A chloroplast retrograde signal, 3'-phosphoadenosine 5'-phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination

Wannarat Pornsiriwong; Gonzalo M. Estavillo; Kai Xun Chan; Estee E. Tee; Diep Ganguly; Peter A. Crisp; Su Yin Phua; Chenchen Zhao; Jiaen Qiu; Jiyoung Park; Miing Tiem Yong; Nazia Nisar; Arun Kumar Yadav; Benjamin Schwessinger; John Rathjen; Christopher I. Cazzonelli; Philippa B. Wilson; Matthew Gilliham; Zhong-Hua Chen; Barry J. Pogson

A chloroplast retrograde signal, 3'-phosphoadenosine 5'-phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination

Wannarat Pornsiriwong, Gonzalo M. Estavillo, Kai Xun Chan, Estee E. Tee, Diep Ganguly, Peter A. Crisp, Su Yin Phua, Chenchen Zhao, Jiaen Qiu, Jiyoung Park, Miing Tiem Yong, Nazia Nisar, Arun Kumar Yadav, Benjamin Schwessinger, John Rathjen, Christopher I. Cazzonelli, Philippa B. Wilson, Matthew Gilliham, Zhong-Hua Chen, Barry J. Pogson

Western Sydney University

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

127 Citations (Scopus)

Abstract

Organelle-nuclear retrograde signaling regulates gene expression, but its roles in specialized cells and integration with hormonal signaling remain enigmatic. Here we show that the SAL1-PAP (3 0 -phosphoadenosine 5 0 - phosphate) retrograde pathway interacts with abscisic acid (ABA) signaling to regulate stomatal closure and seed germination in Arabidopsis. Genetically or exogenously manipulating PAP bypasses the canonical signaling components ABA Insensitive 1 (ABI1) and Open Stomata 1 (OST1); priming an alternative pathway that restores ABA-responsive gene expression, ROS bursts, ion channel function, stomatal closure and drought tolerance in ost12. PAP also inhibits wild type and abi1-1 seed germination by enhancing ABA sensitivity. PAP-XRN signaling interacts with ABA, ROS and Ca 2+; up-regulating multiple ABA signaling components, including lowly-expressed Calcium Dependent Protein Kinases (CDPKs) capable of activating the anion channel SLAC1. Thus, PAP exhibits many secondary messenger attributes and exemplifies how retrograde signals can have broader roles in hormone signaling, allowing chloroplasts to finetune physiological responses.

Original language	English
Article number	e23361
Number of pages	34
Journal	eLife
Volume	6
Publication status	Published - 21 Mar 2017

Bibliographical note

Publisher Copyright:
© Pornsiriwong et al.

Open Access - Access Right Statement

Copyright Pornsiriwong et al. This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use and redistribution provided that the original author and source are credited.

Keywords

abscisic acid
arabidopsis
chloroplasts
gene expression

Cite this

Pornsiriwong, W., Estavillo, G. M., Chan, K. X., Tee, E. E., Ganguly, D., Crisp, P. A., Phua, S. Y., Zhao, C., Qiu, J., Park, J., Yong, M. T., Nisar, N., Yadav, A. K., Schwessinger, B., Rathjen, J., Cazzonelli, C. I., Wilson, P. B., Gilliham, M., Chen, Z.-H., & Pogson, B. J. (2017). A chloroplast retrograde signal, 3'-phosphoadenosine 5'-phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination. eLife, 6, Article e23361.

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title = "A chloroplast retrograde signal, 3'-phosphoadenosine 5'-phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination",

abstract = "Organelle-nuclear retrograde signaling regulates gene expression, but its roles in specialized cells and integration with hormonal signaling remain enigmatic. Here we show that the SAL1-PAP (3 0 -phosphoadenosine 5 0 - phosphate) retrograde pathway interacts with abscisic acid (ABA) signaling to regulate stomatal closure and seed germination in Arabidopsis. Genetically or exogenously manipulating PAP bypasses the canonical signaling components ABA Insensitive 1 (ABI1) and Open Stomata 1 (OST1); priming an alternative pathway that restores ABA-responsive gene expression, ROS bursts, ion channel function, stomatal closure and drought tolerance in ost12. PAP also inhibits wild type and abi1-1 seed germination by enhancing ABA sensitivity. PAP-XRN signaling interacts with ABA, ROS and Ca 2+; up-regulating multiple ABA signaling components, including lowly-expressed Calcium Dependent Protein Kinases (CDPKs) capable of activating the anion channel SLAC1. Thus, PAP exhibits many secondary messenger attributes and exemplifies how retrograde signals can have broader roles in hormone signaling, allowing chloroplasts to finetune physiological responses.",

