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      Species name: Lettuce (Lactuca sativa L)
      Overview
    Lettuce (Lactuca sativa L.) is an annual plant in the daisy family, Compositae (Asteraceae), tribe Lactuceae of subfamily Cichorioideae (K?ístková et al., 2008). L. sativa is diploid with 2n=2x=18 chromosomes. The genome size has been estimated by flow cytometry to be ~2.3 pg (Koopman & De Jong, 1996) or 2.5 Gb by (Michaelson et al., 1991). This has been corroborated by whole genome sequencing and assembly of L. sativa cv. Salinas at ~2.7 Gb. It is inbreeding with limited genetic diversity within cultivated types (Hill et al., 1996). There are four well-established major species within the subsection Lactuca, cultivated L. sativa and three wild species, L. serriola, L. saligna, and L. virosa, as well as several less well characterized species (Feráková, 1977). Wild species, particularly L. serriola, have been sources of disease resistance genes (Crute, 1988 & 1992); however, they remain a rich potential source of variation that has not been accessed systematically (Sicard et al. , 1999; Lebeda & Zinkernagel, 2003; Beharav et al. , 2006; Kuang et al. , 2008).

    The name of the genus is derived from lac, Latin for milk, due to the plant’s milky latex that exudes from the stem when cut. The earliest description of lettuce is in carvings at the temple of Senusret I at Karnak in Egypt. Lettuce was considered an aphrodisiac food in ancient Egypt. Lactucarium (or "Lettuce Opium") is a mild opiate-like substance in the latex of all types of lettuce. Ancient Greek physicians recognized that lettuce could act as a sleep-inducing agent. Both Romans and Egyptians took advantage of this by eating lettuce at the end of a meal to induce sleep (http://en.wikipedia.org/wiki/Lactuca_sativa). Lettuce was introduced to the New World by Christopher Columbus. It is now used worldwide as a leaf vegetable. It is eaten either raw in salads, sandwiches, hamburgers, tacos, and many other dishes, or cooked, as in Chinese cuisine, in which the stem is as important as the leaf. Lettuce is a low calorie food and is a source of vitamin A and folic acid. Because of the volume eaten, it is significant part of the American diet.

    Cultivated lettuce was likely domesticated from the successful weed L. serriola (Lindvist, 1960; Kesseli et al. , 1991; de Vries et al., 1997). L. sativa and L. serriola can be readily crossed and there are no major barriers to gene flow between these species (Lindqvist, 1960). Cultivated lettuce initially has a short stem (rosette stage), but when it flowers (bolts), the stem and branches lengthen and produce many flower heads (Figures 1 & 2). Domestication has resulted in slower bolting, exaggeration of the leaves at the rosette stage, a variety of leaf shapes and colors, lower latex content, and a non-shattering involucre.

    Lettuce is an important vegetable crop species and ranks as one of the top ten most valuable crops in the U.S. with an annual value of over $2 billion (Anon., 2011). The United States is the second largest lettuce-producing country behind China (http://usda.mannlib.cornell.edu/usda/current/lettuce/lettuce-01-14-2009.pdf). There are five commonly recognized types of lettuce that are consumed as leaves (Figures 3 & 4) plus the stem and oil seed types.

    • Crisphead or Iceberg: Large tightly wrapped heads of thick, crisp leaves. Popular in the US because it ships and stores well; ~80% of production occurs in California and Arizona and is then shipped throughout the US. Lowest nutritional value of all the lettuce types.
    • Cos or Romaine: Tall, upright heads with dark green leaves. Increasingly popular in the US.
    • Leafy or looseleaf: Open heads with loosely bunched leaves of a variety of shapes and colors.
    • Butterhead or bibb: Heads with a loose arrangement of leaves with sweet flavor and tender texture.
    • Batavian or French Crisp: Intermediate between the crisphead and leaf types.
    • Stem. The seed stalk rather than its leaves is eaten. Primarily used in China in stewed and creamed dishes.
    • Oilseed. Very minor type grown for the oil in its large seeds.
    Lettuce is amenable to classical and molecular genetic analyses. The generation time is usually three to five months depending on the genotype and environment, allowing multiple generations each year. Lettuce can be routinely transformed using Agrobacterium tumefaciens; transgenic seed can be generated within 3 to 5 months depending on the genotype (Michelmore et al., 1987). Agrobacterium-mediated transient assays and RNAi are routine (Wroblewski et al., 2005 & 2007). Extensive genetic and genomic tools including the transcriptome genome sequences are now available that are ready to be exploited for lettuce improvement (Matvienko et al., 2013).

