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

Elife. 2017 Mar 21:6:e23361. doi: 10.7554/eLife.23361.

Authors

Wannarat Pornsiriwong^{1

2}, Gonzalo M Estavillo^{1

3}, Kai Xun Chan¹, Estee E Tee¹, Diep Ganguly¹, Peter A Crisp¹, Su Yin Phua¹, Chenchen Zhao⁴, Jiaen Qiu^{5

6}, Jiyoung Park⁷, Miing Tiem Yong⁴, Nazia Nisar¹, Arun Kumar Yadav¹, Benjamin Schwessinger⁸, John Rathjen⁸, Christopher I Cazzonelli^{1

9}, Philippa B Wilson¹, Matthew Gilliham⁵, Zhong-Hua Chen^{4

10}, Barry J Pogson¹

Affiliations

¹ ARC Centre of Excellence in Plant Energy Biology, Research School of Biology, The Australian National University, Acton, Australia.
² Department of Biochemistry, Faculty of Science, Kasetsart University, Bangkok, Thailand.
³ CSIRO Agriculture and Food, Acton, Australia.
⁴ School of Science and Health, Western Sydney University, Richmond, Australia.
⁵ ARC Centre of Excellence in Plant Energy Biology, Department of Plant Science, School of Agriculture, Food and Wine, University of Adelaide, Glen Osmond, Australia.
⁶ Waite Research Institute, University of Adelaide, Glen Osmond, Australia.
⁷ Division of Biological Sciences, Cell and Developmental Biology Section, University of California, San Diego, San Diego, United States.
⁸ Research School of Biology, The Australian National University, Acton, Australia.
⁹ Hawkesbury Institute for the Environment, Western Sydney University, Richmond, Australia.
¹⁰ College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China.

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'-phosphoadenosine 5'- 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 ost1-2. 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 fine-tune physiological responses.

Keywords: 3'-phosphoadenosine 5'-phosphate; A. thaliana; ABA signaling; chloroplast; plant biology; retrograde signaling; seed germination; stomatal closure; xenopus.

Publication types

Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural

MeSH terms

Abscisic Acid / metabolism*
Adenosine Diphosphate / metabolism*
Arabidopsis / physiology*
Chloroplasts / metabolism*
Gene Expression Regulation, Plant
Germination*
Plant Growth Regulators / metabolism
Plant Stomata / physiology*
Signal Transduction*

Substances

Plant Growth Regulators
Adenosine Diphosphate
Abscisic Acid
adenosine 3'-phosphate-5'-phosphate

Grants and funding

R01 GM060396/GM/NIGMS NIH HHS/United States