A chloroplast retrograde signal, 3'-phosphoadenosine 5'-phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination
- Faculty of Science, Kasetsart University, Thailand
- CSIRO Agriculture, Australia
- The Australian National University, Australia
- Western Sydney University, Australia
- University of Adelaide, Australia
- University of California, San Diego, United States
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.
Data availability
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Gene expression profiling of retrograde PAP-signaling and ABA-signaling mutants in response to ABA treatmentPublicly available at the NCBI Gene Expression Omnibus (accession no: GSE84997).
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Transcriptome analysis of Arabidopsis thaliana G protein subunit mutants in response to abscisic acid (ABA)Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE19520).
Article and author information
Author details
Funding
Australian Research Council (CE140100008)
- Wannarat Pornsiriwong
- Gonzalo M Estavillo
- Kai Xun Chan
- Estee E Tee
- Diep Ganguly
- Peter A Crisp
- Su Yin Phua
- Jiaen Qiu
- Nazia Nisar
- Arun Kumar Yadav
- Christopher I Cazzonelli
- Philippa B Wilson
- Matthew Gilliham
National Institutes of Health (GM060396)
- Jiyoung Park
Human Frontier Science Program
- Jiyoung Park
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Dominique C Bergmann, Stanford University/HHMI, United States
Ethics
Animal experimentation: All experimentation involving Xenopus oocytes were performed in strict accordance to the University of Adelaide ethics committee guidelines. All Xenopus experiments received ethical approval (Animal Ethics Application # S-2014-192, University of Adelaide).
Version history
- Received: November 16, 2016
- Accepted: March 16, 2017
- Accepted Manuscript published: March 21, 2017 (version 1)
- Version of Record published: April 26, 2017 (version 2)
- Version of Record updated: May 5, 2017 (version 3)
Copyright
© 2017, Pornsiriwong et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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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
eLife 6:e23361.
https://doi.org/10.7554/eLife.23361
