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Salicylic acid-dependent plant stress signaling via mitochondrial succinate dehydrogenase

Belt, Katharina; Huang, Shaobai; Thatcher, Louise F.; Casarotto, Hayley; Singh, Karam B.; Van Aken, Olivier LU and Millar, A. Harvey (2017) In Plant Physiology 173(4). p.2029-2040
Abstract

Mitochondria are known for their role in ATP production and generation of reactive oxygen species, but little is known about the mechanism of their early involvement in plant stress signaling. The role of mitochondrial succinate dehydrogenase (SDH) in salicylic acid (SA) signaling was analyzed using two mutants: disrupted in stress response1 (dsr1), which is a point mutation in SDH1 identified in a loss of SA signaling screen, and a knockdown mutant (sdhaf2) for SDH assembly factor 2 that is required for FAD insertion into SDH1. Both mutants showed strongly decreased SA-inducible stress promoter responses and low SDH maximum capacity compared to wild type, while dsr1 also showed low succinate affinity, low catalytic efficiency, and... (More)

Mitochondria are known for their role in ATP production and generation of reactive oxygen species, but little is known about the mechanism of their early involvement in plant stress signaling. The role of mitochondrial succinate dehydrogenase (SDH) in salicylic acid (SA) signaling was analyzed using two mutants: disrupted in stress response1 (dsr1), which is a point mutation in SDH1 identified in a loss of SA signaling screen, and a knockdown mutant (sdhaf2) for SDH assembly factor 2 that is required for FAD insertion into SDH1. Both mutants showed strongly decreased SA-inducible stress promoter responses and low SDH maximum capacity compared to wild type, while dsr1 also showed low succinate affinity, low catalytic efficiency, and increased resistance to SDH competitive inhibitors. The SA-induced promoter responses could be partially rescued in sdhaf2, but not in dsr1, by supplementing the plant growth media with succinate. Kinetic characterization showed that low concentrations of either SA or ubiquinone binding site inhibitors increased SDH activity and induced mitochondrial H2O2 production. Both dsr1 and sdhaf2 showed lower rates of SA-dependent H2O2 production in vitro in line with their low SA-dependent stress signaling responses in vivo. This provides quantitative and kinetic evidence that SA acts at or near the ubiquinone binding site of SDH to stimulate activity and contributes to plant stress signaling by increased rates of mitochondrial H2O2 production, leading to part of the SA-dependent transcriptional response in plant cells.

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author
publishing date
type
Contribution to journal
publication status
published
subject
in
Plant Physiology
volume
173
issue
4
pages
12 pages
publisher
American Society of Plant Biologists
external identifiers
  • scopus:85016512377
ISSN
0032-0889
DOI
10.1104/pp.16.00060
language
English
LU publication?
no
id
83d2891f-ad8f-4b0f-b4df-2e110a234414
date added to LUP
2017-05-08 09:23:34
date last changed
2018-01-07 12:02:09
@article{83d2891f-ad8f-4b0f-b4df-2e110a234414,
  abstract     = {<p>Mitochondria are known for their role in ATP production and generation of reactive oxygen species, but little is known about the mechanism of their early involvement in plant stress signaling. The role of mitochondrial succinate dehydrogenase (SDH) in salicylic acid (SA) signaling was analyzed using two mutants: disrupted in stress response1 (dsr1), which is a point mutation in SDH1 identified in a loss of SA signaling screen, and a knockdown mutant (sdhaf2) for SDH assembly factor 2 that is required for FAD insertion into SDH1. Both mutants showed strongly decreased SA-inducible stress promoter responses and low SDH maximum capacity compared to wild type, while dsr1 also showed low succinate affinity, low catalytic efficiency, and increased resistance to SDH competitive inhibitors. The SA-induced promoter responses could be partially rescued in sdhaf2, but not in dsr1, by supplementing the plant growth media with succinate. Kinetic characterization showed that low concentrations of either SA or ubiquinone binding site inhibitors increased SDH activity and induced mitochondrial H<sub>2</sub>O<sub>2</sub> production. Both dsr1 and sdhaf2 showed lower rates of SA-dependent H<sub>2</sub>O<sub>2</sub> production in vitro in line with their low SA-dependent stress signaling responses in vivo. This provides quantitative and kinetic evidence that SA acts at or near the ubiquinone binding site of SDH to stimulate activity and contributes to plant stress signaling by increased rates of mitochondrial H<sub>2</sub>O<sub>2</sub> production, leading to part of the SA-dependent transcriptional response in plant cells.</p>},
  author       = {Belt, Katharina and Huang, Shaobai and Thatcher, Louise F. and Casarotto, Hayley and Singh, Karam B. and Van Aken, Olivier and Millar, A. Harvey},
  issn         = {0032-0889},
  language     = {eng},
  month        = {04},
  number       = {4},
  pages        = {2029--2040},
  publisher    = {American Society of Plant Biologists},
  series       = {Plant Physiology},
  title        = {Salicylic acid-dependent plant stress signaling via mitochondrial succinate dehydrogenase},
  url          = {http://dx.doi.org/10.1104/pp.16.00060},
  volume       = {173},
  year         = {2017},
}