Classical and molecular genetics of Bremia lactucae, cause of lettuce downy mildew

  • Richard MichelmoreEmail author
  • Joan Wong


Lettuce downy mildew caused by Bremia lactucae has long been a model for understanding biotrophic oomycete–plant interactions. Initial research involved physiological and cytological studies that have been reviewed earlier. This review provides an overview of the genetic and molecular analyses that have occurred in the past 25 years as well as perspectives on future directions. The interaction between B. lactucae and lettuce (Lactuca sativa) is determined by an extensively characterized gene-for-gene relationship. Resistance genes have been cloned from L. sativa that encode proteins similar to resistance proteins isolated from other plant species. Avirulence genes have yet to be cloned from B. lactucae, although candidate sequences have been identified on the basis of motifs present in secreted avirulence proteins characterized from other oomycetes. Bremia lactucae has a minimum of 7 or 8 chromosome pairs ranging in size from 3 to at least 8 Mb and a set of linear polymorphic molecules that range in size between 0.3 and 1.6 Mb and are inherited in a non-Mendelian manner. Several methods indicated the genome size of B. lactucae to be ca. 50 Mb, although this is probably an underestimate, comprising approximately equal fractions of highly repeated sequences, intermediate repeats, and low-copy sequences. The genome of B. lactucae still awaits sequencing. To date, several EST libraries have been sequenced to provide an incomplete view of the gene space. Bremia lactucae has yet to be transformed, but regulatory sequences from it form components of transformation vectors used for other oomycetes. Molecular technology has now advanced to the point where rapid progress is likely in determining the molecular basis of specificity, mating type, and fungicide insensitivity.


Bremia lactucae Lettuce Virulence Resistance Oomycete 



The work described here has been the result of many people’s efforts spread over the past 25 years. We thank them all for their contributions. Financial support has come from numerous sources including sustained support from the California Lettuce Research Board and the USDA CREES National Research Initiative.


  1. Abramovitch, R. B., Kim, Y. J., Chen, S., Dickman, M. B., & Martin, G. B. (2003). Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO Journal, 22, 60–69.PubMedCrossRefGoogle Scholar
  2. Alfano, J. R., Charkowski, A. O., Deng, W. L., Badel, J. L., Petnicki-Ocwieja, T., van Dijk, K., et al. (2000). The Pseudomonas syringae Hrp pathogenicity island has a tripartite mosaic structure composed of a cluster of type III secretion genes bounded by exchangeable effector and conserved effector loci that contribute to parasitic fitness and pathogenicity in plants. Proceedings of the National Academy of Sciences of the United States of America, 97, 4856–4861.PubMedCrossRefGoogle Scholar
  3. Allen, R. L., Bittner-Eddy, P. D., Grenville-Briggs, L. J., Meitz, J. C., Rehmany, A. P., Rose, L. E., et al. (2004). Host–parasite co-evolutionary conflict between Arabidopsis and downy mildew. Science, 306, 1957–1960.PubMedCrossRefGoogle Scholar
  4. American Phytopathological Society (2006). Microbial genomic sequencing. Perspectives of the American Phytopathological Society (Revised 2006).
