Uncoupling High Light Responses from Singlet Oxygen Retrograde Signaling and Spatial-Temporal Systemic Acquired Acclimation.
Distinct ROS signaling pathways initiated by singlet oxygen ((1)O2) or superoxide and hydrogen peroxide have been attributed to either cell death or acclimation, respectively. Recent studies have revealed that more complex antagonistic and synergistic relationships exist within and between these pathways. As specific chloroplastic ROS signals are difficult to study, rapid systemic signaling experiments using localized high light (HL) stress or ROS treatments were used in this study to uncouple signals required for direct HL and ROS perception and distal systemic acquired acclimation (SAA). A qPCR approach was chosen to determine local perception and distal signal reception. Analysis of a thylakoidal ascorbate peroxidase mutant (tapx), the (1)O2-retrograde signaling double mutant (ex1/ex2), and an apoplastic signaling double mutant (rbohD/F) revealed that tAPX and EXECUTER 1 are required for both HL and systemic acclimation stress perception. Apoplastic membrane-localized RBOHs were required for systemic spread of the signal but not for local signal induction in directly stressed tissues. Endogenous ROS treatments revealed a very strong systemic response induced by a localized 1 h induction of (1)O2 using the conditional flu mutant. A qPCR time course of (1)O2 induced systemic marker genes in directly and indirectly connected leaves revealed a direct vascular connection component of both immediate and longer term SAA signaling responses. These results reveal the importance of an EXECUTER-dependent (1)O2 retrograde signal for both local and long distance RBOH-dependent acclimation signaling that is distinct from other HL signaling pathways, and that direct vascular connections have a role in spatial-temporal SAA induction.
Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University, Canberra, Acton ACT 0200, Australia (M.C., P.C., D.G., M.G., V.A.-B., B.J.P.); Division of Plant Biology, Viikki Plant Science Center, Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland (M.C.); andCEA, CNRS, Aix Marseille Université, UMR 7265 Biologie Végétale et Microbiologie Environnementales, Laboratoire d'Ecophysiologie Moléculaire des Plantes, F-13108 Saint-Paul-lez-Durance, France (S.A., M.H.).
Melanie
0000-0001-5989-4801
M
Carmody
Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University, Canberra, Acton ACT 0200, Australia (M.C., P.C., D.G., M.G., V.A.-B., B.J.P.); Division of Plant Biology, Viikki Plant Science Center, Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland (M.C.); andCEA, CNRS, Aix Marseille Université, UMR 7265 Biologie Végétale et Microbiologie Environnementales, Laboratoire d'Ecophysiologie Moléculaire des Plantes, F-13108 Saint-Paul-lez-Durance, France (S.A., M.H.).
Peter A
0000-0002-3655-0130
PA
Crisp
Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University, Canberra, Acton ACT 0200, Australia (M.C., P.C., D.G., M.G., V.A.-B., B.J.P.); Division of Plant Biology, Viikki Plant Science Center, Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland (M.C.); andCEA, CNRS, Aix Marseille Université, UMR 7265 Biologie Végétale et Microbiologie Environnementales, Laboratoire d'Ecophysiologie Moléculaire des Plantes, F-13108 Saint-Paul-lez-Durance, France (S.A., M.H.).
Stefano
0000-0002-0464-5549
S
d'Alessandro
Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University, Canberra, Acton ACT 0200, Australia (M.C., P.C., D.G., M.G., V.A.-B., B.J.P.); Division of Plant Biology, Viikki Plant Science Center, Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland (M.C.); andCEA, CNRS, Aix Marseille Université, UMR 7265 Biologie Végétale et Microbiologie Environnementales, Laboratoire d'Ecophysiologie Moléculaire des Plantes, F-13108 Saint-Paul-lez-Durance, France (S.A., M.H.).
Diep
0000-0001-6746-0181
D
Ganguly
Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University, Canberra, Acton ACT 0200, Australia (M.C., P.C., D.G., M.G., V.A.-B., B.J.P.); Division of Plant Biology, Viikki Plant Science Center, Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland (M.C.); andCEA, CNRS, Aix Marseille Université, UMR 7265 Biologie Végétale et Microbiologie Environnementales, Laboratoire d'Ecophysiologie Moléculaire des Plantes, F-13108 Saint-Paul-lez-Durance, France (S.A., M.H.).
Matthew
M
Gordon
Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University, Canberra, Acton ACT 0200, Australia (M.C., P.C., D.G., M.G., V.A.-B., B.J.P.); Division of Plant Biology, Viikki Plant Science Center, Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland (M.C.); andCEA, CNRS, Aix Marseille Université, UMR 7265 Biologie Végétale et Microbiologie Environnementales, Laboratoire d'Ecophysiologie Moléculaire des Plantes, F-13108 Saint-Paul-lez-Durance, France (S.A., M.H.).
Michel
M
Havaux
Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University, Canberra, Acton ACT 0200, Australia (M.C., P.C., D.G., M.G., V.A.-B., B.J.P.); Division of Plant Biology, Viikki Plant Science Center, Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland (M.C.); andCEA, CNRS, Aix Marseille Université, UMR 7265 Biologie Végétale et Microbiologie Environnementales, Laboratoire d'Ecophysiologie Moléculaire des Plantes, F-13108 Saint-Paul-lez-Durance, France (S.A., M.H.).
Verónica
V
Albrecht-Borth
Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University, Canberra, Acton ACT 0200, Australia (M.C., P.C., D.G., M.G., V.A.-B., B.J.P.); Division of Plant Biology, Viikki Plant Science Center, Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland (M.C.); andCEA, CNRS, Aix Marseille Université, UMR 7265 Biologie Végétale et Microbiologie Environnementales, Laboratoire d'Ecophysiologie Moléculaire des Plantes, F-13108 Saint-Paul-lez-Durance, France (S.A., M.H.) barry.pogson@anu.edu.au.
Barry J
0000-0003-1869-2423
BJ
Pogson
D000064:Acclimatization / Q000502:physiology*; D000447:Aldehydes / Q000378:metabolism; D000872:Anthocyanins / Q000378:metabolism; D017360:Arabidopsis / Q000502:physiology*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D060387:Ascorbate Peroxidases / Q000235:genetics / Q000378:metabolism; D004224:Diterpenes / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D008027:Light; D009154:Mutation; D018515:Plant Leaves / Q000502:physiology; D030821:Plants, Genetically Modified; D017382:Reactive Oxygen Species / Q000378:metabolism; D015398:Signal Transduction; D026082:Singlet Oxygen / Q000378:metabolism*; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism
D000447:Aldehydes; D000872:Anthocyanins; D029681:Arabidopsis Proteins; D060387:Ascorbate Peroxidases; D004224:Diterpenes; D017382:Reactive Oxygen Species; D026082:Singlet Oxygen; D014157:Transcription Factors; C481743:ELIP2 protein, Arabidopsis; C521350:EXECUTER1 protein, Arabidopsis; C535225:RRTF1 protein, Arabidopsis; C516241:STZ protein, Arabidopsis; C516118:beta-cyclocitral