Nitric oxide sensing in plants is mediated by proteolytic control of group VII ERF transcription factors

Daniel J Gibbs; Nurulhikma Md Isa; Mahsa Movahedi; Jorge Lozano-Juste; Guillermina M Mendiondo; Sophie Berckhan; Nora Marín-de la Rosa; Jorge Vicente Conde; Cristina Sousa Correia; Simon P Pearce; George W Bassel; Bulut Hamali; Prabhavathi Talloji; Daniel F A Tomé; Alberto Coego; Jim Beynon; David Alabadí; Andreas Bachmair; José León; Julie E Gray; Frederica L Theodoulou; Michael J Holdsworth

doi:10.1016/j.molcel.2013.12.020

Nitric oxide sensing in plants is mediated by proteolytic control of group VII ERF transcription factors

Daniel J Gibbs, Nurulhikma Md Isa, Mahsa Movahedi, Jorge Lozano-Juste, Guillermina M Mendiondo, Sophie Berckhan, Nora Marín-de la Rosa, Jorge Vicente Conde, Cristina Sousa Correia, Simon P Pearce, George W Bassel, Bulut Hamali, Prabhavathi Talloji, Daniel F A Tomé, Alberto Coego, Jim Beynon, David Alabadí, Andreas Bachmair, José León, Julie E GrayFrederica L Theodoulou, Michael J Holdsworth

Biosciences

Research output: Contribution to journal › Article › peer-review

197 Citations (Scopus)

Abstract

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.

Original language	English
Pages (from-to)	369-79
Number of pages	11
Journal	Molecular Cell
Volume	53
Issue number	3
DOIs	https://doi.org/10.1016/j.molcel.2013.12.020
Publication status	Published - 6 Feb 2014

Bibliographical note

Keywords

Abscisic Acid
Arabidopsis Proteins
Basic-Leucine Zipper Transcription Factors
Gene Expression Regulation, Plant
Germination
Nitric Oxide
Oxygen
Plant Stomata
Proteolysis
Signal Transduction
Transcription Factors

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Gibbs, D. J., Md Isa, N., Movahedi, M., Lozano-Juste, J., Mendiondo, G. M., Berckhan, S., Marín-de la Rosa, N., Vicente Conde, J., Sousa Correia, C., Pearce, S. P., Bassel, G. W., Hamali, B., Talloji, P., Tomé, D. F. A., Coego, A., Beynon, J., Alabadí, D., Bachmair, A., León, J., ... Holdsworth, M. J. (2014). Nitric oxide sensing in plants is mediated by proteolytic control of group VII ERF transcription factors. Molecular Cell, 53(3), 369-79. https://doi.org/10.1016/j.molcel.2013.12.020

@article{87ea092f17314ed1b18bb3e600253cc3,

title = "Nitric oxide sensing in plants is mediated by proteolytic control of group VII ERF transcription factors",

abstract = "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.",

keywords = "Abscisic Acid, Arabidopsis Proteins, Basic-Leucine Zipper Transcription Factors, Gene Expression Regulation, Plant, Germination, Nitric Oxide, Oxygen, Plant Stomata, Proteolysis, Signal Transduction, Transcription Factors",

author = "Gibbs, {Daniel J} and {Md Isa}, Nurulhikma and Mahsa Movahedi and Jorge Lozano-Juste and Mendiondo, {Guillermina M} and Sophie Berckhan and {Mar{\'i}n-de la Rosa}, Nora and {Vicente Conde}, Jorge and {Sousa Correia}, Cristina and Pearce, {Simon P} and Bassel, {George W} and Bulut Hamali and Prabhavathi Talloji and Tom{\'e}, {Daniel F A} and Alberto Coego and Jim Beynon and David Alabad{\'i} and Andreas Bachmair and Jos{\'e} Le{\'o}n and Gray, {Julie E} and Theodoulou, {Frederica L} and Holdsworth, {Michael J}",

year = "2014",

month = feb,

day = "6",

doi = "10.1016/j.molcel.2013.12.020",

language = "English",

volume = "53",

pages = "369--79",

journal = "Molecular Cell",

issn = "1097-2765",

publisher = "Elsevier",

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Gibbs, DJ, Md Isa, N, Movahedi, M, Lozano-Juste, J, Mendiondo, GM, Berckhan, S, Marín-de la Rosa, N, Vicente Conde, J, Sousa Correia, C, Pearce, SP, Bassel, GW, Hamali, B, Talloji, P, Tomé, DFA, Coego, A, Beynon, J, Alabadí, D, Bachmair, A, León, J, Gray, JE, Theodoulou, FL & Holdsworth, MJ 2014, 'Nitric oxide sensing in plants is mediated by proteolytic control of group VII ERF transcription factors', Molecular Cell, vol. 53, no. 3, pp. 369-79. https://doi.org/10.1016/j.molcel.2013.12.020

TY - JOUR

T1 - Nitric oxide sensing in plants is mediated by proteolytic control of group VII ERF transcription factors

AU - Gibbs, Daniel J

AU - Md Isa, Nurulhikma

AU - Movahedi, Mahsa

AU - Lozano-Juste, Jorge

AU - Mendiondo, Guillermina M

AU - Berckhan, Sophie

AU - Marín-de la Rosa, Nora

AU - Vicente Conde, Jorge

AU - Sousa Correia, Cristina

AU - Pearce, Simon P

AU - Bassel, George W

AU - Hamali, Bulut

AU - Talloji, Prabhavathi

AU - Tomé, Daniel F A

AU - Coego, Alberto

AU - Beynon, Jim

AU - Alabadí, David

AU - Bachmair, Andreas

AU - León, José

AU - Gray, Julie E

AU - Theodoulou, Frederica L

AU - Holdsworth, Michael J

PY - 2014/2/6

Y1 - 2014/2/6

N2 - 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.

AB - 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.

KW - Abscisic Acid

KW - Arabidopsis Proteins

KW - Basic-Leucine Zipper Transcription Factors

KW - Gene Expression Regulation, Plant

KW - Germination

KW - Nitric Oxide

KW - Oxygen

KW - Plant Stomata

KW - Proteolysis

KW - Signal Transduction

KW - Transcription Factors

U2 - 10.1016/j.molcel.2013.12.020

DO - 10.1016/j.molcel.2013.12.020

M3 - Article

C2 - 24462115

SN - 1097-2765

VL - 53

SP - 369

EP - 379

JO - Molecular Cell

JF - Molecular Cell

IS - 3

ER -

Nitric oxide sensing in plants is mediated by proteolytic control of group VII ERF transcription factors

Abstract

Bibliographical note

Keywords

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