Home LiteratureArticle Details
PMID: 10922039 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Genetic complexity of pathogen perception by plants: the example of Rcr3, a tomato gene required specifically by Cf-2.

Dixon MS, Golstein C, Thomas CM, van Der Biezen EA, Jones JD

Abstract

Genetic analysis of plant-pathogen interactions has demonstrated that resistance to infection is often determined by the interaction of dominant plant resistance (R) genes and dominant pathogen-encoded avirulence (Avr) genes. It was postulated that R genes encode receptors for Avr determinants. A large number of R genes and their cognate Avr genes have now been analyzed at the molecular level. R gene loci are extremely polymorphic, particularly in sequences encoding amino acids of the leucine-rich repeat motif. A major challenge is to determine how Avr perception by R proteins triggers the plant defense response. Mutational analysis has identified several genes required for the function of specific R proteins. Here we report the identification of Rcr3, a tomato gene required specifically for Cf-2-mediated resistance. We propose that Avr products interact with host proteins to promote disease, and that R proteins "guard" these host components and initiate Avr-dependent plant defense responses.

MeSH Terms
Biological Evolution Chromosome Mapping Genes, Plant Lycopersicon esculentum/genetics,microbiology
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Dixon M S
The Sainsbury Laboratory, John Innes Centre, Norwich Research Park, Colney Lane, Norwich NR4 7UH, United Kingdom.
Golstein C
Thomas C M
van Der Biezen E A
Jones J D
References (80)
80 references, click to expand
  1. Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily.
    Plant J. 1999 Nov;20(3):317-32 PMID: 10571892
  2. Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis.
    Plant Cell. 1999 Nov;11(11):2099-112 PMID: 10559437
  3. Innate immunity: impact on the adaptive immune response.
    Curr Opin Immunol. 1997 Feb;9(1):4-9 PMID: 9039775
  4. The domains of death: evolution of the apoptosis machinery.
    Trends Biochem Sci. 1999 Feb;24(2):47-53 PMID: 10098397
  5. A second gene at the tomato Cf-4 locus confers resistance to cladosporium fulvum through recognition of a novel avirulence determinant
    Plant J. 1999 Nov;20(3):279-88 PMID: 10571888
  6. MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways.
    Mol Cell. 1998 Aug;2(2):253-8 PMID: 9734363
  7. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems.
    Science. 1999 Mar 19;283(5409):1911-4 PMID: 10082464
  8. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process.
    Genome Res. 1998 Nov;8(11):1113-30 PMID: 9847076
  9. Arabidopsis RelA/SpoT homologs implicate (p)ppGpp in plant signaling.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3747-52 PMID: 10725385
  10. AFLP: a new technique for DNA fingerprinting.
    Nucleic Acids Res. 1995 Nov 11;23(21):4407-14 PMID: 7501463
  11. PLANT DISEASE RESISTANCE GENES.
    Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:575-607 PMID: 15012275
  12. Widespread distribution and fitness contribution of Xanthomonas campestris avirulence gene avrBs2.
    Nature. 1990 Jul 26;346(6282):385-6 PMID: 2374611
  13. Rapid Avr9- and Cf-9 -dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses.
    Plant Cell. 1999 Feb;11(2):273-87 PMID: 9927644
  14. Type III secretion machines: bacterial devices for protein delivery into host cells.
    Science. 1999 May 21;284(5418):1322-8 PMID: 10334981
  15. Toll gates for pathogen selection.
    Nature. 1999 Oct 21;401(6755):755-6 PMID: 10548095
  16. The biotrophic fungus Cladosporium fulvum circumvents Cf-4-mediated resistance by producing unstable AVR4 elicitors.
    Plant Cell. 1997 Mar;9(3):367-79 PMID: 9090881
  17. Characterization of a 34-kDa soybean binding protein for the syringolide elicitors.
    Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):3306-11 PMID: 9501258
  18. The tomato Cf-9 disease resistance gene functions in tobacco and potato to confer responsiveness to the fungal avirulence gene product avr 9
    Plant Cell. 1998 Aug;10(8):1251-66 PMID: 9707527
  19. Successful search for a resistance gene in tomato targeted against a virulence factor of a fungal pathogen.
    Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):9014-8 PMID: 9671796
  20. Xa21D encodes a receptor-like molecule with a leucine-rich repeat domain that determines race-specific recognition and is subject to adaptive evolution.
