Richard W. Michelmore

 

 

The Genome Center and Department of Plant Sciences (CA&ES)
Section of Molecular and Cellular Biology (CBS)
Medical Microbiology and Immunology (SOM)
University of California, Davis, CA 95616
Telephone: 530-752-1729
FAX: 530- 752-0436
E-mail:
Lab web page

Education

University of Cambridge , England . B.A. 1976. Natural Sciences.
University of Cambridge, England. Ph.D. 1979. Natural Sciences.

Professional Experience

1976 - 1979 Predoctoral Researcher, University of Cambridge, England.
1979 - 1980 Postdoctoral Researcher, India.
1980 - 1982 Postdoctoral Researcher, University of Cambridge, England.
1982 - 1988 Assistant Professor, University of California, Davis.
1988 - 1992 Associate Professor, University of California, Davis.
1989 - 1990 Sabbatical, CSIRO, Division of Plant Industry, Australia.
1991 Acting Chair, Genetics Graduate Group, UC Davis.
1992 - present Professor, University of California, Davis.
1997 – 2003 Chair, Genetics Graduate Group, UC Davis.
2003 – present Director, UC Davis Genome Center.

Honors, Committees etc.

Lucy Ernst Scholarship, 1977 - 1979.
Royal Society, London - Indian National Science Academy, Travel Fellowship, 1979 - 1980.
Research Fellowship, Downing College, University of Cambridge, 1981 - 1982.
NSF Eukaryotic Genetics Review Panel. 1988.
Science and Technology Coordinating Committee for the USDA Plant Genome Mapping Program, 1989 - 1992.
USDA CRGO Plant Genome Review Panel, 1991, 1993.
Associate Editor, Molecular Plant Microbe Interactions, 1991 - 1992. Senior Editor, 1992 - 1994. Panel Manager, USDA NRI Plant Genome Panel, 1997.
Scientific Advisory Board, NSF Pine Genome Project, 1999 - 2002.
Scientific Advisory Board, NSF Potato Genome Project, 1999 - present.
Panel member, USDA IFAFS Plant Genome Program.
Fellow, American Association for the Advancement of Science, 2002.
Co-Editor, Plant Cell, 2003 - 2006.
Novozymes Inc. Endowed Chair in Genomics, 2003 - present.

Research

Our research is focused on the comparative and functional genomics of disease resistance in plants, particularly Arabidopsis, tomato and lettuce. Our investigations of Arabidopsis involve the large-scale genomic analysis of resistance gene function and evolution in Arabidopsis as well as a comparative genomics analysis of resistance across multiple species. Our studies of disease resistance in tomato focus on structure-function analyses on the resistance gene Pto, Prf and dissection of the Pto-mediated disease resistance signaling pathway. Studies on lettuce and its pathogens includes classical studies of disease resistance, development of detailed genetic maps using molecular markers, studies on transgene expression and characterization of resistance genes at the molecular level. All of these projects are supported by the lab bioinformatics group.
Plants express hundreds, maybe thousands, of disease resistance genes. Many of these are related at the sequence level and therefore by inference at the functional level. Approximately 0.7% of the annotated genes in Arabidopsis encode NBS-LRR proteins. We are conducting a genome-wide analysis to determine whether all function as resistance genes or whether they are involved in other aspects of plant biology (http://niblrrs.ucdavis.edu/). This has involved a bioinformatics analysis and reannotation of the gene family, global expression analysis using a range of approaches, and microarray analysis of known resistance resistance phenotypes in collaboration with others. We are also conducting a comparative analysis of resistance genes within and between genotypes in lettuce, tomato and Arabidopsis as well as other species to determine the mechanisms that control the evolution of resistance gene specificities (http://charge.ucdavis.edu/). These studies range from population genetics to molecular analysis of spontaneous mutations. These experiments revealed that some resistance genes are not evolving as fast had been previously supposed and led us to a new model for the evolution of resistance genes. An ultimate aim of these studies is to be able to direct the evolution of resistance genes ex planta using DNA shuffling, to recognize new ligands. In addition, we are conducting a large-scale yeast two-hybrid analysis to detect interactions between bacterial, fungal, or oomycete effectors and candidate plant targets. 

