Host-Microbe Interactions: Shaping the Evolution of the Plant Immune Response

The evolution of the plant immune response has culminated in a highly effective defense system that is able to resist potential attack by microbial pathogens. The primary immune response is referred to as PAMP-triggered immunity (PTI) and has evolved to recognize common features of microbial pathogens. In the coevolution of host-microbe interactions, pathogens acquired the ability to deliver effector proteins to the plant cell to suppress PTI, allowing pathogen growth and disease. In response to the delivery of pathogen effector proteins, plants acquired surveillance proteins (R proteins) to either directly or indirectly monitor the presence of the pathogen effector proteins. In this review, taking an evolutionary perspective, we highlight important discoveries over the last decade about the plant immune response.

[1]  Jonathan D. G. Jones,et al.  Bacterial disease resistance in Arabidopsis through flagellin perception , 2004, Nature.

[2]  J. Ecker,et al.  Arabidopsis RIN4 Is a Target of the Type III Virulence Effector AvrRpt2 and Modulates RPS2-Mediated Resistance , 2003, Cell.

[3]  B. Tyler,et al.  The Avr 1 b Locus of Phytophthora sojae Encodes an Elicitor and a Regulator Required for Avirulence on Soybean Plants Carrying Resistance Gene Rps 1 b , 2004 .

[4]  S. Chisholm,et al.  Molecular Basis for the RIN4 Negative Regulation of RPS2 Disease Resistancew⃞ , 2005, The Plant Cell Online.

[5]  Travis Harrison,et al.  A Host-Targeting Signal in Virulence Proteins Reveals a Secretome in Malarial Infection , 2004, Science.

[6]  B. Tyler,et al.  The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps1b. , 2004, Molecular plant-microbe interactions : MPMI.

[7]  I. Somssich,et al.  Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Lihuang Zhu,et al.  Activation of a COI1-dependent pathway in Arabidopsis by Pseudomonas syringae type III effectors and coronatine. , 2004, The Plant journal : for cell and molecular biology.

[9]  G. Martin,et al.  A Bacterial Inhibitor of Host Programmed Cell Death Defenses Is an E3 Ubiquitin Ligase , 2006, Science.

[10]  T. Torto-Alalibo,et al.  A Kazal-like Extracellular Serine Protease Inhibitor from Phytophthora infestans Targets the Tomato Pathogenesis-related Protease P69B* , 2004, Journal of Biological Chemistry.

[11]  Pierre J.G.M. de Wit Cf9 and Avr9, two major players in the gene-for-gene game. , 1995, Trends in microbiology.

[12]  B. Kunkel,et al.  Cross talk between signaling pathways in pathogen defense. , 2002, Current opinion in plant biology.

[13]  M. Axtell,et al.  Genetic and molecular evidence that the Pseudomonas syringae type III effector protein AvrRpt2 is a cysteine protease , 2003, Molecular microbiology.

[14]  Jonathan D. G. Jones,et al.  Cladosporium Avr2 Inhibits Tomato Rcr3 Protease Required for Cf-2-Dependent Disease Resistance , 2005, Science.

[15]  S. He,et al.  A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[16]  C. Tobias,et al.  Plants expressing the Pto disease resistance gene confer resistance to recombinant PVX containing the avirulence gene AvrPto. , 1999, The Plant journal : for cell and molecular biology.

[17]  M. Quail,et al.  An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[18]  J. Dangl,et al.  The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[19]  M. G. Kim,et al.  Two Pseudomonas syringae Type III Effectors Inhibit RIN4-Regulated Basal Defense in Arabidopsis , 2005, Cell.

[20]  J. Vossen,et al.  The Tomato R Gene Products I-2 and Mi-1 Are Functional ATP Binding Proteins with ATPase Activity , 2002, The Plant Cell Online.

[21]  B. Thomma,et al.  The complexity of disease signaling in Arabidopsis. , 2001, Current opinion in immunology.

