Pto Mutants Differentially ActivatePrf-Dependent, avrPto-Independent Resistance and Gene-for-Gene Resistance1

Pto confers disease resistance toPseudomonas syringae pv tomato carrying the cognate avrPto gene. Overexpression ofPto under the cauliflower mosaic virus 35S promoter activates spontaneous lesions and confers disease resistance in tomato (Lycopersicon esculentum) plants in the absence ofavrPto. Here, we show that these AvrPto-independent defenses require a functional Prf gene. Several Pto-interacting (Pti) proteins are thought to play a role in Pto-mediated defense pathways. To test if interactions with Pti proteins are required for the AvrPto-independent defense responses by Pto overexpression, we isolated several Pto mutants that were unable to interact with one or more Pti proteins, but retained normal interaction with AvrPto. Overexpression of two mutants,PtoG50S and PtoR150S , failed to activate AvrPto-independent defense responses or confer enhanced resistance to the virulent P. s. pv tomato. When introduced into plants carrying 35S::Pto, 35S::PtoG50S dominantly suppressed the AvrPto-independent resistance caused by former transgene. 35S::Pto G50S also blocked the induction of a number of defense genes by the wild-type 35S::Pto. However, 35S::Pto G50S and 35S::Pto R150S plants were completely resistant to P. s. pv tomato (avrPto), indicating a normal gene-for-gene resistance. Furthermore, 35S::Pto G50S plants exhibited normal induction of defense genes in recognition of avrPto. Thus, the AvrPto-independent defense activation and gene-for-gene resistance mediated by Pto are functionally separable.

[1]  Xiaoyan Tang,et al.  Overexpression of Pto induces a salicylate-independent cell death but inhibits necrotic lesions caused by salicylate-deficiency in tomato plants. , 2002, Molecular plant-microbe interactions : MPMI.

[2]  Lihuang Zhu,et al.  Overexpression of Pti5 in tomato potentiates pathogen-induced defense gene expression and enhances disease resistance to Pseudomonas syringae pv. tomato. , 2001, Molecular plant-microbe interactions : MPMI.

[3]  Xiaoyan Tang,et al.  Expression of 35S::Pto globally activates defense-related genes in tomato plants. , 2001, Plant physiology.

[4]  J. D. Jones,et al.  No evidence for binding between resistance gene product Cf-9 of tomato and avirulence gene product AVR9 of Cladosporium fulvum. , 2001, Molecular plant-microbe interactions : MPMI.

[5]  Jonathan D. G. Jones,et al.  Plant pathogens and integrated defence responses to infection , 2001, Nature.

[6]  G. Martin,et al.  The Pseudomonas AvrPto Protein Is Differentially Recognized by Tomato and Tobacco and Is Localized to the Plant Plasma Membrane , 2000, Plant Cell.

[7]  F. Qu,et al.  HRT Gene Function Requires Interaction between a NAC Protein and Viral Capsid Protein to Confer Resistance to Turnip Crinkle Virus , 2000, Plant Cell.

[8]  B. Valent,et al.  Direct interaction of resistance gene and avirulence gene products confers rice blast resistance , 2000, The EMBO journal.

[9]  P. He,et al.  A cluster of mutations disrupt the avirulence but not the virulence function of AvrPto. , 2000, Molecular plant-microbe interactions : MPMI.

[10]  R. Michelmore,et al.  avrPto enhances growth and necrosis caused by Pseudomonas syringae pv.tomato in tomato lines lacking either Pto or Prf. , 2000, Molecular plant-microbe interactions : MPMI.

[11]  G. Martin,et al.  Pti4 Is Induced by Ethylene and Salicylic Acid, and Its Product Is Phosphorylated by the Pto Kinase , 2000, Plant Cell.

[12]  Zhou,et al.  Pseudomonas syringae pv tomato induces the expression of tomato EREBP-like genes pti4 and pti5 independent of ethylene, salicylate and jasmonate , 1999, The Plant journal : for cell and molecular biology.

[13]  R. Michelmore,et al.  Constitutively active Pto induces a Prf‐dependent hypersensitive response in the absence of avrPto , 1999, The EMBO journal.

[14]  G. Martin,et al.  Overexpression of Pto Activates Defense Responses and Confers Broad Resistance , 1999, Plant Cell.

[15]  E. A. van der Biezen,et al.  Plant disease-resistance proteins and the gene-for-gene concept. , 1998, Trends in biochemical sciences.

[16]  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.

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

[18]  Y. Okinaka,et al.  Characterization of a 34-kDa soybean binding protein for the syringolide elicitors. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[19]  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.

[20]  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.

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

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

[23]  Daniel T. Lavelle,et al.  Tomato Prf Is a Member of the Leucine-Rich Repeat Class of Plant Disease Resistance Genes and Lies Embedded within the Pto Kinase Gene Cluster , 1996, Cell.

[24]  G. Bonnema,et al.  A High-Affinity Binding Site for the AVR9 Peptide Elicitor of Cladosporium fulvum Is Present on Plasma Membranes of Tomato and Other Solanaceous Plants. , 1996, The Plant cell.

[25]  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.

[26]  F. Carland,et al.  Tomato mutants altered in bacterial disease resistance provide evidence for a new locus controlling pathogen recognition. , 1994, The Plant cell.

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

[28]  T. A. Brown,et al.  Enhanced transformation of tomato co-cultivated with Agrobacterium tumefaciens C58C1Rifr::pGSFR1161 in the presence of acetosyringone , 1993, Plant Cell Reports.

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

[30]  G. Martin,et al.  Thr38 and Ser198 are Pto autophosphorylation sites required for the AvrPto–Pto‐mediated hypersensitive response , 2022 .