  5. Andrews, J. H. (1975). Distribution of label from 3H-glucose and 3H-leucine in lettuce cotyledons during early stages of infection with Bremia lactucae. Canadian Journal of Botany, 53, 1103–1115.Google Scholar
  6. Armstrong, M. R., Whisson, S. C., Pritchard, L., Bos, J. L., Venter, E., Avrova, A. O., et al. (2005). An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proceedings of the National Academy of Sciences of the United States of America, 102, 7766–7771.PubMedCrossRefGoogle Scholar
  7. Beharav, A., Lewinsohn, D., Lebeda, A., & Nevo, E. (2006). New wild Lactuca genetic resources with resistance against Bremia lactucae. Genetic Resources and Crop Evolution, 53, 467–474.CrossRefGoogle Scholar
  8. Bennett, M., Gallagher, M., Fagg, J., Bestwick, C., Paul, T., Beale, M., et al. (1996). The hypersensitive reaction, membrane damage and accumulation of autofluorescent phenolics in lettuce cells challenged by Bremia lactucae. Plant Journal, 9, 851–865.CrossRefGoogle Scholar
  9. Bestwick, C. S., Brown, I. R., & Mansfield, J. W. (1998). Localized changes in peroxidase activity accompany hydrogen peroxide generation during the development of a nonhost hypersensitive reaction in lettuce. Plant Physiology, 118, 1067–1078.PubMedCrossRefGoogle Scholar
  10. Bhattacharjee, S., Hiller, L. N., Liolios, K., Win, J., Kanneganti, T.-D., Young, C., et al. (2006). The malarial host-targeting signal is conserved in the Irish potato famine pathogen. PLoS Pathogens, 2, 50.CrossRefGoogle Scholar
  11. Birch, P. R., Rehmany, A. P., Pritchard, L., Kamoun, S., & Beynon, J. L. (2006). Trafficking arms: Oomycete effectors enter host plant cells. Trends in Microbiology, 14, 8–11.PubMedCrossRefGoogle Scholar
  12. Bonnier, F. J. K., Reinink, K., & Groenwold, R. (1994). Genetic analysis of Lactuca accessions with new major gene resistance to lettuce downy mildew. Phytopathology, 84, 462–468.CrossRefGoogle Scholar
  13. Brown, S., Koike, S., Ochoa, O., Laemmlen, F., & Michelmore, R. W. (2004). Insensitivity to the fungicide, fosetyl-aluminum, in California isolates of lettuce downy mildew, Bremia lactucae. Plant Disease, 46, 1059–1069.Google Scholar
  14. Chamnanpunt, J., Shan, W.-X., & Tyler, B. M. (2001). High frequency mitotic gene conversion in genetic hybrids of the oomycete Phytophthora sojae. Proceedings of the National Academy of Sciences of the United States of America, 98, 14530–14535.PubMedCrossRefGoogle Scholar
  15. Chang, J. H., Urbach, J. M., Law, T. F., Arnold, L. W., Hu, A., Gombar, S., et al. (2005). A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae. Proceedings of the National Academy of Sciences of the United States of America, 102, 2549–2554.PubMedCrossRefGoogle Scholar
  16. Chin, D. B., Arroyo-Garcia, R., Ochoa, O., Kesseli, R. V., Lavelle, D. O., & Michelmore, R. W. (2001). Recombination and spontaneous mutation at the major cluster of resistance genes in lettuce (Lactuca sativa). Genetics, 157, 831–849.PubMedGoogle Scholar
  17. Crute, I. R., & Johnson, A. G. (1976). The genetic relationship between races of Bremia lactucae and cultivars of Lactuca sativa. Annals of Applied Biology, 83, 125–137.CrossRefGoogle Scholar
  18. Crute, I. R., & Norwood, J. M. (1978). Incomplete specific resistance to Bremia lactucae in lettuce. Annals of Applied Biology, 89, 467–474.CrossRefGoogle Scholar
  19. Crute, I. R., Norwood, J. M., & Gordon, P. L. (1987). The occurrence, characteristics, and distribution in the United Kingdom of resistance to phenylamide fungicides in Bremia lactucae (lettuce downy mildew). Plant Pathology, 36, 297–315.CrossRefGoogle Scholar
  20. Dioh, W., Tharreau, D., Notteghem, J.-L., Orbach, M., & Lebrun, M.-H. (2000). Mapping of avirulence genes in the rice blast fungus, Magnaporthe grisea, with RFLP and RAPD markers. Molecular Plant–Microbe Interactions, 13, 217–227.PubMedCrossRefGoogle Scholar
