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Inheritance and genetic mapping of resistance to Alternaria alternata f. sp. lycopersici in Lycopersicon pennellii

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Abstract

The fungal pathogen Alternaria alternata f. sp. lycopersici produces AAL-toxins that function as chemical determinants of the Alternaria stem canker disease in the tomato (Lycopersicon esculentum). In resistant cultivars, the disease is controlled by the Asc locus on chromosome 3. Our aim was to characterize novel sources of resistance to the fungus and of insensitivity to the host-selective AAL-toxins. To that end, the degree of sensitivity of wild tomato species to AAL-toxins was analyzed. Of all members of the genus Lycopersicon, only L. cheesmanii was revealed to be sensitive to AAL-toxins and susceptible to fungal infection. Besides moderately insensitive responses from some species, L. pennellii and L. peruvianum were shown to be highly insensitive to AAL-toxins as well as resistant to the pathogen. Genetic analyses showed that high insensitivity to AAL-toxins from L. pennellii is inherited in tomato as a single complete dominant locus. This is in contrast to the incomplete dominance of insensitivity to AAL-toxins of L. esculentum. Subsequent classical genetics, RFLP mapping and allelic testing indicated that high insensitivity to AAL-toxins from L. pennellii is conferred by a new allele of the Asc locus.

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References

  • Alexander LJ, Hoover MM (1955) Disease resistance in wild species of tomato. Ohio Agric Exp Stn Res Bull 752:1–76

    Google Scholar 

  • Bino RJ, Franken J, Witsenboer HMA, Hille J, Dons JJM (1988) Effects of Alternaria alternata f. sp. lycopersici toxins on pollen. Theor Appl Genet 76:204–208

    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 

  • Bournival BL, Vallejos CE, Scott JW (1990) Genetic analysis of resistances to races l and 2 of Fusarium oxysporum f. sp. lycopersici from the wild tomato Lycopersicon pennellii. Theor Appl Genet 79:641–645

    Google Scholar 

  • Caldas ED, Jones AD, Ward B, Winter CK, Gilchrist DG (1994) Structural characterization of three new AAL-toxins produced by Alternaria alternata f. sp. lycopersici. J Agric Food Chem 42:327–333

    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 

  • Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995

    Google Scholar 

  • Clouse SD, Gilchrist DG (1987) Interaction of the asc locus in F8 paired lines of tomato with Alternaria alternata f. sp. lycopersici and AAL-toxin. Phytopathology 77:80–82

    Google Scholar 

  • Clouse SD, Martensen AN, Gilchrist DG (1985) Rapid purification of host-specific pathotoxins from Alternaria alternata f. sp. lycopersici by solid-phase adsorption on octadecylsilane. J Chromatogr 350:255–263

    Google Scholar 

  • De Vicente MC, Tanksley SD (1991) Genome-wide reduction in recombination of backcross progeny derived from male versus female gametes in an interspecific cross of tomato. Theor Appl Genet 83:173–178

    Google Scholar 

  • Doolittle SP (1953) The use of wild Lycopersicon species for tomato disease control. Phytopathology 44:409–414

    Google Scholar 

  • Eshed Y, Abu-abied M, Saranga Y, Zamir D (1992) Lycopersicon esculentum lines containing small overlapping introgressions from L. pennellii. Theor Appl Genet 83:1027–1034

    Google Scholar 

  • Foolad MR, Jones RA (1993) Mapping salt-tolerance genes in tomato (Lycopersicon esculentum) using trait-based marker analysis. Theor Appl Genet 87:184–192

    Google Scholar 

  • Fuson GB, Pratt D (1988) Effects of the host-selective toxins of Alternaria alternata f. sp. lycopersici on suspension-cultured tomato cells. Physiol Biochem 78:1641–1648

    Google Scholar 

  • Gilchrist DG, Grogan RG (1976) Production and nature of a hostspecific toxin from Alternaria alternata f. sp. lycopersici. Physiol Biochem 66:165–171

    Google Scholar 

  • Grogan RG, Kimble KA, Misaghi I (1975) A stem canker disease of tomato caused by Alternaria alternata f. sp. lycopersici. Phytopathology 65:880–886

    Google Scholar 

  • Hammond-Kosack KE, Jones JDG (1994) Incomplete dominance of tomato Cf genes for resistance to Cladosporium fulvum. Mol Plant-Microbe Interact 7:58–70

    Google Scholar 

  • Jones DA, Dickinson MJ, Balint-Kurti PJ, Dixon MS, Jones JDG (1993) 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. Mol Plant-Microbe Interact 6:348–357

    Google Scholar 

  • Koornneef M, Bade J, Hanhart C, Horsman K, Schel J, Soppe W, Verkerk R, Zabel P (1993) Characterization and mapping of a gene controlling shoot regeneration in tomato. Plant 13:131–141

    Google Scholar 

  • Lamprecht SC, Marasas WFO, Alberts JF, Cawood ME, Gelderblom WCA, Shephard GS, Thiel PG, Calitz FJ (1994) Phytotoxicity of fumonisins and TA-toxin to corn and tomato. Phytopathology 84:383–391

    Google Scholar 

  • Laterrot H (1976) Localisation chromosomique de I 2 chez la tomate contrôlant la résistance au pathotype 2 de Fusarium oxysporum f. lycopersici. Ann Amélior Plantes 26:485–491

    Google Scholar 

  • 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 262:1432–1436

    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 

  • Moussatos V, Witsenboer H, Hille J, Gilchrist D (1993) Behaviour of the disease resistance gene Asc in protoplasts of Lycopersicon esculentum Mill. Physiol Mol Plant Pathol 43:225–236

