Overexpression of Pto Activates Defense Responses and Confers Broad Resistance

The tomato disease resistance (R) gene Pto specifies race-specific resistance to the bacterial pathogen Pseudomonas syringae pv tomato carrying the avrPto gene. Pto encodes a serine/threonine protein kinase that is postulated to be activated by a physical interaction with the AvrPto protein. Here, we report that overexpression of Pto in tomato activates defense responses in the absence of the Pto–AvrPto interaction. Leaves of three transgenic tomato lines carrying the cauliflower mosaic virus 35S::Pto transgene exhibited microscopic cell death, salicylic acid accumulation, and increased expression of pathogenesis-related genes. Cell death in these plants was limited to palisade mesophyll cells and required light for induction. Mesophyll cells of 35S::Pto plants showed the accumulation of autofluorescent compounds, callose deposition, and lignification. When inoculated with P. s. tomato without avrPto, all three 35S::Pto lines displayed significant resistance and supported less bacterial growth than did nontransgenic lines. Similarly, the 35S::Pto lines also were more resistant to Xanthomonas campestris pv vesicatoria and Cladosporium fulvum. These results demonstrate that defense responses and general resistance can be activated by the overexpression of an R gene.

[1]  B. Staskawicz,et al.  Genetically engineered broad-spectrum disease resistance in tomato. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[2]  A. Bent,et al.  Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[3]  G. Martin,et al.  The myristylation motif of Pto is not required for disease resistance. , 1998, Molecular plant-microbe interactions : MPMI.

[4]  W. Van Camp,et al.  Defense activation and enhanced pathogen tolerance induced by H2O2 in transgenic tobacco. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[5]  R. Mittler,et al.  Post-Transcriptional Suppression of Cytosolic Ascorbate Peroxidase Expression during Pathogen-Induced Programmed Cell Death in Tobacco , 1998, Plant Cell.

[6]  D. Llewellyn,et al.  Induction of Cell Death in Transgenic Plants Expressing a Fungal Glucose Oxidase , 1998 .

[7]  M. Coleman,et al.  Map positions of 47 Arabidopsis sequences with sequence similarity to disease resistance genes. , 1997, The Plant journal : for cell and molecular biology.

[8]  D F Klessig,et al.  The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. , 1997, The Plant cell.

[9]  E. Lam,et al.  Characterization of acquired resistance in lesion-mimic transgenic potato expressing bacterio-opsin. , 1997, Molecular plant-microbe interactions : MPMI.

[10]  P. Vera,et al.  Two PR-1 genes from tomato are differentially regulated and reveal a novel mode of expression for a pathogenesis-related gene during the hypersensitive response and development. , 1997, Molecular plant-microbe interactions : MPMI.

[11]  G. Martin,et al.  The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis‐element of pathogenesis‐related genes , 1997, The EMBO journal.

[12]  D. Klessig,et al.  Development of necrosis and activation of disease resistance in transgenic tobacco plants with severely reduced catalase levels. , 1997, The Plant journal : for cell and molecular biology.

[13]  S. Briggs,et al.  A Novel Suppressor of Cell Death in Plants Encoded by the Lls1 Gene of Maize , 1997, Cell.

[14]  M. Wolter,et al.  The Barley Mlo Gene: A Novel Control Element of Plant Pathogen Resistance , 1997, Cell.

[15]  C. Dean,et al.  A Novel Zinc Finger Protein Is Encoded by the Arabidopsis LSD1 Gene and Functions as a Negative Regulator of Plant Cell Death , 1997, Cell.

[16]  G. Martin,et al.  Alleles of Pto and Fen occur in bacterial speck-susceptible and fenthion-insensitive tomato cultivars and encode active protein kinases. , 1997, The Plant cell.

[17]  Jeff H. Chang,et al.  Molecular Basis of Gene-for-Gene Specificity in Bacterial Speck Disease of Tomato , 1996, Science.

[18]  G. Martin,et al.  Initiation of Plant Disease Resistance by Physical Interaction of AvrPto and Pto Kinase , 1996, Science.

[19]  G. Kotliar,et al.  The Metal-Insulator Transition in Correlated Disordered Systems , 1996, Science.

[20]  J. Dangl,et al.  Death Don't Have No Mercy: Cell Death Programs in Plant-Microbe Interactions. , 1996, The Plant cell.

[21]  Jonathan D. G. Jones,et al.  Resistance gene-dependent plant defense responses. , 1996, The Plant cell.

[22]  T. Jabs,et al.  Initiation of Runaway Cell Death in an Arabidopsis Mutant by Extracellular Superoxide , 1996, Science.

[23]  C. Pieterse,et al.  Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. , 1996, The Plant cell.

[24]  T. Pryor,et al.  Disease Lesion Mimicry Caused by Mutations in the Rust Resistance Gene rp1. , 1996, The Plant cell.

[25]  W. Frommer,et al.  Systemic Acquired Resistance Mediated by the Ectopic Expression of Invertase: Possible Hexose Sensing in the Secretory Pathway. , 1996, The Plant cell.

