Skip to main content
Article thumbnail
Location of Repository

Common and contrasting themes in host cell-targeted effectors from bacterial, fungal, oomycete and nematode plant symbionts described using the Gene Ontology

By Trudy Torto-Alalibo, Candace W Collmer, Magdalen Lindeberg, David Bird, Alan Collmer and Brett M Tyler

Abstract

A wide diversity of plant-associated symbionts, including microbes, produce proteins that can enter host cells, or are injected into host cells in order to modify the physiology of the host to promote colonization. These molecules, termed effectors, commonly target the host defense signaling pathways in order to suppress the defense response. Others target the gene expression machinery or trigger specific modifications to host morphology or physiology that promote the nutrition and proliferation of the symbiont. When recognized by the host's surveillance machinery, which includes cognate resistance (R) gene products, defense responses are engaged to restrict pathogen proliferation. Effectors from diverse symbionts may be delivered into plant cells via varied mechanisms, including whole organism cellular entry (viruses, some bacteria and fungi), type III and IV secretion (in bacteria), physical injection (nematodes and insects) and protein translocation signal sequences (oomycetes and fungi). This mini-review will summarize both similarities and differences in effectors and effector delivery systems found in diverse plant-associated symbionts as well as how these are described with Plant-Associated Microbe Gene Ontology (PAMGO) terms

Topics: Review
Publisher: BioMed Central
OAI identifier: oai:pubmedcentral.nih.gov:2654663
Provided by: PubMed Central
Download PDF:
Sorry, we are unable to provide the full text but you may find it at the following location(s):
  • http://www.pubmedcentral.nih.g... (external link)
  • Suggested articles