    Google Scholar 

  • Overduin B, Hogenhout SA, Van der Biezen EA, Haring MA, Nijkamp HJJ, Hille J (1993) The Asc locus for resistance to Alternaria stem canker in tomato does not encode the enzyme aspartate carbamoyltransferase. Mol Gen Genet 240:43–48

    Google Scholar 

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

    Google Scholar 

  • Rick CM (1969) Controlled introgression of chromosomes of Solanum pennellii into Lycopersicon esculentum: segregation and recombination. Genetics 62:753–768

    Google Scholar 

  • Rommens CMT, Rudenko GN, Dijkwel PPD, Van Haaren MJJ, Ouwerkerk PBF, Blok KM, Nijkamp HJJ, Hille J (1992) Characterization of the Ac/Ds behaviour in transgenic plants using plasmid rescue. Plant Mol Biol 20:61–70

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • 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 78:755–759

    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

    Google Scholar 

  • Schwartz E, Shen D, Aebersold R, McGrath JM, Pichersky E, Green BR (1991) Nucleotide sequence and chromosomal location of Cab11 and Cab12, the genes for the fourth polypeptide of the photosystem I light-harvesting antenna (LHCI). FEBS Lett 280:229–234

    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 

  • Siler DJ, Gilchrist DG (1982) Determination of host-selective phytotoxins from Alternaria alternata f. sp. lycopersici as their maleyl derivatives by high-performance liquid chromatography. J Chromatogr 238:167–173

    Google Scholar 

  • Siler DJ, Gilchrist DG (1983) Properties of host specific toxins produced by Alternaria alternata f. sp. lycopersici in culture and in tomato plants. Physiol Plant Pathol 23:265–274

    Google Scholar 

  • Stam P (1993) Construction of integrated genetic linkage maps by means of a new computer package: JoinMap. Plant J 3:739–744

    Google Scholar 

  • Stevens MA, Rick CM (1986) Genetics and breeding. In: Atherton JG, Rudich J (eds) The tomato crop, a scientific basis for crop improvement. Chapman and Hall, New York, pp 35–100

    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, Fineda O, Röder MS, Wing RA, Wu W, Young ND (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160

    Google Scholar 

  • Taylor IB (1986) Biosystematics of the tomato. In: Atherton JG, Rudich J (eds) The tomato crop, a scientific basis for crop improvement. Chapman and Hall, New York, pp 1–34

    Google Scholar 

  • Thomas CM, Jones DA, English JJ, Carroll BJ, Bennetzen JF, Harrison K, Burbidge A, Bishop GJ, Jones JDG (1994) Analysis of the chromosomal distribution of transposon-carrying TDNAs in tomato using the inverse polymerase chain reaction. Mol Gen Genet 242:573–585

    Google Scholar 

  • Van der Beek JG, Verkerk R, Zabel P, Lindhout P (1992) Mapping strategy for resistance in tomato based on RFLPs between cultivars: Cf9 (resistance to Cladosporium fulvum) on chromosome 1. Theor Appl Genet 84:106–112

    Google Scholar 

  • Van der Biezen EA, Overduin B, Kneppers TJA, Mesbah L, Nijkamp HJJ, Hille J (1994a) Molecular genetic characterisation of the Asc locus of tomato conferring resistance to the fungal pathogen Alternaria alternata f. sp. lycopersici. Euphytica 79:205–218

    Google Scholar 

  • Van der Biezen EA, Overduin B, Nijkamp HJJ, Hille J (1994b) Integrated genetic map of tomato chromosome 3. Tomato Genet Coop Rep 44:8–10

    Google Scholar 

  • Wang IF, Stall RE, Vallejos (1994) Genetic analysis of a complex hypersensitive reaction to bacterial spot in tomato. Phytopathology 84:126–132

    Google Scholar 

  • Witsenboer HMA, Schaik CE, Bino RJ, Löffler HIM, Nijkamp HJJ, Hille J (1988) Effects of Alternaria alternata f. sp. lycopersici toxins at different levels of tomato plant cell development. Plant Sci 56:253–260

    Google Scholar 

  • Witsenboer HMA, Van de Griend EG, Tiersma JB, Nijkamp HJJ, Hille J (1989) Tomato resistance to Alternaria stem canker: localization in host genotypes and functional expression compared to non-host resistance. Theor Appl Genet 78:457–462

    Google Scholar 

  • Witsenboer HMA, Kloosterziel KM, Hateboer G, Nijkamp HJJ, Hille J (1992) Tomato susceptibility to Alternaria stem canker: parameters involved in host-specific toxin-induced leaf necrosis. Plant Sci 81:127–134

    Google Scholar 

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Author notes

  1. Bert Overduin

    Present address: CEPRAP, University of California at Davis, CA95616, USA

Authors and Affiliations

  1. Department of Genetics, Institute for Molecular Biological Sciences, BioCentrum Amsterdam, Vrije Universiteit, De Boelelaan 1087, 1081, HV Amsterdam, The Netherlands

    Erik A. van der Biezen, Tatyana Glagotskaya, Bert Overduin, H. John, J. Nijkamp & Jacques Hille

Authors
  1. Erik A. van der Biezen
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  2. Tatyana Glagotskaya
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  3. Bert Overduin
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  4. H. John
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  5. J. Nijkamp
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  6. Jacques Hille
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Communicated by H. Saedler

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van der Biezen, E.A., Glagotskaya, T., Overduin, B. et al. Inheritance and genetic mapping of resistance to Alternaria alternata f. sp. lycopersici in Lycopersicon pennellii . Molec. Gen. Genet. 247, 453–461 (1995). https://doi.org/10.1007/BF00293147

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  • DOI: https://doi.org/10.1007/BF00293147

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