A Solanum lycopersicum × Solanum pimpinellifolium Linkage Map of Tomato Displaying Genomic Locations of R-Genes, RGAs, and Candidate Resistance/Defense-Response ESTs

We have identified an accession (LA2093) within the tomato wild species Solanum pimpinellifolium with many desirable characteristics, including biotic and abiotic stress tolerance and good fruit quality. To utilize the full genetic potential of LA2093 in tomato breeding, we have developed a linkage map based on an F2 population of a cross between LA2093 and a tomato breeding line, using 115 RFLP, 94 EST, and 41 RGA markers. The map spanned 1002.4 cM of the 12 tomato chromosomes with an average marker distance of 4.0 cM. The length of the map and linear order of the markers were in good agreement with the published maps of tomato. The ESTs were chosen based on their sequence similarities with known resistance or defense-response genes, signal-transduction factors, transcriptional regulators, and genes encoding pathogenesis-related proteins. Locations of several ESTs and RGAs coincided with locations of several known tomato resistance genes and quantitative resistance loci (QRLs), suggesting that candidate-gene approach may be effective in identifying and mapping new R genes. This map will be useful for marker-assisted exploitation of desirable traits in LA2093 and other S. pimpinellifolium accessions, and possibly for utilization of genetic variation within S. lycopersicum.

[1]  S. Tanksley,et al.  Use of isogenic lines and simultaneous probing to identify DNA markers tightly linked to the tm-2a gene in tomato. , 1988, Genetics.

[2]  M. Foolad Genetic analysis of salt tolerance during vegetative growth in tomato, Lycopersicon esculentum Mill. , 1996 .

[3]  S. Tanksley,et al.  Molecular mapping of the py-1 gene for resistance to corky root rot (Pyrenochaeta lycopersici) in tomato , 1998, Theoretical and Applied Genetics.

[4]  M. Foolad Recent Advances in Genetics of Salt Tolerance in Tomato , 2004, Plant Cell, Tissue and Organ Culture.

[5]  R. Mago,et al.  Resistance gene analogues from rice: cloning, sequencing and mapping , 1999, Theoretical and Applied Genetics.

[6]  S. Tanksley,et al.  Seed banks and molecular maps: unlocking genetic potential from the wild. , 1997, Science.

[7]  M. Foolad,et al.  A genetic map of Prunus based on an interspecific cross between peach and almond , 1995, Theoretical and Applied Genetics.

[8]  M. Foolad,et al.  Mapping salt-tolerance genes in tomato (Lycopersicon esculentum) using trait-based marker analysis , 1993, Theoretical and Applied Genetics.

[9]  G. Bonnema,et al.  The Cf-ECP2 gene is linked to, but not part of, the Cf-4/Cf-9 cluster on the short arm of chromosome 1 in tomato , 1999, Molecular and General Genetics MGG.

[10]  S. Tanksley,et al.  An interspecific backcross of Lycopersicon esculentum x L. hirsutum: linkage analysis and a QTL study of sexual compatibility factors and floral traits. , 1997, Genetics.

[11]  D. Zamir,et al.  Mapping and introgression of a tomato yellow leaf curl virus tolerance gene, TY-1 , 1994, Theoretical and Applied Genetics.

[12]  C. Vallejos,et al.  An isozyme marker for resistance to race 3 of Fusarium oxysporum f. sp. lycopersici in tomato , 1989, Theoretical and Applied Genetics.

[13]  S. Tanksley,et al.  Mapping of Ve in tomato: a gene conferring resistance to the broad-spectrum pathogen, Verticillium dahliae race 1 , 1999, Theoretical and Applied Genetics.

[14]  J. D. Jones,et al.  RFLP linkage analysis of the Cf-4 and Cf-9 genes for resistance toCladosporium fulvum in tomato , 1994, Theoretical and Applied Genetics.

[15]  M. Koornneef,et al.  RFLP markers linked to the root knot nematode resistance gene Mi in tomato , 1991, Theoretical and Applied Genetics.

[16]  D. Rhoads,et al.  Mapping the Sw-5 locus for tomato spotted wilt virus resistance in tomatoes using RAPD and RFLP analyses , 1995, Theoretical and Applied Genetics.

