Skip to main content

Advertisement

Log in

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

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

The I-3 gene from the wild tomato species Lycopersicon pennellii confers resistance to race 3 of the devastating vascular wilt pathogen Fusarium oxysporum f. sp. lycopersici. As an initial step in a positional cloning strategy for the isolation of I-3, we converted restriction fragment length polymorphism and conserved orthologue set markers, known genes and a resistance gene analogue (RGA) mapping to the I-3 region into PCR-based sequence characterised amplified region (SCAR) and cleaved amplified polymorphic sequence (CAPS) markers. Additional PCR-based markers in the I-3 region were generated using the randomly amplified DNA fingerprinting (RAF) technique. SCAR, CAPS and RAF markers were used for high-resolution mapping around the I-3 locus. The I-3 gene was localised to a 0.3-cM region containing a RAF marker, eO6, and an RGA, RGA332. RGA332 was cloned and found to correspond to a putative pseudogene with at least two loss-of-function mutations. The predicted pseudogene belongs to the Toll interleukin-1 receptor-nucleotide-binding site-leucine-rich-repeat sub-class of plant disease resistance genes. Despite the presence of two RGA332 homologues in L. esculentum, DNA gel blot and PCR analysis suggests that no other homologues are present in lines carrying I-3 that could be alternative candidates for the gene.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aarts MGM, te Lintel Hekkert B, Holub EB, Beynon JL, Stiekema WJ, Pereira A (1998) Identification of R-gene homologous DNA fragments genetically linked to disease resistance loci in Arabidopsis thaliana. Mol Plant Microbe Interact 11:251–258

    CAS  PubMed  Google Scholar 

  • Alexander LJ, Tucker CM (1945) Physiologic specialization in the tomato wilt fungus Fusarium oxysporum f. sp. lycopersici. J Agric Res 70:303–313

    Google Scholar 

  • Alpert KB, Pear JR, Martineau B, Houck CM, Chetelat RT, DeVerna JW (1990) Several fruit specific cDNAs map to chromosome 7. Rep Tomato Genet Coop 40:5

    Google Scholar 

  • Beier H, Grimm M (2001) Misreading of termination codons in eukaryotes by natural nonsense suppressor tRNAs. Nucleic Acids Res 29:4767–4782

    Article  CAS  PubMed  Google Scholar 

  • Bohn GW, Tucker CM (1939) Immunity to fusarium wilt in the tomato. Science 89:603–604

    Google Scholar 

  • 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 78:489–494

    Google Scholar 

  • Burbidge A, Lindhout P, Grieve TM, Schumacher K, Theres K, van Heusden AW, Bonnema AB, Woodman KJ, Taylor IB (2001) Re-orientation and integration of the classical and interspecific linkage maps of the long arm of tomato chromosome 7. Theor Appl Genet 103:443–454

    Article  CAS  Google Scholar 

  • Chetelat RT, DeVerna JW (1991) Expression of unilateral incompatibility in pollen of Lycopersicon pennellii is determined by major loci on chromosomes 1, 6 and 10. Theor Appl Genet 82:704–712

    Google Scholar 

  • Collins NC, Webb CA, Seah S, Ellis JG, Hulbert SH, Pryor A (1998) The isolation and mapping of disease resistance gene analogs in maize. Mol Plant Microbe Interact 11:968–978

    CAS  PubMed  Google Scholar 

  • Collins N, Drake J, Ayliffe M, Sun Q, Ellis J, Hulbert S, Pryor T (1999) Molecular characterization of the maize Rp1-D rust resistance haplotype and its mutants. Plant Cell 11:1365–1376

    CAS  PubMed  Google Scholar 

  • Creusot F, Macadre C, Ferrier Cana E, Riou C, Geffroy V, Sevignac M, Dron M, Langin T (1999) Cloning and molecular characterisation of three members of the NBS-LRR subfamily located in the vicinity of the Co-2 locus for anthracnose resistance in Phaseolus vulgaris. Genome 42:254–264

    CAS  PubMed  Google Scholar 

  • Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833

    CAS  PubMed  Google Scholar 

  • Davis RM, Kimble KA, Farrar JJ (1988) A third race of Fusarium oxysporum f. sp. lycopersici identified in California. Plant Dis 72:453

    Google Scholar 

  • Dodds PN, Lawrence GJ, Ellis JG (2001) Six amino acid changes confined to the leucine-rich repeat β-strand/β-turn motif determine the difference between the P and P2 rust resistance specificities in flax. Plant Cell 13:163–178

