Plant Disease Resistance Genes: Function Meets Structure.

The coevolution of interacting plants and microbes has given rise to a diverse array of exchanged signals and responses. Microbes that elicit a host response can be met variously with hospitable acceptance (as is the case with symbionts such as nitrogen-fixing Rhizobium bacteria), with tardy recognition and moderately effective defenses (as for most interactions that result in disease), or with a strong and rapid defense response that blocks further infection (Dixon and Lamb, 1990; Keen, 1990; Long and Staskawicz, 1993). This latter form of disease resistance forms the subject of this review and is known variously as race-specific resistance, gene-for-gene resistance, or hypersensitive resistance. Activation of gene-for-gene resistance typically depends on specific recognition of the invading pathogen by the plant (Keen, 1990). Numerous individual plant genes have been identified that control gene-for-gene resistance, and these genes are known as resistance (R) genes. Study of gene-for-gene resistance might be justified solely by the intrigue of plant-pathogen coevolution or as a model for signal transduction research in which an organism perceives and responds to its environment. However, the topic takes on greater interest dueto its pivotal impact on crop health and food production. Plant diseases cause billions of dollars in lost harvest annually, and in some instances, these losses have severe consequences for humans (Agrios, 1988; Schumann, 1991). One of the most convenient, inexpensive, and environmentally sound ways to control plant disease is to utilize disease-resistam varieties, and plant breeders make extensive use of classically defined R genes (Agrios, 1988). Recent work has revealed the structure of a number of plant R genes, and a striking degree of similarity among these genes has been observed. After briefly introducing the subject of R genes and avirulence (Avo genes, this review provides an overview of the conserved structural components that are predicted in the proteins encoded by R genes. The cloning of R genes has stimulated additional research that is also discussed, including structure-function analysis of R gene-encoded proteins, isolation of additional R genes, identification of functionally related components of the defense signal transduction cascade, and engineering of improved disease resistance in plants. RESISTANCE GENES, AVIRULENCE GENES, AND PLANT DEFENSE

[1]  P. Albersheim,et al.  Host-Pathogen Interactions : XXXIII. A Plant Protein Converts a Fungal Pathogenesis Factor into an Elicitor of Plant Defense Responses. , 1989, Plant physiology.

[2]  J. Giraudat,et al.  RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. , 1994, Science.

[3]  S. Dinesh-Kumar,et al.  The product of the tobacco mosaic virus resistance gene N: Similarity to toll and the interleukin-1 receptor , 1994, Cell.

[4]  J. D. Jones,et al.  Developmentally regulated cell death on expression of the fungal avirulence gene Avr9 in tomato seedlings carrying the disease-resistance gene Cf-9. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[5]  A. Lupas,et al.  Predicting coiled coils from protein sequences , 1991, Science.

[6]  B. Staskawicz,et al.  Prokaryotic plant parasites , 1993, Cell.

[7]  F. Ausubel,et al.  Isolation of Arabidopsis genes that differentiate between resistance responses mediated by the RPS2 and RPM1 disease resistance genes. , 1996, The Plant cell.

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

[9]  Jonathan D. G. Jones,et al.  The Tomato Cf-2 Disease Resistance Locus Comprises Two Functional Genes Encoding Leucine-Rich Repeat Proteins , 1996, Cell.

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

[11]  W. Knogge,et al.  The race‐specific elicitor, NIP1, from the barley pathogen, Rhynchosporium secalis, determines avirulence on host plants of the Rrs1 resistance genotype. , 1995, The EMBO journal.

[12]  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.

[13]  A. Bent,et al.  Plant disease resistance genes: interactions with pathogens and their improved utilization to control plant diseases. , 1993 .

[14]  X. Wang,et al.  The PR5K receptor protein kinase from Arabidopsis thaliana is structurally related to a family of plant defense proteins. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[15]  A. Bent,et al.  Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. , 1991, The Plant cell.

[16]  M. Yoder,et al.  New domain motif: the structure of pectate lyase C, a secreted plant virulence factor. , 1993, Science.

[17]  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.

[18]  G. Schumann,et al.  Plant Diseases: Their Biology and Social Impact , 1992 .

[19]  G. Martin,et al.  Expression of the Tomato Pto Gene in Tobacco Enhances Resistance to Pseudomonas syringae pv tabaci Expressing avrPto. , 1995, The Plant cell.

[20]  R. Dixon,et al.  Increased disease susceptibility of transgenic tobacco plants with suppressed levels of preformed phenylpropanoid products. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[21]  T. Hunter,et al.  The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. , 1988, Science.

[22]  J. Ecker,et al.  Disease development in ethylene-insensitive Arabidopsis thaliana infected with virulent and avirulent Pseudomonas and Xanthomonas pathogens. , 1992, Molecular plant-microbe interactions : MPMI.

