An NADPH-Oxidase/Polyamine Oxidase Feedback Loop Controls Oxidative Burst Under Salinity.
The apoplastic polyamine oxidase (PAO) catalyzes the oxidation of the higher polyamines spermidine and spermine, contributing to hydrogen peroxide (H2O2) accumulation. However, it is yet unclear whether apoplastic PAO is part of a network that coordinates the accumulation of reactive oxygen species (ROS) under salinity or if it acts independently. Here, we unravel that NADPH oxidase and apoplastic PAO cooperate to control the accumulation of H2O2and superoxides (O2·-) in tobacco (Nicotiana tabacum). To examine to what extent apoplastic PAO constitutes part of a ROS-generating network, we examined ROS accumulation in guard cells of plants overexpressing or down-regulating apoplastic PAO (lines S2.2 and A2, respectively) or down-regulating NADPH oxidase (line AS-NtRbohD/F). The H2O2-specific probe benzene sulfonyl-H2O2showed that, under salinity, H2O2increased in S2.2 and decreased in A2 compared with the wild type. Surprisingly, the O2·--specific probe benzene sulfonyl-So showed that O2·-levels correlated positively with that of apoplastic PAO (i.e. showed high and low levels in S2.2 and A2, respectively). By using AS-NtRbohD/F lines and a pharmacological approach, we could show that H2O2and O2·-accumulation at the onset of salinity stress was dependent on NADPH oxidase, indicating that NADPH oxidase is upstream of apoplastic PAO. Our results suggest that NADPH oxidase and the apoplastic PAO form a feed-forward ROS amplification loop, which impinges on oxidative state and culminates in the execution of programmed cell death. We propose that the PAO/NADPH oxidase loop is a central hub in the plethora of responses controlling salt stress tolerance, with potential functions extending beyond stress tolerance.
Department of Biology, University of Crete, Voutes University Campus, Heraklion 700 13, Greece (K.G., E.A., K.A.R.-A.).|Department of Biology, Sunchon National University, 57922 Chonnam, South Korea (Y.J.K., K.Y.P.).|Department of Plant Biology and Linnean Center of Plant Sciences, Swedish University of Agricultural Sciences, Uppsala BioCentrum, 750 07 Uppsala, Sweden (P.N.M.).|Department of Biology, National and Kapodistrian University of Athens, Panepistimioupolis, Ilissia, Athens 118 55, Greece (C.V., A.R.); and.|Biological Research Centre, Hungarian Academy of Sciences, H-6726 Szeged, Hungary (K.G.).
Katalin
0000-0002-5631-6843
K
Gémes
Department of Biology, University of Crete, Voutes University Campus, Heraklion 700 13, Greece (K.G., E.A., K.A.R.-A.).|Department of Biology, Sunchon National University, 57922 Chonnam, South Korea (Y.J.K., K.Y.P.).|Department of Plant Biology and Linnean Center of Plant Sciences, Swedish University of Agricultural Sciences, Uppsala BioCentrum, 750 07 Uppsala, Sweden (P.N.M.).|Department of Biology, National and Kapodistrian University of Athens, Panepistimioupolis, Ilissia, Athens 118 55, Greece (C.V., A.R.); and.|Biological Research Centre, Hungarian Academy of Sciences, H-6726 Szeged, Hungary (K.G.).
Yu Jung
0000-0002-1233-250X
YJ
Kim
Department of Biology, University of Crete, Voutes University Campus, Heraklion 700 13, Greece (K.G., E.A., K.A.R.-A.); plpm@sunchon.ac.kr panagiotis.moschou@slu.se poproube@biology.uoc.gr.|Department of Biology, Sunchon National University, 57922 Chonnam, South Korea (Y.J.K., K.Y.P.); plpm@sunchon.ac.kr panagiotis.moschou@slu.se poproube@biology.uoc.gr.|Department of Plant Biology and Linnean Center of Plant Sciences, Swedish University of Agricultural Sciences, Uppsala BioCentrum, 750 07 Uppsala, Sweden (P.N.M.); plpm@sunchon.ac.kr panagiotis.moschou@slu.se poproube@biology.uoc.gr.|Department of Biology, National and Kapodistrian University of Athens, Panepistimioupolis, Ilissia, Athens 118 55, Greece (C.V., A.R.); and plpm@sunchon.ac.kr panagiotis.moschou@slu.se poproube@biology.uoc.gr.|Biological Research Centre, Hungarian Academy of Sciences, H-6726 Szeged, Hungary (K.G.) plpm@sunchon.ac.kr panagiotis.moschou@slu.se poproube@biology.uoc.gr.
Ky Young
KY
Park
Department of Biology, University of Crete, Voutes University Campus, Heraklion 700 13, Greece (K.G., E.A., K.A.R.-A.); plpm@sunchon.ac.kr panagiotis.moschou@slu.se poproube@biology.uoc.gr.|Department of Biology, Sunchon National University, 57922 Chonnam, South Korea (Y.J.K., K.Y.P.); plpm@sunchon.ac.kr panagiotis.moschou@slu.se poproube@biology.uoc.gr.|Department of Plant Biology and Linnean Center of Plant Sciences, Swedish University of Agricultural Sciences, Uppsala BioCentrum, 750 07 Uppsala, Sweden (P.N.M.); plpm@sunchon.ac.kr panagiotis.moschou@slu.se poproube@biology.uoc.gr.|Department of Biology, National and Kapodistrian University of Athens, Panepistimioupolis, Ilissia, Athens 118 55, Greece (C.V., A.R.); and plpm@sunchon.ac.kr panagiotis.moschou@slu.se poproube@biology.uoc.gr.|Biological Research Centre, Hungarian Academy of Sciences, H-6726 Szeged, Hungary (K.G.) plpm@sunchon.ac.kr panagiotis.moschou@slu.se poproube@biology.uoc.gr.
