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Chloroplast-generated reactive oxygen species play a major role in localized cell death during the non-host interaction between tobacco and Xanthomonas campestris pv. vesicatoria

Matias Zurbriggen, Néstor Carrillo, Vanesa Tognetti UGent, Michael Melzer, Martin Peisker, Bettina Hause and Mohammad-Reza Hajirezaei (2009) PLANT JOURNAL. 60(6). p.962-973
abstract
Attempted infection of plants by pathogens elicits a complex defensive response. In many non-host and incompatible host interactions it includes the induction of defence-associated genes and a form of localized cell death (LCD), purportedly designed to restrict pathogen advance, collectively known as the hypersensitive response (HR). It is preceded by an oxidative burst, generating reactive oxygen species (ROS) that are proposed to cue subsequent deployment of the HR, although neither the origin nor the precise role played by ROS in the execution of this response are completely understood. We used tobacco plants expressing cyanobacterial flavodoxin to address these questions. Flavodoxin is an electron shuttle present in prokaryotes and algae that, when expressed in chloroplasts, specifically prevents ROS formation in plastids during abiotic stress episodes. Infiltration of tobacco wild-type leaves with high titres of Xanthomonas campestris pv. vesicatoria (Xcv), a non-host pathogen, resulted in ROS accumulation in chloroplasts, followed by the appearance of localized lesions typical of the HR. In contrast, chloroplast ROS build-up and LCD were significantly reduced in Xcv-inoculated plants expressing plastid-targeted flavodoxin. Metabolic routes normally inhibited by pathogens were protected in the transformants, whereas other aspects of the HR, including the induction of defence-associated genes and synthesis of salicylic and jasmonic acid, proceeded as in inoculated wild-type plants. Therefore, ROS generated in chloroplasts during this non-host interaction are essential for the progress of LCD, but do not contribute to the induction of pathogenesis-related genes or other signalling components of the response.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
SYSTEMIC ACQUIRED-RESISTANCE, TRANSGENIC TOBACCO, HYPERSENSITIVE RESPONSE, PATHOGEN INFECTION, SOLANUM-TUBEROSUM, oxidative stress, chloroplasts, non-host resistance, reactive oxygen species, flavodoxin, plant-pathogen interactions, PSEUDOMONAS-SYRINGAE, BACTERIAL FLAVODOXIN, DISEASE RESISTANCE, ARABIDOPSIS-THALIANA, MICROBE INTERACTIONS
journal title
PLANT JOURNAL
Plant J.
volume
60
issue
6
pages
12 pages
Web of Science type
Article
Web of Science id
000272590000004
JCR category
PLANT SCIENCES
JCR impact factor
6.946 (2009)
JCR rank
6/172 (2009)
JCR quartile
1 (2009)
ISSN
0960-7412
DOI
10.1111/j.1365-313X.2009.04010.x
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
846535
handle
http://hdl.handle.net/1854/LU-846535
date created
2010-01-29 18:16:45
date last changed
2010-02-10 15:49:21
@article{846535,
  abstract     = {Attempted infection of plants by pathogens elicits a complex defensive response. In many non-host and incompatible host interactions it includes the induction of defence-associated genes and a form of localized cell death (LCD), purportedly designed to restrict pathogen advance, collectively known as the hypersensitive response (HR). It is preceded by an oxidative burst, generating reactive oxygen species (ROS) that are proposed to cue subsequent deployment of the HR, although neither the origin nor the precise role played by ROS in the execution of this response are completely understood. We used tobacco plants expressing cyanobacterial flavodoxin to address these questions. Flavodoxin is an electron shuttle present in prokaryotes and algae that, when expressed in chloroplasts, specifically prevents ROS formation in plastids during abiotic stress episodes. Infiltration of tobacco wild-type leaves with high titres of Xanthomonas campestris pv. vesicatoria (Xcv), a non-host pathogen, resulted in ROS accumulation in chloroplasts, followed by the appearance of localized lesions typical of the HR. In contrast, chloroplast ROS build-up and LCD were significantly reduced in Xcv-inoculated plants expressing plastid-targeted flavodoxin. Metabolic routes normally inhibited by pathogens were protected in the transformants, whereas other aspects of the HR, including the induction of defence-associated genes and synthesis of salicylic and jasmonic acid, proceeded as in inoculated wild-type plants. Therefore, ROS generated in chloroplasts during this non-host interaction are essential for the progress of LCD, but do not contribute to the induction of pathogenesis-related genes or other signalling components of the response.},
  author       = {Zurbriggen, Matias and Carrillo, N{\'e}stor and Tognetti, Vanesa and Melzer, Michael and Peisker, Martin and Hause, Bettina and Hajirezaei, Mohammad-Reza},
  issn         = {0960-7412},
  journal      = {PLANT JOURNAL},
  keyword      = {SYSTEMIC ACQUIRED-RESISTANCE,TRANSGENIC TOBACCO,HYPERSENSITIVE RESPONSE,PATHOGEN INFECTION,SOLANUM-TUBEROSUM,oxidative stress,chloroplasts,non-host resistance,reactive oxygen species,flavodoxin,plant-pathogen interactions,PSEUDOMONAS-SYRINGAE,BACTERIAL FLAVODOXIN,DISEASE RESISTANCE,ARABIDOPSIS-THALIANA,MICROBE INTERACTIONS},
  language     = {eng},
  number       = {6},
  pages        = {962--973},
  title        = {Chloroplast-generated reactive oxygen species play a major role in localized cell death during the non-host interaction between tobacco and Xanthomonas campestris pv. vesicatoria},
  url          = {http://dx.doi.org/10.1111/j.1365-313X.2009.04010.x},
  volume       = {60},
  year         = {2009},
}

Chicago
Zurbriggen, Matias, Néstor Carrillo, Vanesa Tognetti, Michael Melzer, Martin Peisker, Bettina Hause, and Mohammad-Reza Hajirezaei. 2009. “Chloroplast-generated Reactive Oxygen Species Play a Major Role in Localized Cell Death During the Non-host Interaction Between Tobacco and Xanthomonas Campestris Pv. Vesicatoria.” Plant Journal 60 (6): 962–973.
APA
Zurbriggen, M., Carrillo, N., Tognetti, V., Melzer, M., Peisker, M., Hause, B., & Hajirezaei, M.-R. (2009). Chloroplast-generated reactive oxygen species play a major role in localized cell death during the non-host interaction between tobacco and Xanthomonas campestris pv. vesicatoria. PLANT JOURNAL, 60(6), 962–973.
Vancouver
1.
Zurbriggen M, Carrillo N, Tognetti V, Melzer M, Peisker M, Hause B, et al. Chloroplast-generated reactive oxygen species play a major role in localized cell death during the non-host interaction between tobacco and Xanthomonas campestris pv. vesicatoria. PLANT JOURNAL. 2009;60(6):962–73.
MLA
Zurbriggen, Matias, Néstor Carrillo, Vanesa Tognetti, et al. “Chloroplast-generated Reactive Oxygen Species Play a Major Role in Localized Cell Death During the Non-host Interaction Between Tobacco and Xanthomonas Campestris Pv. Vesicatoria.” PLANT JOURNAL 60.6 (2009): 962–973. Print.