Skip to main content
SpringerLink
Log in

Molecular analysis of irradiation-induced and spontaneous deletion mutants at a disease resistance locus inLactuca sativa

  • Original Paper
  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Abstract

The major cluster of disease resistance genes in lettuce (Lactuca sativa) contains at least nine downy mildew resistance genes (Dm) spanning a genetic distance of 20 cM and a physical distance of at least 6 Mb. Nine molecular markers that were genetically tightly linked toDm3 were used to analyze nine independent deletion mutants and construct a map of the region surroundingDm3. This analysis identified a linear order of deletion breakpoints and markers along the chromosome. There was no evidence for chromosomal rearrangements associated with the deletions. The region is not highly recombinagenic and the deletion breakpoints provided greater genetic resolution than meiotic recombinants. The region contains a mixture of high- and low-copy-number sequences; no single-copy sequences were detected. Three markers hybridized to low-copy-number families of sequences that are duplicated predominantly close toDm3. This was not true for sequences related to the triose-phosphate isomerase gene; these had been shown previously to be linked toDm3, as well as to two independent clusters ofDm genes, and elsewhere in the genome. Two spontaneous mutants ofDm3 were identified; several markers flankingDm3 are absent in one of these two mutants. The stability of theDm3 region was also studied by analyzing the genotypes of diverse related cultivars. The 1.5 Mb region surroundingDm3 has remained stable through many generations of breeding with and without selection forDm3 activity.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bennetzen JL, In Qin MM, Ingels S, Ellingboe AH (1988) Allelespecific andMutator-associated instability at theRp1 disease-resistance locus of maize. Nature 322:369–370

    Google Scholar 

  • Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Giraudat J, Leung J, Staskawicz BS (1994)Rsp2 ofArabidopsis thaliana — a leucine-rich repeat class of plant disease resistance genes. Science 265:1856–1860

    PubMed  Google Scholar 

  • Bernatzky R, Tanksley SD (1986) Genetics of actin-related sequences in tomato. Theor Appl Genet 72:314–321

    Google Scholar 

  • Crute IR, Johnson AG (1976) The genetic relationship between races ofBremia lactucae and cultivars ofLactuca sativa. Ann Appl Biol 83:125–137

    Google Scholar 

  • Dickinson MJ, Jones DA, Jones JDG (1993) Close linkage betweenCf 2/Cf 5 andMi resistance loci in tomato. Mol Plant-Microbe Interact 6:341–347

    PubMed  Google Scholar 

  • Ellis JG, Lawrence GJ, Finnegan EJ, Anderson PA (1995) Contrasting complexity of two rust resistance loci in flax. Proc Natl Acad Sci (USA) 92:4185–4188

    PubMed  Google Scholar 

  • Farrara BF, Ilott TW, Michelmore RW (1987) Genetic analysis of factors for resistance to downy mildew (Bremia lactucae) in species of lettuce (Lactuca sativa andL. serriola). Plant Pathol 36:499–514

    Google Scholar 

  • Flor HH (1956) The complementary genic systems in flax and its rust. Adv Genet 8:29–54

    Google Scholar 

  • Grant MR, Godiard L, Straube E, Ashfiled T, Lewald J, Sattler A, Innes RW, Dangl JL (1995) Structure of theArabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269:843–846

    PubMed  Google Scholar 

  • Hong KS, Richter TE, Bennetzen JL, Hulbert SH (1993) Complex duplications in maize lines. Mol Gen Genet 239:115–121

    PubMed  Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

  • Islam MR, Mayo GME (1990) A compendium of host genes in flax conferring resistance to flax rust. Plant Breed 104:89–100

    Google Scholar 

  • Jahoor A, Jacobi A, Schuller CME, Fischbeck G (1993) Genetical and RFLP studies at theMla locus conferring powdery mildew resistance in barley. Theor Appl Genet 85:713–718

    Google Scholar 

  • Johal GS, Briggs SP (1992) Reductase activity encoded by theHM1 disease resistance gene in maize. Science 258:985–987

    PubMed  Google Scholar 

  • Johnson AG, Laxton SA, Crute IR, Gordon PL, Norwood JM (1978) Further work on the genetics of race-specific resistance in lettuce (Lactuca sativa) to downy mildew (Bremia lactucae). Ann Appl Biol 89:257–264

    Google Scholar 

  • Jones DA, Thomas CM, Hammond-Kasack KE, Balint-Kurti PJ, Jones JDG (1994) Isolation of the tomatoCf-9 gene for resistance toCladosporium fulvum by transposon tagging. Science 266:789–793

    PubMed  Google Scholar 

  • Kesseli RV, Witsenboer H, Vandemark GJ, Stangellini ME, Michelmore RW (1993) Recessive resistance toPlasmopara lactucaeradicis maps by bulked segregant analysis to a cluster of dominant resistance genes in lettuce. Mol Plant-Microbe Interact 6:722–728

    Google Scholar 

  • Kush GS, Rick CM (1968) Cytogenetic analysis of the tomato genome by means of induced deficiencies. Chromosoma 23:452–484

    Google Scholar 

  • Lawrence G, Finnegan J, Aliffe M, Ellis J (1995) TheL6 gene for flax rust resistance is related to theArabidopsis bacterial resistance geneRPS2 and the tobacco viral resistance geneN. Plant Cell 7:1195–1206

