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Regulation of SCFTIR1/AFBs E3 ligase assembly by S-nitrosylation of Arabidopsis SKP1-like1 impacts on auxin signaling.

Redox Biol. 2018 Sep;18:200-210. Epub 2018 Jul 06
María José Iglesias 1 , María Cecilia Terrile 1 , Natalia Correa-Aragunde 1 , Silvana Lorena Colman 1 , Alicia Izquierdo-Álvarez 2 , Diego Fernando Fiol 1 , Ramiro París 1 , Nuria Sánchez-López 3 , Anabel Marina 4 , Luz Irina A Calderón Villalobos 5 , Mark Estelle 6 , Lorenzo Lamattina 1 , Antonio Martínez-Ruiz 7 , Claudia Anahí Casalongué 8
María José Iglesias 1 , María Cecilia Terrile 1 , Natalia Correa-Aragunde 1 , Silvana Lorena Colman 1 , Alicia Izquierdo-Álvarez 2 , Diego Fernando Fiol 1 , Ramiro París 1 , Nuria Sánchez-López 3 , Anabel Marina 4 , Luz Irina A Calderón Villalobos 5 , Mark Estelle 6 , Lorenzo Lamattina 1 , Antonio Martínez-Ruiz 7 , Claudia Anahí Casalongué 8
+ et al

[No authors listed]

Author information
  • 1 Instituto de Investigaciones Biológicas, UE-CONICET-UNMDP, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Mar del Plata, Argentina.
  • 2 Servicio de Inmunología, Hospital Universitario de La Princesa, Instituto de Investigación Sanitaria Princesa (IIS-IP), Madrid, Spain.
  • 3 Servicio de Inmunología, Hospital Universitario de La Princesa, Instituto de Investigación Sanitaria Princesa (IIS-IP), Madrid, Spain; Servicio de Proteómica, Centro de Biología Molecular "Severo Ochoa", CSIC-UAM, Madrid, Spain.
  • 4 Servicio de Proteómica, Centro de Biología Molecular "Severo Ochoa", CSIC-UAM, Madrid, Spain.
  • 5 Molecular Signal Processing Department, IPB-Leibniz Institute of Plant Biochemistry, Halle (Saale), Germany.
  • 6 Section of Cell and Developmental Biology, University of California San Diego, San Diego, USA; Howard Hughes Medical Institute, University of California San Diego, San Diego, USA.
  • 7 Servicio de Inmunología, Hospital Universitario de La Princesa, Instituto de Investigación Sanitaria Princesa (IIS-IP), Madrid, Spain; Centro de Investigación Biomédica en Red de Enfermedades Cardiovasculares (CIBERCV), Spain.
  • 8 Instituto de Investigaciones Biológicas, UE-CONICET-UNMDP, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Mar del Plata, Argentina. Electronic address: casalong@mdp.edu.ar.

摘要


The F-box proteins (FBPs) TIR1/AFBs are the substrate recognition subunits of SKP1-cullin-F-box (SCF) ubiquitin ligase complexes and together with Aux/IAAs form the auxin co-receptor. Although tremendous knowledge on auxin perception and signaling has been gained in the last years, SCFTIR1/AFBs complex assembly and stabilization are emerging as new layers of regulation. Here, we investigated how nitric oxide (NO), through S-nitrosylation of ASK1 is involved in SCFTIR1/AFBs assembly. We demonstrate that ASK1 is S-nitrosylated and S-glutathionylated in cysteine (Cys) 37 and Cys118 residues in vitro. Both, in vitro and in vivo protein-protein interaction assays show that NO enhances ASK1 binding to CUL1 and TIR1/AFB2, required for SCFTIR1/AFB2 assembly. In addition, we demonstrate that Cys37 and Cys118 are essential residues for proper activation of auxin signaling pathway in planta. Phylogenetic analysis revealed that Cys37 residue is only conserved in SKP proteins in Angiosperms, suggesting that S-nitrosylation on Cys37 could represent an evolutionary adaption for SKP1 function in flowering plants. Collectively, these findings indicate that multiple events of redox modifications might be part of a fine-tuning regulation of SCFTIR1/AFBs for proper auxin signal transduction.

KEYWORDS: ASK1, Arabidopsis thaliana, Auxin signaling, Nitric oxide, SCF E3 ligase complex