Molecular Targets and Biological Functions of cAMP Signaling in Arabidopsis

Ruqiang Xu; Yanhui Guo; Song Peng; Jinrui Liu; Panyu Li; Wenjing Jia; Junheng Zhao

doi:10.3390/biom11050688

Molecular Targets and Biological Functions of cAMP Signaling in Arabidopsis

Ruqiang Xu, Yanhui Guo, Song Peng, Jinrui Liu, Panyu Li, Wenjing Jia, Junheng Zhao

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

24 Scopus citations

Abstract

Cyclic AMP (cAMP) is a pivotal signaling molecule existing in almost all living organisms. However, the mechanism of cAMP signaling in plants remains very poorly understood. Here, we employ the engineered activity of soluble adenylate cyclase to induce cellular cAMP elevation in Arabidopsis thaliana plants and identify 427 cAMP-responsive genes (CRGs) through RNA-seq analysis. Induction of cellular cAMP elevation inhibits seed germination, disturbs phytohormone contents, promotes leaf senescence, impairs ethylene response, and compromises salt stress tolerance and pathogen resistance. A set of 62 transcription factors are among the CRGs, supporting a prominent role of cAMP in transcriptional regulation. The CRGs are significantly overrepresented in the pathways of plant hormone signal transduction, MAPK signaling, and diterpenoid biosynthesis, but they are also implicated in lipid, sugar, K+, nitrate signaling, and beyond. Our results provide a basic framework of cAMP signaling for the community to explore. The regulatory roles of cAMP signaling in plant plasticity are discussed.

Original language	English (US)
Pages (from-to)	688
Journal	Biomolecules
Volume	11
Issue number	5
DOIs	https://doi.org/10.3390/biom11050688
State	Published - May 3 2021
Externally published	Yes

Bibliographical note

KAUST Repository Item: Exported on 2021-05-10
Acknowledgements: The authors wish to thank Chris Gehring from King Abdullah University of Science and Technology, Saudi Arabia, for providing pDEST17-AtKUP71−100 plasmid. The Gateway@-compatible vector pTA7001-DEST was a gift from Roger Innes (Addgene plasmid # 71745; http:
//n2t.net/addgene:71745 (accessed on 20 March 2021); RRID: Addgene_71745).
This publication acknowledges KAUST support, but has no KAUST affiliated authors.

ASJC Scopus subject areas

General Medicine

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title = "Molecular Targets and Biological Functions of cAMP Signaling in Arabidopsis",

abstract = "Cyclic AMP (cAMP) is a pivotal signaling molecule existing in almost all living organisms. However, the mechanism of cAMP signaling in plants remains very poorly understood. Here, we employ the engineered activity of soluble adenylate cyclase to induce cellular cAMP elevation in Arabidopsis thaliana plants and identify 427 cAMP-responsive genes (CRGs) through RNA-seq analysis. Induction of cellular cAMP elevation inhibits seed germination, disturbs phytohormone contents, promotes leaf senescence, impairs ethylene response, and compromises salt stress tolerance and pathogen resistance. A set of 62 transcription factors are among the CRGs, supporting a prominent role of cAMP in transcriptional regulation. The CRGs are significantly overrepresented in the pathways of plant hormone signal transduction, MAPK signaling, and diterpenoid biosynthesis, but they are also implicated in lipid, sugar, K+, nitrate signaling, and beyond. Our results provide a basic framework of cAMP signaling for the community to explore. The regulatory roles of cAMP signaling in plant plasticity are discussed.",

author = "Ruqiang Xu and Yanhui Guo and Song Peng and Jinrui Liu and Panyu Li and Wenjing Jia and Junheng Zhao",

note = "KAUST Repository Item: Exported on 2021-05-10 Acknowledgements: The authors wish to thank Chris Gehring from King Abdullah University of Science and Technology, Saudi Arabia, for providing pDEST17-AtKUP71−100 plasmid. The Gateway@-compatible vector pTA7001-DEST was a gift from Roger Innes (Addgene plasmid # 71745; http: //n2t.net/addgene:71745 (accessed on 20 March 2021); RRID: Addgene_71745). This publication acknowledges KAUST support, but has no KAUST affiliated authors.",

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AU - Xu, Ruqiang

AU - Guo, Yanhui

AU - Peng, Song

AU - Liu, Jinrui

AU - Li, Panyu

AU - Jia, Wenjing

AU - Zhao, Junheng

N1 - KAUST Repository Item: Exported on 2021-05-10 Acknowledgements: The authors wish to thank Chris Gehring from King Abdullah University of Science and Technology, Saudi Arabia, for providing pDEST17-AtKUP71−100 plasmid. The Gateway@-compatible vector pTA7001-DEST was a gift from Roger Innes (Addgene plasmid # 71745; http: //n2t.net/addgene:71745 (accessed on 20 March 2021); RRID: Addgene_71745). This publication acknowledges KAUST support, but has no KAUST affiliated authors.

PY - 2021/5/3

Y1 - 2021/5/3

N2 - Cyclic AMP (cAMP) is a pivotal signaling molecule existing in almost all living organisms. However, the mechanism of cAMP signaling in plants remains very poorly understood. Here, we employ the engineered activity of soluble adenylate cyclase to induce cellular cAMP elevation in Arabidopsis thaliana plants and identify 427 cAMP-responsive genes (CRGs) through RNA-seq analysis. Induction of cellular cAMP elevation inhibits seed germination, disturbs phytohormone contents, promotes leaf senescence, impairs ethylene response, and compromises salt stress tolerance and pathogen resistance. A set of 62 transcription factors are among the CRGs, supporting a prominent role of cAMP in transcriptional regulation. The CRGs are significantly overrepresented in the pathways of plant hormone signal transduction, MAPK signaling, and diterpenoid biosynthesis, but they are also implicated in lipid, sugar, K+, nitrate signaling, and beyond. Our results provide a basic framework of cAMP signaling for the community to explore. The regulatory roles of cAMP signaling in plant plasticity are discussed.

AB - Cyclic AMP (cAMP) is a pivotal signaling molecule existing in almost all living organisms. However, the mechanism of cAMP signaling in plants remains very poorly understood. Here, we employ the engineered activity of soluble adenylate cyclase to induce cellular cAMP elevation in Arabidopsis thaliana plants and identify 427 cAMP-responsive genes (CRGs) through RNA-seq analysis. Induction of cellular cAMP elevation inhibits seed germination, disturbs phytohormone contents, promotes leaf senescence, impairs ethylene response, and compromises salt stress tolerance and pathogen resistance. A set of 62 transcription factors are among the CRGs, supporting a prominent role of cAMP in transcriptional regulation. The CRGs are significantly overrepresented in the pathways of plant hormone signal transduction, MAPK signaling, and diterpenoid biosynthesis, but they are also implicated in lipid, sugar, K+, nitrate signaling, and beyond. Our results provide a basic framework of cAMP signaling for the community to explore. The regulatory roles of cAMP signaling in plant plasticity are discussed.

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VL - 11

SP - 688

JO - Biomolecules

JF - Biomolecules

IS - 5

ER -

Molecular Targets and Biological Functions of cAMP Signaling in Arabidopsis

Abstract

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