A major focus of our studies on tomato is on understanding and engineering the early events in resistance of tomato to Pseudomonas syringae pv tomato. We are dissecting the signal transduction pathway involving the Prf, Pto and Fen genes. We have completely sequenced the Pto locus from resistant and susceptible haplotypes. This revealed that a variety of unequal cross-over events had occurred in the evolution of this locus. Ligand-independent, constitutive gain-of-function variants provided powerful tools to investigate the function of Pto and its homologs. Subsequently, we have been investigating the role of Prf (a NBS-LRR protein) in the Pto-mediated resistance pathway. We are using DNA shuffling to dissect the functional domains of Pto for binding pathogen-derived ligands and signaling downstream to induce the resistance response.

The classical genetic studies of lettuce involve screening lettuce germplasm for resistance, determining its genetic basis, and introgression of resistance into genotypes that are resistant to multiple diseases. Most of our efforts have focused on resistance to downy mildew (Bremia lactucae), corky root (Rhizomonas suberifaciens), and lettuce mosaic virus. We are expanding our efforts on resistance to bacterial diseases and Verticillium dahliae. These classical studies provide genotypes for our molecular investigations as well as advanced breeding lines for the commercial breeding industry. We are also continually monitoring variation in B. lactucae to understand the basis of variation in the pathogen and direct the deployment of resistance genes. We have developed a genetic map for B. lactucae. We are also generating extensive sets of ESTs from B. lactucae to identify candidate avirulence genes.

We developed a detailed genetic map of lettuce using a variety of molecular markers (http://compositdb.ucdavis.edu/). Numerous resistance genes have been mapped and molecular markers identified for them. Genes for resistance to diverse pathogens are clustered in the genome indicating a common origin and function. The genetics and evolution of resistance is being analyzed in wild and cultivated populations.  We have developed and are using a 6.6 million feature Affymetrix Genechip representing 35,000 unigenes for massively parallel genotyping and mapping.

We are coordinating The Compositae Genome Project (http://compgenomics.ucdavis.edu) to develop genomics tools for species within the Compositae, particularly lettuce and sunflower, to determine the degree of synteny between lettuce, sunflower and Arabidopsis, and to exploit functional information being generated in model species such as Arabidopsis. This involves a large-scale EST sequencing project, SNP development, and mapping of candidate genes to agriculturally important traits. Candidate genes are being validated by RNAi.
We developed stable and transient transformation systems for lettuce mediated by Agrobacterium tumefaciens. However, while it is relatively easy to introduce DNA into lettuce, transgenes are often not expressed well in stable transgenics. The reasons for this are under investigation. Transient assays work very well in lettuce and are being used to investigate the reactions to numerous bacterial effector proteins.
We utilize a combination of map-based and candidate gene strategies to clone genes for disease resistance. We saturated target regions with molecular markers (RAPDs and AFLPs), generated a BAC library with large genomic inserts, isolated numerous induced mutants of Dm genes, and constructed a detailed genetic and physical map of the largest cluster of resistance genes. We have also isolated resistance gene homologs using degenerate oligonucleotide primers to sequences that are conserved in resistance genes cloned from other species. The cloning of Dm3 was confirmed by transgenic complementation experiments. We are now developing more efficient approaches to clone additional resistance genes. RNAi is being used to demonstrate which resistances are conferred by NBS-LRR proteins.

The lab bioinformatics group supports all the above projects. This involves the acquisition and curation of genetic, sequence and microarray data, queries of EST data, the analysis of microarray data, and building tools for comparative genomics.


Teaching

I teach Plants and People (PLB12), a General Education undergraduate course for non-majors that introduces students to the importance of plants in their lives with a particular emphasis on the future impacts of biotechnology. I teach an advanced graduate level course Biotechnology and Genetics of Plant Improvement (VC220); this is a critical consideration of the integration of biotechnology and classical plant breeding. Graduate students in my lab belong to the Genetics, Plant Biology, or Plant Pathology Graduate Groups.

Selected References (Since 1991)

Michelmore, R.W., I. Paran, and R.V. Kesseli (1991). Identification of markers linked to disease resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions using segregating populations. Proc. Natl. Acad. Sci. 88:9828-9832.

