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SHORT-ROOT deficiency alleviates the cell death phenotype of the Arabidopsis catalase2 mutant under photorespiration-promoting conditions

Cezary Waszczak, Pavel Kerchev, Per Mühlenbock UGent, Frank Hoeberichts UGent, Katrien Van Der Kelen, Amna Mhamdi, Patrick Willems UGent, Jordi Denecker, Robert Kumpf, Graham Noctor, et al. (2016) PLANT CELL. 28(8). p.1844-1859
abstract
Hydrogen peroxide (H2O2) can act as a signaling molecule that influences various aspects of plant growth and development, including stress signaling and cell death. To analyze molecular mechanisms that regulate the response to increased H2O2 levels in plant cells, we focused on the photorespiration-dependent peroxisomal H2O2 production in Arabidopsis thaliana mutants lacking CATALASE2 (CAT2) activity (cat2-2). By screening for second-site mutations that attenuate the PSII maximum efficiency (F-v'/F-m') decrease and lesion formation linked to the cat2-2 phenotype, we discovered that a mutation in SHORT-ROOT (SHR) rescued the cell death phenotype of cat2-2 plants under photorespiration-promoting conditions. SHR deficiency attenuated H2O2-dependent gene expression, oxidation of the glutathione pool, and ascorbate depletion in a cat2-2 genetic background upon exposure to photorespiratory stress. Decreased glycolate oxidase and catalase activities together with accumulation of glycolate further implied that SHR deficiency impacts the cellular redox homeostasis by limiting peroxisomal H2O2 production. The photorespiratory phenotype of cat2-2 mutants did not depend on the SHR functional interactor SCARECROW and the sugar signaling component ABSCISIC ACID INSENSITIVE4, despite the requirement for exogenous sucrose for cell death attenuation in cat2-2 shr-6 double mutants. Our findings reveal a link between SHR and photorespiratory H2O2 production that has implications for the integration of developmental and stress responses.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
DEFENSE RESPONSES, SPECTROMETRY DATA, SHOOT GRAVITROPISM, SIGNAL-TRANSDUCTION, GENE-EXPRESSION, RADIAL ORGANIZATION, OXIDATIVE STRESS, PEROXISOMAL HYDROGEN-PEROXIDE, DIFFERENTIAL EXPRESSION ANALYSIS, PLANT DEVELOPMENT
journal title
PLANT CELL
Plant Cell
volume
28
issue
8
pages
1844 - 1859
Web of Science type
Article
Web of Science id
000386169200009
JCR category
PLANT SCIENCES
JCR impact factor
8.688 (2016)
JCR rank
6/211 (2016)
JCR quartile
1 (2016)
ISSN
1040-4651
DOI
10.1105/tpc.16.00038
project
Biotechnology for a sustainable economy (Bio-Economy)
language
English
UGent publication?
yes
classification
A1
additional info
the first two authors contributed equally to this work
copyright statement
I have transferred the copyright for this publication to the publisher
id
8174704
handle
http://hdl.handle.net/1854/LU-8174704
date created
2016-11-28 13:22:33
date last changed
2016-12-19 15:48:37
@article{8174704,
  abstract     = {Hydrogen peroxide (H2O2) can act as a signaling molecule that influences various aspects of plant growth and development, including stress signaling and cell death. To analyze molecular mechanisms that regulate the response to increased H2O2 levels in plant cells, we focused on the photorespiration-dependent peroxisomal H2O2 production in Arabidopsis thaliana mutants lacking CATALASE2 (CAT2) activity (cat2-2). By screening for second-site mutations that attenuate the PSII maximum efficiency (F-v'/F-m') decrease and lesion formation linked to the cat2-2 phenotype, we discovered that a mutation in SHORT-ROOT (SHR) rescued the cell death phenotype of cat2-2 plants under photorespiration-promoting conditions. SHR deficiency attenuated H2O2-dependent gene expression, oxidation of the glutathione pool, and ascorbate depletion in a cat2-2 genetic background upon exposure to photorespiratory stress. Decreased glycolate oxidase and catalase activities together with accumulation of glycolate further implied that SHR deficiency impacts the cellular redox homeostasis by limiting peroxisomal H2O2 production. The photorespiratory phenotype of cat2-2 mutants did not depend on the SHR functional interactor SCARECROW and the sugar signaling component ABSCISIC ACID INSENSITIVE4, despite the requirement for exogenous sucrose for cell death attenuation in cat2-2 shr-6 double mutants. Our findings reveal a link between SHR and photorespiratory H2O2 production that has implications for the integration of developmental and stress responses.},
  author       = {Waszczak, Cezary and Kerchev, Pavel and M{\"u}hlenbock, Per and Hoeberichts, Frank and Van Der Kelen, Katrien and Mhamdi, Amna and Willems, Patrick and Denecker, Jordi and Kumpf, Robert and Noctor, Graham and Messens, Joris and Van Breusegem, Frank},
  issn         = {1040-4651},
  journal      = {PLANT CELL},
  keyword      = {DEFENSE RESPONSES,SPECTROMETRY DATA,SHOOT GRAVITROPISM,SIGNAL-TRANSDUCTION,GENE-EXPRESSION,RADIAL ORGANIZATION,OXIDATIVE STRESS,PEROXISOMAL HYDROGEN-PEROXIDE,DIFFERENTIAL EXPRESSION ANALYSIS,PLANT DEVELOPMENT},
  language     = {eng},
  number       = {8},
  pages        = {1844--1859},
  title        = {SHORT-ROOT deficiency alleviates the cell death phenotype of the Arabidopsis catalase2 mutant under photorespiration-promoting conditions},
  url          = {http://dx.doi.org/10.1105/tpc.16.00038},
  volume       = {28},
  year         = {2016},
}

Chicago
Waszczak, Cezary, Pavel Kerchev, Per Mühlenbock, Frank Hoeberichts, Katrien Van Der Kelen, Amna Mhamdi, Patrick Willems, et al. 2016. “SHORT-ROOT Deficiency Alleviates the Cell Death Phenotype of the Arabidopsis Catalase2 Mutant Under Photorespiration-promoting Conditions.” Plant Cell 28 (8): 1844–1859.
APA
Waszczak, C., Kerchev, P., Mühlenbock, P., Hoeberichts, F., Van Der Kelen, K., Mhamdi, A., Willems, P., et al. (2016). SHORT-ROOT deficiency alleviates the cell death phenotype of the Arabidopsis catalase2 mutant under photorespiration-promoting conditions. PLANT CELL, 28(8), 1844–1859.
Vancouver
1.
Waszczak C, Kerchev P, Mühlenbock P, Hoeberichts F, Van Der Kelen K, Mhamdi A, et al. SHORT-ROOT deficiency alleviates the cell death phenotype of the Arabidopsis catalase2 mutant under photorespiration-promoting conditions. PLANT CELL. 2016;28(8):1844–59.
MLA
Waszczak, Cezary, Pavel Kerchev, Per Mühlenbock, et al. “SHORT-ROOT Deficiency Alleviates the Cell Death Phenotype of the Arabidopsis Catalase2 Mutant Under Photorespiration-promoting Conditions.” PLANT CELL 28.8 (2016): 1844–1859. Print.