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

Author:

Pornsiriwong Wannarat12,Estavillo Gonzalo M13,Chan Kai Xun1ORCID,Tee Estee E1,Ganguly Diep1,Crisp Peter A1ORCID,Phua Su Yin1,Zhao Chenchen4,Qiu Jiaen56,Park Jiyoung7,Yong Miing Tiem4,Nisar Nazia1,Yadav Arun Kumar1,Schwessinger Benjamin8,Rathjen John8,Cazzonelli Christopher I19,Wilson Philippa B1,Gilliham Matthew5ORCID,Chen Zhong-Hua410,Pogson Barry J1ORCID

Affiliation:

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.

Funder

Australian Research Council

ScAwake

Thai Government

The Australian National University

Grains Research and Development Corporation

National Institutes of Health

Human Frontier Science Program

Meat and Livestock Australia

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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