Judelson, H.S., B. Tyler, and R.W. Michelmore (1991). Stable transformation of the potato late blight fungus, Phytophthora infestans. Molec. Plant-Microbe Interact. 4:602-607.

Paran, I., R.V. Kesseli, and R.W. Michelmore (1991). Identification of RFLP and RAPD markers linked to downy mildew resistance genes in lettuce using near-isogenic lines. Genome 34:1021-1027.

Vandemark, G.J., M.E. Stangellini, S.L. Rasmussen, and R.W. Michelmore (1991). Inheritance of resistance in lettuce to Plasmopara lactucae-radicis.Phytopathology 82:272-274.

Judelson, H.S., B.M. Tyler, and R.W. Michelmore (1992). Regulatory sequences for expressing genes in oomycete fungi. Mol. Gen. Genet. 234:138-146.

Paran, I., R.V. Kesseli, and R.W. Michelmore (1992). Recent amplification of triose phosphate isomerase related sequences in lettuce. Genome 35:627-635.

Michelmore, R.W., R.V. Kesseli, D.M. Francis, I.Paran, M.G. Fortin, and C.-H. Yang (1992). Strategies for cloning plant disease resistance genes. In: Molecular Plant Pathology - A Practical Approach. Ed. S. Gurr, M.J. McPherson and D.J. Bowles. IRL Press, Oxford. Vol. 2, pp233-288.

Judelson, H.S. and R.W. Michelmore (1992). Temperature and genotype interactions in the expression of host resistance in lettuce downy mildew. Physiol. Molec. Plant Pathol. 40:233-245.

Michelmore, R.W., Anderson, P.A., Witsenboer, H., Kesseli, R.V., Paran, I., Francis, D.M. and Ochoa, O. (1993). Molecular markers and genome analysis in the manipulation of lettuce downy mildew. In: Advances in Molecular Genetics of Plant Microbe Interactions, eds E. Nester & D.-P. Verma, 2:517-523.

Paran, I. and R.W. Michelmore (1993). Development of reliable PCR-based markers linked to downy mildew resistance genes in lettuce. Theor. Appl. Genet. 85:985-993.

Kesseli, R.V., Paran, I., Ochoa, O., Wang, W.-C., and Michelmore, R.W. (1993). Linkage map of lettuce (Lactuca sativa). In: Genetic Maps, 6th Ed. S. J. O'Brien (ed.). Cold Spring Harbor Press. 6.229-233.

Yang, C.-H., J. Ellis, and R.W. Michelmore. (1993). Infrequent transposition of Ac in lettuce. Pl. Mol. Biol. 22:973-805.

Yang, C.-H., Scofield, S., Caroll, B., Jones, J., Michelmore, R.W. (1993). Transposition of Ds in plants of lettuce. Mol. Gen. Genet. 241:389-398.

Francis, D.M. and R.W. Michelmore (1993). Two classes of chromosome-sized molecules are present in Bremia lactucae. Exptal. Mycol. 17:284-300.

Kesseli, R.V., Witsenboer, H., Vandemark, G.J., Stangellini, M.E., and Michelmore, R.W. (1993). Recessive resistance to Plasmopara lactucae-radicis maps by bulked segregant analysis to a cluster of dominant resistance genes in lettuce. Mol. Pl. Microbe Interact. 6:722-728.

Judelson, H.S., Dudler, R., Pieterse, C.M.J., Unkles, S.E. and 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.

Kesseli, R.V., I. Paran, and R.W. Michelmore (1994). Analysis of a detailed genetic linkage map of Lactuca sativa (lettuce) constructed from RFLP and RAPD markers. Genetics 136:1435-1446.

Okubara, P., P. Anderson, R. W. Michelmore (1994). Mutation analysis of genes for resistance to downy mildew in lettuce. Genetics 137:867-874.

Michelmore, R.W., Anderson, P., Okubara, P., Witsenboer, H. (1994). Clusters of resistance genes in lettuce: map-based cloning in non-intensively studied species. NATO ASI series, Vol. H 81, Pl. Mol. Biol. Eds. G. Coruzzi & P. Puigdomenech. Springer-Verlag, Berlin. pp 501-509.