    PubMed  Google Scholar 

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

    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

    PubMed  Google Scholar 

  • McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801

    PubMed  Google Scholar 

  • Michelmore RW (1995) Isolation of disease resistance genes from crop plants. Curr Opin Biotechnol 6:145–152

    Google Scholar 

  • Michelmore RW, Kesseli RV, Francis DM, Paran I, Fortin MG, Yang C-H (1992) Strategies for cloning plant disease resistance genes. In Gurr SJ, McPherson MJ, Bowles DJ (eds) Molecular plant pathology: a practical approach, vol 2. Oxford University Press, Oxford, pp. 233–288

    Google Scholar 

  • Mindrinos M, Katagirti F, Yu GL, Ausubel FM (1994) TheArabidopsis thaliana disease resistance geneRPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78:1089–1099

    PubMed  Google Scholar 

  • Okubara PA, Anderson PA, Ochoa OE, Michelmore RW (1994) Mutants of downy mildew resistance inLactuca sativa. Genetics 137:867–874

    PubMed  Google Scholar 

  • Paran I, Kesseli RV, Westphal L, Michelmore RW (1992) Recent amplification of triose phosphate isomerase-related sequences in lettuce. Genome 35:627–635

    PubMed  Google Scholar 

  • Paran I, Michelmore RW (1993) Development of reliable PCR-based markers linked to downy mildew resistance genes in lettuce. Theor Appl Genet 5:985–993

    Google Scholar 

  • Pryor A (1987) The origin and structure of fungal disease resistance in plants. Trends Genet 3:157–161

    Google Scholar 

  • Pryor T, Ellis J (1993) The genetic complexity of fungal resistance genes in plants. Adv Plant Pathol 10:281–305

    Google Scholar 

  • Robbins MA, Witsenboer H, Michelmore RW, Laliberte J-F, Fortin MG (1994) Genetic mapping of turnip mosaic virus resistance inLactuca sativa. Theor Appl Genet 89:583–589

    Google Scholar 

  • Salmeron JM, Barker SJ, Carland FM, Mehta AY, Staskawicz BJ (1994) Tomato mutants altered in bacterial disease resisance provide evidence for a locus controlling pathogen recognition. Plant Cell 6:511–520

    PubMed  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 

  • Saxena KMS, Hooker AL (1968) On the structure of a gene for disease resistance in maize. Proc Natl Acad Sci USA 68: 1300–1305

    Google Scholar 

  • Shirley BW, Hanley S, Goodman HM (1992) Effects of ionizing radiation on a plant genome: analysis of twoArabidopsis transparent testa mutations. Plant Cell 4:333–347

    PubMed  Google Scholar 

  • Staskawicz BJ, Ausubel FM, Baker BJ, Ellis JG, Jones JG (1995) Molecular genetics of plant disease resistance. Science 268:661–667

    PubMed  Google Scholar 

  • Sudupak MA, Bennetzen JL, Hulbert SH (1993) Unequal exchange and meiotic instability ofRp1 region disease resistance genes in maize. Genetics 132:119–125

    Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414

    PubMed  Google Scholar 

  • Whitham S, Dinesh Kumar SP, Choi D, Hehl R, Carr C, Baker B (1994) The product of the tobacco mosic virus resistance geneN — similarity to Toll and the Interleukin-1 receptor. Cell 78:1101–1115

    PubMed  Google Scholar 

  • Wing RA, Rastogi VK, Zhang H-B, Paterson AH, Tanksley SD (1993) An improved method of plant megabase DNA isolation in agarose microbeads suitable for physical mapping and YAC cloning. Plant J 4:893–898

    PubMed  Google Scholar 

  • Wise RP, Ellingboe AH (1985) Fine structure and instability of theMl-a locus in barley. Genetics 111:113–130

    PubMed  Google Scholar 

  • Witsenboer H, Kesseli RV, Fortin M, Stangellini 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

    Google Scholar 

  • Zabeau M, Vos P (1993) Selective restriction fragment amplification: a general method for DNA fingerprinting. European Patent Application 92402629.7. Publ No 0 534 858 A1

  • Zhang HB, Zhao XP, Ding XL, Paterson AH, Wing RA (1995) Preparation of megabase-size DNA from plant nuclei. Plant J 7:175–184

    Google Scholar 

Download references

Author information

Author notes

  1. P. A. Anderson

    Present address: CSIRO, Division of Plant Industry, 2601, Canberra, ACT, Australia

  2. P. A. Okubara

    Present address: Department of Environmental Horticulture, University of California, 95616, Davis, CA, USA

Authors and Affiliations

  1. Department of Vegetable Crops, University of California, 95616, Davis, CA, USA

    P. A. Anderson, P. A. Okubara, R. Arroyo-Garcia, B. C. Meyers & R. W. Michelmore

Authors
  1. P. A. Anderson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. A. Okubara
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. Arroyo-Garcia
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. B. C. Meyers
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. R. W. Michelmore
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by R. G. Herrmann

Rights and permissions

Reprints and permissions

About this article

Cite this article

Anderson, P.A., Okubara, P.A., Arroyo-Garcia, R. et al. Molecular analysis of irradiation-induced and spontaneous deletion mutants at a disease resistance locus inLactuca sativa . Molec. Gen. Genet. 251, 316–325 (1996). https://doi.org/10.1007/BF02172522

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02172522

Key words

Search

Navigation