    Citations

    1. (2006). A catalogue of the effector secretome of plant pathogenic oomycetes. Annu Rev Phytopathol
    2. (2000). A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. Plant Cell
    3. (2007). A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature
    4. (2006). a type III effector essential for Erwinia amylovora pathogenicity and growth in planta, induces cell death in host apple and nonhost tobacco plants. Mol Plant Microbe Interact
    5. (2002). Albersheim P: Molecular cloning and characterization of glucanase inhibitor proteins: coevolution of a counterdefense mechanism by plant pathogens. Plant Cell
    6. (2007). Alfano JR: A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature
    7. (2008). Alfano JR: Phytopathogen type III effector weaponry and their plant targets. Curr Opin Plant Biol
    8. An introduction to the Gene Ontology [http://www.geneontol ogy.org/GO.doc.shtml]
    9. (2009). BM: Common themes in nutrient acquisition by plant symbiotic microbes, described by the Gene Ontology.
    10. (2008). BM: RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members. Proc Natl Acad Sci USA
    11. (2008). BM: RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogenencoded machinery. Plant Cell
    12. (2004). BM: The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps1b. Mol Plant Microbe Interact
    13. (2005). BN: The Pseudomonas syringae phytotoxin coronatine promotes virulence by overcoming salicylic-acid-dependent defences in Arabidopsis thaliana. Mol Plant Pathol
    14. (2001). Castagnone-Sereno P: Molecular cloning of a cDNA encoding an amphid-secreted putative avirulence protein from the root-knot nematode Meloidogyne incognita. Mol Plant Microbe Interact
    15. (2007). Cell biology of plant-oomycete interactions.
    16. (2005). Cherevach I, et al.: An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proc Natl Acad Sci USA
    17. (2006). Collmer A: Closing the circle on the discovery of genes encoding Hrp regulon members and type III secretion system effectors in the genomes of three model Pseudomonas syringae strains. Mol Plant Microbe Interact
    18. (2004). Collmer A: Type III secretion system effector proteins: Double agents in bacterial disease and plant defense. Annual Review of Phytopathology
    19. (2009). Collmer CW: Gene Ontology annotation highlights shared and divergent pathogenic strategies of type III effector proteins deployed by the plant pathogen Pseudomonas syringae pv tomato DC3000 and animal pathogenic Escherichia coli strains.
    20. (2009). Common processes in pathogenesis by fungal and oomycete plant pathogens, described with Gene Ontology terms.
    21. (2006). Computational and comparative analyses of 150 full-length cDNA sequences from the oomycete plant pathogen Phytophthora infestans. Fungal Genet Biol
    22. (2008). Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b. Plant Cell
    23. (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol
    24. (2006). Dangl JL: The plant immune system. Nature
    25. (2008). de Vries RP: The secretome of the maize pathogen Ustilago maydis. Fungal Genet Biol
    26. (2007). Defense suppression by virulence effectors of bacterial phytopathogens. Curr Opin Plant Biol
    27. (2000). Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. Embo J
    28. (2005). EL: A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana. Molecular Plant Pathology
    29. (2007). Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol
    30. (1998). Endogenous cellulases in animals: isolation of beta-1, 4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proc Natl Acad Sci USA
    31. (2009). Entering and breaking: virulence effector proteins of oomycete plant pathogens. Cell Microbiol
    32. (2002). Expression of a Phytophthora sojae necrosis-inducing protein occurs during transition from biotrophy to necrotrophy. Plant J
    33. (2003). GB: Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. Embo J
    34. Gene Ontology [ h t t p : /
    35. (2000). Gene Ontology: tool for the unification of biology.
    36. (2004). Gheysen G: Secretions of plant-parasitic nematodes: a molecular update. Gene
    37. (2007). GJ: The role of secreted proteins in diseases of plants caused by rust, powdery mildew and smut fungi. Curr Opin Microbiol
    38. (2006). Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell
    39. (2007). Hogenhout SA: A functional genetic assay for nuclear trafficking in plants.
    40. (2003). Innes RW: Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science
    41. (2006). Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature
    42. (2007). JD: The downy mildew effector proteins ATR1 and ATR13 promote disease susceptibility in Arabidopsis thaliana. Plant Cell
    43. (2007). JG: Avirulence proteins of rust fungi: penetrating the host-haustorium barrier.
    44. (2005). JL: Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell
    45. (2006). JL: Subterfuge and manipulation: Type III effector proteins of phytopathogenic bacteria. Annual Review of Microbiology
    46. (1937). JM: The feeding of hollow-spear nematodes on other nematodes. Science
    47. (2007). JT: A J domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses. Curr Biol
    48. (2005). JT: Bioinformatics correctly identifies many type III secretion substrates in the plant pathogen Pseudomonas syringae and the biocontrol isolate P. fluorescens SBW25. Mol Plant Microbe Interact
    49. (2006). Kamoun S: The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana.
    50. (2003). KN: Meloidogyne javanica chorismate mutase 1 alters plant cell development. Mol Plant Microbe Interact
    51. (2007). Magnaporthe as a model for understanding hostpathogen interactions. Annu Rev Phytopathol
    52. (1997). Mendgen K: Characterization of in planta-induced rust genes isolated from a haustorium-specific cDNA library. Mol Plant Microbe Interact
    53. (2002). Molecular basis of recognition between Phytophthora pathogens and their hosts. Annu Rev Phytopathol
    54. (2001). Molecular secrets of bacterial type III effector proteins. Trends Plant Sci
    55. (1992). M√ľnch A: The parasitic behaviour of 2nd-stage juveniles of Meloidogyne incognita in roots of Arabidopsis thaliana. Nematologica
    56. (2008). Namba S: Phytoplasmas: bacteria that manipulate plants and insects. Mol Plant Pathol
    57. (1994). Parasitic strategies of root nematodes and associated host cell responses. Annu Rev Phytopathol
    58. (2005). PE: Molecular aspects of cyst nematodes. Mol Plant Pathol
    59. (2006). Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science
    60. (2005). PJ: Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science
    61. (2006). PJ: Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol Plant Microbe Interact
    62. (2002). Plant infection and the establishment of fungal biotrophy. Trends Plant Sci
    63. (2001). Plant pathogens and integrated defence responses to infection. Nature
    64. (2008). Rhizobial secreted proteins as determinants of host specificity in the rhizobium-legume symbiosis.
    65. (2008). Robatzek S: Breaking the barriers: microbial effector molecules subvert plant immunity. Annu Rev Phytopathol
    66. (2004). S: A Kazal-like extracellular serine protease inhibitor from Phytophthora infestans targets the tomato pathogenesis-related protease P69B.
    67. (2005). S: A Second Kazal-like protease inhibitor from Phytophthora infestans inhibits and interacts with the apoplastic pathogenesis-related protease P69B of tomato. Plant Physiol
    68. (2009). Setubal JC: Protein secretion systems in bacterial-host associations, and their description in the Gene Ontology.
    69. (2001). Signal and nutrient exchange at biotrophic plant fungus interfaces. Current Opinion in Plant Biology
    70. (2003). Staskawicz BJ: Genetic and molecular evidence that the Pseudomonas syringae type III effector protein AvrRpt2 is a cysteine protease. Mol Microbiol
    71. (2004). SY: A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants.
    72. (2003). SY: A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc Natl Acad Sci USA
    73. (2005). The genome sequence of the rice blast fungus Magnaporthe grisea. Nature
    74. (2009). The Plant-Associated Microbe Gene Ontology (PAMGO) Consortium: Community development of new Gene Ontology terms describing biological processes involved in microbe-host interactions.
    75. (2007). TJ: Active uptake of cyst nematode parasitism proteins into the plant cell nucleus.
    76. (2006). Tomato Pto encodes a functional N-myristoylation motif that is required for signal transduction in Nicotiana benthamiana.
    77. (2006). Type III effector proteins from the plant pathogen Xanthomonas and their role in the interaction with host plant.
    78. (2008). VM: Silencing a candidate nematode effector gene corresponding to the tomato resistance gene Mi-1 leads to acquisition of virulence. Mol Plant Microbe Interact
    79. (2005). Voegele RT: Identification of a protein from rust fungi transferred from haustoria into infected plant cells. Mol Plant Microbe Interact
    80. (2006). Wolf-Watz H: Protein delivery into eukaryotic cells by type III secretion machines. Nature
    81. (2004). Zhou JM: Activation of a COI1-dependent pathway in Arabidopsis by Pseudomonas syringae type III effectors and coronatine.

    To submit an update or takedown request for this paper, please submit an Update/Correction/Removal Request.