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

Research output: Contribution to journalArticle

37 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 (30 -phosphoadenosine 50 - 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 Ca2+; 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 languageEnglish (US)
Article numbere23361
JournaleLife
Volume6
DOIs
StatePublished - Mar 21 2017

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Abscisic Acid
Chloroplasts
Germination
Phosphates
Seeds
Gene expression
Seed
Gene Expression
Droughts
Ion Channels
Arabidopsis
Drought
Organelles
Anions
Hormones

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A chloroplast retrograde signal, 3’phosphoadenosine 5’-phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination. / Pornsiriwong, Wannarat; Estavillo, Gonzalo M.; Chan, Kai Xun; Tee, Estee E.; Ganguly, Diep; Crisp, Peter A.; Phua, Su Yin; Zhao, Chenchen; Qiu, Jiaen; Park, Jiyoung; Yong, Miing Tiem; Nisar, Nazia; Yadav, Arun Kumar; Schwessinger, Benjamin; Rathjen, John; Cazzonelli, Christopher I.; Wilson, Philippa B.; Gilliham, Matthew; Chen, Zhong Hua; Pogson, Barry J.

In: eLife, Vol. 6, e23361, 21.03.2017.

Research output: Contribution to journalArticle

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, ZH & 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. https://doi.org/10.7554/eLife.23361
Pornsiriwong, Wannarat ; Estavillo, Gonzalo M. ; Chan, Kai Xun ; Tee, Estee E. ; Ganguly, Diep ; Crisp, Peter A. ; Phua, Su Yin ; Zhao, Chenchen ; Qiu, Jiaen ; Park, Jiyoung ; Yong, Miing Tiem ; Nisar, Nazia ; Yadav, Arun Kumar ; Schwessinger, Benjamin ; Rathjen, John ; Cazzonelli, Christopher I. ; Wilson, Philippa B. ; Gilliham, Matthew ; Chen, Zhong Hua ; Pogson, Barry J. / A chloroplast retrograde signal, 3’phosphoadenosine 5’-phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination. In: eLife. 2017 ; Vol. 6.
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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 (30 -phosphoadenosine 50 - 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 Ca2+; 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.",
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AU - Chan, Kai Xun

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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.

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