Michelmore, R.W., Kesseli, R.V., and Ryder, E.J. (1994). Genetic mapping in lettuce. In: DNA Markers in Plants, eds, R.L. Phillips and I.K. Vasil. Kluwer Acad. Pub. pp 223-239.

Maisoneuve, B., Anderson, P. and Michelmore, R.W. (1994). Rapid mapping of two genes for resistance to downy mildew derived from Lactuca serriola to existing clusters of resistance genes. Theor. Appl. Genet. 89:96-104.

Robbins, M.A., Witsenboer, H., Michelmore, R.W. Laliberte, J.-F., and Fortin M.G. (1994). Genetic mapping of turnip mosaic virus resistance in Lactuca sativa. Theor. Appl. Genet. 89:583-589.

Michelmore, R.W. (1995). Isolation of disease resistance genes from crop plants. Curr. Opinions in Biotechnology 6:145-152.

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. Theor. Appl. Genet. 91:178-188.

Michelmore, R. (1995). Molecular approaches to manipulation of disease resistance genes. Annu. Rev. Phytopathol. 15:393-427.

Anderson, P. A., Okubara, P.A., Arroyo-Garcia, R., Meyers, B.C., Michelmore, R.W. (1996). Molecular analysis of irradiation-induced and spontaneous deletion mutants at a disease resistance locus in Lactuca sativa. Mol. Gen. Genet. 251:316-325.

Michelmore, R.W. (1996). Big news for plant transformation. (Commentary) Nature Biotechnology 14:1653-1654.

Michelmore, R.W. (1996). Flood warning: resistance genes unleashed. (News and Views) Nature Genetics 14:376-378.

Scofield, S.R. Tobias, C.M., Rathjen, J.P., Chang, J.H., 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.

Hill, M., Witsenboer, H., Zabeau, M., Vos, P., Kesseli, R., Michelmore, R. W. (1996). AFLP fingerprinting as a tool for studying genetic relationships in Lactuca spp. Theor. Appl. Genet. 93:1202-1210.

Kesseli, R., H. Witsenboer, M. Hill, Y.-H. Zhang, M. Chase and R. Michelmore. (1996). Genome organization and evolution of disease resistance genes in Lactuca spp. and the prospects for comparative mapping in the compositae. In Proc. Int. Compositae Conf., Kew, 1994. Vol. 2. Biology and Utilization. Eds. P. Caligari & D.J.N. Hind. Royal Botanic Gardens, Kew. pp 1-8.

Kesseli, R. V. and Michelmore, R. W. (1997). The Compositae: systematically fascinating but specifically neglected. In: Genome Mapping in Plants, A.H. Paterson ed. R.G. Landes Co. Georgetown, TX. pp179 - 191.

Fritjers, A.C.J., Zhang, Z., van Damme, M., Wang, G.-L., Ronald, P.C. and Michelmore, R.W. (1997). Construction of a bacterial artificial chromosome library containing large EcoRI and HindIII genomic fragments of lettuce. Theor. Appl. Genet. 3:390-399.

Okubara, P.A., Arroyo-Garcia, R., Shen, K.A., Mazier, M. Kim, Shinje, S., Michelmore, R.W. (1997). A transgenic mutant of Lactuca sativa (lettuce) with a T-DNA tightly linked to the loss of downy mildew resistance. Molec. Plant Microbe Interact. 10:970-977.

Witsenboer, H., Vogel, J., Michelmore, R.W. (1998). Identification, genetic localization and allelic diversity of selectively amplified microsatelite polymorphic loci (SAMPL) in lettuce and wild relatives (Lactuca spp.). Genome 40:923-936.

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 Interac. 11:815-823.