[23]  B. Staskawicz,et al.  Characterization of a gene from a tomato pathogen determining hypersensitive resistance in non-host species and genetic analysis of this resistance in bean. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[24]  K. Century,et al.  NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[25]  S. Hanks,et al.  Protein kinase catalytic domain sequence database: identification of conserved features of primary structure and classification of family members. , 1991, Methods in enzymology.

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

[27]  E. Hafen,et al.  Genetic dissection of signal transduction mediated by the sevenless receptor tyrosine kinase in Drosophila. , 1993, Progress in neurobiology.

[28]  P. Low,et al.  Plant and human neutrophil oxidative burst complexes contain immunologically related proteins. , 1996, Biochimica et biophysica acta.

[29]  K. Matsushima,et al.  The IL‐1 receptor signaling pathway , 1994, Journal of leukocyte biology.

[30]  B. Staskawicz,et al.  Widespread distribution and fitness contribution of Xanthomonas campestris avirulence gene avrBs2 , 1990, Nature.

[31]  T Pawson,et al.  Introduction: Protein Kinases , 1994, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[32]  J. Dangl,et al.  Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance , 1995, Science.

[33]  J. Culver,et al.  Identification of an elicitor active site within the three-dimensional structure of the tobacco mosaic tobamovirus coat protein. , 1996, The Plant cell.

[34]  I. Crute,et al.  Genetics and Utilization of Pathogen Resistance in Plants. , 1996, The Plant cell.

[35]  F. Ausubel,et al.  The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats , 1994, Cell.

[36]  B. Rolfe,et al.  Working Models of Specific Recognition in Plant-Microbe Interactions , 1990 .

[37]  T. Ashfield,et al.  Soybean resistance genes specific for different Pseudomonas syringae avirulence genes are allelic, or closely linked, at the RPG1 locus. , 1995, Genetics.

[38]  R. Dixon,et al.  Enhanced Protection Against Fungal Attack by Constitutive Co–expression of Chitinase and Glucanase Genes in Transgenic Tobacco , 1994, Bio/Technology.

[39]  P. D. Wit.  Molecular characterization of gene-for-gene systems in plant-fungus interactions and the application of avirulence genes in control of plant pathogens. , 1992 .

[40]  Alan M. Jones,et al.  Logjam at the Styx: Programmed cell death in plants , 1996 .

[41]  R. Forrest,et al.  Polygalacturonase, PGIP and oligogalacturonides in cell-cell communication. , 1994, Biochemical Society transactions.

[42]  R. Cressman,et al.  Transgenic Plants with Enhanced Resistance to the Fungal Pathogen Rhizoctonia solani , 1991, Science.

[43]  B. Staskawicz,et al.  Intergeneric transfer and functional expression of the tomato disease resistance gene Pto. , 1995, The Plant cell.

[44]  J. Ryals,et al.  Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[45]  C. Lamb.  Plant disease resistance genes in signal perception and transduction , 1994, Cell.

[46]  J. Kan,et al.  Cloning and characterization of cDNA of avirulence gene avr9 of the fungal pathogen Cladosporium fulvum, causal agent of tomato leaf mold. , 1991 .

[47]  J. Dangl,et al.  Interference between Two Specific Pathogen Recognition Events Mediated by Distinct Plant Disease Resistance Genes. , 1996, The Plant cell.

[48]  E. Finnegan,et al.  The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. , 1995, The Plant cell.

[49]  D. Baulcombe,et al.  The coat protein of potato virus X is a strain-specific elicitor of Rx1-mediated virus resistance in potato. , 1995, The Plant journal : for cell and molecular biology.

[50]  P. R. Sibbald,et al.  The P-loop--a common motif in ATP- and GTP-binding proteins. , 1990, Trends in biochemical sciences.

[51]  J. Stein,et al.  Signaling the Arrest of Pollen Tube Development in Self-Incompatible Plants , 1994, Science.

[52]  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.

[53]  S. Briggs,et al.  Reductase activity encoded by the HM1 disease resistance gene in maize. , 1992, Science.

[54]  J. Walton,et al.  Host-selective toxins: agents of compatibility. , 1996, The Plant cell.

[55]  D. Baulcombe,et al.  Use of a gene expression system based on potato virus X to rapidly identify and characterize a tomato Pto homolog that controls fenthion sensitivity. , 1995, The Plant cell.

[56]  T. Traut.  The functions and consensus motifs of nine types of peptide segments that form different types of nucleotide-binding sites. , 1994, European journal of biochemistry.

[57]  A. Sattler,et al.  A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. , 1994, The Plant cell.

[58]  U. Bonas,et al.  Race-specificity of plant resistance to bacterial spot disease determined by repetitive motifs in a bacterial avirulence protein , 1992, Nature.

[59]  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.

