Online citations, reference lists, and bibliographies.
← Back to Search

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 D. Zurbriggen, N. Carrillo, V. Tognetti, M. Melzer, M. Peisker, B. Hause, Mohammad-Reza Hajirezaei
Published 2009 · Biology, Medicine

Cite This
Download PDF
Analyze on Scholarcy
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.
This paper references
Redox control of systemic acquired resistance.
P. Fobert (2005)
Specific roles of alpha- and gamma-tocopherol in abiotic stress responses of transgenic tobacco.
A. Abbasi (2007)
Induction of Jasmonate Biosynthesis in Arbuscular Mycorrhizal Barley Roots1,2
B. Hause (2002)
The Arabidopsis dnd1 "defense, no death" gene encodes a mutated cyclic nucleotide-gated ion channel.
S. Clough (2000)
News from the frontline: recent insights into PAMP-triggered immunity in plants.
B. Schwessinger (2008)
Enhanced plant tolerance to iron starvation by functional substitution of chloroplast ferredoxin with a bacterial flavodoxin
V. Tognetti (2007)
Light perception in plant disease defence signalling.
S. Karpiński (2003)
Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping.
J. Glazebrook (2003)
Hypersensitive response-related death
M. Heath (2004)
Systemic Acquired Resistance Mediated by the Ectopic Expression of Invertase: Possible Hexose Sensing in the Secretory Pathway.
K. Herbers (1996)
Pathogen-induced, NADPH oxidase–derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana
M. A. Torres (2005)
Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development.
M. A. Torres (2005)
The Authors Journal compilation a 2009
Matias D. Zurbriggen (2009)
Host and non-host pathogens elicit different jasmonate/ethylene responses in Arabidopsis.
L. Zimmerli (2004)
Fresh insights into processes of nonhost resistance.
H. Thordal-Christensen (2003)
Caspases and programmed cell death in the hypersensitive response of plants to pathogens
Olga María del Pozo (1998)
Fatty Acid Hydroperoxides and H2O2 in the Execution of Hypersensitive Cell Death in Tobacco Leaves1[w]
Jean-Luc Montillet (2005)
Photosynthesis and carbohydrate metabolism in tobacco leaves during an incompatible interaction with Phytophthora nicotianae
J. Scharte (2005)
Controlled cell death, plant survival and development
Eric Lam (2004)
An improved monobromobimane assay for glutathione utilizing tris- (2-carboxyethyl)phosphine as the reductant.
M. Anderson (1999)
Ascorbic Acid Deficiency Activates Cell Death and Disease Resistance Responses in Arabidopsis1
Valeria R Pavet (2005)
Non-host resistance in plants: new insights into an old phenomenon.
T. Nürnberger (2005)
Quantitative Nature of Arabidopsis Responses during Compatible and Incompatible Interactions with the Bacterial Pathogen Pseudomonas syringae Online version contains Web-only data. Article, publication date, and citation information can be found at
Yi Tao (2003)
Microarray analysis and redox control of gene expression in the cyanobacterium Synechocystis sp. PCC 6803.
A. Singh (2004)
NPR1: the spider in the web of induced resistance signaling pathways.
C. Pieterse (2004)
Quantitative nature of Arabidopsis responses
Y. Tao (2003)
Fatty acid hydroperoxides
J. L. Montillet (2005)
Nonhost resistance: how much do we know?
K. Mysore (2004)
The tomato resistance protein Bs4 is a predicted non-nuclear TIR-NB-LRR protein that mediates defense responses to severely truncated derivatives of AvrBs4 and overexpressed AvrBs3.
S. Schornack (2004)
Expression profiling soybean response to Pseudomonas syringae reveals new defense-related genes and rapid HR-specific downregulation of photosynthesis.
Ji-Jun Zou (2005)
Abrogation of disease development in plants expressing animal antiapoptotic genes
M. Dickman (2001)
The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea
Eri M Govrin (2000)
Functional analysis of a leucine aminopeptidase fromSolanum tuberosum L.
K. Herbers (2004)
The plant immune system
J. Jones (2006)
Plant-microbe interactions to probe regulation of plant carbon metabolism.
Sophia Biemelt (2006)
The conserved Xanthomonas campestris pv. vesicatoria effector protein XopX is a virulence factor and suppresses host defense in Nicotiana benthamiana.
