The brassinosteroid receptor BRI1 can generate cGMP enabling cGMP-dependent downstream signaling

Janet I. Wheeler; Aloysius Tze Wong; Claudius Marondedze; Arnoud J. Groen; Lusisizwe Kwezi; Lubna Freihat; Jignesh Vyas; Misjudeen Raji; Helen R. Irving; Christoph A Gehring

doi:10.1111/tpj.13589

The brassinosteroid receptor BRI1 can generate cGMP enabling cGMP-dependent downstream signaling

Janet I. Wheeler, Aloysius Tze Wong, Claudius Marondedze, Arnoud J. Groen, Lusisizwe Kwezi, Lubna Freihat, Jignesh Vyas, Misjudeen Raji, Helen R. Irving, Christoph A Gehring

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

42 Scopus citations

Abstract

The brassinosteroid receptor BRASSINOSTEROID INSENSITIVE 1 (BRI1) is a member of the leucine rich repeat receptor like kinase family. The intracellular kinase domain of BRI1 is an active kinase and also encapsulates a guanylate cyclase catalytic centre. Using liquid chromatography tandem mass spectrometry, we confirmed that the recombinant cytoplasmic domain of BRI1 generates pmol amounts of cGMP per μg protein with a preference for magnesium over manganese as a co-factor. Importantly, a functional BRI1 kinase is essential for optimal cGMP generation. Therefore, the guanylate cyclase activity of BRI1 is modulated by the kinase while cGMP, the product of the guanylate cyclase, in turn inhibits BRI1 kinase activity. Furthermore, we show using Arabidopsis root cell cultures that cGMP rapidly potentiates phosphorylation of the downstream substrate BRASSINOSTEROID SIGNALING KINASE 1 (BSK1). Taken together, our results suggest that cGMP acts as a modulator that enhances downstream signaling while dampening signal generation from the receptor. This article is protected by copyright. All rights reserved.

Original language	English (US)
Pages (from-to)	590-600
Number of pages	11
Journal	The Plant Journal
Volume	91
Issue number	4
DOIs	https://doi.org/10.1111/tpj.13589
State	Published - Jun 12 2017

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: Support from the Australian Research Council’s Discovery funding scheme (project numbers DP0878194 and DP110104164), the National Research Foundation South Africa (grant numbers 78843; IRF2009021800047) and La Trobe University School of Life Science Publication Booster Award is gratefully acknowledged. We also thank Dr Yu Hua Wang (Monash University) for preparing the G1073K mutant construct and Dr Victor Muleya (Monash University) for helpful discussions.

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10.1111/tpj.13589

https://repository.kaust.edu.sa/bitstream/10754/623663/1/Wheeler_et_al-2017-The_Plant_Journal.pdf

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title = "The brassinosteroid receptor BRI1 can generate cGMP enabling cGMP-dependent downstream signaling",

abstract = "The brassinosteroid receptor BRASSINOSTEROID INSENSITIVE 1 (BRI1) is a member of the leucine rich repeat receptor like kinase family. The intracellular kinase domain of BRI1 is an active kinase and also encapsulates a guanylate cyclase catalytic centre. Using liquid chromatography tandem mass spectrometry, we confirmed that the recombinant cytoplasmic domain of BRI1 generates pmol amounts of cGMP per μg protein with a preference for magnesium over manganese as a co-factor. Importantly, a functional BRI1 kinase is essential for optimal cGMP generation. Therefore, the guanylate cyclase activity of BRI1 is modulated by the kinase while cGMP, the product of the guanylate cyclase, in turn inhibits BRI1 kinase activity. Furthermore, we show using Arabidopsis root cell cultures that cGMP rapidly potentiates phosphorylation of the downstream substrate BRASSINOSTEROID SIGNALING KINASE 1 (BSK1). Taken together, our results suggest that cGMP acts as a modulator that enhances downstream signaling while dampening signal generation from the receptor. This article is protected by copyright. All rights reserved.",

author = "Wheeler, {Janet I.} and Wong, {Aloysius Tze} and Claudius Marondedze and Groen, {Arnoud J.} and Lusisizwe Kwezi and Lubna Freihat and Jignesh Vyas and Misjudeen Raji and Irving, {Helen R.} and Gehring, {Christoph A}",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: Support from the Australian Research Council{\textquoteright}s Discovery funding scheme (project numbers DP0878194 and DP110104164), the National Research Foundation South Africa (grant numbers 78843; IRF2009021800047) and La Trobe University School of Life Science Publication Booster Award is gratefully acknowledged. We also thank Dr Yu Hua Wang (Monash University) for preparing the G1073K mutant construct and Dr Victor Muleya (Monash University) for helpful discussions.",

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AU - Gehring, Christoph A

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N2 - The brassinosteroid receptor BRASSINOSTEROID INSENSITIVE 1 (BRI1) is a member of the leucine rich repeat receptor like kinase family. The intracellular kinase domain of BRI1 is an active kinase and also encapsulates a guanylate cyclase catalytic centre. Using liquid chromatography tandem mass spectrometry, we confirmed that the recombinant cytoplasmic domain of BRI1 generates pmol amounts of cGMP per μg protein with a preference for magnesium over manganese as a co-factor. Importantly, a functional BRI1 kinase is essential for optimal cGMP generation. Therefore, the guanylate cyclase activity of BRI1 is modulated by the kinase while cGMP, the product of the guanylate cyclase, in turn inhibits BRI1 kinase activity. Furthermore, we show using Arabidopsis root cell cultures that cGMP rapidly potentiates phosphorylation of the downstream substrate BRASSINOSTEROID SIGNALING KINASE 1 (BSK1). Taken together, our results suggest that cGMP acts as a modulator that enhances downstream signaling while dampening signal generation from the receptor. This article is protected by copyright. All rights reserved.

AB - The brassinosteroid receptor BRASSINOSTEROID INSENSITIVE 1 (BRI1) is a member of the leucine rich repeat receptor like kinase family. The intracellular kinase domain of BRI1 is an active kinase and also encapsulates a guanylate cyclase catalytic centre. Using liquid chromatography tandem mass spectrometry, we confirmed that the recombinant cytoplasmic domain of BRI1 generates pmol amounts of cGMP per μg protein with a preference for magnesium over manganese as a co-factor. Importantly, a functional BRI1 kinase is essential for optimal cGMP generation. Therefore, the guanylate cyclase activity of BRI1 is modulated by the kinase while cGMP, the product of the guanylate cyclase, in turn inhibits BRI1 kinase activity. Furthermore, we show using Arabidopsis root cell cultures that cGMP rapidly potentiates phosphorylation of the downstream substrate BRASSINOSTEROID SIGNALING KINASE 1 (BSK1). Taken together, our results suggest that cGMP acts as a modulator that enhances downstream signaling while dampening signal generation from the receptor. This article is protected by copyright. All rights reserved.

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The brassinosteroid receptor BRI1 can generate cGMP enabling cGMP-dependent downstream signaling

Abstract

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