Advertisement

Theoretical and Applied Genetics

, Volume 118, Issue 1, pp 57–75 | Cite as

High resolution genetic and physical mapping of the I-3 region of tomato chromosome 7 reveals almost continuous microsynteny with grape chromosome 12 but interspersed microsynteny with duplications on Arabidopsis chromosomes 1, 2 and 3

  • G. T. T. Lim
  • G.-P. Wang
  • M. N. Hemming
  • D. J. McGrath
  • D. A. JonesEmail author
Original Paper

Abstract

The tomato I-3 gene introgressed from the Lycopersicon pennellii accession LA716 confers resistance to race 3 of the fusarium wilt pathogen Fusarium oxysporum f. sp. lycopersici. We have improved the high-resolution map of the I-3 region of tomato chromosome 7 with the development and mapping of 31 new PCR-based markers. Recombinants recovered from L. esculentum cv. M82 × IL7-2 F2 and (IL7-2 × IL7-4) × M82 TC1F2 mapping populations, together with recombinants recovered from a previous M82 × IL7-3 F2 mapping population, were used to position these markers. A significantly higher recombination frequency was observed in the (IL7-2 × IL7-4) × M82 TC1F2 mapping population based on a reconstituted L. pennellii chromosome 7 compared to the other two mapping populations based on smaller segments of L. pennellii chromosome 7. A BAC contig consisting of L. esculentum cv. Heinz 1706 BACs covering the I-3 region has also been established. The new high-resolution map places the I-3 gene within a 0.38 cM interval between the molecular markers RGA332 and bP23/gPT with an estimated physical size of 50–60 kb. The I-3 region was found to display almost continuous microsynteny with grape chromosome 12 but interspersed microsynteny with Arabidopsis thaliana chromosomes 1, 2 and 3. An S-receptor-like kinase gene family present in the I-3 region of tomato chromosome 7 was found to be present in the microsyntenous region of grape chromosome 12 but was absent altogether from the A. thaliana genome.

Keywords

Mapping Population Arabidopsis Chromosome Grape Genome Tomato Chromosome Fusarium Wilt Resistance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank Mondher Bouzayen, for provision of tomato chromosome 7 BAC sequences prior to their publication on the SGN and Genbank databases; Steve Dempsey, Research School of Biological Sciences, The Australian National University, Canberra, Australia for plant care; Theresa Fulton, Cornell University, Ithaca, New York, USA for provision of the TM18 and TM23 marker sequences prior to publication on the SGN website; Heidi Martin, Queensland Department of Primary Industries and Fisheries, Indooroopilly, Queensland, Australia for the provision of cultures of Fusarium oxysporum f. sp. lycopersici race 3 for pathogen screening; Steve Tanksley, Cornell University, Ithaca, New York, USA for provision of the TG572 sequence prior to submission to Genbank and correction on the SGN database; and Ian Walker, Queensland Department of Primary Industries and Fisheries, Bowen, Queensland, Australia for assistance with pathogen screening. Guo-Ping Wang was funded by the Biotechnology Research Centre, Research School of Biological Sciences, The Australian National University, Canberra, Australia and the Cooperative Research Centre for Tropical Plant Protection, Brisbane Queensland, Australia. This work was funded in large part by the Cooperative Research Centre for Tropical Plant Protection, in which The Australian National University, The University of Queensland and the Queensland Department of Primary Industries and Fisheries were participants.

Supplementary material

122_2008_876_MOESM1_ESM.doc (32 kb)
Summary of the contents of the tables (DOC 32 kb)
122_2008_876_MOESM2_ESM.doc (78 kb)
List of genomic sequences, predicted coding sequences and predicted protein sequences (DOC 77 kb)
122_2008_876_MOESM3_ESM.xls (86 kb)
Results of BlastP searches of the Arabidopsis and grape protein databases and TblastN searches of the tomato unigene database (XLS 86 kb)
122_2008_876_MOESM4_ESM.xls (92 kb)
Results of BlastX searches of the Arabidopsis, grape and poplar protein databases (XLS 92 kb)
122_2008_876_MOESM5_ESM.xls (22 kb)
Results of BlastP searches of the Arabidopsis, grape and poplar protein databases and TblastN searches of the tomato unigene database (XLS 21 kb)

