1. Plant Biology
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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

  1. Wannarat Pornsiriwong
  2. Gonzalo M Estavillo
  3. Kai Xun Chan
  4. Estee E Tee
  5. Diep Ganguly
  6. Peter A Crisp
  7. Su Yin Phua
  8. Chenchen Zhao
  9. Jiaen Qiu
  10. Jiyoung Park
  11. Miing Tiem Yong
  12. Nazia Nisar
  13. Arun Kumar Yadav
  14. Benjamin Schwessinger
  15. John Rathjen
  16. Christopher I Cazzonelli
  17. Philippa B Wilson
  18. Matthew Gilliham
  19. Zhong-Hua Chen
  20. Barry J Pogson  Is a corresponding author
  1. Faculty of Science, Kasetsart University, Thailand
  2. CSIRO Agriculture, Australia
  3. The Australian National University, Australia
  4. Western Sydney University, Australia
  5. University of Adelaide, Australia
  6. University of California, San Diego, United States
Research Article
  • Cited 69
  • Views 4,333
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Cite this article as: eLife 2017;6:e23361 doi: 10.7554/eLife.23361

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.

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Article and author information

Author details

  1. Wannarat Pornsiriwong

    Department of Biochemistry, Faculty of Science, Kasetsart University, Bangkok, Thailand
    Competing interests
    The authors declare that no competing interests exist.
  2. Gonzalo M Estavillo

    CSIRO Agriculture, Canberra, Australia
    Competing interests
    The authors declare that no competing interests exist.
  3. Kai Xun Chan

    ARC Centre of Excellence in Plant Energy Biology, The Australian National University, Acton, Australia
    Competing interests
    The authors declare that no competing interests exist.
  4. Estee E Tee

    ARC Centre of Excellence in Plant Energy Biology, The Australian National University, Acton, Australia
    Competing interests
    The authors declare that no competing interests exist.
  5. Diep Ganguly

    ARC Centre of Excellence in Plant Energy Biology, The Australian National University, Acton, Australia
    Competing interests
    The authors declare that no competing interests exist.
  6. Peter A Crisp

    ARC Centre of Excellence in Plant Energy Biology, The Australian National University, Acton, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3655-0130
  7. Su Yin Phua

    ARC Centre of Excellence in Plant Energy Biology, The Australian National University, Acton, Australia
    Competing interests
    The authors declare that no competing interests exist.
  8. Chenchen Zhao

    School of Science and Health, Western Sydney University, Richmond, Australia
    Competing interests
    The authors declare that no competing interests exist.
  9. Jiaen Qiu

    ARC Centre of Excellence in Plant Energy Biology, University of Adelaide, Adelaide, Australia
    Competing interests
    The authors declare that no competing interests exist.
  10. Jiyoung Park

    Division of Biological Sciences, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Miing Tiem Yong

    School of Science and Health, Western Sydney University, Richmond, Australia
    Competing interests
    The authors declare that no competing interests exist.
  12. Nazia Nisar

    ARC Centre of Excellence in Plant Energy Biology, The Australian National University, Acton, Australia
    Competing interests
    The authors declare that no competing interests exist.
  13. Arun Kumar Yadav

    ARC Centre of Excellence in Plant Energy Biology, The Australian National University, Acton, Australia
    Competing interests
    The authors declare that no competing interests exist.
  14. Benjamin Schwessinger

    Research School of Biology, The Australian National University, Acton, Australia
    Competing interests
    The authors declare that no competing interests exist.
  15. John Rathjen

    Research School of Biology, The Australian National University, Acton, Australia
    Competing interests
    The authors declare that no competing interests exist.
  16. Christopher I Cazzonelli

    Hawkesbury Institute for the Environment, Western Sydney University, Richmond, Australia
    Competing interests
    The authors declare that no competing interests exist.
  17. Philippa B Wilson

    ARC Centre of Excellence in Plant Energy Biology, The Australian National University, Acton, Australia
    Competing interests
    The authors declare that no competing interests exist.
  18. Matthew Gilliham

    ARC Centre of Excellence in Plant Energy Biology, University of Adelaide, Adelaide, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0666-3078
  19. Zhong-Hua Chen

    School of Science and Health, Western Sydney University, Richmond, Australia
    Competing interests
    The authors declare that no competing interests exist.
  20. Barry J Pogson

    ARC Centre of Excellence in Plant Energy Biology, The Australian National University, Acton, Australia
    For correspondence
    barry.pogson@anu.edu.au
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1869-2423

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.

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).

Reviewing Editor

  1. Dominique C Bergmann, Stanford University/HHMI, United States

Publication history

  1. Received: November 16, 2016
  2. Accepted: March 16, 2017
  3. Accepted Manuscript published: March 21, 2017 (version 1)
  4. Version of Record published: April 26, 2017 (version 2)
  5. 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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Further reading

    1. Plant Biology
    Sonia Accossato et al.
    Short Report Updated

    Chloroplast biogenesis describes the transition of non-photosynthetic proplastids to photosynthetically active chloroplasts in the cells of germinating seeds. Chloroplast biogenesis requires the import of thousands of nuclear-encoded preproteins by essential import receptor TOC159. We demonstrate that the small ubiquitin-related modifier (SUMO) pathway crosstalks with the ubiquitin–proteasome pathway to affect TOC159 stability during early plant development. We identified a SUMO3-interacting motif (SIM) in the TOC159 GTPase domain and a SUMO3 covalent SUMOylation site in the membrane domain. A single K to R substitution (K1370R) in the M-domain disables SUMOylation. Compared to wild-type TOC159, TOC159K1370R was destabilized under UPS-inducing stress conditions. However, TOC159K1370R recovered to same protein level as wild-type TOC159 in the presence of a proteasome inhibitor. Thus, SUMOylation partially stabilizes TOC159 against UPS-dependent degradation under stress conditions. Our data contribute to the evolving model of tightly controlled proteostasis of the TOC159 import receptor during proplastid to chloroplast transition.

    1. Cell Biology
    2. Plant Biology
    Samuel James Watson et al.
    Research Article Updated

    The chloroplast proteome contains thousands of different proteins that are encoded by the nuclear genome. These proteins are imported into the chloroplast via the action of the TOC translocase and associated downstream systems. Our recent work has revealed that the stability of the TOC complex is dynamically regulated by the ubiquitin-dependent chloroplast-associated protein degradation pathway. Here, we demonstrate that the TOC complex is also regulated by the small ubiquitin-like modifier (SUMO) system. Arabidopsis mutants representing almost the entire SUMO conjugation pathway can partially suppress the phenotype of ppi1, a pale-yellow mutant lacking the Toc33 protein. This suppression is linked to increased abundance of TOC proteins and improvements in chloroplast development. Moreover, data from molecular and biochemical experiments support a model in which the SUMO system directly regulates TOC protein stability. Thus, we have identified a regulatory link between the SUMO system and the chloroplast protein import machinery.