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
Affiliations
Wannarat Pornsiriwong
ARC Centre of Excellence in Plant Energy Biology, Research School of Biology, The Australian National University, Acton, Australia; Department of Biochemistry, Faculty of Science, Kasetsart University, Bangkok, Thailand
Gonzalo M Estavillo
ARC Centre of Excellence in Plant Energy Biology, Research School of Biology, The Australian National University, Acton, Australia; CSIRO Agriculture and Food, Acton, Australia
ARC Centre of Excellence in Plant Energy Biology, Research School of Biology, The Australian National University, Acton, Australia
Su Yin Phua
ARC Centre of Excellence in Plant Energy Biology, Research School of Biology, The Australian National University, Acton, Australia
Chenchen Zhao
School of Science and Health, Western Sydney University, Richmond, Australia
Jiaen Qiu
ARC Centre of Excellence in Plant Energy Biology, Department of Plant Science, School of Agriculture, Food and Wine, University of Adelaide, Glen Osmond, Australia; Waite Research Institute, University of Adelaide, Glen Osmond, Australia
Jiyoung Park
Division of Biological Sciences, Cell and Developmental Biology Section, University of California, San Diego, San Diego, United States
Miing Tiem Yong
School of Science and Health, Western Sydney University, Richmond, Australia
Nazia Nisar
ARC Centre of Excellence in Plant Energy Biology, Research School of Biology, The Australian National University, Acton, Australia
Arun Kumar Yadav
ARC Centre of Excellence in Plant Energy Biology, Research School of Biology, The Australian National University, Acton, Australia
Benjamin Schwessinger
Research School of Biology, The Australian National University, Acton, Australia
John Rathjen
Research School of Biology, The Australian National University, Acton, Australia
Christopher I Cazzonelli
ARC Centre of Excellence in Plant Energy Biology, Research School of Biology, The Australian National University, Acton, Australia; Hawkesbury Institute for the Environment, Western Sydney University, Richmond, Australia
Philippa B Wilson
ARC Centre of Excellence in Plant Energy Biology, Research School of Biology, The Australian National University, Acton, Australia
ARC Centre of Excellence in Plant Energy Biology, Department of Plant Science, School of Agriculture, Food and Wine, University of Adelaide, Glen Osmond, Australia
Zhong-Hua Chen
School of Science and Health, Western Sydney University, Richmond, Australia; College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China
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.