    Multiple genetic maps have been generated using several intra-specific (Landry et al., 1987; Kesseli et al., 1994; Waycott et al., 1999; Hayashi et al., 2008) and inter-specific populations (Johnson et al., 2000; Jeuken et al., 2001; Syed et al., 2006; McHale et al., 2009) using a variety of molecular markers to provide increasingly dense maps as different technologies became available. Particular markers often only segregated in one or a few of these populations which hampered the transfer of genetic and phenotypic information among the different maps. A single integrated map of lettuce with 2,744 loci was therefore constructed that combined seven separate maps into nine chromosomal linkage groups (Truco et al., 2007). The majority of these maps rely on anonymous RFLP, RAPD, and AFLP markers.

    One of the populations used to produce the integrated map was a RIL (Recombinant Inbred Line) population resulting from an inter-specific cross between L. sativa cv. Salinas x L. serriola acc. US96UC23. This has emerged as a core reference mapping population and now comprises 356 F7:8 RILs. Sets of these RILs have been distributed to researchers worldwide for diverse studies. This population has also been genotyped for genes involved in disease resistance (McHale et al., 2009) and candidate genes for horticultural and domestication traits (Lavelle, 2009) as well as phenotyped for multiple traits (Argyris et al., 2005 & 2008; Zhang et al., 2007; Hartman et al., 2012). An ultra-high density, transcript-based genetic map has been generated from this reference mapping population; this consists of 12,842 unigenes mapped in 3,696 genetic bins distributed over nine chromosomal linkage groups (Truco et al., 2013). A large amount of genotypic and phenotypic information for this RIL population is available in the Compositae Genome Project database (http://compgenomics.ucdavis.edu).

    We collaborated with BGI, Shenzhen to sequence the lettuce genome (L. sativa cv. Salinas) with funding from an international consortium of ten breeding companies. The sequencing has been completed and the draft genome assembled into 15,471 scaffolds comprising 2.5 Gb of the 2.7 Gb genome with a contig N50 of 11.7 kb and a scaffold N50 of 461 kb. Of the scaffolds that contained multiple mapped unigenes (over 60% of the assembled genome), 95% are genetically consistent with our ultra-dense transcript-based map; most of the remaining mapped scaffolds analyzed were simple chimeras. We have placed these validated scaffolds into chromosomal linkage groups relative to numerous phenotypes including disease resistance genes. Additional scaffolds have been placed into the chromosomal linkage groups based on sequencing of the gene-space of the core mapping population. The genome has been annotated using the BGI and MAKER pipelines to provide ca. 45,000 gene models. These data are publicly available as of August 2012 (http://lgr.genomecenter.ucdavis.edu; http://www.ncbi.nlm.nih.gov/bioproject/173551).

    Lettuce is grown as extensive monocultures, often with several crops per year. Such intensive production makes the crop susceptible to major epidemics and lettuce suffers from several economically important pests and diseases ( http://michelmorelab.ucdavis.edu/index.php?link=disease) (Davis et al., 1997). These are currently controlled by a combination of genetic resistance, cultural practices, and chemical protection including the application of over 1.6 million pounds of insecticides and fungicides (USDA-NASS, 2007). When genetic sources of disease resistance are available, breeding is the cheapest, cleanest, safest, and most dependable method of crop protection available. Breeding efforts have consequently emphasized disease resistance and resistance to physiological disorders.

    Lettuce downy mildew (http://bremia.ucdavis.edu/), caused by Bremia lactucae, is the most important disease affecting lettuce worldwide. Several other diseases ( http://michelmorelab.ucdavis.edu/index.php?link=disease) are problematic in lettuce (Davis et al., 1997). These include bacterial corky root caused by Sphingomonas suberifaciens, and fungal diseases such as lettuce drop caused by Sclerotinia minor and S. sclerotiorum, lettuce anthracnose caused by Microdochium panattonianum, grey mold (Botrytis cinerea), and wilts caused by Fusarium oxysporum and Verticillium dahliae. There are also several viral diseases of varying importance such as lettuce mosaic, lettuce dieback, lettuce big vein, beet western yellows, and tomato bushy stunt. Other pathogens, such as powdery mildew (Erysiphe cichoracearum), bacterial spot (Xanthomonas campestris pv. vitians), lettuce infectious yellows, turnip mosaic virus, and tomato spotted wilt virus are present but currently rarely cause significant losses.

