Maintenance of genetic variation in plants and pathogens involves complex networks of gene-for-gene interactions

Molecular Plant Pathology

Volumn 10, Issue 4, 2009, Pages 449-457

  Hall, Sharon A ^a   Allen, Rebecca L ^a   Baumber, Rachel E ^a   Baxter, Laura A ^a   Fisher, Kate ^a   Bittner Eddy, Peter D ^a   Rose, Laura E ^b   Holub, Eric B ^a   Beynon, Jim L ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; RPP13 PROTEIN, ARABIDOPSIS;

ALLELE; ARABIDOPSIS; ARTICLE; GENE REGULATORY NETWORK; GENETIC EPISTASIS; GENETIC VARIABILITY; GENETICS; HOST PATHOGEN INTERACTION; MICROBIOLOGY; NUCLEOTIDE SEQUENCE; OOMYCETES; PHYLOGENY;

ALLELES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; EPISTASIS, GENETIC; GENE REGULATORY NETWORKS; GENETIC VARIATION; HOST-PATHOGEN INTERACTIONS; OOMYCETES; PHYLOGENY;

ARABIDOPSIS; ARABIDOPSIS THALIANA; HYALOPERONOSPORA; HYALOPERONOSPORA PARASITICA; PERONOSPORA;

EID: 67249103740     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2009.00544.x     Document Type: Article

References (37)