References

  1. Alexander LJ, Tucker CM (1945) Physiologic specialization in the tomato wilt fungus Fusarium oxysporum f. sp. lycopersici. J Agric Res 70:303–313Google Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  3. Bohn GW, Tucker CM (1939) Immunity to Fusarium wilt in the tomato. Science 89:603–604PubMedCrossRefGoogle Scholar
  4. Bonnema G, Schipper D, van Heusden S, Zabel P, Lindhout P (1997) Tomato chromosome 1: high resolution genetic and physical mapping of the short arm in an interspecific Lycopersicon esculentum × L. peruvianum cross. Mol Gen Genet 253:455–462PubMedCrossRefGoogle Scholar
  5. Bournival BL, Scott JW, Vallejos CE (1989) An isozyme marker for resistance to race 3 of Fusarium oxysporum f. sp. lycopersici in tomato. Theor Appl Genet 78:489–494CrossRefGoogle Scholar
  6. Burbidge A, Grieve TM, Jackson A, Thompson A, McCarty DR, Taylor IB (1999) Characterization of the ABA-deficient tomato mutant notabilis and its relationship with maize Vp14. Plant J 17:427–431PubMedCrossRefGoogle Scholar
  7. Burge C, Karlin S (1997) Prediction of complete gene structures in human genomic DNA. J Mol Biol 268:78–94PubMedCrossRefGoogle Scholar
  8. Canady MA, Ji Y, Chetelat RT (2006) Homeologous recombination in Solanum lycopersicoides introgression lines of cultivated tomato. Genetics 174:1775–1788PubMedCrossRefGoogle Scholar
  9. Chellemi DO, Dankers HA (1992) First report of Fusarium oxysporum f. sp. lycopersici race 3 on tomato in northwest Florida and Georgia. Plant Dis 76:861Google Scholar
  10. Chen X, Shang J, Chen D, Lei C, Zou Y, Zhai W, Liu G, Xu J, Ling Z, Cao G, Ma B, Wang Y, Zhao X, Li S, Zhu L (2006) A B-lectin receptor kinase gene conferring rice blast resistance. Plant J 46:794–804PubMedCrossRefGoogle Scholar
  11. Cirulli M, Alexander LJ (1966) A comparison of pathogenic isolates of Fusarium oxysporum f. sp. lycopersici and different sources of resistance in tomato. Phytopathology 56:1301–1304Google Scholar
  12. Davis RM, Kimble KA, Farrar JJ (1988) A third race of Fusarium oxysporum f. sp. lycopersici identified in California. Plant Dis 72:453CrossRefGoogle Scholar
  13. van Bentem S, Vossen JH, Vermeer JEM, de Vroomen MJ, Gadella TWJ Jr, Haring MA, Cornelissen BJC (2003) The subcellular localization of plant protein phosphatase 5 isoforms is determined by alternative splicing. Plant Physiol 133:702–712CrossRefGoogle Scholar
  14. Edwards K, Johnstone C, Thompson C (1991) A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res 19:1349PubMedCrossRefGoogle Scholar
  15. Fulton TM, Van der Hoeven R, Eannetta NT, Tanksley SD (2002) Identification, analysis and utilization of Conserved Ortholog Set markers for comparative genomics in higher plants. Plant Cell 14:1457–1467PubMedCrossRefGoogle Scholar
  16. Giraudat J, Beaudoin N, Serizet C (2003) Mapping mutations using molecular markers. EMBO Course—practical course on genetic and molecular analysis of Arabidopsis http://www.isv.cnrs-gif.fr/embo99/manuals/pdf/ch2.pdf
  17. Grant MR, McDowell JM, Sharpe AG, de Torres Zabala M, Lydiate DJ, Dangl JL (1998) Independent deletions of a pathogen-resistance gene in Brassica and Arabidopsis. Proc Natl Acad Sci USA 95:15843–15848PubMedCrossRefGoogle Scholar
  18. Grattidge R, O’Brien RG (1982) Occurrence of a third race of Fusarium wilt of tomatoes in Queensland. Plant Dis 66:165–166Google Scholar
  19. Haanstra JPW, Wye C, Verbakel H, Meijer-Dekens F, van den Berg P, Odinot P, van Heusden AW, Tanksley SD, Lindhout P, Peleman J (1999) An integrated high-density RFLP-AFLP map of tomato based on two Lycopersicon esculentum × L. pennellii F2 populations. Theor Appl Genet 99:254–271CrossRefGoogle Scholar
  20. Hemming MN, Basuki S, McGrath DJ, Carroll BJ, Jones DA (2004) Fine mapping of the tomato I-3 gene for fusarium wilt resistance and elimination of a co-segregating resistance gene analogue as a candidate for I-3. Theor Appl Genet 109:409–418PubMedCrossRefGoogle Scholar