  21. Eenink, A. H., Groenwold, R., & Bijker, W. (1983). Partial resistance in lettuce downy mildew (Bremia lactucae). 4. Resistance after natural, semi-artificial and artificial infestation and examples of mutual interference of resistance levels. Euphytica, 32, 139–149.CrossRefGoogle Scholar
  22. Espinosa, A., Guo, M., Tam, V. C., Fu, Z. Q., & Alfano, J. R. (2003). The Pseudomonas syringae type III-secreted protein HopPtoD2 possesses protein tyrosine phosphatase activity and suppresses programmed cell death in plants. Molecular Microbiology, 49, 377–387.PubMedCrossRefGoogle Scholar
  23. Fabritius, A. L., & Judelson, H. S. (1997). Mating-type loci segregate aberrantly in Phytophthora infestans but normally in Phytophthora parasitica: Implications for models of mating-type determination. Current Genetics, 32, 60–65.PubMedCrossRefGoogle Scholar
  24. Farrara, B., Ilott, T. W., & Michelmore, R. W. (1987). Genetic analysis of factors for resistance to downy mildew (Bremia lactucae) in species of lettuce (Lactuca sativa and L. serriola). Plant Pathology, 36, 499–514.CrossRefGoogle Scholar
  25. Farrara, B., & Michelmore, R. W. (1987). Identification of new sources of resistance to downy mildew in Lactuca germplasm. HortScience, 22, 647–649.Google Scholar
  26. Francis, D. M., Hulbert, S. H., & Michelmore, R. W. (1990). Genome size and complexity of the obligate fungal pathogen, Bremia lactucae. Experimental Mycology, 14, 299–309.CrossRefGoogle Scholar
  27. Francis, D. M., & Michelmore, R. W. (1993). Two classes of chromosome-sized molecules are present in Bremia lactucae. Experimental Mycology, 17, 284–300.CrossRefGoogle Scholar
  28. Fu, Z. Q., Guo, M., Jeong, B.-R., Tian, F., Elthon, T. E., Cerny, R. L., et al. (2007). A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature, 447, 284–288.PubMedCrossRefGoogle Scholar
  29. Galagan, J. E., Calvo, S. E., Cuomo, C., Ma, L.-J., Wortman, J. R., Batzoglou, S., et al. (2005). Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature, 438, 1105–1115.PubMedCrossRefGoogle Scholar
  30. Göker, M., Voglmayer, H., Reithmüller, A., & Oberwinkler, F. (2007). How do obligate parasties evolve? A multi-gene phylogenetic analysis of the downy mildews. Fungal Genetics and Biology, 44, 105–122.PubMedCrossRefGoogle Scholar
  31. Govers, F., & Gijzen, M. (2006). Phytophthora genomics: The plant destroyers’ genome decoded. Molecular Plant–Microbe Interactions, 19, 1295–1301.PubMedCrossRefGoogle Scholar
  32. Grant, S. R., Fisher, E. J., Chang, J. H., Mole, B. M., & Dangl, J. L. (2006). Subterfuge and manipulation: Type III effector proteins of phytopathogenic bacteria. Annual Review of Microbiology, 60, 425–429.PubMedCrossRefGoogle Scholar
  33. Greenberg, J., & Vinatzer, B. A. (2003). Identifying type III effectors of plant pathogens and analyzing their interaction with plant cells. Current Opinion in Microbiology, 6, 20–28.PubMedCrossRefGoogle Scholar
  34. Gustafsson, I. (1989). Potential sources of resistance to lettuce downy mildew (Bremia lactucae) in different Lactuca species. Euphytica, 40, 227–232.Google Scholar
  35. Gustafsson, M., Liljeroth, E., & Gustafsson, I. (1985). Pathogenic variation and sexual reproduction in Swedish populations of Bremia lactucae. Theoretical and Applied Genetics, 70, 643–649.CrossRefGoogle Scholar
  36. Guttman, D. S., Vinatzer, B. A., Sarkar, S. F., Ranall, M. V., Kettler, G., & Greenberg, J. T. (2002). A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science, 295, 1722–1726.PubMedCrossRefGoogle Scholar
  37. Hulbert, S. H., Hott, T. W., Legg, E. J., Lincoln, S. E., Lander, E. S., & Michelmore, R. W. (1988). Genetic analysis of the fungus, Bremia lactucae, using restriction fragment length polymorphisms. Genetics, 120, 947–958.PubMedGoogle Scholar