Meyers, B.C., Chin, D.B., Shen, K.A., Sivaramakrishnan, S., Lavelle, D.O., Zhang, Z., Michelmore, R.W. (1998). The major resistance gene cluster in lettuce is highly duplicated and spans several megabases. Plant Cell 10:1817-1832. (http://www.plantcell.org/)

Meyers, B.C., Shen, K.A., Rohani, P., Gaut, B.S., Michelmore, R.W. (1998). Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection. Plant Cell 10:1833-1846. (http://www.plantcell.org/)

Michelmore, R.W. and 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. (http://www.genome.org/)

Shiue, Y.-L., Bickel, L.A., Caetano, A.R., Millon, L.V., Clark, R., Eggleston, M.L., Michelmore, R.W., Bailey, E., Guerin, G., Godard, S., Mickelson, J.R., Valberg, S.J., Murray, J.D., Bowling, A.T. (1999). A syntenic map of the horse genome comprised of 240 microsatellite and RAPD markers. Animal Genetics 30:1-9.

Waycott, W., Fort, S., Ryder, E.J., Michelmore, R.W. (1999). Mapping of twelve morphological genes relative to molecular markers in lettuce (Lactuca sativa L.). Heredity 82:245-251.

Rathjen, J.P., Chang, J.H., Staskawicz, B.S., Michelmore, R.W. (1999). Activated Pto mediates the AvrPto-dependent hypersensitive disease resistance response in N. benthamiana and tomato. EMBO J 18:3232-3240.

Sicard, D., Woo, W.-W., Arroyo-Garcia, R., Ochoa. O., Nguyen, D., Korol, A., Nevo, E., and Michelmore, R.W. (1999). Molecular diversity at the major cluster of disease resistance genes in cultivated and wild Lactuca spp. Theor. Appl. Genet. 99:405-418.

Meyers, B.C., Dickerman, A.W., Michelmore, R.W., Sivaramakrishnan, S., Sobral, B.W. and Young, N.D. (1999). Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J. 20:317-332.

Irwin S.V., Kesseli R.V., Waycott W., Ryder E.J. Cho J.J., and Michelmore R.W. (1999). Identification of PCR-based markers flanking the recessive LMV resistance gene mo1 in an intraspecific cross of lettuce. Genome 42:982-986.

Michelmore R.W. (1999). Structure, function and evolution of resistance gene clusters in plants, particularly the Pto and Dm3 loci. Proc. 9th Int. Congr. Mol. Plant Microbe Interact. pp 232-237.

Michelmore, R.W. (2000). Genomic approaches to plant disease resistance. Curr. Opin. Plant Biol. 3:125-131.

Chang, J.H., Rathjen, J.P. Bernal, A.J., Staskawicz, B.J., Michelmore, R.W. (2000). AvrPto enhances growth and necrosis caused by Pseudomonas syringae pv. tomato in tomato lines lacking functional Pto or Prf genes. Mol. Plant Microbe Interact. 13: 568-571.

Johnson, W.C., Jackson, L.E. Ochoa, O., van Wijk, R., Peleman, J., St Clair, D.A., Michelmore, R.W. (2000). A shallow-rooted crop and its wild progenitor differ at loci determining root architecture and deep soil water extraction. Theor. Appl. Genet. 101:1066-1073.

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.

Chang, J.H., Tobias, C.M., Staskawicz, B.J., Michelmore, R.W. (2001). Functional studies of the bacterial avirulence protein AvrPto by mutational analysis. Mol. Plant Microbe Interact. 14:451-459.

Gedil, M.A., Slabaugh, M.B., Berry, S., Johnson, R., Michelmore, R.W., Miller, J., Gulya, T., Knapp, S.J. (2001). Candidate disease resistance genes in sunflower cloned using conserved nucleotide binding site motifs: genetic mapping and linkage to the Pi1 gene for resistance to downy mildew. Genome 44:205-212.

Kozik, A., Kochetkova, E., Michelmore, R.W. (2002). GenomePixelizer – a visualization program for comparative genomics within and between species. Bioinformatics 18:335-336.

Shen, K.A., Chin, D.B., Arroyo-Garcia, R., Ochoa, O.E., Lavelle, D.O., Wroblewski, T., Meyers B.C., and Michelmore, R.W. (2002). Dm3 is one member of a large constitutively-expressed family of NBS-LRR encoding genes. Mol. Plant Microbe Interact. 15:251-261.

