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

doi:10.7554/eLife.23361

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

Plant and Microbial Biology

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

111 Scopus citations

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 language	English (US)
Article number	e23361
Journal	eLife
Volume	6
DOIs	https://doi.org/10.7554/eLife.23361
State	Published - Mar 21 2017

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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. https://doi.org/10.7554/eLife.23361

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

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title = "A chloroplast retrograde signal, 3{\textquoteright}phosphoadenosine 5{\textquoteright}-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 (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.",

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 Chen, {Zhong Hua} and Pogson, {Barry J.}",

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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

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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 (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.

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

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