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A genetic linkage map of the soybean cyst nematode Heterodera glycines

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Abstract

A genetic linkage map of the soybean cyst nematode (SCN) Heterodera glycines was constructed using a population of F2 individuals obtained from matings between two highly inbred SCN lines, TN16 and TN20. The AFLP fingerprinting technique was used to genotype 63 F2 progeny with two restriction enzyme combinations (EcoRI/MseI and PstI/TaqI) and 38 primer combinations. The same F2 population was also genotyped for Hg-cm-1 (H. glycines chorismate mutase-1), a putative virulence gene, using real-time quantitative PCR. Some of the markers were found to be distributed non-randomly. Even so, of the 230 markers analyzed, 131 could be mapped onto ten linkage groups at a minimum LOD of 3.0, for a total map distance of 539 cM. The Hg-cm-1 locus mapped to linkage group III together with 16 other markers. The size of the H. glycines genome was estimated to be in the range of 630–743 cM, indicating that the current map represents 73–86% of the genome, with a marker density of one per 4.5 cM, and a physical/genetic distance ratio of between 124 kb/cM and 147 kb/cM. This genetic map will be of great assistance in mapping H. glycines markers to genes of interest, such as nematode virulence genes and genes that control aspects of nematode parasitism.

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References

  • Albertson DG, Thomson JN (1982) The kinetochores of Caenorhabditis elegans. Chromosoma 86:409–428

    Google Scholar 

  • Albertson DG, Thomson JN (1993) Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans. Chromosome Res 1:15–26

    Google Scholar 

  • Alonso-Blanco C, Peeters AJM, Koomneef M, Lister C, Dean C, Van den Bosch N, Pot J, Kuiper MTR (1998) Development of an AFLP based linkage map of L er, Col and Cvi Arabidopsis thaliana ecotypes and construction of L er/Cvi recombinant inbred line population. Plant J 14:259–271

    Google Scholar 

  • Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (eds) (1992) Short protocols in molecular biology, 2nd edn. Wiley, New York

    Google Scholar 

  • Barnes TM, Kohara Y, Coulson A, Hekimi S (1995) Meiotic recombination, noncoding DNA and genomic organization in Caenorhabditis elegans. Genetics 141:159–179

    Google Scholar 

  • Bekal S, Niblack TL, Lambert KN (2003) A chorismate mutase from the soybean cyst nematode Heterodera glycines shows polymorphisms that correlate with virulence. Mol Plant Microbe Interact 16:439–446

    Google Scholar 

  • Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71–94

    Google Scholar 

  • Burr B, Evola SV, Burr FA, Beckmann JS (1983) The application of restriction fragment length polymorphism to plant breeding. In: Setlow JK, Hollaender A (eds) Genetic engineering, vol 5. Plenum Press, New York, pp 45–59

  • Chakravarti A, Lasher LK, Reefer JE (1991) A maximum likelihood method for estimating genome length using genetic linkage data. Genetics 128:175–182

    CAS  PubMed  Google Scholar 

  • Concibido VC, Denny RL, Boutin SR, Hautea R, Orf JH, Young ND (1994) DNA marker analysis of loci underlying resistance to soybean cyst nematode (Heterodera glycines Ichinohe). Crop Sci 34:240–346

    Google Scholar 

  • Concibido VC, Lange DA, Denny RL, Orf JH, Young ND (1997) Genome mapping of soybean cyst nematode resistance genes in ’Peking’, PI90763, and PI88788 using DNA markers. Crop Sci 37:258–264

    Google Scholar 

  • Dong K, Opperman CH (1997) Genetic analysis of parasitism in the soybean cyst nematode Heterodera glycines. Genetics 146:1311–1318

    Google Scholar 

  • Edgley ML, Riddle DL (1993) The nematode Caenorhabditis elegans. In: O’Brien SJ (ed) Genetic maps: locus maps of complex genomes, 6th edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 3.281–3.318

    Google Scholar 

  • Endo BY (1992) Cellular responses to infection. In: Riggs RD, Wrather JA (eds) Biology and management of the soybean cyst nematode. APS Press, St. Paul, pp 37–49

    Google Scholar 

  • Fishman L, Kelly AJ, Morgan E, Willis JH (2001) A genetic map in the Mimulus guttatus species complex reveals transmission ratio distortion due to heterospecific interactions. Genetics 159:1701–1716

    CAS  PubMed  Google Scholar 

  • Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS (2001) Identification of putative parasitism genes expressed in the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Mol Plant-Microbe Interact 14:1247–1254

    Google Scholar 

  • Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS (2003) The parasitome of the phytonematode Heterodera glycines. Mol Plant Microbe Interact 16:720–726

    Google Scholar 

  • Goldstein P, Triantaphyllou AC (1980) The ultrastructure of sperm development in the plant-parasitic nematode Meloidogyne hapla. J Ultrastr Res 71:143–153