  38. Hulbert, S. H., & Michelmore, R. W. (1985). Linkage analysis of genes for resistance to downy mildew (Bremia lactucae) in lettuce (Lactuca sativa). Theoretical and Applied Genetics, 70, 520–528.CrossRefGoogle Scholar
  39. Hulbert, S. H., & Michelmore, R. W. (1987). DNA restriction fragment length polymorphism and somatic variation in the lettuce downy mildew fungus, Bremia lactucae. Molecular Plant–Microbe Interactions, 1, 17–24.Google Scholar
  40. Ilott, T. W., Durgan, M. E., & Michelmore, R. W. (1987). Genetics of virulence in California populations of Bremia lactucae (lettuce downy mildew). Phytopathology, 77, 1381–1386.CrossRefGoogle Scholar
  41. Ilott, T. W., Hulbert, S. H., & Michelmore, R. W. (1989). Genetic analysis of the gene-for-gene interaction between lettuce (Lactuca sativa) and Bremia lactucae. Phytopathology, 79, 888–897.CrossRefGoogle Scholar
  42. Ingram, D. S. (1981). Physiology and biochemistry of host–parasite interaction. In D. M. Spencer (Ed.), The downy mildews (pp. 143–163). London: Academic.Google Scholar
  43. Ingram, D. S., Sargent, J. A., & Tommerup, I. C. (1976). Structural aspects of infection by biotrophic fungi. In J. Friend, & D. R. Threlfall (Eds.), Biochemical aspects of plant–parasite relationships (pp. 43–78). New York: Academic.Google Scholar
  44. Jackson, R. W., Athanassopoulos, E., Tsiamis, G., Mansfield, J. W., Sesma, A., Arnold, D. L., et al. (1999). Identification of a pathogenicity island, which contains genes for virulence and avirulence, on a large native plasmid in the bean pathogen Pseudomonas syringae pathovar phaseolicola. Proceedings of the National Academy of Sciences of the United States of America, 96, 10875–10880.PubMedCrossRefGoogle Scholar
  45. Jamir, Y., Guo, M., Oh, H. S., Petnicki-Ocwieja, T., Chen, S., Tang, X., et al. (2004). Identification of Pseudomonas syringae type III effectors that can suppress programmed cell death in plants and yeast. Plant Journal, 37, 554–565.PubMedCrossRefGoogle Scholar
  46. Jeuken, M., & Lindhout, P. (2002). Lactuca saligna, a non-host for lettuce downy mildew (Bremia lactucae), harbors a new race-specific Dm gene and three QTLs for resistance. Theoretical and Applied Genetics, 105, 384–391.PubMedCrossRefGoogle Scholar
  47. Jones, J. D., & Dangl, J. L. (2006). The plant immune system. Nature, 444, 323–329.PubMedCrossRefGoogle Scholar
  48. Judelson, H. S., Dudler, R., Pieterse, C. M. J., Unkles, S. E., & Michelmore, R. W. (1993). Expression and antisense inhibition of transgenes in Phytophthora infestans is modulated by choice of promoter and position effects. Gene, 133, 63–69.PubMedCrossRefGoogle Scholar
  49. Judelson, H. S., & Michelmore, R. W. (1989). Structure and expression of a gene encoding heat-shock protein Hsp70 from the oomycete fungus Bremia lactucae. Gene, 79, 207–217.PubMedCrossRefGoogle Scholar
  50. Judelson, H. S., & Michelmore, R. W. (1990). Highly abundant and stage-specific mRNAs in the obligate pathogen Bremia lactucae. Molecular Plant–Microbe Interactions, 3, 225–232.PubMedGoogle Scholar
  51. Judelson, H. S., & Michelmore, R. W. (1991). Transient expression of genes in the oomycete Phytophthora infestans using Bremia lactucae regulatory sequences. Current Genetics, 19, 453–459.CrossRefGoogle Scholar
  52. Judelson, H. S., & Michelmore, R. W. (1992). Temperature and genotype interactions in the expression of host resistance in lettuce downy mildew. Physiological and Molecular Plant Pathology, 40, 233–245.CrossRefGoogle Scholar
  53. Judelson, H. S., Tyler, B., & Michelmore, R. W. (1991). Stable transformation of the potato late blight fungus, Phytophthora infestans. Molecular Plant–Microbe Interactions, 4, 602–607.PubMedGoogle Scholar
  54. Judelson, H. S., Tyler, B. M., & Michelmore, R. W. (1992). Regulatory sequences for expressing genes in oomycete fungi. Molecular and General Genetics, 234, 138–146.PubMedGoogle Scholar