    CAS  PubMed  Google Scholar 

  • Dwyer KG, Kandasamy MK, Mahosky DI, Acciai J, Kudish BI, Miller JE, Nasrallah ME, Nasrallah JB (1994) A superfamily of S locus-related sequences in Arabidopsis: diverse structures and expression patterns. Plant Cell 6:1829–1843

    Article  CAS  PubMed  Google Scholar 

  • 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 19:1349

    CAS  PubMed  Google Scholar 

  • Ellis J, Dodds P, Pryor T (2000) Structure, function and evolution of plant disease resistance genes. Curr Opin Plant Biol 3:278–284

    CAS  PubMed  Google Scholar 

  • Eshed Y, Zamir D (1994) A genomic library of Lycopersicon pennellii in L. esculentum: A tool for fine mapping of genes. Euphytica 79:175–179

    CAS  Google Scholar 

  • 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 14:1457–1467

    Google Scholar 

  • Ganal MW, Tanksley SD (1996) Recombination around the Tm2a and Mi resistance genes in different crosses of Lycopersicon peruvianum. Theor Appl Genet 92:101–108

    Article  CAS  Google Scholar 

  • Ganal MW, Czihal R, Hannappel U, Kloos DU, Polley A, Ling HQ (1998) Sequencing of cDNA clones from the genetic map of tomato (Lycopersicon esculentum). Genome Res 8:842–847

    CAS  PubMed  Google Scholar 

  • Giovannoni J, Yen H, Shelton B, Miller S, Vrebalov J, Kannan P, Tieman D, Hackett R, Grierson D, Klee H (1999) Genetic mapping of ripening and ethylene-related loci in tomato. Theor Appl Genet 98:1005–1013

    Article  CAS  Google Scholar 

  • 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

  • Grattidge R, O’Brien RG (1982) Occurrence of a third race of Fusarium wilt of tomatoes in Queensland. Plant Dis 66:165–166

    Google Scholar 

  • Haanstra JPW, Wye C, Verbakel H, Meijer-Dekens F, van der Berg P, Odinot P, van Heusden AW, Tanksley S, 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 99:254–271

    Article  CAS  Google Scholar 

  • Hall T (1999) bioedit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hamilton CM, Frary A, Xu Y, Tanksley SD, Zhang HB (1999) Construction of tomato genomic DNA libraries in a binary-BAC (BIBAC) vector. Plant J 18:223–229

    CAS  Google Scholar 

  • Hancock CN, Kondo K, Beecher B, McClure B (2003) The S-locus and unilateral incompatibility. Philos Trans R Soc London Ser B 358:1133–1140

    Article  CAS  Google Scholar 

  • Harrell L, Melcher U, Atkins JF (2002) Predominance of six different hexanucleotide recoding signals 3’ of read-through stop codons. Nucleic Acids Res 30:2011–2017

    Article  CAS  PubMed  Google Scholar 

  • Harrison PM, Gerstein M (2002) Studying genomes through the aeons: protein families, pseudogenes and proteome evolution. J Mol Biol 318:1155–1174

    Article  CAS  PubMed  Google Scholar 

  • Ho JY, Weide R, Ma HM, van Wordragen MF, Lambert KN, Koornneef M, Zabel P, Williamson VM (1992) The root-knot nematode resistance gene (Mi) in tomato: construction of a molecular linkage map and identification of dominant cDNA markers in resistance genotypes. Plant J 2:971–982

    CAS  PubMed  Google Scholar 

  • Holdsworth MJ, Bird CR, Ray J, Schuch W, Grierson D (1987) Structure and expression of an ethylene related mRNA from tomato. Nucleic Acids Res 15:731–739

    CAS  PubMed  Google Scholar 

  • Jones DA, Jones JDG (1997) The role of leucine rich repeat proteins in plant defences. Adv Bot Res 24:89–167

    Google Scholar 

  • Kachroo A, Schopfer CR, Nasrallah ME, Nasrallah JB (2001) Allele-specific receptor-ligand interactions in Brassica self-incompatibility. Science 293:1824–1826

    Article  CAS  PubMed  Google Scholar 

  • Kanazin V, Marek LF, Shoemaker RC (1996) Resistance gene analogs are conserved and clustered in soybean. Proc Natl Acad Sci USA 93:11746–11750