[26]  P. Low,et al.  The oxidative burst in plant defense: Function and signal transduction , 1996 .

[27]  G. Martin,et al.  The tomato gene Pti1 encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response , 1995, Cell.

[28]  Li-li Chen,et al.  A Receptor Kinase-Like Protein Encoded by the Rice Disease Resistance Gene, Xa21 , 1995, Science.

[29]  D. Klessig,et al.  Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense responses. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[30]  J. Bennetzen,et al.  New rust resistance specificities associated with recombination in the Rp1 complex in maize. , 1995, Genetics.

[31]  S. Briggs,et al.  Disease lesion mimics of maize: A model for cell death in plants , 1995 .

[32]  G. Martin,et al.  The Pto Bacterial Resistance Gene and the Fen Insecticide Sensitivity Gene Encode Functional Protein Kinases with Serine/Threonine Specificity , 1995, Plant physiology.

[33]  BJ Staskawicz,et al.  Molecular genetics of plant disease resistance , 1995, Science.

[34]  T. Hunter,et al.  Protein kinases and phosphatases: The Yin and Yang of protein phosphorylation and signaling , 1995, Cell.

[35]  V. Shulaev,et al.  Coordinated Activation of Programmed Cell Death and Defense Mechanisms in Transgenic Tobacco Plants Expressing a Bacterial Proton Pump. , 1995, The Plant cell.

[36]  D. Klessig,et al.  A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. , 1994, The Plant cell.

[37]  Alex Levine,et al.  H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response , 1994, Cell.

[38]  S. Seo,et al.  Expression of the gene for a small GTP binding protein in transgenic tobacco elevates endogenous cytokinin levels, abnormally induces salicylic acid in response to wounding, and increases resistance to tobacco mosaic virus infection. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[39]  X. Tang,et al.  Pistil-Specific and Ethylene-Regulated Expression of 1-Aminocyclopropane-1-Carboxylate Oxidase Genes in Petunia Flowers. , 1994, The Plant cell.

[40]  J. Dangl,et al.  Arabidopsis mutants simulating disease resistance response , 1994, Cell.

[41]  F. Ausubel,et al.  Programmed cell death in plants: A pathogen-triggered response activated coordinately with multiple defense functions , 1994, Cell.

[42]  S. Briggs,et al.  A tale of two mimics; transposon mutagenesis and characterization of two disease lesion mimic mutations of maize , 1994 .

[43]  R. Dixon,et al.  Early events in the activation of plant defense responses , 1994 .

[44]  D. Klessig,et al.  Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. , 1993, Science.

[45]  G. Martin,et al.  Map-based cloning of a protein kinase gene conferring disease resistance in tomato. , 1993, Science.

[46]  J. Schell,et al.  Altered response to viral infection by tobacco plants perturbed in ubiquitin system. , 1993 .

[47]  J. Leach,et al.  Effect of light on incompatible interactions between Xanthomonas oryzae pv oryzae and rice , 1993 .

[48]  Jonathan D. G. Jones,et al.  Use of fungal transformants expressing ß-glucuronidase activity to detect and measure hyphal biomass in infected plant tissues , 1993 .

[49]  F. Carland,et al.  The cloned avirulence gene avrPto induces disease resistance in tomato cultivars containing the Pto resistance gene , 1992, Journal of bacteriology.

[50]  V. Walbot Maize Mutants for the 21st Century , 1991 .

[51]  D. Meinke Perspectives on Genetic Analysis of Plant Embryogenesis. , 1991, The Plant cell.

[52]  T. Yoshikawa,et al.  Active oxygen species. , 1988 .

[53]  M. Bevan,et al.  GUS fusions: beta‐glucuronidase as a sensitive and versatile gene fusion marker in higher plants. , 1987, The EMBO journal.

[54]  B. Lewis,et al.  Variation in stem infections caused by aggressive and non‐aggressive isolates of Leptosphaeria maculans on Brassica napus var. oleifera , 1987 .

[55]  John W. Scott,et al.  Sources of Resistance to Bacterial Spot in Tomato , 1986, Hortscience.

[56]  M. Marchetti Spontaneous Occurrence of the Sekiguchi Lesion in Two American Rice Lines: Its Induction, Inheritance, and Utilization , 1983 .

[57]  V. Walbot,et al.  Disease lesion mimics in maize. I. Effect of genetic background, temperature, developmental age, and wounding on necrotic spot formation with Les1. , 1982, Developmental biology.

[58]  B. J. Deverall,et al.  Comparison of histological and physiological responses to Phakopsora pachyrhizi in resistant and susceptible soybean , 1980 .

[59]  H H Flor,et al.  Current Status of the Gene-For-Gene Concept , 1971 .

[60]  L. Sequeira,et al.  Differentiation of races of Pseudomonas solanacearum by a leaf infiltration technique. , 1970 .

[61]  W. Eschrich,et al.  Identification of Cauose by its Diachrome and Fluorochrome Reactions , 1964 .

[62]  A. N. Langford Autogenous necrosis in tomatoes immune from Cladosporium fulvum Cooke. , 1948, Canadian journal of research.