[17]  S. Tanksley,et al.  RFLP analysis of phylogenetic relationships and genetic variation in the genus Lycopersicon , 1990, Theoretical and Applied Genetics.

[18]  S. Tanksley,et al.  Map-based cloning of the tomato genomic region that spans the Sw-5 tospovirus resistance gene in tomato , 1997, Molecular and General Genetics MGG.

[19]  J. Palmer,et al.  Chloroplast DNA evolution and phylogenetic relationships in Lycopersicon. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[20]  R. Verkerk,et al.  Acid phosphatase-11, a tightly linked molecular marker for root-knot nematode resistance in tomato: from protein to gene, using PCR and degenerate primers containing deoxyinosine , 1991, Plant Molecular Biology.

[21]  A. W. van Heusden,et al.  Three QTLs from Lycopersicon peruvianum confer a high level of resistance to Clavibactermichiganensis ssp. michiganensis , 1999, Theoretical and Applied Genetics.

[22]  C. Vallejos,et al.  Genomic localization of tomato genes that control a hypersensitive reaction to Xanthomonas campestris pv. vesicatoria (Doidge) dye. , 1995, Genetics.

[23]  D. Zamir,et al.  RFLP mapping of I1, a new locus in tomato conferring resistance against Fusarium oxysporum f. sp. lycopersici race 1 , 1991, Theoretical and Applied Genetics.

[24]  N. Young,et al.  Genetic dissection of oligogenic resistance to bacterial wilt in tomato. , 1994, Molecular plant-microbe interactions : MPMI.

[25]  Daniel T. Lavelle,et al.  Tomato Prf Is a Member of the Leucine-Rich Repeat Class of Plant Disease Resistance Genes and Lies Embedded within the Pto Kinase Gene Cluster , 1996, Cell.

[26]  M. Joosten,et al.  Additional Resistance Gene(s) Against Cladosporium fulvum Present on the Cf-9 Introgression Segment Are Associated with Strong PR Protein Accumulation , 1998 .

[27]  D. D. Kosambi The estimation of map distances from recombination values. , 1943 .

[28]  B. Mangin,et al.  Polygenic resistance of tomato plants to bacterial wilt in the French West Indies , 1996 .

[29]  C. Mathieu,et al.  Identification of a short rDNA spacer sequence highly specific of a tomato line containing Tm-1 gene introgressed from Lycopersicon hirsutum , 1990, Theoretical and Applied Genetics.

[30]  S. Tanksley,et al.  Genetic analysis of RFLPs, GATA microsatellites and RAPDs in a cross between L. esculentum and L. pimpinellifolium , 1996, Theoretical and Applied Genetics.

[31]  H. Laterrot,et al.  Linkage between Frl (Fusarium oxysporum f.sp. radicis‐lycopersici resistance) and Tm‐2 (tobacco mosaic virus resistance‐2) loci in tomato (Lycopersicon esculentum) , 1997 .

[32]  M. Daly,et al.  MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. , 1987, Genomics.

[33]  G. Martin,et al.  Deductions about the Number, Organization, and Evolution of Genes in the Tomato Genome Based on Analysis of a Large Expressed Sequence Tag Collection and Selective Genomic Sequencing Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010478. , 2002, The Plant Cell Online.

[34]  B. Stamova,et al.  Inheritance and genetic mapping of cucumber mosaic virus resistance introgressed from Lycopersicon chilense into tomato , 2000, Theoretical and Applied Genetics.

[35]  J. D. Jones,et al.  Genetic and molecular analysis of tomato Cf genes for resistance to Cladosporium fulvum. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[36]  R. Verkerk,et al.  Localization of genes for bacterial canker resistance in Lycopersicon peruvianum using RFLPs , 1995, Theoretical and Applied Genetics.

[37]  I. Kaloshian,et al.  Mapping a new nematode resistance locus in Lycopersicon peruvianum , 1995, Theoretical and Applied Genetics.

[38]  B. Trognitz,et al.  A new look at incompatibility relationships in higher plants , 1993, Sexual Plant Reproduction.

[39]  I. Kaloshian,et al.  A PCR-based marker tightly linked to the nematode resistance gene, Mi, in tomato , 1994, Theoretical and Applied Genetics.