M. Metz (2005)
Chloroplast Signaling and LESION SIMULATING DISEASE1 Regulate Crosstalk between Light Acclimation and Immunity in Arabidopsis[W]
Per Mühlenbock (2008)
Complex regulation of gene expression, photosynthesis and sugar levels by pathogen infection
Katharina B. Bonfig (2004)
Evidence for expression level-dependent modulation of carbohydrate status and viral resistance by the potato leafroll virus movement protein in transgenic tobacco plants.
D. Hofius (2001)
Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens.
J. Glazebrook (2005)
Bacterial elicitation and evasion of plant innate immunity
R. B. Abramovitch (2006)
Jasmonate is involved in the induction of tyrosine aminotransferase and tocopherol biosynthesis in Arabidopsis thaliana
Iris Sandorf (2002)
The necrotroph Botrytis cinerea induces a non-host type II resistance mechanism in Pinus pinaster suspension-cultured cells.
H. Azevedo (2008)
Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens.
B. P. Thomma (1998)
Specific Roles of α- and γ-Tocopherol in Abiotic Stress Responses of Transgenic Tobacco1[W][OA]
A. Abbasi (2007)
Infection with virulent and avirulent P. syringae strains differentially affects photosynthesis and sink metabolism in Arabidopsis leaves
Katharina B. Bonfig (2006)
The Role of the Jasmonate Response in Plant Susceptibility to Diverse Pathogens with a Range of Lifestyles1[w]
J. Thaler (2004)
Complex regulation of gene expression, photosynthesis and sugar levels by pathogen infection in tomato
S. Berger (2004)
Multiple Hormones Act Sequentially to Mediate a Susceptible Tomato Pathogen Defense Response1
P. O'donnell (2003)
Biosynthesis and metabolism of jasmonates
F. Schaller (2004)
Functional Replacement of Ferredoxin by a Cyanobacterial Flavodoxin in Tobacco Confers Broad-Range Stress Tolerance[W]
V. Tognetti (2006)
Expression of the Xanthomonas campestris pv. vesicatoria hrp gene cluster, which determines pathogenicity and hypersensitivity on pepper and tomato, is plant inducible.
R. Schulte (1992)
Disabling surveillance: bacterial type III secretion system effectors that suppress innate immunity
A. Espinosa (2004)
The role of photosynthetic electron transport in the oxidative degradation of chloroplastic glutamine synthetase
Palatnik (1999)
Decreased sucrose content triggers starch breakdown and respiration in stored potato tubers (Solanum tuberosum).
Mohammad-Reza Hajirezaei (2003)
Method for the extraction of the volatile compound salicylic acid from tobacco leaf material.
M. Verberne (2002)
The hypersensitive response; the centenary is upon us but how much do we know?
L. Mur (2008)
Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis.
Yuko Sasaki-Sekimoto (2005)
Post-Transcriptional Suppression of Cytosolic Ascorbate Peroxidase Expression during Pathogen-Induced Programmed Cell Death in Tobacco
R. Mittler (1998)
Knockout of Arabidopsis accelerated-cell-death11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense.
P. Brodersen (2002)
Small changes in the activity of chloroplastic NADP(+)-dependent ferredoxin oxidoreductase lead to impaired plant growth and restrict photosynthetic activity of transgenic tobacco plants.
Mohammad-Reza Hajirezaei (2002)
Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection.
R. Mittler (1999)
VANTED: A system for advanced data analysis and visualization in the context of biological networks
B. Junker (2005)
Detoxification of 2,4-dinitrotoluene by transgenic tobacco plants expressing a bacterial flavodoxin.
V. Tognetti (2007)
Reactive oxygen gene network of plants.
R. Mittler (2004)
Molecular genetics of plant disease resistance
B. Staskawicz (1995)
Combating stress with flavodoxin: a promising route for crop improvement.
Matias D. Zurbriggen (2008)
Stress‐inducible flavodoxin from photosynthetic microorganisms. The mystery of flavodoxin loss from the plant genome
Matias D. Zurbriggen (2007)
Host-Microbe Interactions: Shaping the Evolution of the Plant Immune Response
S. Chisholm (2006)
Jasmonate Biochemical Pathway
A. Gfeller (2010)
Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade.
Y. Liu (2007)
Using a modified ferrous oxidation-xylenol orange (FOX) assay for detection of lipid hydroperoxides in plant tissue.
J. M. Delong (2002)
Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning.
A. Sturm (1999)
Improved method for the isolation of RNA from plant tissues.
J. Logemann (1987)

This paper is referenced by
Mla- and Rom1-mediated control of microRNA398 and chloroplast copper/zinc superoxide dismutase regulates cell death in response to the barley powdery mildew fungus.
