Classical and molecular genetics of Bremia lactucae, cause of lettuce downy mildew
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.
KeywordsBremia 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.
- 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
- American Phytopathological Society (2006). Microbial genomic sequencing. Perspectives of the American Phytopathological Society (Revised 2006). http://22.214.171.124/members/ppb/PDFs/MicrobialGenomicsSeq06.pdf.
- 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
- 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
- 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
- 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
- Farrara, B., & Michelmore, R. W. (1987). Identification of new sources of resistance to downy mildew in Lactuca germplasm. HortScience, 22, 647–649.Google Scholar
- Gustafsson, I. (1989). Potential sources of resistance to lettuce downy mildew (Bremia lactucae) in different Lactuca species. Euphytica, 40, 227–232.Google Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- Michelmore, R. W., & Ingram, D. S. (1980). Heterothallism in Bremia lactucae. Transactions of the British Mycological Society, 75, 47–56.Google Scholar
- Michelmore, R. W., & Ingram, D. S. (1982). Secondary homothallism in Bremia lactucae. Transactions of the British Mycological Society, 78, 1–9.Google Scholar
- 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
- 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
- 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
- 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
- US Department of Agriculture (2003). Agricultural chemical usage: 2002 vegetables summary. http://usda.mannlib.cornell.edu/reports/nassr/other/pcu-bb/agcv0703.pdf.
- US Department of Agriculture (2006). USDA Economics, Statistics and Market Information System (ESMIS). http://usda.mannlib.cornell.edu/MannUsda/homepage.do.
- 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