Chang, J.H., Tai, Y.-S., Bernal, A.J., Lavelle, D.T., Staskawicz, B.J., Michelmore, R.W. (2002). Functional analysis of the Pto resistance gene family in tomato. Mol. Plant Microbe Interact. 15:281-191.

Michelmore, R.W. (2002). Natural and artificial evolution of disease resistance genes. Proc. 10th Int. Congr. Mol. Plant Microbe Interact. pp 23 – 29.

Kozik, A., Michelmore, R.W., Knapp, S.J., Matvienko, M., S., Rieseberg, L., Lin, H., van Damme, M., Lavelle, D., Chevalier, P., Ziegle, J., Ellison, P. Kolkman, J., Slabaugh, M.S., Livingston, K., Zhou, Lai, Z., Church, S., Edberg, S., Jackson, L., Bradford, K., et al. (2002). Lettuce and Sunflower ESTs from the Compositae Genome Project. http://compgenomics.ucdavis.edu/.

Mondragón-Palomino, M., Meyers, B.C., Michelmore, R.W., Gaut, B.S. (2002). Patterns of Positive Selection in the Complete NBS-LRR Gene Family of Arabidopsis thaliana. Genome Res. 12: 1305-1315.

Meyers, B.C., Morgante, M, and Michelmore, R.W. (2002). TIR-X and TIT-NBS proteins: two new families related to disease resistance TIR-NBS-LRR proteins encoded in Arabidopsis and other plant species. Plant Journal 32:77-92.

Saltveit M.E., Ochoa, O., Reinaldo Campos-Vargas, R., and Richard Michelmore, R.W. (2003). Lines of lettuce selected for ethylene insensitivity at the seedling stage displayed variable responses to ethylene or wounding in mature heads. Postharvest Biology and Technology27:277-283.

Meyers, B.C., Kozik, A., Griego, A., Kuang, H. and Michelmore, R.W. (2003). Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell15:809-834.

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 Biology39:16-30.

Michelmore, R.W. (2003). Impact zone: genomics and breeding for durable disease resistance. Current Opinion in Plant Biology6:397-404.

Moreno-Vaquez, S., Ochoa, O., Faber, N., Chao, S., Jacobs, J.M.E., Maisonneuve, B., Kesseli, R., Michelmore, R.W. (2003). SNP-based codominant markers for a recessive gene conferring resistance to corky root rot (Rhizomonas suberifaciens) in lettuce (Lactuca sativa). Genome 46:10-59-1069.

Cannon S.B., Kozik A., Chan B., Michelmore R., Young N.D. (2003). DiagHunter and GenoPix2D: programs for genomic comparisons, large-scale homology-discovery, and visualization. Genome Biology 4:R68.

Brown, S., Koike, S., Ochoa, O., Laemmlen, F. and Michelmore, R.W. (2004). Insensitivity to the fungicide, fosetyl-aluminum, in California isolates of lettuce downy mildew, Bremia lactucae. Plant Disease 46:1059-1069.

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 resistance gene RPP13 in Arabidopsis thaliana. Genetics 166:1517-1527.

Kuang, H., Woo, S.-S., Meyers, B., Nevo, E. and Michelmore, R.W. (2004). Multiple genetic processes result in heterogeneous rates of evolution within the major cluster of disease resistance genes in lettuce. Plant Cell 16: 2870-2894.

Kim, K., West, M.A.L., Michelmore, R.W., St. Clair, D.A., and Doerge , R.W. (2004). Old methods for new ideas: genetic dissection of the determinants of gene expression levels. Stadler Symposium.

Wroblewski, T., Tomczak, A., and Michelmore, R. W. (2005). Optimization of Agrobacterium-mediated transient assays of gene expression in lettuce, tomato and Arabidopsis. Plant Biotechnology Journal3 :259-273.

Bernal, A., Pan, Q., Pollack, J., Rose, L., Willets, N., Kozik, A., Michelmore, R. (2005). Functional dissection of the Pto resistance gene using DNA shuffling. J. Biol. Chem. 280:23073-83.

Rose, L., Langley , C., Bernal, A., Michelmore, R. (2005). Natural variation in the Pto pathogen resistance gene within species of wild tomato (Lycopersicon): I. Functional analysis of Pto alleles. Genetics 171: 1-13.