W. Xu (2014)
Studies on Arabidopsis ERF9 and NSL2 involved in stress responses
Yosuke Maruyama (2018)
The putative phospholipase Lip2 counteracts oxidative damage and influences the virulence of Ustilago maydis.
Scott C Lambie (2017)
Molecular crosstalk between PAMP-triggered immunity and photosynthesis.
Vera Göhre (2012)
La résistance du colza à la hernie peut-elle être modulée par la fertilisation azotée ?
Y. Aigu (2017)
A non-structural protein encoded by Rice Dwarf Virus targets to the nucleus and chloroplast and inhibits local RNA silencing
Feng Gao (2020)
Protein phosphatases meet reactive oxygen species in plant signaling networks
Malathi Bheri (2019)
Chloroplast Redox Status Modulates Genome-Wide Plant Responses during the Non-host Interaction of Tobacco with the Hemibiotrophic Bacterium Xanthomonas campestris pv. vesicatoria
Juan J. Pierella Karlusich (2017)
Arabidopsis Heterotrimeric G-Proteins Play a Critical Role in Host and Nonhost Resistance against Pseudomonas syringae Pathogens
S. Lee (2013)
Plastidic protein Cdf1 is essential in Arabidopsis embryogenesis
Maki Kawai-Yamada (2013)
Active photosynthetic inhibition mediated by MPK3/MPK6 is critical to effector-triggered immunity
J. Su (2018)
Engineering the future. Development of transgenic plants with enhanced tolerance to adverse environments
Matias D. Zurbriggen (2010)
Specific localization and measurement of hydrogen peroxide in Arabidopsis thaliana cell suspensions and protoplasts elicited by COS-OGA
Quentin Ledoux (2014)
Feedback inhibition of the general phenylpropanoid and flavonol biosynthetic pathways upon a compromised flavonol-3-O-glycosylation
Ruohe Yin (2012)
Flavodoxin displays dose-dependent effects on photosynthesis and stress tolerance when expressed in transgenic tobacco plants
Romina D. Ceccoli (2012)
Membrane-Associated Ubiquitin Ligase SAUL1 Suppresses Temperature- and Humidity-Dependent Autoimmunity in Arabidopsis.
Eva-Maria Disch (2016)
Superoxide dismutase activity in kumquat leaves infected with Xanthomonas axonopodis pv. citri
N. Kumar (2011)
Plant and bacterial systems biology as platform for plant synthetic bio(techno)logy.
Matias D. Zurbriggen (2012)
Emerging Complexity in Reactive Oxygen Species Production and Signaling during the Response of Plants to Pathogens1
Tamara Vellosillo (2010)
Arabidopsis ILITHYIA protein is necessary for proper chloroplast biogenesis and root development independent of eIF2α phosphorylation.
I. Faus (2018)
Overexpression of the rice gene OsSIZ1 in Arabidopsis improves drought-, heat-, and salt-tolerance simultaneously
Neelam Mishra (2018)
Chemical Genomic Analyses of Plant-pathogen Interactions
Karl J Schreiber (2012)
Suppression of Reactive Oxygen Species Accumulation in Chloroplasts Prevents Leaf Damage but Not Growth Arrest in Salt-Stressed Tobacco Plants
A. Lodeyro (2016)
The long goodbye: the rise and fall of flavodoxin during plant evolution.
Juan J. Pierella Karlusich (2014)
Reactive oxygen species as transducers of sphinganine-mediated cell death pathway
M. Saucedo-García (2011)
Licensed to Kill: Mitochondria, Chloroplasts, and Cell Death
O. V. Aken (2015)
NADPH-dependent thioredoxin reductase C plays a role in nonhost disease resistance against Pseudomonas syringae pathogens by regulating chloroplast-generated reactive oxygen species
Y. Ishiga (2016)
Comparative proteomic analysis of tobacco expressing cyanobacterial flavodoxin and its wild type under drought stress.
Javad Gharechahi (2015)
Reactive oxygen species generating and scavenging systems play critical role in conferring leaf spot disease resistance in Withania somnifera (L.) Dunal
B. Singh (2020)
Regulation of primary plant metabolism during plant-pathogen interactions and its contribution to plant defense
C. Rojas (2014)
In planta induced changes in the native plasmid profile of Pseudomonas syringae pathover phaseolicola strain 1302A.
Helen C. Neale (2013)
Chloroplasts at the Crossroad of Photosynthesis, Pathogen Infection and Plant Defense
Y. Lu (2018)
See more
Semantic Scholar Logo Some data provided by SemanticScholar