1. Allen, R.L., Bittner-Eddy, P.D., Grenville-Briggs, L.J., Meitz, J.C., Rehmany, A.P., Rose, L.E. and Beynon, J.L. (2004) Host-parasite coevolutionary conflict between Arabidopsis and downy mildew. Science, 306, 1957-1960.
2. Allen, R.L., Meitz, J.C., Baumber, R.E., Hall, S.A., Lee, S.C, Rose L.E. and Beynon, J.L. (2008) Natural variation reveals key amino acids in a downy mildew effector that alters recognition specificity by an Arabidopsis resistance gene. Mol. Plant Pathol. 9, 511-523.
3. Axtell, M.J. and Staskawicz, B.J. (2003) Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell, 112, 369-377.
4. Bakker, E.G., Toomajian, C., Kreitman, M. and Bergelson, J. (2006) A genome wide survey of R gene polymorphisms in Arabidopsis. Plant Cell, 18, 1803-1818.
5. van der Biezen, E.A. and Jones, J.D.G. (1998) Plant disease resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23, 454456.
6. van der Biezen, E.A., Freddie, C.T., Kahn, K., Parker, J. and Jones, J.D.G. (2002) Arabidopsis RPP4 is a member of the RPP5 multigene family of TIR-NB-LRR genes and confers downy mildew resistance through multiple signalling components. Plant J. 29, 439-451.
7. Bis grove, S.R., Simonich, M.T., Smith, N.M., Sattler, A. and Innes, R.W. (1994) A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell, 6, 927-933.
8. Bittner-Eddy, P., Can, C., Gunn, N., Pinei, M., Tor, M., Crute, I., Holub, E.B and Beynon J. (1999) Genetic and physical mapping of the RPP13 locus, in Arabidopsis, responsible for specific recognition of several Peronospora parasitica (downy mildew) isolates. Mol. Plant-Microbe Interact. 12, 792-802.
9. Bittner-Eddy, P.D., Crute, I.R., Holub, E.B. and Beynon, J.L. (2000) RPP13 is a simple locus in Arabidopsis thaliana for alleles that specify downy mildew resistance to different avirulence determinants in Peronospora parasitica. Plant J. 21, 177-188.
10. Botella, M.A., Parker, J.E., Frost, L.N., Bittner-Eddy, P.D., Beynon, J.L., Daniels, M.J., Holub, E.B. and Jones, J.D. (1998) Three genes of the Arabidopsis RPP1 complex resistance locus recognise distinct Peronospora parasitica avirulence determinants. Plant Cell, 10, 1847-1860.
11. Cooley, M.B., Pathirana, S., Wu, H.J., Kachroo, P. and Klessig, D.F. (2000) Members of the Arabidopsis HRT/RPP8 family of resistance genes confer resistance to both viral and oomycete pathogens. Plant Cell, 12, 663-676.
12. Ding, J., Cheng, H., Jin, X., Araki, H., Yang, Y. and Tian, D. (2007a) Contrasting patterns of evolution between allelic groups at a single locus in Arabidopsis. Genetica, 129, 235-242.
13. Ding, J., Zhang, W., Jing, Z., Chen, J.Q. and Tian, D. (2007b) Unique pattern of R-gene variation within populations in Arabidopsis. Mol. Genet. Genomics, 277, 619-629.
14. Dodds, P.N., Lawrence, GJ., Catanzariti, A.-M., Ayliffe, M.A. and Ellis, J.G. (2004) The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell, 16, 755-768.
15. Dodds, P.N., Lawrence, G.J., Catanzariti, A.M., Teh, T., Wang, C.-I.A., Aycliffe, M.A., Kobe, B. and Ellis, J.G. (2006) Direct protein interaction underlies gene for gene specificity and co-evolution of the flax resistance genes and flax rust avirulence genes. Proc. Natl. Acad. Sci. USA, 103, 8888-8893.
16. Goker, M., Reithmuller, A., Voglmayr, H., Weiss, M. and Oberwinkler, F. (2004) Phylogeny of Hyaloperonospora based on nuclear ribosomal internal transcribed spacer sequences. Mycol. Prog. 3, 83-94.
17. Grant, M.R., Godiard, L., Straube, E., Ashfield, T., Lewald, J., Sattler, A., Innes, R.W. and Dangl, J.L. (1995) Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science, 269, 843-846.
18. Holub, E.B. (2001) The arms race is ancient history in Arabidopsis, the wildflower. Nat. Rev. Genet. 2, 516-527.
19. Holub, E.B. (2008) Natural history of Arabidopsis thaliana and oomycete symbioses. Eur. J. Plant Pathol. 122, 91-109
20. Holub, E.B., Beynon, J.L. and Crute, I.R. (1994) Phenotypic and genotypic characterisation of interactions between isolates of Peronospora parasitica and accessions of Arabidopsis thaliana. Mol. Plant-Microbe. Interact. 7, 223-239.
21. Jia, Y., McAdams, S.A., Bryan, G.T., Hershey, H.P. and Valent, B. (2000) Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 19, 4004-4014.
22. Kim, Y.J., Lin, N.C. and Martin, G.B. (2002) Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell, 109, 589-598.
23. Kim, M.G., da Cunha, L., McFaII, A.J., Belkhadir, Y., DebRoy, S., Dangl, J.L. and MacKey, D. (2005) Two Pseudomonas syringae Type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. Cell, 121, 749-759.
24. Mackey, D., Belkhadir, Y., Alonso, J. and Ecker, J. (2003) Arabidopsis RIN4 is a target of the Type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell, 112, 379-389.
25. Maddison, D.R. and Maddison, W.P. (2000) MacClade 4: Analysis of Phylogeny and Character Evolution. Sunderland, MA: Sinauer Associates.
26. McDowell, J.M., Dhandaydham, M., Long, T.A., Aarts, M.G.M., Goff, S., Holub, E. and Dangl, J. (1998) Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell, 10, 1861-1874.
27. Parker, J.E., Coleman, M.J., Szabo, V., Frost, L.N., Schmidt, R. van der Biezen, E.A., Moores, T., Dean, C., Daniels, M.J. and Jones, J.D.G. (1997) The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the Toll and interleukin-1 receptors with N and L6. Plant Cell, 9, 879-894.
28. Rehmany, A.P., Gordon, A., Rose, L.E., Allen, R.L., Armstrong, M.R., Whisson, S.C., Kamoun, S., Tyler, B.M., Birch, P.R.J. and Beynon, J.L. (2005) Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell, 17, 1839-1850.
29. Ronald, P.C., Salmeron, J.M., Carland, F.M. and Staskawicz, B.J. (1992) The cloned avirulence gene avrPto induces disease resistance in tomato cultivars containing the Pto resistance gene. J. Bacteriol. 174, 16041611.
30. Rose, L.E., Bittner-Eddy, P.D., Langley, C.H., Holub, E.B., Michelmore, R.W. and Beynon, J.L. (2004) The maintenance of extreme amino acid diversity at the disease resistance gene, RPP13, in Arabidopsis thaliana. Genetics, 166, 1517-1527.
31. Scofield, S.R., Tobias, C., Rathjen, J.R., Chang, J.A., Lavelle, D.T., Michelmore, R.W. and Staskawicz, B.J. (1996) Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science, 274, 2063-2065.
32. Sinapidou, E., Williams, K., Nott, L., Bahkt, S., Tor, M., Crute, I., Bittner-Eddy, P. and Beynon, J. (2004) Two TIR:NB:LRR genes are required to specify resistance to Peronospora parasitica isolate Cala2 in Arabidopsis. Plant J. 38, 898-909.
33. Sohn, K.H., Lei, R., Nemri, A. and Jones, J.D.G. (2007) The downy mildew effector proteins ATR1 and ATR13 promote disease susceptibility in Arabidopsis thaliana. Plant Cell, 19, 4077-4090.
34. Swofford, D.L. (2003) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0b10. Sunderland, MA: Sinauer Associates.
35. Tang, X., Frederick, R.D., Zhou, J., Halterman, D.A., Jia, Y. and Martin, G.B. (1996) Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science, 274, 2060-2063.
36. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 22, 4673-4680.
37. Vos, P., Simons, G., Jesse, T., Wijbrandi, J., Heinen, L., Hogers, R., Frijters, A., Groenendijk, J., Diergaarde, P., Reijans, M., FierensOnstenk, J., de Both, M., Johan Peleman, J. and Liharska, T. (1998) The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nat Biotechnol. 16, 1365-1369.