    Resistance is known for most but not all lettuce diseases. Over 52 phenotypically characterized resistance genes have been identified in lettuce (McHale et al., 2009; Truco & Michelmore, unpublished). Although major genes for downy mildew resistance (Dm genes) are highly effective and have been widely used, they have had limited lifespans because they have been rendered ineffective by changes in the pathogen (Ilott et al., 1987; Michelmore & Wong, 2008). The interaction between lettuce and Bremia lactucae, the causal agent of lettuce downy mildew, is one of the most extensively characterized gene-for-gene plant-pathogen relationships (Crute & Johnson, 1976; Farrara et al., 1987; Hulbert & Michelmore, 1985; Michelmore et al., 1984; Norwood & Crute, 1984; Norwood et al., 1983; Ilott et al., 1987 & 1989). At least 25 major Dm genes are now known that provide resistance against specific isolates of B. lactucae in a gene-for-gene manner (Farrara et al., 1987; Bonnier et al., 1994; Maisonneuve et al., 1994; Jeuken & Lindhout, 2002). The known Dm genes are located in five clusters in the genome (Hulbert & Michelmore, 1985; Farrara et al., 1987; Bonnier et al., 1994). The major cluster contains over nine genetically separable Dm specificities, as well as resistance to root aphid. Another large cluster contains several Dm genes, resistance to the root-infecting downy mildew Plasmopara lactucae-radicis, and the hypersensitive reaction to Turnip Mosaic Virus (Witsenboer et al., 1995).

    The Dm3 and Dm7 downy mildew resistance genes have been cloned through combinations of map-based cloning, candidate gene, RNAi, and mutant analysis approaches (Shen et al., 1998 & 2002; Christopoulou et al., unpublished). Both encode nucleotide-binding-site and leucine-rich-repeat (NBS-LRR) proteins, similar to genes cloned from other species for resistance to downy mildews and other pathogens (McHale et al., 2006). Dm3 is a member of the large RGC2 (Resistance Gene Candidate2) multigene family (Meyers et al., 1998a & b). The RGC2 cluster is not highly recombinagenic; it exhibits a recombination frequency 18 times lower than the genome-wide average (Chin et al., 2001). Numerous haplotypes and homologs at the RGC2 cluster of resistance genes have been identified. Fifty-one different haplotypes were identified in 74 accessions studied using molecular markers diagnostic of the RGC2 cluster (Sicard et al., 1999). The copy number of RGC2 paralogs at a locus varies from 12 to over 30 (Kuang et al., 2004). The large number of different haplotypes is consistent with there being a minimum of several hundred distinct Dm genes in Lactuca species and indicates that wild germplasm will be a rich source of new resistance genes that can be introgressed and pyramided using molecular markers.

    Supplemental information is available at: http://cgpdb.ucdavis.edu/supplemental_data/lmh_2008/ and http://michelmorelab.ucdavis.edu.
      Resources
      Images of Lactuca sativa
      
      Figure 1: Five lettuce types. Photo by Oswaldo Ochoa
      
      Figure 2: Field planting of different breeding lines. Photo by Oswaldo Ochoa
      
      Figure 3: Flowering plants and details of lettuce flowers. Photo by Oswaldo Ochoa
      
      Figure 4: Domestication traits in lettuce. Photo by Oswaldo Ochoa
      
      Figure 5: Lettuce Seeds. Photo by Alex Kozik.
      Publications


    Anonymous. 2011 http://usda.mannlib.cornell.edu/MannUsda/viewDocumentInfo.do?documentID=1576

    Argyris J, Truco MJ, Ochoa O, Knapp SJ, Still DW, Lenssen GM, Schut JW, Michelmore RW, Bradford KJ. (2005). Quantitative trait loci associated with seed and seedling traits in Lactuca. Theor. Appl. Genet. 111:1365-1376

    Argyris JM, Dahal P, Hayashi E, Still DW, Bradford KJ. (2008). Genetic variation for lettuce seed thermoinhibition is associated with temperature-sensitive expression of abscisic acid, gibberellins, and ethylene biosynthesis, metabolism, and response genes. Plant Physiol. 148:926-947