    Google Scholar 

  • Habu Y, Fuka-Tanaka S, Hisatomi Y, Iida S (1997) Amplified restriction fragment length polymorphism mRNA fingerprinting using a single restriction enzyme that recognizes a 4-bp sequence. Biochem Biophys Res Comm 234:516–521

    Article  CAS  PubMed  Google Scholar 

  • Hulbert SH, Ilott TW, Legg EJ, Lincoln SE, Lander ES, Michelmore RW (1988) Genetic analysis of the fungus, Bremia lactucae, using restriction fragment length polymorphisms. Genetics 120:947–958

    CAS  PubMed  Google Scholar 

  • Keim P, Schupp JM, Travis SE, Clayton K, Zhu T, Shi L, Ferreira A, Webb DM (1997) A high density genetic map of soybean based upon AFLP markers. Crop Sci 37:537–543

    CAS  Google Scholar 

  • Knapp SJ, Holloway JL, Bridges WC (1995) Mapping dominant markers using F2 matings. Theor Appl Genet 91:74–81

    Google Scholar 

  • Koenning SR, Barker KR (1998) Survey of Heterodera glycines races and other plant-parasitic nematodes on soybean in North Carolina. Suppl J Nematol 30:569–576

    Google Scholar 

  • Lambert KN, Bekal S, Domier LL, Niblack TL, Noel GR, Smyth C (2005) Selection of Heterodera glycines chorismate mutase-1 alleles on nematode-resistant soybean. Mol Plant Microbe Interact (in press)

  • Lange K, Boehnke M (1982) How many polymorphic genes will it take to span the human genome? Am J Hum Genet 34:842–845

    CAS  PubMed  Google Scholar 

  • Lapp NA, Triantaphyllou AC (1972) Relative DNA content and chromosomal relationships of some Meloidogyne,Heterodera, and Meloidodera spp. (Nematoda: Heteroderidae). J Nematol 4:287–291

    Google Scholar 

  • Liu BH (1998) Statistical genomics: linkage, mapping, and QTL analysis. CRC Press, Boca Raton

    Google Scholar 

  • Marra M et al (1999) A map for sequence analysis of the Arabidopsis thaliana genome. Nat Genet 22:265–270

    Google Scholar 

  • McCarter JP, Mitrevia M, Clifton SW, Bird DM, Waterston RH (2003) Nematode gene sequences: update for December 2003. J Nematol 35:465–469

    CAS  Google Scholar 

  • McReynolds LA, DeSimone SM, Williams SA (1986) Cloning and comparison of repeated DNA sequences from the human filarial parasite Brugia malayi and the animal parasite Brugia pahangi. Proc Natl Acad Sci USA 83:797–801

    Google Scholar 

  • Mudge J, Gregan PB, Kenworthy JP, Orf JH, Young ND (1997) Two microsatellite markers that flank the major soybean cyst nematode resistance locus. Crop Sci 37:1611–1615

    Google Scholar 

  • Niblack TL, Tylka GL, Riggs RD (2004) Nematode pathogens of soybean. In: Boerma HR, Specht JE (eds) Soybeans: improvement, production, and uses, 3rd edn. American Society of Agronomy, Madison, pp 821–851

    Google Scholar 

  • Opperman CH, Bird DM (1998) The soybean cyst nematode, Heterodera glycines: a genetic model system for the study of plant-parasitic nematodes. Curr Opin Plant Biol 1:342–346

    Google Scholar 

  • Rouppe van der Voort JNAM, van Enckevort ELJG, Pijnacker LP, Helder J, Gommers FJ, Bakker J (1996) Chromosome number of the potato cyst nematode Globodera rostochiensis. Fundam Appl Nematol 19:369–374

    Google Scholar 

  • Rouppe van der Voort JNAM, van Zandvoort P, van Eck HJ, Folkertsma RT, Hutten RB, Draaistra J, Gommers FJ, Jacobsen E, Helder J, Bakker J (1997) Use of allele specificity of comigrating AFLP markers to align genetic maps from different potato genotypes. Mol Gen Genet 255:438–447

    Article  PubMed  Google Scholar 

  • Rouppe van der Voort JNAM, van Eck HJ, van Zandvoort PM, Overmars H, Helder J, Bakker J (1999) Linkage analysis by genotyping of sibling populations: a genetic map for the potato cyst nematode constructed using “pseudo-F2” mapping strategy. Mol Gen Genet 261:1021–1031

    Google Scholar 

  • Saal B, Wricke G (2002) Clustering of amplified fragment length polymorphism markers in a linkage map of rye. Plant Breed 121:117–123

    Google Scholar 

  • Shoemaker RC, Specht JE (1995) Integration of the soybean molecular and classical genetic linkage group. Crop Sci 35:436–446

    Google Scholar 

  • Tanksley SD et al (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160

    CAS  PubMed  Google Scholar 

  • Tanksley SD, Young ND, Paterson AH, Bonierbale MW (1989) RFLP mapping in plant breeding: new tools for an old science. Biotechnology 7:257–264

