosylation of the trihelix TF GT-1, which promotes its binding to HEAT SHOCK TRANSCRIPTION FACTOR A2 ( HsfA2 ) promoter ( He et al., 2022 ). During germination, Cys S -nitrosylation has been described as an important PTM, where high temperature and the photoreceptor phytochrome B (phyB) modulate antagonistically LONG HYPOCOTYL IN FAR-RED (HFR1)-SNO to coordinate seed thermotolerance ( Ying et al., 2022 ).…”