    Argyris J, Truco MJ, Ochoa O, McHale L, Dahal P, Van Deynze A, Michelmore RW, Bradford KJ. (2011). A gene encoding an abscisic acid biosynthetic enzyme (LsNCED4) collocates with the high temperature germination locus Htg6.1 in lettuce (Lactuca sp.). Theor. Appl. Genet. 122:95-108

    Beharav A., Lewinsohn D, Lebeda A, Nevo E. (2006). New wild Lactuca genetic resources with resistance against Bremia lactucae. Genet. Resour. Crop Evol. 53:467-474

    Bonnier FJM, Reinink K, Groenwald R. (1994). Genetic analysis of Lactuca accessions with new major gene resistance to lettuce downy mildew. Phytopathol. 84:462-468

    CGPDB. Compositae Genome Project database (2007) http://cgpdb.ucdavis.edu/

    Chin DB, Arroyo-Garcia R, Ochoa O, Kesseli RV, Lavelle DO, Michelmore RW. (2001). Recombination and spontaneous mutation at the major cluster of resistance genes in lettuce (Lactuca sativa). Genetics 157:831-849

    Crute IR. (1988). The impact of breeding on pest and disease control in lettuce. Aspects Appl. Biol. 17:305-312

    Crute IR. (1992). The role of resistance breeding in the integrated control of downy mildew (Bremia lactucae) in protected lettuce. Euphytica 63:95-102

    Crute IR, Johnson AG. (1976). The genetic relationship between races of Bremia lactucae and cultivars of Lactuca sativa. Ann. Appl. Biol. 83:125-137

    Davis RM, Subbarao KV, Raid RN, Kurtz EA. (1997). Compendium of lettuce diseases. APS Press, St. Paul, MN de Vries IM. (1997). Origin and domestication of Lactuca sativa L. Genet. Resources Crop Evol. 44:165-174

    Farrara B, Michelmore RW. (1987). Identification of new sources of resistance in Lactuca spp. HortScience 22:647-649

    Farrara B, Illott TW, Michelmore RW. (1987). Genetic analysis of factors for resistance to downy mildew (Bremia lactucae) in lettuce (Lactuca sativa). Plant Pathol. 36:499-514

    Feráková V. (1977). The genus Lactuca in Europe. Komenský University Press, Bratislava (Czechoslovakia) Hartman Y, Hooftman DA, Uwimana B, van de Wiel CCM, Smulders MJM et al. (2012). Genomic regions in crop–wild hybrids of lettuce are affected differently in different environments: implications for crop breeding. Evolutionary Applications 5:629-640

    Hayashi E, Aoyama N, Still DW. (2008). Quantitative trait loci associated with lettuce seed germination under different temperature and light environments. Genome 51: 928-947

    Hayes RJ, McHale LK, Vallad GE, Truco M-J, Michelmore RW, Klosterman SJ, Maruthachalam K, Krishna V, Subbarao KV. (2011). The inheritance of resistance to Verticillium wilt caused by race 1 isolates of Verticillium dahliae in the lettuce cultivar La Brillante. Theor. Appl. Genet. 123:509-517

    Hill W, Caballero A, Dempfle L. (1996). Prediction of response to selection within families. Genet. Sel. Evol. 28:379-383

    Hulbert SH, Michelmore RW. (1985). Linkage analysis of genes for resistance to downy mildew (Bremia lactucae) in lettuce (Lactuca sativa). Theor. Appl. Genet. 70:520-528

    Ilott TW, Durgan ME, Michelmore RW. (1987). Genetics of virulence in California populations of Bremia lactucae (Lettuce Downy Mildew). Phytopathol. 77:1381-1386

    Ilott TW, Hulbert SH, Michelmore RW. (1989). Genetic analysis of the gene-for-gene interaction between lettuce (Lactuca sativa) and Bremia lactucae. Phytopathol. 79:888-897

    Jeuken M, van Wijk R, Peleman J, Linhout P. (2001). An integrated interspecific AFLP map of lettuce (Lactuca) based on two L. sativa x L. saligna F2 populations. Theor. Appl. Genet. 103:638–647

    Jeuken MJ, 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. Theor. Appl. Genet. 105:384-391

    Johnson WC, Jackson LE, Ochoa O, van Wijk R, Peleman J, St. Clair DA, Michelmore RW. (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

    Kesseli RV, Ochoa O, Michelmore RW. (1991). Variation at RFLP loci in Lactuca spp. and the origin of cultivated lettuce (L. sativa). Genome 34: 430-436