  21. Jaillon O, Aury J-M, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyère C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Le Clainche I, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave F, Pè ME, Valle G, Morgante M, Caboche M, Adam-Blondon A-F, Weissenbach J, Quétier F, Wincker P (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–468PubMedCrossRefGoogle Scholar
  22. Kawchuk LM, Hachey J, Lynch DR, Kulcsar F, van Rooijen G, Waterer DR, Robertson A, Kokko E, Byers R, Howard RJ, Fischer R, Prufer D (2001) Tomato Ve disease resistance genes encode cell surface-like receptors. Proc Natl Acad Sci USA 98:6511–6515PubMedCrossRefGoogle Scholar
  23. Ku H-M, Vision T, Liu J, Tanskley SD (2000) Comparing sequenced segments of the tomato and Arabidopsis genomes: large-scale duplication followed by selective gene loss creates a network of synteny. Proc Natl Acad Sci USA 97:9121–9126PubMedCrossRefGoogle Scholar
  24. Khush GS, Rick CM (1963) Meiosis in hybrids between Lycopersicon esculentum and Solanum pennellii. Genetica 33:167–183CrossRefGoogle Scholar
  25. Laterrot H (1976) Localisation chromosomique de I2 chez la tomate controlant la resistance au pathotype 2 de Fusarium oxysporum f. sp. lycopersici. Ann Amelior Plant 26:485–491Google Scholar
  26. Lim GTT, Wang G-P, Hemming MN, Basuki S, McGrath DJ, Carroll BJ, Jones DA (2006) Mapping the I-3 gene for resistance to Fusarium wilt in tomato: application of an I-3 marker in tomato improvement and progress towards the cloning of I-3. Australas Plant Pathol 35:671–680CrossRefGoogle Scholar
  27. Lomsadze A, Ter-Hovhannisyan V, Chernoff YO, Borodovsky M (2005) Gene identification in novel eukaryotic genomes by self-training algorithm. Nucleic Acids Res 33:6494–6506PubMedCrossRefGoogle Scholar
  28. Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu T, Earle ED, Tanksley SD (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432–1436PubMedCrossRefGoogle Scholar
  29. McGrath DJ, Gillespie D, Vawdrey L (1987) Inheritance of resistance to Fusarium oxysporum f. sp. lycopersici races 2 and 3 in Lycopersicon pennellii. Aust J Agric Res 38:729–733CrossRefGoogle Scholar
  30. Meyer S, Nagel A, Gebhardt C (2005) PoMaMo—a comprehensive database for potato genome data. Nucleic Acids Res 33:D666–D670PubMedCrossRefGoogle Scholar
  31. Mueller LA, Solow TH, Taylor N, Skwarecki B, Buels R, Binns J, Lin C, Wright MH, Ahrens R, Wang Y, Herbst EV, Keyder ER, Menda N, Zamir D, Tanksley SD (2005) The SOL Genomics Network. A comparative resource for Solanaceae biology and beyond. Plant Physiol 138:1310–1317PubMedCrossRefGoogle Scholar
  32. Oh K, Hardeman K, Ivanchenko MG, Ellard-Ivey M, Nebenfuhr A, White TJ, Lomax TL (2002) Fine mapping in tomato using microsynteny with the Arabidopsis genome: the Diageotropica (Dgt) locus. Genome Biol 3:research0049.1–0049.11Google Scholar
  33. Ori N, Eshed Y, Paran I, Presting G, Aviv D, Tanskley S, Zamir D, Fluhr R (1997) The I2C family from the wilt disease resistance locus I2 belongs to the nucleotide binding, leucine-rich repeat superfamily of plant resistance genes. Plant Cell 9:521–532PubMedCrossRefGoogle Scholar
  34. Paddock EF (1950) A tentative assignment of Fusarium-immunity locus to linkage group 5 in tomato. Genetics 35:683–684Google Scholar
  35. Reis A, Costa H, Boiteux LS, Lopes CA (2005) First report of Fusarium oxysporum f. sp. lycopersici race 3 on tomato in Brazil. Fitopatol Bras 30:426–428Google Scholar
  36. Rossberg M, Theres K, Acarkan A, Herrero R, Schmitt T, Schumacher K, Schmitz G, Schmidt R (2001) Comparative sequence analysis reveals extensive microcolinearity in the Lateral Suppressor regions of the tomato, Arabidopsis, and Capsella genomes. Plant Cell 13:979–988PubMedCrossRefGoogle Scholar
  37. Sarfatti M, Abu-Abied M, Katan J, Zamir D (1991) RFLP mapping of I1, a new locus in tomato conferring resistance against Fusarium oxysporum f. sp. lycopersici race 1. Theor Appl Genet 82:22–26CrossRefGoogle Scholar