[40]  S. Tanksley,et al.  Toward a saturated linkage map in tomato based on isozymes and random cDNA sequences. , 1986, Genetics.

[41]  S. Tanksley,et al.  Genetic mapping of a wide spectrum nematode resistance gene (Hero) against Globodera rostochiensis in tomato. , 1995, Molecular plant-microbe interactions : MPMI.

[42]  S. Tanksley,et al.  Yield and quality evaluations on a pair of processing tomato lines nearly isogenic for the Tm2a gene for resistance to the tobacco mosaic virus , 2004, Euphytica.

[43]  B. Mangin,et al.  Temporal and multiple quantitative trait loci analyses of resistance to bacterial wilt in tomato permit the resolution of linked loci. , 1999, Genetics.

[44]  S. Tanksley,et al.  The I2C family from the wilt disease resistance locus I2 belongs to the nucleotide binding, leucine-rich repeat superfamily of plant resistance genes. , 1997, The Plant cell.

[45]  R. Shoemaker,et al.  Resistance gene analogs are conserved and clustered in soybean. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[46]  A. Bent,et al.  Plant Disease Resistance Genes: Function Meets Structure. , 1996, The Plant cell.

[47]  P. Thoquet,et al.  Genetic mapping of Ph-2, a single locus controlling partial resistance to Phytophthora infestans in tomato , 1998 .

[48]  D. Leister,et al.  A PCR–based approach for isolating pathogen resistance genes from potato with potential for wide application in plants , 1996, Nature Genetics.

[49]  F. Vedel,et al.  Identification of RAPD markers linked to a locus involved in quantitative resistance to TYLCV in tomato by bulked segregant analysis , 1997, Theoretical and Applied Genetics.

[50]  G. Martin,et al.  Map-based cloning of a protein kinase gene conferring disease resistance in tomato. , 1993, Science.

[51]  J. G. Beek,et al.  Resistance to powdery mildew (Oidium lycopersicum) in Lycopersicon hirsutum is controlled by an incompletely-dominant gene Ol-1 on chromosome 6 , 1994, Theoretical and Applied Genetics.

[52]  I. Kaloshian,et al.  The nematode resistance gene Mi of tomato confers resistance against the potato aphid. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[53]  J. Beynon,et al.  Identification of R-gene homologous DNA fragments genetically linked to disease resistance loci in Arabidopsis thaliana. , 1998, Molecular plant-microbe interactions : MPMI.

[54]  J. Deverna,et al.  Expression of unilateral incompatibility in pollen of Lycopersicon pennellii is determined by major loci on chromosomes 1, 6 and 10 , 1991, Theoretical and Applied Genetics.

[55]  M. Foolad,et al.  A molecular linkage map of tomato based on a cross between Lycopersicon esculentum andL. pimpinellifolium and its comparison with other molecular maps of tomato , 1999 .

[56]  D. S. St. Clair,et al.  Mapping of QTLs for lycopene and other fruit traits in a Lycopersicon esculentum × L. pimpinellifolium cross and comparison of QTLs across tomato species , 1999, Molecular Breeding.

[57]  S. Tanksley,et al.  Methods for detection of single or low copy sequences in tomato on southern blots , 1986, Plant Molecular Biology Reporter.

[58]  M. Foolad,et al.  A molecular linkage map of tomato displaying chromosomal locations of resistance gene analogs based on a Lycopersicon esculentum x Lycopersicon hirsutum cross. , 2002, Genome.

[59]  C. Rick Controlled Introgression of Chromosomes of SOLANUM PENNELLII into LYCOPERSICON ESCULENTUM: Segregation and Recombination. , 1969, Genetics.

[60]  H. Agrama,et al.  RFLP-based Analysis of Recombination among Resistance Genes to Fusarium Wilt Races 1, 2, and 3 in Tomato , 2004 .

[61]  D. Bouchez,et al.  Disease resistance gene homologs correlate with disease resistance loci of Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[62]  B. Keller,et al.  Molecular cloning of a new receptor-like kinase gene encoded at the Lr10 disease resistance locus of wheat. , 1997, The Plant journal : for cell and molecular biology.