    Kesseli R, Witsenboer H, Stanghellini M, Vandermark G, Michelmore R. (1993). Recessive resistance to Plasmopara lactucae radicis maps by bulked segregant analysis to a cluster of dominant disease resistance genes in lettuce. Molec. Plant-Microbe Interact. 6:722-728

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

    Koopman WJM, De Jong JH. (1996). A numerical analysis of karyotypes and DNA amounts in lettuce cultivars and species (Lactuca subsect. Lactuca, Compositae. Acta Bot. Neerl. 45:211-222

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

    K?ístková E, Doležalová I, Lebeda A, Vinter V, Novotná A. (2008). Description of morphological characters of lettuce (Lactuca sativa L.) genetic resources. Hort. Sci. (Prague) 35:113–129

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

    Kuang H, Ochoa OE, Nevo E, Michelmore RW. (2006). The disease resistance gene Dm3 is infrequent in natural populations of Lactuca serriola due to deletions and frequent gene conversions. Plant J. 47:38-48

    Kuang H, Caldwell K, Meyers BC, Michelmore RW. (2008). Frequent sequence exchanges between homologs of RPP8 in Arabidopsis are not necessarily associated with genomic proximity. Plant J. 54:69-80

    Landry BS, Kesseli RV, Farrara B, Michelmore RW. (1987). A genetic map of lettuce (Lactuca sativa L.) with restriction fragment length polymorphism, isozyme, disease resistance and morphological markers. Genetics 116:331-337

    Lavelle DO. (2009). Genetics of candidate genes for developmental and domestication-related traits in lettuce. Ph.D. dissertation in Genetics, U. C. Davis Lebeda A, Zinkernagel V. (2003). Characterization of new highly virulent German isolates of Bremia lactucae and efficiency of resistance in wild Lactuca ssp. germplasm. J. Phytopathol. 151:274-282

    Lindqvist K. (1960). Inheritance studies in lettuce. Hereditas 46:387–470

    Maisonneuve B, Bellec Y, Anderson P, Michelmore RW. (1994). Rapid mapping of two genes for resistance to downy mildew from Lactuca serriola to existing clusters of resistance genes. Theor. Appl. Genet. 89:96-104

    Matvienko M, Kozik A, Froenicke L, Lavelle D, Martineau B, Perroud B, Michelmore R. (2013). Consequences of normalizing transcriptomic and genomic libraries of plant genomes using a duplex-specific nuclease and tetramethylammonium chloride. PLoS One. 8:e55913

    McHale L, Tan XP, Koehl P, Michelmore RW. (2006). Plant NBS-LRR proteins: adaptable guards. Genome Biol. 7:212

    McHale LK, Truco MJ, Kozik A, Wroblewski T, Ochoa OE, Lahre KA, Knapp SJ, Michelmore RW. (2009). The genomic architecture of disease resistance in lettuce. Theor. Appl. Genet. 118:565-580

    Meyers BC, Chin DB, Shen KA, Sivaramakrishnan S, Lavelle DO, Zhang Z, Michelmore RW. (1998a). The major resistance gene cluster in lettuce is highly duplicated and spans several megabases. Plant Cell 10:1817-1832

    Meyers BC, Shen KA, Rohani P, Gaut BS, Michelmore RW. (1998b). Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection. Plant Cell 10:1833-1846

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    Michelmore RW. (1994). Lettuce breeding. California Iceberg Lettuce Research Program Report pp. 34 – 44

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

    Michelmore RW. (2003). The impact zone: genomics and breeding for durable disease resistance. Curr. Opin. Plant Biol. 6:397-404

    Michelmore R, Kozik A, Truco MJ, Matviencho M, Ochoa O, van Damme M, Lavelle D, Lin H, Pande B, McHale L, et al. (2003). ESTs and candidate gene approaches in the Compositae Genome Project. In: van Hintum TJL, Lebeda A, Pink D, Schut JW, editors. Proceedings of the EUCARPIA Meeting on Leafy Vegetables.. 2003 March 19–21; Noordwijkerhout, The Netherlands. Wageningen (The Netherlands): Centre for Genetic Resources. pp. 131–136

    Michelmore RW, Christopoulou M, Caldwell K. (2013). Impacts of resistance gene genetics, function, and evolution on a durable future. Ann. Rev. Phytopathol., in press.