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

[23]  H. Gehrig,et al.  Geosiphon pyriforme, a fungus forming endocytobiosis withNostoc (Cyanobacteria), is an ancestral member of the glomales: Evidence by SSU rRNA Analysis , 1996, Journal of Molecular Evolution.

[24]  K. Sjolander,et al.  Molecular characterization of proteolytic cleavage sites of the Pseudomonas syringae effector AvrRpt2. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[25]  J. Parker,et al.  Interplay of signaling pathways in plant disease resistance. , 2000, Trends in genetics : TIG.

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

[27]  Michael J. Axtell,et al.  Initiation of RPS2-Specified Disease Resistance in Arabidopsis Is Coupled to the AvrRpt2-Directed Elimination of RIN4 , 2003, Cell.

[28]  P. Dodds,et al.  The Melampsora lini AvrL567 Avirulence Genes Are Expressed in Haustoria and Their Products Are Recognized inside Plant Cells , 2004, The Plant Cell Online.

[29]  M. B. Mudgett New insights to the function of phytopathogenic bacterial type III effectors in plants. , 2005, Annual review of plant biology.

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

[31]  Nandini Krishnamurthy,et al.  Phylogenomic Analysis of the Receptor-Like Proteins of Rice and Arabidopsis1[w] , 2005, Plant Physiology.

[32]  U. Bonas,et al.  Basal defenses induced in pepper by lipopolysaccharides are suppressed by Xanthomonas campestris pv. vesicatoria. , 2004, Molecular plant-microbe interactions : MPMI.

[33]  J. Galán,et al.  Chaperone release and unfolding of substrates in type III secretion , 2005, Nature.

[34]  P. Dodds,et al.  Haustorially Expressed Secreted Proteins from Flax Rust Are Highly Enriched for Avirulence Elicitors[W] , 2005, The Plant Cell Online.

[35]  Jack E. Dixon,et al.  Cleavage of Arabidopsis PBS1 by a Bacterial Type III Effector , 2003, Science.

[36]  Adrian Ozinsky,et al.  Toll-like receptors: key mediators of microbe detection. , 2002, Current opinion in immunology.

[37]  P. D. de Wit,et al.  Fungal avirulence genes: structure and possible functions. , 1998, Fungal genetics and biology : FG & B.

[38]  K. Niehaus,et al.  The N Terminus of Bacterial Elongation Factor Tu Elicits Innate Immunity in Arabidopsis Plants , 2004, The Plant Cell Online.

[39]  S. Kauppinen,et al.  Pep‐13, a plant defense‐inducing pathogen‐associated pattern from Phytophthora transglutaminases , 2002, The EMBO journal.

[40]  Jeff H. Chang,et al.  A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Sophien Kamoun,et al.  A Second Kazal-Like Protease Inhibitor from Phytophthora infestans Inhibits and Interacts with the Apoplastic Pathogenesis-Related Protease P69B of Tomato1 , 2005, Plant Physiology.

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

[43]  S. Dinesh-Kumar,et al.  Mechanisms of plant resistance to viruses , 2005, Nature Reviews Microbiology.

[44]  R. Michelmore,et al.  The Maintenance of Extreme Amino Acid Diversity at the Disease Resistance Gene, RPP13, in Arabidopsis thaliana , 2004, Genetics.

[45]  David Mackey,et al.  RIN4 Interacts with Pseudomonas syringae Type III Effector Molecules and Is Required for RPM1-Mediated Resistance in Arabidopsis , 2002, Cell.

[46]  W. Zhu,et al.  AvrXa10 contains an acidic transcriptional activation domain in the functionally conserved C terminus. , 1998, Molecular plant-microbe interactions : MPMI.

[47]  David A Jones,et al.  Plant innate immunity - direct and indirect recognition of general and specific pathogen-associated molecules. , 2004, Current opinion in immunology.

[48]  J. Beynon,et al.  Host-Parasite Coevolutionary Conflict Between Arabidopsis and Downy Mildew , 2004, Science.

[49]  F. Chumley,et al.  A Telomeric Avirulence Gene Determines Efficacy for the Rice Blast Resistance Gene Pi-ta , 2000, Plant Cell.

