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

Research output: Contribution to journalArticlepeer-review

63 Scopus citations

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 (30 -phosphoadenosine 50 - 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 ost12. 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 finetune physiological responses.

Original languageEnglish (US)
Article numbere23361
JournaleLife
Volume6
DOIs
StatePublished - Mar 21 2017

Bibliographical note

Funding Information:
We thank J Schroeder (UC San Diego), S Assmann (Penn State Univ), I Small (Univ. Western Australia), as well as S Tyerman (Univ. Adelaide) for advice and critical comments; S Cutler (UC Riverside) for the snrk triple mutant; M Knight (Durham) for the cas mutant; Y Todoroki (Shizuoka Univ) for providing AS2; T Neeman, E Williams and K Murray (ANU) for help with statistical analyses; M Pitt for initial work on the double mutants; B Zhang and MR Blatt (Glasgow Univ) for plasmid DNAs of ion channels; WSU Confocal Bio-Imaging Facility for usage of confocal microscope; A Athman (Univ. Adelaide) for cloning and in-situ PCR assistance; S Yee (Australian National University) for work on the Col-0 background double mutants, Z-Y Wang (Australian National University) for assistance with the ost1-2 xrn2-1 xrn3-3 triple mutants, J Jimenez-Berni, R White and P Chandler (CSIRO) for help with infra-red thermography, microscopy, and the methods for ABA quantification, respectively. We received financial support from the ARC Centre of Excellence in Plant Energy Biology (CE140100008) and scholarships to WP (Thai Government and ScAWAKE), KXC (ANU), PAC (Grains Research Development Council), PBW (Meat and Livestock Australia), SYP (ANU), DG (GRDC, ANU), EET (ANU) and JP (HFSP Long-term fellowship). ZHC is supported by an ARC DECRA (DE140101143) and a 1000-Plan Project, China. A National Institutes of Health grant (GM060396) awarded to Julian Schroeder also funded research in this manuscript. Array data is available at NCBI GEO Database (GSE84997).

Publisher Copyright:
© Pornsiriwong et al.

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