    Plant Cell. 1998 May;10(5):765-79 PMID: 9596635
  21. The helicase domain of the TMV replicase proteins induces the N-mediated defence response in tobacco.
    Plant J. 1999 Apr;18(1):67-75 PMID: 10341444
  22. The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIR-NBS-LRR family of disease-resistance genes.
    Plant J. 1999 Nov;20(3):265-77 PMID: 10571887
  23. Molecular analysis of the avirulence gene avr9 of the fungal tomato pathogen Cladosporium fulvum fully supports the gene-for-gene hypothesis.
    Plant J. 1992 May;2(3):359-66 PMID: 1303800
  24. Comparison of the hypersensitive response induced by the tomato Cf-4 and Cf-9 genes in Nicotiana spp.
    Mol Plant Microbe Interact. 2000 Apr;13(4):465-9 PMID: 10755310
  25. Phylogenetic perspectives in innate immunity.
    Science. 1999 May 21;284(5418):1313-8 PMID: 10334979
  26. Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection.
    Plant Cell. 1998 Nov;10(11):1833-46 PMID: 9811792
  27. cDNA-AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles.
    Plant Cell. 2000 Jun;12(6):963-77 PMID: 10852940
  28. The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis.
    Cell. 1997 May 16;89(4):575-85 PMID: 9160749
  29. Genetic and molecular analysis of tomato Cf genes for resistance to Cladosporium fulvum.
    Philos Trans R Soc Lond B Biol Sci. 1998 Sep 29;353(1374):1413-24 PMID: 9800204
  30. Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato.
    Cell. 1997 Dec 12;91(6):821-32 PMID: 9413991
  31. The avrRpm1 gene of Pseudomonas syringae pv. maculicola is required for virulence on Arabidopsis.
    Mol Plant Microbe Interact. 1995 May-Jun;8(3):444-53 PMID: 7655064
  32. Identification of Two Genes Required in Tomato for Full Cf-9-Dependent Resistance to Cladosporium fulvum.
    Plant Cell. 1994 Mar;6(3):361-374 PMID: 12244240
  33. Signal transduction pathways activated by the IL-1 receptor family: ancient signaling machinery in mammals, insects, and plants.
    J Leukoc Biol. 1998 Jun;63(6):650-7 PMID: 9620655
  34. The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho-related protein.
    Plant Cell. 1999 Mar;11(3):393-406 PMID: 10072399
  35. Caspases and programmed cell death in the hypersensitive response of plants to pathogens.
    Curr Biol. 1998 Oct 8;8(20):1129-32 PMID: 9778530
  36. Natural selection at major histocompatibility complex loci of vertebrates.
    Annu Rev Genet. 1998;32:415-35 PMID: 9928486
  37. Lipoproteins take their toll on the host.
    Curr Biol. 1999 Dec 2;9(23):R879-82 PMID: 10607553
  38. The coat protein of potato virus X is a strain-specific elicitor of Rx1-mediated virus resistance in potato.
    Plant J. 1995 Dec;8(6):933-41 PMID: 8580963
  39. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants.
    EMBO J. 1987 Dec 20;6(13):3901-7 PMID: 3327686
  40. Resistance gene-dependent activation of a calcium-dependent protein kinase in the plant defense response.
    Plant Cell. 2000 May;12(5):803-16 PMID: 10810151
  41. Structure and evolution of the rp1 complex conferring rust resistance in maize.
    Annu Rev Phytopathol. 1997;35:293-310 PMID: 15012525
  42. The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6.
    Plant Cell. 1997 Jun;9(6):879-94 PMID: 9212464
  43. Evolution by the birth-and-death process in multigene families of the vertebrate immune system.
    Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7799-806 PMID: 9223266
  44. Nod1, an Apaf-1-like activator of caspase-9 and nuclear factor-kappaB.
    J Biol Chem. 1999 May 21;274(21):14560-7 PMID: 10329646
  45. Molecular Basis of Gene-for-Gene Specificity in Bacterial Speck Disease of Tomato
    Science. 1996 Dec 20;274(5295):2063-5 PMID: 8953034
  46. The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase.
    Plant Cell. 1999 Oct;11(10):1925-34 PMID: 10521522
  47. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3.
    Cell. 1997 Aug 8;90(3):405-13 PMID: 9267021
  48. The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals.
    Curr Biol. 1998 Mar 26;8(7):R226-7 PMID: 9545207
  49. Three genes of the Arabidopsis RPP1 complex resistance locus recognize distinct Peronospora parasitica avirulence determinants.
    Plant Cell. 1998 Nov;10(11):1847-60 PMID: 9811793
  50. Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene.
    Nature. 1994 Jan 27;367(6461):384-6 PMID: 8114941
  51. Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9.
    Plant Cell. 1997 Dec;9(12):2209-24 PMID: 9437864
  52. Identification of amplified restriction fragment polymorphism (AFLP) markers tightly linked to the tomato Cf-9 gene for resistance to Cladosporium fulvum.