  55. Kamoun, S. (2006). A catalogue of the effector secretome of plant pathogenic oomycetes. Annual Review on Phytopathology, 44, 41–60.CrossRefGoogle Scholar
  56. Kuang, H., Ochoa, O. E., Nevo, E., & Michelmore, R. W. (2006). The disease resistance gene Dm3 is infrequent in natural populations of Lactuca serriola due to deletions and frequent gene conversions. Plant Journal, 47, 38–48.PubMedCrossRefGoogle Scholar
  57. Kuang, H., Woo, S.-S., Meyers, B. C., Nevo, E., & Michelmore, R. W. (2004). Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell, 16, 2870–2894.PubMedCrossRefGoogle Scholar
  58. Lebeda, A., & Blok, I. (1990). Sexual compatibility types of Bremia lactucae originating from Lactuca serriola. Netherlands Journal of Plant Pathology, 96, 51–54.CrossRefGoogle Scholar
  59. Lebeda, A., Sedlarova, M., Petrivalsky, M., & Prokopova, J. (2008). Diversity of defense mechanisms in plant–pathogen interactions: A case study of Lactuca spp.–Bremia lactucae. European Journal of Plant Pathology (this issue).Google Scholar
  60. Lebeda, A., & Zinkernagel, V. (2003). Characterization of new highly virulent German isolates of Bremia lactucae and efficiency of resistance in wild Lactuca germplasm. Journal of Phytopathology, 151, 274–282.Google Scholar
  61. MacGregor, T., Bhattacharyya, M., Tyler, B., Bhat, B., Schmitthenner, A. F., & Gijzen, M. (2002). Genetic and physical mapping of Avr1a in Phytophthora sojae. Genetics, 160, 949–959.PubMedGoogle Scholar
  62. Maclean, D. J., Sargent, J. A., Tommerup, I. C., & Ingram, D. S. (1974). Hypersensitivity as a primary event in resistance to fungal parasites. Nature, 249, 186–187.PubMedCrossRefGoogle Scholar
  63. Maclean, D. J., & Tommerup, I. C. (1979). Histology and physiology of compatibility and incompatibility between lettuce and the downy mildew fungus, Bremia lactucae Regel. Physiological Plant Pathology, 14, 291–312.CrossRefGoogle Scholar
  64. Maisonneuve, B., Anderson, P., & Michelmore, R. W. (1994). Rapid mapping of two genes for resistance to downy mildew derived from Lactuca serriola to existing clusters of resistance genes. Theoretical and Applied Genetics, 89, 96–104.CrossRefGoogle Scholar
  65. Mandel, M. A., Crouch, V. W., Gunawardena, U. P., Harper, T. M., & Orbach, M. J. (1997). Physical mapping of the Magnaporthe grisea Avr1-MARA locus reveals the virulent allele contains two deletions. Molecular Plant–Microbe Interactions, 10, 1102–1105.CrossRefGoogle Scholar
  66. McHale, L., Tan, X., Koehl, P., & Michelmore, R. W. (2006). Plant NBS-LRR proteins: Adaptable guards. Genome Biology, 7, 212.PubMedCrossRefGoogle Scholar
  67. Meyers, B. C., Chin, D. B., Shen, K. A., Sivaramakrishnan, S., Lavelle, D. O., Zhang, Z., et al. (1998a). The major resistance gene cluster in lettuce is highly duplicated and spans several megabases. Plant Cell, 10, 1817–1832.PubMedCrossRefGoogle Scholar
  68. Meyers, B. C., Shen, K. A., Rohani, P., Gaut, B. S., & Michelmore, R. W. (1998b). Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection. Plant Cell, 10, 1833–1846.PubMedCrossRefGoogle Scholar
  69. Michelmore, R. W., & Ingram, D. S. (1980). Heterothallism in Bremia lactucae. Transactions of the British Mycological Society, 75, 47–56.Google Scholar
  70. Michelmore, R. W., & Ingram, D. S. (1981). The origin of gametangia in the heterothallic isolates of Bremia lactucae Regel. Transactions of the British Mycological Society, 76, 425–432.CrossRefGoogle Scholar
  71. Michelmore, R. W., & Ingram, D. S. (1982). Secondary homothallism in Bremia lactucae. Transactions of the British Mycological Society, 78, 1–9.Google Scholar
  72. Michelmore, R. W., & Meyers, B. C. (1998). Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Research, 8, 1113–1130.PubMedGoogle Scholar