[63]  D. Baulcombe,et al.  A potato hypersensitive resistance gene against potato virus X maps to a resistance gene cluster on chromosome 5 , 1997, Theoretical and Applied Genetics.

[64]  Yuling Bai,et al.  QTLs for tomato powdery mildew resistance (Oidium lycopersici) in Lycopersicon parviflorum G1.1601 co-localize with two qualitative powdery mildew resistance genes. , 2003, Molecular plant-microbe interactions : MPMI.

[65]  A. Feinberg,et al.  A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. , 1983, Analytical biochemistry.

[66]  Eric S. Lander,et al.  Resolution of quantitative traits into Mendelian factors by using a complete linkage map of restriction fragment length polymorphisms , 1988, Nature.

[67]  A. Palloix,et al.  Recessive resistance genes against potyviruses are localized in colinear genomic regions of the tomato (Lycopersicon spp.) and pepper (Capsicum spp.) genomes , 2002, Theoretical and Applied Genetics.

[68]  I. Kaloshian,et al.  The heat-stable root-knot nematode resistance gene Mi-9 from Lycopersicon peruvianum is localized on the short arm of chromosome 6 , 2003, Theoretical and Applied Genetics.

[69]  H. Ashrafi,et al.  GENETICS OF EARLY BLIGHT RESISTANCE IN TOMATO , 2005 .

[70]  S. Tanksley,et al.  Production of interspecific F1 hybrids, BC1, BC2 and BC3 populations between Lycopersicon esculentum and two accessions of Lycopersicon peruvianum carrying new root-knot nematode resistance genes , 1997, Euphytica.

[71]  M. Foolad Genetic Analysis of Salt Tolerance during Vegetative Growth in Tomato , 1996 .

[72]  M. Foolad Unilateral incompatibility as a major cause of skewed segregation in the cross between Lycopersicon esculentum and L. pennellii , 1996, Plant Cell Reports.

[73]  Paxton Payton,et al.  Use of genomics tools to isolate key ripening genes and analyse fruit maturation in tomato. , 2002, Journal of experimental botany.

[74]  C. Vallejos,et al.  Xv4-vrxv4: a new gene-for-gene interaction identified between Xanthomonas campestris pv. vesicatoria race T3 and wild tomato relative Lycopersicon pennellii. , 2000, Molecular plant-microbe interactions : MPMI.

[75]  C. Vallejos,et al.  Genetic analysis of resistances to races 1 and 2 of Fusarium oxysporum f. sp. lycopersici from the wild tomato Lycopersicon pennellii , 1990, Theoretical and Applied Genetics.

[76]  H. Leung,et al.  Genome scanning for resistance-gene analogs in rice, barley, and wheat by high-resolution electrophoresis , 1998, Theoretical and Applied Genetics.

[77]  E. Lander,et al.  Mendelian factors underlying quantitative traits in tomato: comparison across species, generations, and environments. , 1991, Genetics.

[78]  M. Foolad,et al.  Identification of QTLs for early blight (Alternaria solani) resistance in tomato using backcross populations of a Lycopersicon esculentum × L. hirsutum cross , 2002, Theoretical and Applied Genetics.

[79]  R. Verkerk,et al.  Mapping strategy for resistance genes in tomato based on RFLPs between cultivars: Cf9 (resistance to Cladosporium fulvum) on chromosome 1 , 1992, Theoretical and Applied Genetics.

[80]  B. Overduin,et al.  Inheritance and genetic mapping of resistance to Alternaria alternata f. sp. lycopersici in Lycopersicon pennellii , 1995, Molecular and General Genetics MGG.

[81]  G. Kuo,et al.  Mapping a wild tomato introgression associated with tomato yellow leaf curl virus resistance in a cultivated tomato line. , 2000 .

[82]  J. Nelson QGENE: software for marker-based genomic analysis and breeding , 1997, Molecular Breeding.

[83]  I. K. Vasil,et al.  Plant improvement and somatic cell genetics. , 1982 .

[84]  F. Takken,et al.  Genetic and physical analysis of a YAC contig spanning the fungal disease resistance locus Asc of tomato (Lycopersicon esculentum) , 1999, Molecular and General Genetics MGG.