    Plant J. 1995 Nov;8(5):785-94 PMID: 8528290
  53. Molecular characterization of the maize Rp1-D rust resistance haplotype and its mutants.
    Plant Cell. 1999 Jul;11(7):1365-76 PMID: 10402435
  54. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21.
    Science. 1995 Dec 15;270(5243):1804-6 PMID: 8525370
  55. Functional, c-myc-tagged Cf-9 resistance gene products are plasma-membrane localized and glycosylated.
    Plant J. 2000 Mar;21(6):529-36 PMID: 10758503
  56. A family of human receptors structurally related to Drosophila Toll.
    Proc Natl Acad Sci U S A. 1998 Jan 20;95(2):588-93 PMID: 9435236
  57. The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins.
    Cell. 1996 Feb 9;84(3):451-9 PMID: 8608599
  58. Identification of three putative signal transduction genes involved in R gene-specified disease resistance in Arabidopsis.
    Genetics. 1999 May;152(1):401-12 PMID: 10224270
  59. 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.
    Cell. 1996 Jul 12;86(1):123-33 PMID: 8689679
  60. Effect of three suppressors on the expression of powdery mildew resistance genes in barley.
    Genome. 1996 Jun;39(3):492-8 PMID: 18469911
  61. The tomato Cf-5 disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number.
    Plant Cell. 1998 Nov;10(11):1915-25 PMID: 9811798
  62. Advances in the molecular genetic analysis of the flax-flax rust interaction.
    Annu Rev Phytopathol. 1997;35:271-91 PMID: 15012524
  63. The leucine-rich repeat: a versatile binding motif.
    Trends Biochem Sci. 1994 Oct;19(10):415-21 PMID: 7817399
  64. Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis.
    Nature. 1999 Aug 12;400(6745):667-71 PMID: 10458161
  65. AvrPto-dependent Pto-interacting proteins and AvrPto-interacting proteins in tomato.
    Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):8836-40 PMID: 10922043
  66. Initiation of Plant Disease Resistance by Physical Interaction of AvrPto and Pto Kinase
    Science. 1996 Dec 20;274(5295):2060-3 PMID: 8953033
  67. The AVR9 race-specific elicitor of Cladosporium fulvum is processed by endogenous and plant proteases.
    Plant Physiol. 1993 Sep;103(1):91-6 PMID: 8208859
  68. Role of cytochrome c and dATP/ATP hydrolysis in Apaf-1-mediated caspase-9 activation and apoptosis.
    EMBO J. 1999 Jul 1;18(13):3586-95 PMID: 10393175
  69. Role of CED-4 in the activation of CED-3.
    Nature. 1997 Aug 21;388(6644):728-9 PMID: 9285582
  70. Arabidopsis is susceptible to infection by a downy mildew fungus.
    Plant Cell. 1990 May;2(5):437-45 PMID: 2152169
  71. K+ channels of Cf-9 transgenic tobacco guard cells as targets for Cladosporium fulvum Avr9 elicitor-dependent signal transduction.
    Plant J. 1999 Aug;19(4):453-62 PMID: 10504567
  72. Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis.
    Plant Cell. 1998 Nov;10(11):1861-74 PMID: 9811794
  73. A High-Affinity Binding Site for the AVR9 Peptide Elicitor of Cladosporium fulvum Is Present on Plasma Membranes of Tomato and Other Solanaceous Plants.
    Plant Cell. 1996 May;8(5):929-938 PMID: 12239406
  74. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis.
    Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):10306-11 PMID: 9707643
  75. Plant disease-resistance proteins and the gene-for-gene concept.
    Trends Biochem Sci. 1998 Dec;23(12):454-6 PMID: 9868361
  76. Human CARD4 protein is a novel CED-4/Apaf-1 cell death family member that activates NF-kappaB.
    J Biol Chem. 1999 May 7;274(19):12955-8 PMID: 10224040
  77. Inhibition of the mitogen-activated protein kinase kinase superfamily by a Yersinia effector.
    Science. 1999 Sep 17;285(5435):1920-3 PMID: 10489373
  78. Cell activation and apoptosis by bacterial lipoproteins through toll-like receptor-2.
    Science. 1999 Jul 30;285(5428):736-9 PMID: 10426996
  79. The polarisation of the anterior-posterior and dorsal-ventral axes during Drosophila oogenesis.
    Curr Opin Genet Dev. 1999 Aug;9(4):396-404 PMID: 10449356
  80. Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors.
    Science. 1999 Jul 30;285(5428):732-6 PMID: 10426995
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2000-08-01
Pages
8807-14
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC34016
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]