Panagiotis N
0000-0001-7212-0595
PN
Moschou
Department of Biology, University of Crete, Voutes University Campus, Heraklion 700 13, Greece (K.G., E.A., K.A.R.-A.).|Department of Biology, Sunchon National University, 57922 Chonnam, South Korea (Y.J.K., K.Y.P.).|Department of Plant Biology and Linnean Center of Plant Sciences, Swedish University of Agricultural Sciences, Uppsala BioCentrum, 750 07 Uppsala, Sweden (P.N.M.).|Department of Biology, National and Kapodistrian University of Athens, Panepistimioupolis, Ilissia, Athens 118 55, Greece (C.V., A.R.); and.|Biological Research Centre, Hungarian Academy of Sciences, H-6726 Szeged, Hungary (K.G.).
Efthimios
0000-0003-4072-3599
E
Andronis
Department of Biology, University of Crete, Voutes University Campus, Heraklion 700 13, Greece (K.G., E.A., K.A.R.-A.).|Department of Biology, Sunchon National University, 57922 Chonnam, South Korea (Y.J.K., K.Y.P.).|Department of Plant Biology and Linnean Center of Plant Sciences, Swedish University of Agricultural Sciences, Uppsala BioCentrum, 750 07 Uppsala, Sweden (P.N.M.).|Department of Biology, National and Kapodistrian University of Athens, Panepistimioupolis, Ilissia, Athens 118 55, Greece (C.V., A.R.); and.|Biological Research Centre, Hungarian Academy of Sciences, H-6726 Szeged, Hungary (K.G.).
Chryssanthi
C
Valassaki
Department of Biology, University of Crete, Voutes University Campus, Heraklion 700 13, Greece (K.G., E.A., K.A.R.-A.).|Department of Biology, Sunchon National University, 57922 Chonnam, South Korea (Y.J.K., K.Y.P.).|Department of Plant Biology and Linnean Center of Plant Sciences, Swedish University of Agricultural Sciences, Uppsala BioCentrum, 750 07 Uppsala, Sweden (P.N.M.).|Department of Biology, National and Kapodistrian University of Athens, Panepistimioupolis, Ilissia, Athens 118 55, Greece (C.V., A.R.); and.|Biological Research Centre, Hungarian Academy of Sciences, H-6726 Szeged, Hungary (K.G.).
Andreas
A
Roussis
Department of Biology, University of Crete, Voutes University Campus, Heraklion 700 13, Greece (K.G., E.A., K.A.R.-A.); plpm@sunchon.ac.kr panagiotis.moschou@slu.se poproube@biology.uoc.gr.|Department of Biology, Sunchon National University, 57922 Chonnam, South Korea (Y.J.K., K.Y.P.); plpm@sunchon.ac.kr panagiotis.moschou@slu.se poproube@biology.uoc.gr.|Department of Plant Biology and Linnean Center of Plant Sciences, Swedish University of Agricultural Sciences, Uppsala BioCentrum, 750 07 Uppsala, Sweden (P.N.M.); plpm@sunchon.ac.kr panagiotis.moschou@slu.se poproube@biology.uoc.gr.|Department of Biology, National and Kapodistrian University of Athens, Panepistimioupolis, Ilissia, Athens 118 55, Greece (C.V., A.R.); and plpm@sunchon.ac.kr panagiotis.moschou@slu.se poproube@biology.uoc.gr.|Biological Research Centre, Hungarian Academy of Sciences, H-6726 Szeged, Hungary (K.G.) plpm@sunchon.ac.kr panagiotis.moschou@slu.se poproube@biology.uoc.gr.
Kalliopi A
0000-0001-8188-6656
KA
Roubelakis-Angelakis
D017209:Apoptosis / Q000187:drug effects; D025461:Feedback, Physiological / Q000187:drug effects; D006861:Hydrogen Peroxide / Q000378:metabolism; D019255:NADPH Oxidases / Q000378:metabolism*; D010084:Oxidation-Reduction / Q000187:drug effects; D000587:Oxidoreductases Acting on CH-NH Group Donors / Q000378:metabolism*; D054046:Plant Stomata / Q000166:cytology / Q000187:drug effects; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D016897:Respiratory Burst / Q000187:drug effects; D054712:Salinity; D012965:Sodium Chloride / Q000494:pharmacology; D013095:Spermidine / Q000378:metabolism; D013481:Superoxides / Q000378:metabolism; D014026:Nicotiana / Q000187:drug effects / Q000378:metabolism*; D000097667:Polyamine Oxidase
D006861:Hydrogen Peroxide; D019255:NADPH Oxidases; D000587:Oxidoreductases Acting on CH-NH Group Donors; D012333:RNA, Messenger; D012965:Sodium Chloride; D013095:Spermidine; D013481:Superoxides; D000097667:Polyamine Oxidase