    CAS  PubMed  Google Scholar 

  • Kusaba M, Dwyer K, Hendershot J, Vrebalov J, Nasrallah JB, Nasrallah ME (2001) Self-incompatibility in the genus Arabidopsis: characterization of the S locus in the outcrossing A. lyrata and its autogamous relative A. thaliana. Plant Cell 13:627–643

    CAS  PubMed  Google Scholar 

  • Lagudah ES, Moullet O, Appels R (1997) Map-based cloning of a gene sequence encoding a nucleotide-binding domain and a leucine-rich region at the Cre3 nematode resistance locus of wheat. Genome 40:659–665

    CAS  PubMed  Google Scholar 

  • Leister D, Ballvora A, Salamini F, Gebhardt C (1996) A PCR-based approach for isolating pathogen resistance genes from potato with potential for wide application in plants. Nat Genet 14:421–429

    CAS  PubMed  Google Scholar 

  • Liharska TB, Koornneef M, van Wordragen M, van Kammen A, Zabel P (1996) Tomato chromosome 6: effect of alien chromosomal segments on recombination frequencies. Genome 39:485–491

    CAS  Google Scholar 

  • Liu YS, Zamir D (1999) Second generation L. pennellii introgression lines and the concept of bin mapping. Rep Tomato Genet Coop 49:26–30

    Google Scholar 

  • Mago R, Nair S, Mohan M (1999) Resistance gene analogues from rice: cloning, sequencing and mapping. Theor Appl Genet 99:50–57

    Article  CAS  Google Scholar 

  • 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 38:729–733

    Google Scholar 

  • Messeguer R, Ganal M, de Vincente MC, Young ND, Bolkan H, Tanksley SD (1991) High resolution RFLP map around the root-knot nematode resistance gene (Mi) in tomato. Theor Appl Genet 82:529–536

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Meyers BC, Dickerman AW, Michelmore RW, Sivaramakrishnan S, Sobral BW, Young ND (1999) Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J 20:317–332

    Article  CAS  PubMed  Google Scholar 

  • Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834.

    Article  CAS  PubMed  Google Scholar 

  • Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM (1998) The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307–1319

    CAS  PubMed  Google Scholar 

  • Nasrallah J, Kao T, Goldberg M, Nasrallah M (1985) A cDNA clone encoding an S-locus-specific glycoprotein from Brassica oleracea. Nature 5:373–384

    Google Scholar 

  • Ohmori T, Murata M, Motoyoshi F (1998) Characterisation of disease resistance gene-like sequences in near-isogenic lines of tomato. Theor Appl Genet 96:331–338

    CAS  Google Scholar 

  • Paal JM, Gebhardt C, Salamini F (2004) Molecular cloning of the Gro1 gene for potato resistance to the root cyst nematode Globodera rostochiensis using a candidate gene approach. Genbank accessions AY196151–AY196163. http://www.ncbi.nlm.nih.gov:80/entrez/query.fcgi?db=Nucleotide

  • Paddock E (1950) A tentative assignment of Fusarium-immunity locus to linkage group 5 in tomato. Genetics 35:683–684

    Google Scholar 

  • Pan Q, Liu YS, Budai-Hadrian O, Sela M, Carmel-Goren L, Zamir D, Fluhr R (2000a) Comparative genetics of nucleotide binding site-leucine rich repeat resistance gene homologues in the genomes of two dicotyledons: tomato and Arabidopsis. Genetics 155:309–322

    CAS  PubMed  Google Scholar 

  • Pan Q, Wendel J, Fluhr R (2000b) Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes. J Mol Evol 50:203–213

    CAS  PubMed  Google Scholar 

  • Pastuglia M, Roby D, Dumas C, Cock JM (1997) Rapid induction by wounding and bacterial infection of an S gene family receptor-like kinase gene in Brassica oleracea. Plant Cell 9:49–60

    CAS  PubMed  Google Scholar 

  • Pastuglia M, Swarup R, Rocher A, Saindrenan P, Roby D, Dumas C, Cock JM (2002) Comparison of the expression patterns of two small gene families of S gene family receptor kinase genes during the defence response in Brassica oleracea and Arabidopsis thaliana. Gene 282:215–225

    Article  CAS  PubMed  Google Scholar 

  • Pear JR, Ridge N, Rasmussen R, Rose RE, Houck CM (1989) Isolation and characterization of a fruit-specific cDNA and the corresponding genomic clone from tomato. Plant Mol Biol 13:639–651

    CAS  PubMed  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer 3 on the WWW for general users and biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386