  38. Sarfatti M, Katan J, Fluhr R, Zamir D (1989) An RFLP marker in tomato linked to the Fusarium oxysporum resistance gene I2. Theor Appl Genet 78:755–759CrossRefGoogle Scholar
  39. Scott JW, Jones JP (1989) Monogenic resistance in tomato to Fusarium oxysporum f. sp. lycopersici race 3. Euphytica 40:49–53Google Scholar
  40. Sela-Buurlage MB, Budai-Hadrian O, Pan Q, Carmel-Goren L, Vunsch R, Zamir D, Fluhr R (2001) Genome-wide dissection of Fusarium resistance in tomato reveals multiple complex loci. Mol Genet Genomics 265:1104–1111PubMedCrossRefGoogle Scholar
  41. Simons G, Groenendijk J, Wijbrandi J, Reijans M, Groenen J, Diergaarde P, Van der Lee T, Bleeker M, Onstenk J, de Both M, Haring M, Mes J, Cornelissen B, Zabeau M, Vos P (1998) Dissection of the Fusarium I2 gene cluster in tomato reveals six homologs and one active gene copy. Plant Cell 10:1055–1068PubMedCrossRefGoogle Scholar
  42. Stall RE, Walter JM (1965) Selection and inheritance of resistance in tomato to isolates of races 1 and 2 of the Fusarium wilt organism. Phytopathology 55:1213–1215Google Scholar
  43. Tanksley SD, Costello W (1991) The size of the L. pennellii chromosome 7 segment containing the I-3 gene in tomato breeding lines as measured by RFLP probing. Rep Tomato Genet Coop 41:60–61Google Scholar
  44. Tanksley SD, Ganal MW, Martin GB (1995) Chromosome landing: a paradigm for map-based gene cloning in plants with large genomes. Trends Genet 11:63–68PubMedCrossRefGoogle Scholar
  45. Tanksley SD, Ganal MW, Prince JP, de Vicente MC, Bonierbale MW, Broun P, Fulton TM, Giovannoni JJ, Grandillo S, Martin GB, Messeguer R, Miller JC, Miller L, Paterson AH, Pineda O, Roder MS, Wing RA, Wu W, Young ND (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160PubMedGoogle Scholar
  46. Tatusova TA, Madden TL (1999) BLAST 2 sequences, a new tool for comparing protein and nucleotide sequences. FEMS Microbiol Lett 174:247–250PubMedCrossRefGoogle Scholar
  47. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen G-L, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Dejardin A, dePamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjarvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leple J-C, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouze P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai C-J, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604PubMedCrossRefGoogle Scholar
  48. Valenzuela-Ureta JG, Lawn DA, Heisey RF, Zamudio-Guzman V (1996) First report of Fusarium wilt race 3, caused by Fusarium oxysporum f. sp. lycopersici, of tomato in Mexico. Plant Dis 80:105Google Scholar
  49. van der Knapp E, Sanyal A, Jackson SA, Tanksley SD (2004) High-resolution fine mapping and fluorescence in situ hybridisation analysis of sun, a locus controlling tomato fruit shape, reveals a region of the tomato genome prone to DNA rearrangements. Genetics 168:2127–2140CrossRefGoogle Scholar
  50. Volin RB, Jones JP (1982) A new race of Fusarium wilt of tomato in Florida and sources of resistance. Proc Florida State Hortic Soc 95:268–270Google Scholar
  51. Wang G-P, Lim GTT, Jones DA (2007) Development of PCR-based markers from the tomato glutamate oxaloacetate transaminase isozyme gene family as a means of revitalising old isozyme markers and recruiting new ones. Mol Breeding 19:209–214CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • G. T. T. Lim
    • 1
  • G.-P. Wang
    • 1
    • 2
  • M. N. Hemming
    • 1
    • 3
  • D. J. McGrath
    • 4
  • D. A. Jones
    • 1
    Email author
  1. 1.Plant Cell Biology, Research School of Biological SciencesThe Australian National UniversityCanberraAustralia
  2. 2.College of HorticultureSouth China Agricultural UniversityGuangzhouChina
  3. 3.CSIRO Plant IndustryCanberraAustralia
  4. 4.Queensland Department of Primary Industries and FisheriesBowenAustralia

Personalised recommendations