Nitric oxide sensing in plants is mediated by proteolytic control of group VII ERF transcription factors.
Nitric oxide (NO) is an important signaling compound in prokaryotes and eukaryotes. In plants, NO regulates critical developmental transitions and stress responses. Here, we identify a mechanism for NO sensing that coordinates responses throughout development based on targeted degradation of plant-specific transcriptional regulators, the group VII ethylene response factors (ERFs). We show that the N-end rule pathway of targeted proteolysis targets these proteins for destruction in the presence of NO, and we establish them as critical regulators of diverse NO-regulated processes, including seed germination, stomatal closure, and hypocotyl elongation. Furthermore, we define the molecular mechanism for NO control of germination and crosstalk with abscisic acid (ABA) signaling through ERF-regulated expression of ABSCISIC ACID INSENSITIVE5 (ABI5). Our work demonstrates how NO sensing is integrated across multiple physiological processes by direct modulation of transcription factor stability and identifies group VII ERFs as central hubs for the perception of gaseous signals in plants.
Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, UK.
Daniel J
DJ
Gibbs
Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, UK.
Nurulhikma
N
Md Isa
Department of Molecular Biology and Biotechnology, University of Sheffield, Sheffield S10 2TN, UK.
Mahsa
M
Movahedi
Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas-Universidad Politécnica de Valencia, Ciudad Politécnica de la Innovación, 46022 Valencia, Spain.
Jorge
J
Lozano-Juste
Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, UK.
Guillermina M
GM
Mendiondo
Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, UK.
Sophie
S
Berckhan
Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas-Universidad Politécnica de Valencia, Ciudad Politécnica de la Innovación, 46022 Valencia, Spain.
Nora
N
Marín-de la Rosa
Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, UK.
Jorge
J
Vicente Conde
Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, UK.
Cristina
C
Sousa Correia
Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, UK.
Simon P
SP
Pearce
Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, UK.
George W
GW
Bassel
Department of Biochemistry and Cell Biology, Max F. Perutz Laboratories, University of Vienna, Dr. Bohr Gasse 9, Vienna 1030, Austria.
Bulut
B
Hamali
Department of Biochemistry and Cell Biology, Max F. Perutz Laboratories, University of Vienna, Dr. Bohr Gasse 9, Vienna 1030, Austria.
Prabhavathi
P
Talloji
School of Life Sciences, University of Warwick, Coventry CV4 7AL, UK.
Daniel F A
DF
Tomé
Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas-Universidad Politécnica de Valencia, Ciudad Politécnica de la Innovación, 46022 Valencia, Spain.
Alberto
A
Coego
School of Life Sciences, University of Warwick, Coventry CV4 7AL, UK.
Jim
J
Beynon
Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas-Universidad Politécnica de Valencia, Ciudad Politécnica de la Innovación, 46022 Valencia, Spain.
David
D
Alabadí
Department of Biochemistry and Cell Biology, Max F. Perutz Laboratories, University of Vienna, Dr. Bohr Gasse 9, Vienna 1030, Austria.
Andreas
A
Bachmair
Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas-Universidad Politécnica de Valencia, Ciudad Politécnica de la Innovación, 46022 Valencia, Spain.
José
J
León
Department of Molecular Biology and Biotechnology, University of Sheffield, Sheffield S10 2TN, UK.
Julie E
JE
Gray
Biological Chemistry and Crop Protection Department, Rothamsted Research, Harpenden AL5 2JQ, UK.
Frederica L
FL
Theodoulou
Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, UK. Electronic address: michael.holdsworth@nottingham.ac.uk.
Michael J
MJ
Holdsworth
D000040:Abscisic Acid / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000187:drug effects / Q000235:genetics / Q000378:metabolism*; D050976:Basic-Leucine Zipper Transcription Factors / Q000235:genetics / Q000378:metabolism; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D018525:Germination / Q000187:drug effects / Q000502:physiology; D009569:Nitric Oxide / Q000378:metabolism* / Q000494:pharmacology; D010100:Oxygen / Q000494:pharmacology; D054046:Plant Stomata / Q000187:drug effects; D059748:Proteolysis; D015398:Signal Transduction; D014157:Transcription Factors / Q000187:drug effects / Q000378:metabolism*
C409743:ABI5 protein, Arabidopsis; D029681:Arabidopsis Proteins; D050976:Basic-Leucine Zipper Transcription Factors; D014157:Transcription Factors; D009569:Nitric Oxide; D000040:Abscisic Acid; D010100:Oxygen