  73. Michelmore, R. W., Norwood, J. M., Ingram, D. S., Crute, I. R., & Nicholson, P. (1984). The inheritance of virulence in Bremia lactucae to match resistant factors 3, 4, 5, 6, 8, 9, 10 and 11 in lettuce (Lactuca sativa). Plant Pathology, 33, 301–315.CrossRefGoogle Scholar
  74. Michelmore, R. W., Paran, I., & Kesseli, R. V. (1991). Identification of markers linked to disease resistance genes by bulked segregant analysis: A rapid method to detect markers in specific genomic regions by using segregating populations. Proceedings of the National Academy of Sciences of the United States of America, 88, 9828–9832.PubMedCrossRefGoogle Scholar
  75. Michelmore, R. W., & Sansome, E. R. (1982). Cytological studies of heterothallism and secondary homothallism in Bremia lactucae. Transactions of the British Mycological Society, 79, 291–297.Google Scholar
  76. Nomura, K., Melotto, M., & He, S.-Y. (2005). Suppression of host defense in compatible plant–Pseudomonas syringae interactions. Current Opinion in Plant Biology, 8, 361–368.PubMedCrossRefGoogle Scholar
  77. Norwood, J. M., & Crute, I. R. (1984). The genetic control and expression of specificity in Bremia lactucae (lettuce downy mildew). Plant Pathology, 33, 385–400.CrossRefGoogle Scholar
  78. Norwood, J. M., Michelmore, R. W., Crute, I. R., & Ingram, D. S. (1983). The inheritance of specific virulence of Bremia lactucae (downy mildew) to match resistance factors 1, 2, 4, 6 and 11 in Lactuca sativa (lettuce). Plant Pathology, 32, 176–177.CrossRefGoogle Scholar
  79. Petnicki-Ocwieja, T., Schneider, D. J., Tam, V. C., Chancey, S. T., Shan, L., Jamir, Y., et al. (2002). Genomewide identification of proteins secreted by the Hrp type III protein secretion system of Pseudomonas syringae pv. tomato DC3000. Proceedings of the National Academy of Sciences of the United States of America, 99, 7652–7657.PubMedCrossRefGoogle Scholar
  80. Petrželová, I., & Lebeda, A. (2003). Distribution of compatibility types and occurrence of sexual reproduction in natural populations of Bremia lactucae on wild Lactuca serriola plants. Acta Phytopathologica et Entomologica Hungarica, 38, 43–52.CrossRefGoogle Scholar
  81. Rehmany, A. P., Gordon, A., Rose, L. E., Allen, R. L., Armstrong, M. R., Whisson, S. C., et al. (2005). Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell, 17, 1839–1850.PubMedCrossRefGoogle Scholar
  82. Schettini, T. M., Legg, E. J., & Michelmore, R. W. (1991). Insensitivity to metalaxyl in California populations of Bremia lactucae and resistance of California lettuce cultivars to downy mildew. Phytopathology, 81, 64–69.CrossRefGoogle Scholar
  83. Shan, W., Cao, M., Leung, D., & Tyler, B. M. (2004). The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps1b. Molecular Plant–Microbe Interactions, 17, 394–403.PubMedCrossRefGoogle Scholar
  84. Shen, K. A., Chin, D. B., Arroyo-Garcia, R., Ochoa, O. E., Lavelle, D. O., Wroblewski, T., et al. (2002). Dm3 is one member of a large constitutively-expressed family of NBS-LRR encoding genes. Molecular Plant–Microbe Interactions, 15, 251–261.PubMedCrossRefGoogle Scholar
  85. Shen, K. A., Meyers, B. C., Islam-Faridi, M. N., Chin, D. B., Stelly, D. M., & Michelmore, R. W. (1998). Resistance gene candidates identified using PCR with degenerate primers map to resistance genes clusters in lettuce. Molecular Plant–Microbe Interactions, 11, 815–823.PubMedCrossRefGoogle Scholar
  86. Sicard, D., Legg, E. J., Brown, S., Babu, N., Ochoa, O., & Michelmore, R. W. (2003). A genetic map of the lettuce downy mildew fungus, Bremia lactucae, constructed from molecular markers and avirulence genes. Fungal Genetics and Biology, 39, 16–30.PubMedCrossRefGoogle Scholar