    Michelmore RW, Wong J. (2008). Classical and molecular genetics of Bremia lactucae, cause of lettuce downy mildew. Eur. J. Plant Pathol. 122:19-30

    Michelmore RW, Norwood JM, Ingram DS, Crute IR, Nicholson P. (1984). The inheritance of virulence in Bremia lactucae to match resistance factor III, factor 4, factor 5, factor 6, factor Viii, factor IX, factor 10 and factor 11 in lettuce (Lactuca sativa). Plant Pathol. 33:301-315

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    Michelmore RW, Meyers BC. (1998). Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 8:1113-1130

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

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    Moreno-Vazquez S, Ochoa O, Faber N, Chao S, Jacobs JME, Maisonneuve B, Kesseli R, Michelmore RW. (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

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    Norwood JM, Michelmore RW, Crute IR, Ingram DS. (1983).The inheritance of specific virulence in Bremia lactucae (downy mildew) to match resistance factors 1, 2, 4, 6 and 11 in Lactuca sativa (lettuce). Plant Pathol. 32:177-186

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    Shen KA, Meyers BC, Islam-Faridi MN, Chin DB, Stelly DM, Michelmore RW. (1998). Resistance gene candidates identified using PCR with degenerate primers map to resistance genes clusters in lettuce. Molec. Plant-Microbe Interact. 11:815-823

    Shen KA, Chin DB, Arroyo-Garcia R, Ochoa OE, Lavelle DO, Wroblewski T, Meyers, BC, Michelmore RW. (2002). Dm3 is one member of a large constitutively expressed family of nucleotide binding site-leucine-rich repeat encoding genes. Mol. Plant-Microbe Interact. 15:251-61

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

    Syed NH, Sorensen AP, Antonise R, van de Wiel C, van der Linden CG et al. (2006). A detailed linkage map of lettuce based on SSAP, AFLP and NBS markers. Theor. Appl. Genet. 112:517-527

    Truco MJ, Antonise R, Lavelle D, Ochoa O, Kozik A, Witsenboer H, Fort SB, Jeuken MJW, Kesseli RV, Lindhout P, et al. (2007). A high-density, integrated genetic linkage map of lettuce (Lactuca spp.). Theor. Appl. Genet. 115:735-746

    Truco, MJ, Ashrafi, H, Kozik A, van Leeuwen H, Bowers J, Reyes Chin Wo S, Stoffel K, Xu H, Hill T, van Deynze A, Michelmore RW. (2013). An ultra high-density, transcript-based, genetic map of lettuce. G3: Genes, Genomes, Genetics, 112.004929v3. doi: 10.1534/g3.112.004929.

    USDA-NASS. (2007). Agricultural Chemical Usage: 2006 Vegetables Summary. http://usda.mannlib.cornell.edu/usda/current/AgriChemUsVeg/AgriChemUsVeg-07-25-2007_revision.pdf.

    Waycott W, Fort SB, Ryder EJ, Michelmore RW. (1999). Mapping morphological genes relative to molecular markers in lettuce (Lactuca sativa L.). Heredity 82:245–251

    Witsenboer H, Kesseli RV, Fortin M, Stanghellini M, Michelmore RW. (1995). Sources and genetic structure of a cluster of genes for resistance to three pathogens in lettuce. Theor. Appl. Genet. 91:178-188

    Wroblewski T, Tomczak A, Michelmore RW. (2005). Optimization of Agrobacterium-mediated transient assays of gene expression in lettuce, tomato and Arabidopsis. Plant Biotechnol. J. 3:259-273

    Wroblewski T., Piskurewicz U, Tomczak A, Ochoa O, Michelmore RW. (2007). Multiple resistance specificities are lost due to silencing homologs of the RGC2 NBS-LRR-encoding gene family in lettuce. Plant J. 51:803-818

    Wroblewski T, Caldwell KS, Piskurewicz U, Cavanaugh KA, Xu H, Kozik A, Ochoa O, McHale LK, Lahre K, Jelenska J, Castillo JA, Blumenthal D, Cinatzer BA, Greenberg JT, Michelmore RW. (2009). Comparative large-scale analysis of interactions between several crop species and the effector repertoires from multiple pathovars of Pseudomonas and Ralstonia. Plant Phys. 150:1733-1749

    Zhang FZ, Wagstaff C, Rae AM, Kaur A, Keevil WC, Rothwell SD, Clarkson GJJ, Michelmore RW, Truco MJ, Dixon MS, 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
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