  • Sambrook J, Russell D (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • 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 82:22–26

    CAS  Google Scholar 

  • Schopfer CR, Nasrallah ME, Nasrallah JB (1999) The male determinant of self-incompatibility in Brassica. Science 286:1697–1700

    CAS  PubMed  Google Scholar 

  • Scott JW, Jones JP (1989) Monogenic resistance in tomato to Fusarium oxysporum f. sp. lycopersici race 3. Euphytica 40:49–53

    Google Scholar 

  • Scott JW, Jones JP (1995) Fla. 7547 and Fla. 7481 tomato breeding lines resistant to Fusarium oxysporum f. sp. lycopersici races 1,2 and 3. HortScience 30:645–646

    Google Scholar 

  • 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 265:1104–1111

    Article  PubMed  Google Scholar 

  • Shiu SH, Bleecker AB (2001) Plant receptor-like kinase gene family: diversity, function and signalling. Science’s STKE 113: reference 22. http://stke.sciencemag.org/cgi/content/full/OC_sigtrans;2001/113/re22

  • 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 10:1055–1068

    CAS  Google Scholar 

  • Stein JC, Howlett B, Boyes DC, Nasrallah ME, Nasrallah JB (1991) Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc Natl Acad Sci USA 88:8816–8820

    CAS  PubMed  Google Scholar 

  • Takasaki T, Hatakeyama K, Suzuki G, Watanabe M, Isogai A, Hinata K (2000) The S receptor kinase determines self-incompatibility in Brassica stigmas. Nature 403:913–916

    CAS  PubMed  Google Scholar 

  • Takayama S, Shimosato H, Shiba H, Funato M, Che FS, Watanabe M, Iwano M, Isogai A (2001) Direct ligand-receptor complex interaction controls Brassica self-incompatibility. Nature 413:534–538

    Article  CAS  PubMed  Google Scholar 

  • 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 41:60–61

    Google Scholar 

  • 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 132:1141–1160

    CAS  PubMed  Google Scholar 

  • Tatusova TA, Madden TL (1999) blast 2 sequences, a new tool for comparing protein and nucleotide sequences. FEMS Microbiol Lett 174:247–250

    CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    PubMed  Google Scholar 

  • Traut TW (1994) The functions and consensus motifs of nine types of peptide segments that form different types of nucleotide-binding sites. Eur J Biochem 222:9–19

    CAS  PubMed  Google Scholar 

  • Van der Hoorn RAL, De Wit PJGM, Joosten MHAJ (2002) Balancing selection favors guarding resistance proteins. Trends Plant Sci 7:67–71

    Google Scholar 

  • Volin RB, Jones JP (1982) A new race of Fusarium wilt of tomato in Florida and sources of resistance. Proc Fla State Hortic Soc 95:268–270

    Google Scholar 

  • Waldron J, Peace CP, Searle IR, Furtado A, Wade N, Findlay I, Graham MW, Carroll BJ (2002) Randomly amplified DNA fingerprinting: A culmination of DNA marker technologies based on arbitrarily-primed PCR amplification. J Biomed Biotechnol 2:141–150

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Wang X, Skirpan AL, Kao TH (2003) S-RNase-mediated self-incompatibility. J Exp Bot 54:115–122

    Article  CAS  PubMed  Google Scholar 

  • Yu YG, Buss GR, Saghai Maroof MA (1996) Isolation of a superfamily of candidate disease-resistance genes in soybean based on a conserved nucleotide-binding site. Proc Natl Acad Sci USA 93:11751–11756

    CAS  PubMed  Google Scholar 

  • Zhao Y, Feng XH, Watson JC, Bottino PJ, Kung SD (1994) Molecular cloning and biochemical characterization of a receptor-like serine/threonine kinase from rice. Plant Mol Biol 26:791–803

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was conducted within the Cooperative Research Centre for Tropical Plant Protection, established and supported by the Australian Government’s Cooperative Research Centres Program. The authors would like to thank Dr. Brett Baillie and Dr. Stephen Garland for their involvement in this work, Dr. S. Tanksley for generous provision of the TG clones and Dr. D. Zamir and Dr. J. Scott for generous provision of the IL lines and Fla. introgression lines.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. A. Jones.

Additional information

Communicated by R. Hagemann

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hemming, M.N., Basuki, S., McGrath, D.J. et al. 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, 409–418 (2004). https://doi.org/10.1007/s00122-004-1646-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-004-1646-4

Keywords

Navigation