  87. Sicard, D., Woo, S.-S., Arroyo-Garcia, R., Ochoa, O., Nguyen, D., Korol, A., et al. (1999). Molecular diversity at the major cluster of disease resistance genes in cultivated and wild Lactuca spp. Theoretical and Applied Genetics, 99, 405–418.CrossRefGoogle Scholar
  88. Sugio, A., Yang, B., & White, F. F. (2005). Characterization of the hrpF pathogenicity peninsula of Xanthomonas oryzae pv. oryzae. Molecular Plant–Microbe Interactions, 18, 546–554.PubMedCrossRefGoogle Scholar
  89. The Arabidopsis Genome Initiative (2000). Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796–815.CrossRefGoogle Scholar
  90. Torto, T. A., Li, S., Styer, A., Huitema, E., Testa, A., Gow, N. A., et al. (2003). EST mining and functional expression assays identify extracellular effector proteins from the plant pathogen Phytophthora. Genome Research, 13, 1675–1685.PubMedCrossRefGoogle Scholar
  91. Tyler, B. M. (2002). Molecular basis of recognition between Phytophthora pathogens and their hosts. Annual Review of Phytopathology, 40, 137–167.PubMedCrossRefGoogle Scholar
  92. Tyler, B. M., Tripathy, S., Zhang, X., Dehal, P., Jiang, R. H. Y., Aerts, A., et al. (2006). Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science, 313, 1197–1313.CrossRefGoogle Scholar
  93. US Department of Agriculture (2003). Agricultural chemical usage: 2002 vegetables summary.
  94. US Department of Agriculture (2006). USDA Economics, Statistics and Market Information System (ESMIS).
  95. Voglmayr, H., & Greilhuber, J. (1998). Genome size determination in Peronosporales (Oomycota) by Feulgen image analysis. Fungal Genetics and Biology, 25, 181–195.PubMedCrossRefGoogle Scholar
  96. Voglmayr, H., Riethmüller, A., Göker, M., Weiss, M., & Oberwinkler, F. (2004). Phylogenetic relationships of Plasmopara, Bremia, and other genera of downy mildews with pyriform haustoria based on Bayesian analysis of partial LSU rDNA sequence. Mycological Research, 108, 1011–1024.PubMedCrossRefGoogle Scholar
  97. Whisson, S. C., Boevink, P. C., Moleleki, L., Avrova, A. O., Morales, J. G., Gilroy, E. M., et al. (2007). A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature, 450, 115–118.PubMedCrossRefGoogle Scholar
  98. Win, J., Kanneganti, T. D., Torto-Alalibo, T., & Kamoun, S. (2005). Computational and comparative analyses of 150 full-length cDNA sequences from the oomycete plant pathogen Phytophthora infestans. Fungal Genetics and Biology, 43, 20–33.PubMedCrossRefGoogle Scholar
  99. Witsenboer, H., Kesseli, R. V., Fortin, M., Stangellini, M., & Michelmore, R. W. (1995). Sources and genetic structure of a cluster of genes for resistance to three pathogens in lettuce. Theoretical and Applied Genetics, 91, 178–188.CrossRefGoogle Scholar
  100. Woods, A. M., Didehvar, F., Gay, J. L., & Mansfield, J. W. (1988). Modification of the host plasmalemma in haustorial interactions of Lactuca sativa by Bremia lactucae. Physiological and Molecular Plant Pathology, 33, 299–310.CrossRefGoogle Scholar
  101. Wroblewski, T., Piskurewicz, U., Tomczak, A., Ochoa, O., & Michelmore, R. W. (2007). Silencing of the major family of NBS-LRR-encoding genes in lettuce results in the loss of multiple resistance specificities. Plant Journal, 51, 803–818.PubMedCrossRefGoogle Scholar
  102. Wroblewski, T., Tomczak, A., & Michelmore, R. W. (2005). Optimization of Agrobacterium-mediated transient assays of gene expression in lettuce, tomato and Arabidopsis. Plant Biotechnology Journal, 3, 259–273.PubMedCrossRefGoogle Scholar
  103. Yuen, J. E., & Lorbeer, J. W. (1987). Natural and experimental production of oospores of Bremia lactucae in lettuce in New York. (1987). Plant Disease, 71, 63–64.CrossRefGoogle Scholar

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© KNPV 2008

Authors and Affiliations

  1. 1.The Genome Center and Department of Plant SciencesUniversity of CaliforniaDavisUSA

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