[60]  G. Martin,et al.  A member of the tomato Pto gene family confers sensitivity to fenthion resulting in rapid cell death. , 1994, The Plant cell.

[61]  T. Alber.  Structure of the leucine zipper , 1992, Current Biology.

[62]  C. Boucher,et al.  13 – hrp and avr Genes, Key Determinants Controlling the Interactions between Plants and Gram-negative Phytopathogenic Bacteria , 1995 .

[63]  S. Briggs,et al.  A Biochemical Phenotype for a Disease Resistance Gene of Maize. , 1992, The Plant cell.

[64]  J. Hancock,et al.  Generation of active oxygen in elicited cells of Arabidopsis thaliana is mediated by a NADPH oxidase‐like enzyme , 1996, FEBS letters.

[65]  R. Michelmore.  Molecular approaches to manipulation of disease resistance genes. , 1995, Annual review of phytopathology.

[66]  H. Hamm,et al.  Heterotrimeric G proteins. , 1996, Current opinion in cell biology.

[67]  D. Gabriel,et al.  Intragenic recombination of a single plant pathogen gene provides a mechanism for the evolution of new host specificities , 1995, Journal of bacteriology.

[68]  B. Baker,et al.  Iowa State University From the SelectedWorks of Steven Whitham 1996 The N gene of tobacco confers resistance to tobacco mosaic virus in transgenic tomato , 2017 .

[69]  M. Joosten,et al.  Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene , 1994, Nature.

[70]  D. Jones,et al.  Identification of Two Genes Required in Tomato for Full Cf-9-Dependent Resistance to Cladosporium fulvum. , 1994, The Plant cell.

[71]  J. Bennetzen,et al.  Unequal exchange and meiotic instability of disease-resistance genes in the Rp1 region of maize. , 1993, Genetics.

[72]  P. Schulze-Lefert,et al.  Nar-1 and Nar-2, Two Loci Required for Mla12-Specified Race-Specific Resistance to Powdery Mildew in Barley. , 1994, The Plant cell.

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

[74]  Xinnian Dong,et al.  Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance. , 1994, The Plant cell.

[75]  Hh Flor,et al.  Host-parasite interaction in flax rust–its genetics and other implications , 1955 .

[76]  W. Knogge.  Fungal Infection of Plants. , 1996, The Plant cell.

[77]  J. Ryals,et al.  Signal transduction in systemic acquired resistance. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[80]  J. Beynon,et al.  Phenotypic and genotypic characterization of interactions between isolates of Peronospora parasitica and accessions of Arabidopsis thaliana , 1994 .

[81]  D. Gabriel,et al.  Xanthomonas avirulence/pathogenicity gene family encodes functional plant nuclear targeting signals. , 1995, Molecular plant-microbe interactions : MPMI.

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

[83]  W. Fantl,et al.  Signalling by receptor tyrosine kinases. , 1993, Annual review of biochemistry.

[84]  N. Keen.  Gene-for-gene complementarity in plant-pathogen interactions. , 1990, Annual review of genetics.

[85]  E. Ward,et al.  A Central Role of Salicylic Acid in Plant Disease Resistance , 1994, Science.

[86]  D. Leister,et al.  A PCR–based approach for isolating pathogen resistance genes from potato with potential for wide application in plants , 1996, Nature Genetics.

[87]  R. Dixon,et al.  Molecular Communication in Interactions Between Plants and Microbial Pathogens , 1990 .

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

[89]  J. D. Jones,et al.  Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. , 1994, Science.

[90]  J. Bennetzen,et al.  Allele-specific and Mutator-associated instability at the Rpl disease-resistance locus of maize , 1988, Nature.

[91]  A. Collmer,et al.  Bacterial Pathogens in Plants: Life up against the Wall. , 1996, The Plant cell.

[92]  J. Deisenhofer,et al.  The leucine-rich repeat: a versatile binding motif. , 1994, Trends in biochemical sciences.

[93]  R. Goodman,et al.  The hypersensitive reaction in plants to pathogens: a resistance phenomenon. , 1994 .

[94]  M. Collinge,et al.  Interaction of a protein phosphatase with an Arabidopsis serine-threonine receptor kinase. , 1994, Science.

[95]  L. Guarente.  Strategies for the identification of interacting proteins. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[96]  U. Bonas,et al.  Gene-for-gene relationships specifying disease resistance in Xanthomonas campestris pv. vesicatoria - pepper interactions. , 1990 .

[97]  A. Bent,et al.  Identification of a disease resistance locus in Arabidopsis that is functionally homologous to the RPG1 locus of soybean. , 1993, The Plant journal : for cell and molecular biology.

[98]  Kate J. Graham,et al.  The structures of syringolides 1 and 2, novel C-glycosidic elicitors from Pseudomonas syringae pv. tomato , 1993 .