Argyris J., Truco M.J., Ochoa O., Knapp S.J., Still D.W., Lenssen G.M., Schut J.W., Michelmore R.W., Bradford K.J. (2005).  Quantitative trait loci associated with seed and seedling traits in Lactuca. Theor. Appl. Genet. 111:1365-1376.

Kliebenstein D.J., West M.A., van Leeuwen H., Kim K., Doerge R.W., Michelmore R.W., St Clair D.A. (2006). Genomic survey of gene expression diversity in Arabidopsis thaliana.  Genetics 172:1179-1189.

McHale, L., Tan, X., Koehl, P., Michelmore, R.W. (2006). Plant NBS-LRR proteins: adaptable guards. Genome Biology  7:212.

West, M. A.L., van Leeuwen, H., Kozik, A., Kliebenstein, D. J., Doerge, R. W., St.Clair, D. A., Michelmore, R.W. (2006). High-density haplotyping with microarray-based expression and single feature polymorphism markers in Arabidopsis. Genome Research 16: 702-712.

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.

Bushman, B.S., Scholte, A.A., Cornish, K., Scott, D.J., Brichta, J.L., Vederas, J.C., Ochoa, O., Michelmore, R.W., Shintani, D., Knapp, S.J.  (2006). Identification and characterization of natural rubber from two Lactuca species.  Phytochemistry 67:2590-2596.

Timms, L., Jimenez, R., Chase, M., Lavelle, D., McHale, L., Kozik, A., Lai, Z., Heesacker, A., Knapp, S., Rieseberg, L., Michelmore, R., Kesseli, R. (2006).  Analyses of synteny between Arabidopsis thaliana and species in the Asteraceae reveal a complex network of small syntenic segments and major chromosomal rearrangements.  Genetics 173:2227-35.

Rose, L.E., Michelmore, R.W. & Langley, C.H. (2007).  Natural variation in the Pto disease resistance gene within species of wild tomato (Lycopersicon) II. Population genetics of Pto.  Genetics  175:1307-1319.

West, M.A.L., Kim, K., Kliebenstein, D., van Leeuwen, H., Michelmore, R.W., Doerge, R.W., St Clair, D.A.  (2007). Global eQTL Mapping Reveals the Complex Genetic Architecture of Transcript-Level Variation in Arabidopsis. Genetics 175:1441-50.

Church, S.A., Livingstone, K., Lai, Z., Kozik, A., Knapp, S.J., Michelmore, R.W., Rieseberg, L.H. (2007).  Using variable rate models to identify genes under selection in pairwise comparisons: its validity and limitations for EST sequences. J. Mol. Evol. 64:171-180.

van Leeuwen, H., Kliebenstein, D.J., West, M.A.L., Kim, K., van Poecke, R., Katagiri, F., Michelmore, R.W., Doerge, R.W., St.Clair, D.A. (2007).  Natural variation among Arabidopsis thaliana Accessions for transcriptome response to exogenous salicylic acid.  Plant Cell 19:2099-110.

Zhang, F.Z, Wagstaff, C., Rae, A.M., Kaur, A., Keevil, W.C., Rothwell, S.D., Clarkson, G.J.J., Michelmore, R.W., Truco, M.J., Dixon, M.S., Taylor, G. (2007).  QTL for shelf life in lettuce co-locate with those for leaf biophysical properties but not for leaf developmental traits. J. Exp. Bot. 58: 1433-1449.

Wroblewski, T., Piskurewicz, U., Tomczak, A., Ochoa, O., & Michelmore, R.W. (2007).  Multiple resistance specificities are lost due to silencing homologs of the RGC2 NBS-LRR-encoding gene family in lettuce.  Plant J51:803-818.

Truco, M.J., Antonise, R., Lavelle, D., Ochoa, O., Kozik, A, Witsenboer, H., Fort, S., Jeuken, M.J.W., Kesseli, R. V., Lindhout, P., Michelmore, R.W., Peleman, J. (2007).  A high-density, integrated genetic linkage map of lettuce (Lactuca spp.). Theor. Appl. Genet. 115:735-746.



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