keywords = "abscisic acid, arabidopsis, chloroplasts, gene expression",

author = "Wannarat Pornsiriwong and Estavillo, {Gonzalo M.} and Chan, {Kai Xun} and Tee, {Estee E.} and Diep Ganguly and Crisp, {Peter A.} and Phua, {Su Yin} and Chenchen Zhao and Jiaen Qiu and Jiyoung Park and Yong, {Miing Tiem} and Nazia Nisar and Yadav, {Arun Kumar} and Benjamin Schwessinger and John Rathjen and Cazzonelli, {Christopher I.} and Wilson, {Philippa B.} and Matthew Gilliham and Zhong-Hua Chen and Pogson, {Barry J.}",

note = "Publisher Copyright: {\textcopyright} Pornsiriwong et al.",

year = "2017",

month = mar,

day = "21",

language = "English",

volume = "6",

journal = "eLife",

issn = "2050-084X",

publisher = "eLife Sciences Publications Ltd",

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Pornsiriwong, W, Estavillo, GM, Chan, KX, Tee, EE, Ganguly, D, Crisp, PA, Phua, SY, Zhao, C, Qiu, J, Park, J, Yong, MT, Nisar, N, Yadav, AK, Schwessinger, B, Rathjen, J, Cazzonelli, CI, Wilson, PB, Gilliham, M, Chen, Z-H & Pogson, BJ 2017, 'A chloroplast retrograde signal, 3'-phosphoadenosine 5'-phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination', eLife, vol. 6, e23361.

TY - JOUR

T1 - A chloroplast retrograde signal, 3'-phosphoadenosine 5'-phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination

AU - Pornsiriwong, Wannarat

AU - Estavillo, Gonzalo M.

AU - Chan, Kai Xun

AU - Tee, Estee E.

AU - Ganguly, Diep

AU - Crisp, Peter A.

AU - Phua, Su Yin

AU - Zhao, Chenchen

AU - Qiu, Jiaen

AU - Park, Jiyoung

AU - Yong, Miing Tiem

AU - Nisar, Nazia

AU - Yadav, Arun Kumar

AU - Schwessinger, Benjamin

AU - Rathjen, John

AU - Cazzonelli, Christopher I.

AU - Wilson, Philippa B.

AU - Gilliham, Matthew

AU - Chen, Zhong-Hua

AU - Pogson, Barry J.

PY - 2017/3/21

Y1 - 2017/3/21

N2 - Organelle-nuclear retrograde signaling regulates gene expression, but its roles in specialized cells and integration with hormonal signaling remain enigmatic. Here we show that the SAL1-PAP (3 0 -phosphoadenosine 5 0 - phosphate) retrograde pathway interacts with abscisic acid (ABA) signaling to regulate stomatal closure and seed germination in Arabidopsis. Genetically or exogenously manipulating PAP bypasses the canonical signaling components ABA Insensitive 1 (ABI1) and Open Stomata 1 (OST1); priming an alternative pathway that restores ABA-responsive gene expression, ROS bursts, ion channel function, stomatal closure and drought tolerance in ost12. PAP also inhibits wild type and abi1-1 seed germination by enhancing ABA sensitivity. PAP-XRN signaling interacts with ABA, ROS and Ca 2+; up-regulating multiple ABA signaling components, including lowly-expressed Calcium Dependent Protein Kinases (CDPKs) capable of activating the anion channel SLAC1. Thus, PAP exhibits many secondary messenger attributes and exemplifies how retrograde signals can have broader roles in hormone signaling, allowing chloroplasts to finetune physiological responses.

AB - Organelle-nuclear retrograde signaling regulates gene expression, but its roles in specialized cells and integration with hormonal signaling remain enigmatic. Here we show that the SAL1-PAP (3 0 -phosphoadenosine 5 0 - phosphate) retrograde pathway interacts with abscisic acid (ABA) signaling to regulate stomatal closure and seed germination in Arabidopsis. Genetically or exogenously manipulating PAP bypasses the canonical signaling components ABA Insensitive 1 (ABI1) and Open Stomata 1 (OST1); priming an alternative pathway that restores ABA-responsive gene expression, ROS bursts, ion channel function, stomatal closure and drought tolerance in ost12. PAP also inhibits wild type and abi1-1 seed germination by enhancing ABA sensitivity. PAP-XRN signaling interacts with ABA, ROS and Ca 2+; up-regulating multiple ABA signaling components, including lowly-expressed Calcium Dependent Protein Kinases (CDPKs) capable of activating the anion channel SLAC1. Thus, PAP exhibits many secondary messenger attributes and exemplifies how retrograde signals can have broader roles in hormone signaling, allowing chloroplasts to finetune physiological responses.

KW - abscisic acid

KW - arabidopsis

KW - chloroplasts

KW - gene expression

UR - http://hdl.handle.net/1959.7/uws:39672

M3 - Article

SN - 2050-084X

VL - 6

JO - eLife

JF - eLife

M1 - e23361

ER -

A chloroplast retrograde signal, 3'-phosphoadenosine 5'-phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination

Abstract

Bibliographical note

Open Access - Access Right Statement

Keywords

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