[85]  A. W. van Heusden,et al.  Mapping a novel heat-stable resistance to Meloidogyne in Lycopersicon peruvianum , 1999, Theoretical and Applied Genetics.

[86]  M. Foolad,et al.  Genome Mapping and Molecular Breeding of Tomato , 2007, International journal of plant genomics.

[87]  Jonathan D. G. Jones,et al.  Two complex resistance loci revealed in tomato by classical and RFLP mapping of the Cf-2, Cf-4, Cf-5, and Cf-9 genes for resistance to Cladosporium fulvum , 1993 .

[88]  J. Mes,et al.  Dissection of the Fusarium I2 Gene Cluster in Tomato Reveals Six Homologs and One Active Gene Copy , 1998, Plant Cell.

[89]  M. Murata,et al.  Molecular characterization of RAPD and SCAR markers linked to the Tm-1 locus in tomato , 1996, Theoretical and Applied Genetics.

[90]  S. Warnock A Review of Taxonomy and Phylogeny of the Genus Lycopersicon , 1988, HortScience.

[91]  P. Keim,et al.  Rpg1, a soybean gene effective against races of bacterial blight, maps to a cluster of previously identified disease resistance genes , 1998, Theoretical and Applied Genetics.

[92]  M. Ganal,et al.  The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. , 1998, Development.

[93]  D. Zamir,et al.  An RFLP marker in tomato linked to the Fusarium oxysporum resistance gene I2 , 1989, Theoretical and Applied Genetics.

[94]  C. Rick,et al.  Position of the Stigma in Relation to Fruit Setting of the Tomato , 1969, Botanical Gazette.

[95]  M. Ganal,et al.  Genetic mapping and functional analysis of the tomato Bs4 locus governing recognition of the Xanthomonas campestris pv. vesicatoria AvrBs4 protein. , 2001, Molecular plant-microbe interactions : MPMI.

[96]  G. Martin,et al.  High density molecular linkage maps of the tomato and potato genomes. , 1992, Genetics.

[97]  G. Martin,et al.  A member of the tomato Pto gene family confers sensitivity to fenthion resulting in rapid cell death. , 1994, The Plant cell.

[98]  I. Kaloshian,et al.  Genetic and physical localization of the root-knot nematode resistance locus Mi in tomato , 1998, Molecular and General Genetics MGG.

[99]  S. Tanksley,et al.  QTL analysis of transgressive segregation in an interspecific tomato cross. , 1993, Genetics.

[100]  S. Tanksley,et al.  Evolution of mating systems inLycopersicon hirsutum as deduced from genetic variation in electrophoretic and morphological characters , 1979, Plant Systematics and Evolution.

[101]  I. Kaloshian,et al.  An aphid-resistance locus is tightly linked to the nematode-resistance gene, Mi, in tomato. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[102]  S. Tanksley,et al.  Chromosomal localization and molecular-marker tagging of the powdery mildew resistance gene (Lv) in tomato , 1994, Theoretical and Applied Genetics.

[103]  D. Zamir,et al.  Restriction fragment length polymorphism mapping of the Stemphylium resistance gen in tomato , 1991 .

[104]  R. Bernatzky Genetic mapping and protein product diversity of the self-incompatibility locus in wild tomato (Lycopersicon peruvianum) , 1993, Biochemical Genetics.

[105]  P. Thoquet,et al.  Quantitative trait loci determining resistance to bacterial wilt in tomato cultivar Hawaii7996 , 1996 .

[106]  J. Hachey,et al.  Development of sequence characterized DNA markers linked to a dominant verticillium wilt resistance gene in tomato. , 1998, Genome.

[107]  M. Yano,et al.  An informative linkage map of soybean reveals QTLs for flowering time, leaflet morphology and regions of segregation distortion. , 2001, DNA research : an international journal for rapid publication of reports on genes and genomes.

[108]  D. Zamir,et al.  Correlation of genetic and physical structure in the region surrounding the I2Fusarium oxysporum resistance locus in tomato , 2004, Molecular and General Genetics MGG.

[109]  Y. G. Yu,et al.  Isolation of a superfamily of candidate disease-resistance genes in soybean based on a conserved nucleotide-binding site. , 1996, Proceedings of the National Academy of Sciences of the United States of America.