SAL1-PAP retrograde signaling orchestrates photosynthetic and extracellular reactive oxygen species for stress responses

Simple item page
dc.contributor.authorTee, E.E.
dc.contributor.authorFairweather, S.J.
dc.contributor.authorVo, H.M.
dc.contributor.authorZhao, C.
dc.contributor.authorBreakspear, A.
dc.contributor.authorKimura, S.
dc.contributor.authorCarmody, M.
dc.contributor.authorWrzaczek, M.
dc.contributor.authorBröer, S.
dc.contributor.authorFaulkner, C.
dc.contributor.authorKangasjärvi, J.
dc.contributor.authorChen, Z.-H.
dc.contributor.authorPogson, B.J.
dc.contributor.authorChan, K.X.
dc.date.issued2025
dc.description.abstractCellular responses to abiotic stress involve multiple signals such as reactive oxygen species (ROS), Ca²⁺, abscisic acid (ABA), and chloroplast-to-nucleus retrograde signals such as 3′-phosphoadenosine 5′- -phosphate (PAP). The mechanism(s) by which these messengers intersect for cell regulation remain enigmatic, as do the roles of retrograde signals in specialized cells. Here we demonstrate a mechanistic link enabling ABA and PAP to coordinate chloroplast and plasma membrane ROS production. Contrary to its role in upregulating processes leading to quenching of ROS in foliar tissue, we show that in guard cells, PAP induces chloroplast ROS accumulation via photosynthetic electron transport and apoplast ROS via the RESPIRATORY BURST OXIDASE HOMOLOG (RBOH) proteins. Both subcellular ROS sources are necessary for stress hormone ABA-mediated stomatal closure, as well as PAP-mediated stomatal closure. However, PAP signaling diverges from ABA by activating RBOHD instead of RBOHF. Three calcium-dependent protein kinases (CPKs) transcriptionally induced by PAP, namely CPK13, CPK32, and CPK34, concurrently activate RBOHD and the slow anion channel SLAC1 by phosphorylating two SLAC1 serine (S) residues, including S120, which is also targeted by the ABA signaling kinase OPEN STOMATA 1 (OST1). Consequently, overexpression of the PAP-induced CPKs rescues stomatal closure in ost1. Our data identify chloroplast retrograde signals as critical nodes in cellular stress response networks of guard cells.
dc.description.statementofresponsibilityEstee E. Tee, Stephen J. Fairweather, Hanh M. Vo, Chenchen Zhao, Andrew Breakspear, Sachie Kimura, Melanie Carmody, Michael Wrzaczek, Stefan Bröer, Christine Faulkner, Jaakko Kangasjärvi, Zhong-Hua Chen, Barry J. Pogson, and Kai Xun Chan
dc.identifier.citationThe Plant Journal, 2025; 122(5):e70271-1-e70271-16
dc.identifier.doi10.1111/tpj.70271
dc.identifier.issn0960-7412
dc.identifier.issn1365-313X
dc.identifier.orcidChen, Z.-H. [0000-0002-7531-320X]
dc.identifier.urihttps://hdl.handle.net/2440/147451
dc.language.isoen
dc.publisherWiley
dc.relation.granthttp://purl.org/au-research/grants/arc/DE210100466
dc.relation.granthttp://purl.org/au-research/grants/arc/FT210100366
dc.relation.granthttp://purl.org/au-research/grants/arc/FL190100056
dc.rights© 2025 The Author(s). The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
dc.source.urihttps://doi.org/10.1111/tpj.70271
dc.subjectchloroplast; ROS; retrograde signaling; PAP; SAL1; RESPIRATORY BURST OXIDASE HOMOLOG; calcium-dependent protein kinase; 3`-phosphoadenosine 5`-phosphate (PAP).
dc.subject.meshAbscisic Acid
dc.subject.meshAdenosine Diphosphate
dc.subject.meshArabidopsis
dc.subject.meshArabidopsis Proteins
dc.subject.meshChloroplasts
dc.subject.meshGene Expression Regulation, Plant
dc.subject.meshNADPH Oxidases
dc.subject.meshPhotosynthesis
dc.subject.meshPlant Stomata
dc.subject.meshReactive Oxygen Species
dc.subject.meshSignal Transduction
dc.subject.meshStress, Physiological
dc.titleSAL1-PAP retrograde signaling orchestrates photosynthetic and extracellular reactive oxygen species for stress responses
dc.typeJournal article
pubs.publication-statusPublished

Files

Original bundle
Now showing 1 - 1 of 1
No Thumbnail Available
Name:
hdl_147451.pdf
Size:
2 MB
Format:
Adobe Portable Document Format
Description:
Published version
Download

Collections

Research Outputs