S-Nitrosation of E3 Ubiquitin Ligase Complex Components Regulates Hormonal Signalings in Arabidopsis

TERRILE, MARIA CECILIA; TEBEZ, NURIA MALENA; COLMAN, SILVANA LORENA; MATEOS, JULIETA LISA; MORATO-LÓPEZ, ESPERANZA; SÁNCHEZ-LÓPEZ, NURIA; IZQUIERDO-ÁLVAREZ, ALICIA; MARINA, ANABEL; CALDERÓN VILLALOBOS, LUZ IRINA A.; ESTELLE, MARK; MARTÍNEZ-RUIZ, ANTONIO; FIOL, DIEGO FERNANDO; CASALONGUÉ, CLAUDIA ANAHÍ; IGLESIAS, MARÍA JOSÉ

Frontiers in Plant Science

Frontiers Media SA

Lugar: Laussane; Año: 2022 vol. 12

E3 ubiquitin ligases mediate the last step of the ubiquitination pathway in the ubiquitin-proteasome system (UPS). By targeting transcriptional regulators for their turnover, E3splay a crucial role in every aspect of plant biology. In plants, SKP1/CULLIN1/F-BOXPROTEIN (SCF)-type E3 ubiquitin ligases are essential for the perception and signalingof several key hormones including auxins and jasmonates (JAs). F-box proteins,TRANSPORT INHIBITOR RESPONSE 1 (TIR1) and CORONATINE INSENSITIVE1 (COI1), bind directly transcriptional repressors AUXIN/INDOLE-3-ACETIC ACID(AUX/IAA) and JASMONATE ZIM-DOMAIN (JAZ) in auxin- and JAs-depending manner,respectively, which permits the perception of the hormones and transcriptional activationof signaling pathways. Redox modification of proteins mainly by S-nitrosation ofcysteines (Cys) residues via nitric oxide (NO) has emerged as a valued regulatorymechanism in physiological processes requiring its rapid and versatile integration.Previously, we demonstrated that TIR1 and Arabidopsis thaliana SKP1 (ASK1) aretargets of S-nitrosation, and these NO-dependent posttranslational modificationsenhance protein-protein interactions and positively regulate SCFTIR1 complex assemblyand expression of auxin response genes. In this work, we confirmed S-nitrosation ofCys140 in TIR1, which was associated in planta to auxin-dependent developmental andstress-associated responses. In addition, we provide evidence on the modulation of theSCFCOI1 complex by different S-nitrosation events. We demonstrated that S-nitrosationof ASK1 Cys118 enhanced ASK1-COI1 protein-protein interaction. Overexpression ofnon-nitrosable ask1 mutant protein impaired the activation of JA-responsive genesmediated by SCFCOI1 illustrating the functional relevance of this redox-mediatedregulation in planta. In silico analysis positions COI1 as a promising S-nitrosationtarget, and demonstrated that plants treated with methyl JA (MeJA) or S-nitrosocysteine(NO-Cys, S-nitrosation agent) develop shared responses at a genome-wide level. Thregulation of SCF components involved in hormonal perception by S-nitrosation mayrepresent a key strategy to determine the precise time and site-dependent activationof each hormonal signaling pathway and highlights NO as a pivotal molecular player inthese scenarios.