Redox feedback regulation of ANAC089 signaling alters seed germination and stress response
Pablo Albertos,
Kiyoshi Tatematsu,
Isabel Mateos,
Inmaculada Sánchez-Vicente,
Alejandro Fernández-Arbaizar,
Kazumi Nakabayashi,
Eiji Nambara,
Marta Godoy,
José M. Franco,
Roberto Solano,
Davide Gerna,
Thomas Roach,
Wolfgang Stöggl,
Ilse Kranner,
Carlos Perea-Resa,
Julio Salinas,
Oscar Lorenzo
Affiliations
Pablo Albertos
Department of Botany and Plant Physiology, Instituto Hispano-Luso de Investigaciones Agrarias (CIALE), Facultad de Biología, Universidad de Salamanca, C/Río Duero 12, 37185 Salamanca, Spain
Kiyoshi Tatematsu
Laboratory of Plant Organ Development, National Institute for Basic Biology, Nishigonaka 38, Myodaiji, Okazaki 444-8585, Japan
Isabel Mateos
Department of Botany and Plant Physiology, Instituto Hispano-Luso de Investigaciones Agrarias (CIALE), Facultad de Biología, Universidad de Salamanca, C/Río Duero 12, 37185 Salamanca, Spain
Inmaculada Sánchez-Vicente
Department of Botany and Plant Physiology, Instituto Hispano-Luso de Investigaciones Agrarias (CIALE), Facultad de Biología, Universidad de Salamanca, C/Río Duero 12, 37185 Salamanca, Spain
Alejandro Fernández-Arbaizar
Department of Botany and Plant Physiology, Instituto Hispano-Luso de Investigaciones Agrarias (CIALE), Facultad de Biología, Universidad de Salamanca, C/Río Duero 12, 37185 Salamanca, Spain
Kazumi Nakabayashi
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey TW20 0EX, UK
Eiji Nambara
Department of Cell & Systems Biology, University of Toronto, 25 Willcocks Street, Toronto, ON M5S 3B2, Canada
Marta Godoy
Department of Plant Molecular Genetics, Centro Nacional de Biotecnología-CSIC, Campus Universidad Autónoma, 28049 Madrid, Spain
José M. Franco
Department of Plant Molecular Genetics, Centro Nacional de Biotecnología-CSIC, Campus Universidad Autónoma, 28049 Madrid, Spain
Roberto Solano
Department of Plant Molecular Genetics, Centro Nacional de Biotecnología-CSIC, Campus Universidad Autónoma, 28049 Madrid, Spain
Davide Gerna
Department of Botany and Center for Molecular Biosciences Innsbruck (CMBI), University of Innsbruck, Sternwartestraße 15, Innsbruck A-6020, Austria
Thomas Roach
Department of Botany and Center for Molecular Biosciences Innsbruck (CMBI), University of Innsbruck, Sternwartestraße 15, Innsbruck A-6020, Austria
Wolfgang Stöggl
Department of Botany and Center for Molecular Biosciences Innsbruck (CMBI), University of Innsbruck, Sternwartestraße 15, Innsbruck A-6020, Austria
Ilse Kranner
Department of Botany and Center for Molecular Biosciences Innsbruck (CMBI), University of Innsbruck, Sternwartestraße 15, Innsbruck A-6020, Austria
Carlos Perea-Resa
Departamento de Biotecnología Microbiana y de Plantas, Centro de Investigaciones Biológicas-CSIC, Ramiro de Maeztu, 9, 28040 Madrid, Spain
Julio Salinas
Departamento de Biotecnología Microbiana y de Plantas, Centro de Investigaciones Biológicas-CSIC, Ramiro de Maeztu, 9, 28040 Madrid, Spain
Oscar Lorenzo
Department of Botany and Plant Physiology, Instituto Hispano-Luso de Investigaciones Agrarias (CIALE), Facultad de Biología, Universidad de Salamanca, C/Río Duero 12, 37185 Salamanca, Spain; Corresponding author
Summary: The interplay between the phytohormone abscisic acid (ABA) and the gasotransmitter nitric oxide (NO) regulates seed germination and post-germinative seedling growth. We show that GAP1 (germination in ABA and cPTIO 1) encodes the transcription factor ANAC089 with a critical membrane-bound domain and extranuclear localization. ANAC089 mutants lacking the membrane-tethered domain display insensitivity to ABA, salt, and osmotic and cold stresses, revealing a repressor function. Whole-genome transcriptional profiling and DNA-binding specificity reveals that ANAC089 regulates ABA- and redox-related genes. ANAC089 truncated mutants exhibit higher NO and lower ROS and ABA endogenous levels, alongside an altered thiol and disulfide homeostasis. Consistently, translocation of ANAC089 to the nucleus is directed by changes in cellular redox status after treatments with NO scavengers and redox-related compounds. Our results reveal ANAC089 to be a master regulator modulating redox homeostasis and NO levels, able to repress ABA synthesis and signaling during Arabidopsis seed germination and abiotic stress.