    CAS  Google Scholar 

  • The C. elegans Sequencing Consortium (1998) Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282:2012–2018

    Google Scholar 

  • Van Ooijen JW, Voorrips RE (2001) JoinMap 3.0, software for the calculation of genetic linkage maps. Plant Research International, Wageningen

  • 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

    CAS  PubMed  Google Scholar 

  • Vuylsteke M, Mank R, Antonise R, Bastiaans E, Senior ML, Stuber CW, Melchinger AE, Lübberstedt T, Xia XC, Stam P, Zabeau M (1999) Two high-density AFLP linkage maps of Zea mays L.: analysis of distribution of AFLP markers. Theor Appl Genet 99:921–935

    Article  CAS  Google Scholar 

  • Wang X, Allen R, Ding X, Goellner M, Maier T, de Boer J, Baum TJ, Hussey RS, Davis EL (2001) Signal peptide-selection of cDNA cloned directly from esophageal gland cells of the soybean cyst nematode Heterodera glycines. Mol Plant Microbe Interact 14:536–544

    Google Scholar 

  • Waterston RH et al (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–562

    Article  PubMed  Google Scholar 

  • Waugh R, McLean K, Flavell AJ, Pearce SR, Kumar A, Thomas BBT, Powel W (1997) Genetic distribution of Bare-1-like retrotransposable elements in the barley genome revealed by sequence-specific amplification polymorphism (S-SAP). Mol Gen Genet 253:687–694

    Article  CAS  PubMed  Google Scholar 

  • Webb DM, Baltazar BM, Rao-Arelli AP, Schupp J, Clayton K, Keim P, Beavis WD (1995) Genetic mapping of soybean cyst nematode race 3 resistance loci in the soybean PI437654. Theor Appl Genet 91:574–581

    Google Scholar 

  • Weisemann JM, Mattews BF, Devine TE (1992) Molecular markers located proximal to the soybean cyst nematode resistance gene, Rhg4. Theor Appl Genet 85:136–138

    Google Scholar 

  • Williams SA, Lizotte-Waniewski MR, Foster J, Guiliano D, Daub J, Scott AL, Slatko B, Blaxter ML (2000) The filarial genome project: analysis of the nuclear, mitochondrial and endosymbiont genomes of Brugia malayi. Int J Parasitol 30:411–419

    Article  CAS  PubMed  Google Scholar 

  • Workneh F, Tylka GL, Yang XB, Faghihi J, Ferris JM (1999) Regional assessment of soybean brown stem rot, Phytophthora sojae, and Heterodera glycines using area-frame sampling: prevalence and effects of tillage. Phytopathology 89:204–211

    Google Scholar 

  • Wrather JA, Anderson TR, Arsyad DM, Tan Y, Ploper LD, Porta-Puglia A, Ram HH, Yorinori JT (2001) Soybean disease loss estimates for the top ten soybean-producing countries in 1998. Can J Plant Pathol 23:115–121

    Google Scholar 

  • Young LD (1992) Epiphytology and life cycle. In: Riggs RD, Wrather JA (eds) Biology and management of the soybean cyst nematode. APS Press, St. Paul, pp 27–36

    Google Scholar 

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Acknowledgements

This study was supported by grants from the Illinois Soybean Program Operating Board (ISPOB), the North Central Soybean Research Program (NCSRP), the Soybean Disease Biotechnology Center (SDBC) at the University of Illinois at Urbana-Champaign, and the United Soybean Board (USB). Linkage analyses were conducted in the Computer Laboratory of Dr. T.R. Rocheford, Professor of Crop Sciences at the University of Illinois at Urbana-Champaign. We also wish to thank K. Colgrove, A. Colgrove, R. Heinz, and K. Hajsaid for their technical support. Mention of a trademark or proprietary product does not constitute a guarantee or warranty of the product by the USDA and does not imply its approval to the exclusion of other products that may also be suitable. This work has been carried out in compliance with the current laws governing genetic experimentation in the USA

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Authors and Affiliations

  1. Department of Crop Sciences, University of Illinois at Urbana-Champaign, 1102 South Goodwin Avenue, Urbana, IL, 61801, USA

    N. Atibalentja, S. Bekal, L. L. Domier, T. L. Niblack, G. R. Noel & K. N. Lambert

  2. USDA, ARS, 1102 South Goodwin Avenue, Urbana, IL, 61801, USA

    L. L. Domier & G. R. Noel

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  1. N. Atibalentja
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  2. S. Bekal
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  3. L. L. Domier
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  4. T. L. Niblack
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  5. G. R. Noel
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  6. K. N. Lambert
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Correspondence to K. N. Lambert.

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Communicated by W.R. McCombie

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Atibalentja, N., Bekal, S., Domier, L.L. et al. A genetic linkage map of the soybean cyst nematode Heterodera glycines. Mol Genet Genomics 273, 273–281 (2005). https://doi.org/10.1007/s00438-005-1125-x

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  • DOI: https://doi.org/10.1007/s00438-005-1125-x

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