[50]  T. Boller,et al.  Flagellin perception: a paradigm for innate immunity. , 2002, Trends in plant science.

[51]  Xiaoyan Tang,et al.  Identification of Pseudomonas syringae type III effectors that can suppress programmed cell death in plants and yeast. , 2004, The Plant journal : for cell and molecular biology.

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

[53]  Colwyn M. Thomas,et al.  Molecular interactions between tomato and the leaf mold pathogen Cladosporium fulvum. , 2005, Annual review of phytopathology.

[54]  C. Zipfel,et al.  Plants and animals: a different taste for microbes? , 2005, Current opinion in plant biology.

[55]  W. Zhu,et al.  The virulence factor AvrXa7 of Xanthomonas oryzae pv. oryzae is a type III secretion pathway-dependent nuclear-localized double-stranded DNA-binding protein. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[56]  S. He,et al.  Suppression of host defense in compatible plant-Pseudomonas syringae interactions. , 2005, Current opinion in plant biology.

[57]  J. Dangl,et al.  Common and Contrasting Themes of Plant and Animal Diseases , 2001, Science.

[58]  A. Hotson,et al.  Characterization of the Xanthomonas AvrXv4 effector, a SUMO protease translocated into plant cells. , 2004, Molecular plant-microbe interactions : MPMI.

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

[60]  S. Hedges,et al.  Molecular Evidence for the Early Colonization of Land by Fungi and Plants , 2001, Science.

[61]  F. Ausubel,et al.  MAP kinase signalling cascade in Arabidopsis innate immunity , 2002, Nature.

[62]  S. Tanksley,et al.  Genetic and physical analysis of the rice bacterial blight disease resistance locus, Xa21 , 1992, Molecular and General Genetics MGG.

[63]  S. He,et al.  A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[64]  L. Piater,et al.  Innate immunity in plants and animals: striking similarities and obvious differences , 2004, Immunological reviews.

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

[66]  R. Hilgarth,et al.  Regulation and Function of SUMO Modification* , 2004, Journal of Biological Chemistry.

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

[68]  Kees-Jan Françoijs,et al.  Natural Disulfide Bond-disrupted Mutants of AVR4 of the Tomato Pathogen Cladosporium fulvum Are Sensitive to Proteolysis, Circumvent Cf-4-mediated Resistance, but Retain Their Chitin Binding Ability* , 2003, Journal of Biological Chemistry.

[69]  Fan Yang,et al.  R gene expression induced by a type-III effector triggers disease resistance in rice , 2005, Nature.

[70]  J. Beynon,et al.  Differential Recognition of Highly Divergent Downy Mildew Avirulence Gene Alleles by RPP1 Resistance Genes from Two Arabidopsis Lines , 2005, The Plant Cell Online.

[71]  T. Ashfield,et al.  Convergent Evolution of Disease Resistance Gene Specificity in Two Flowering Plant Families On-line version contains Web-only data. , 2004, The Plant Cell Online.

[72]  T. Boller,et al.  Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. , 1999, The Plant journal : for cell and molecular biology.

[73]  S. Sideris,et al.  The cloned gene, Xa21, confers resistance to multiple Xanthomonas oryzae pv. oryzae isolates in transgenic plants. , 1996, Molecular plant-microbe interactions : MPMI.

[74]  A. Falick,et al.  Activation of a Phytopathogenic Bacterial Effector Protein by a Eukaryotic Cyclophilin , 2005, Science.

[75]  P. D. Wit Cf9 and Avr9, two major players in the gene-for-gene game , 1995 .

[76]  G. Martin,et al.  Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death , 2003, The EMBO journal.

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

[78]  P. Ronald,et al.  Molecular determinants of disease and resistance in interactions of Xanthomonas oryzae pv. oryzae and rice. , 2002, Microbes and infection.

[79]  T. Boller,et al.  FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. , 2000, Molecular cell.

[80]  P. Reymond,et al.  Jasmonate and salicylate as global signals for defense gene expression. , 1998, Current opinion in plant biology.