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Genome-wide analysis of the frequency and distribution of crossovers at male and female meiosis in Sinapis alba L. (white mustard)

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Abstract

We present the first genetic linkage maps of Sinapis alba (white mustard) and a rigorous analysis of sex effects on the frequency and distribution of crossovers at meiosis in this species. Sex-averaged maps representing recombination in two highly heterozygous parents were aligned to give a consensus map consisting of 382 loci defined by restriction fragment length polymorphisms and arranged in 12 linkage groups with no unlinked markers. The loci were distributed in a near-random manner across the genome, and there was little evidence of segregation distortion. From these dense maps, a subset of spaced informative markers was used to establish recombination frequencies assayed separately in male and female gametes and derived from two distinct genetic backgrounds. Analyses of 746 gametes indicated that recombination frequencies were greater in male gametes, with the greatest differences near the ends of linkage groups. Genetic background had a lesser effect on recombination frequencies, with no discernible pattern in the distribution of such differences. The possible causes of sex differences in recombination frequency and the implications for plant breeding are discussed.

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References

  • Benito C, Romero MP, Henriques-Gil N, Llorente F, Figueiras AM (1996) Sex influence on recombination frequency in Secale cereale L. Theor Appl Genet 93:926–931

    Article  Google Scholar 

  • Bennett MD, Smith JB, Heslop-Harrison JS (1982) Nuclear DNA amounts in angiosperms. Proc R Soc London Ser B 216:179–199

    CAS  Google Scholar 

  • Bohuon EJR, Keith DJ, Parkin IAP, Sharpe AG, Lydiate DJ (1996) Alignment of the conserved C genomes of Brassica oleracea and Brassica napus. Theor Appl Genet 93:833–839

    Article  CAS  Google Scholar 

  • Broman KW, Murray JC, Sheffield VC, White RL, Weber JL (1998) Comprehensive human genetic maps: individual and sex-specific variations in recombination. Am J Hum Genet 63:861–869

    Article  CAS  PubMed  Google Scholar 

  • Busso CS, Liu CJ, Hash CT, Witcombe JR, Devos KM, de Wet JMJ, Gale MD (1995) Analysis of recombination rate in female and male gametogenesis in pearl millet (Pennisetum glaucum) using RFLP markers. Theor Appl Genet 90:242–246

    Article  Google Scholar 

  • Delaney DE, Nasuda S, Endo TR, Gill BS, Hulbert SH (1995) Cytologically based physical maps of the group 3 chromosomes of wheat. Theor Appl Genet 91:780–782

    CAS  Google Scholar 

  • Dietrich W, Katz H, Lincoln SE, Shin HS, Friedman J, Dracopoli NC, Lander ES (1992) A genetic map of the mouse suitable for typing intraspecific crosses. Genetics 131:423–447

    CAS  PubMed  Google Scholar 

  • Dietrich W, Miller J, Steen R, Merchant MA, Damron-Boles D, Husain Z, Dredge R, Daly MJ, Ingalls KA, O’Connor TJ, Evans CA, DeAngelis MM, Levinson DM, Kruglyak L, Goodman N, Copeland NG, Jenkins NA, Hawkins TL, Stein L, Page DC, Lander ES (1996) A comprehensive genetic map of the mouse genome. Nature 380:149–152

    Article  CAS  PubMed  Google Scholar 

  • Fisher RA (1935) The logic of inductive inference. J R Soc Statist Ser A 98:39–54

    Google Scholar 

  • Groenen MAM, Crooijmans RPMA, Veenendaal A, Cheng HH, Siwek M, van der Poel JJ (1998) A comprehensive microsatellite linkage map of the chicken genome. Genomics 49:265–274

    Article  CAS  PubMed  Google Scholar 

  • Hohmann U, Graner A, Endo TR, Gill BS, Herrmann RG (1995) Comparison of wheat physical maps with barley linkage maps for group 7 chromosomes. Theor Appl Genet 91:618–626

    CAS  Google Scholar 

  • Jones LE, Rybka K, Lukaszewski AJ (2002) The effect of a deficiency and a deletion on recombination in chromosome 1BL in wheat. Theor Appl Genet 104:1204–1208

    Article  CAS  PubMed  Google Scholar 

  • Kelly AL, Sharpe AG, Nixon JH, Evans EJ, Lydiate DJ (1997) Indistinguishable patterns of recombination resulting from male and female meioses in Brassica napus (oilseed rape). Genome 40:49–56

    CAS  Google Scholar 

  • Kong A, Gudbjartsson DF, Sainz J, Jonsdottir GM, Gudjonsson SA, Richardsson B, Sigurdardottir S, Barnard J, Hallbeck B, Masson G, Shlien A, Palsson ST, Frigge ML, Thorgeirsson TE, Gulcher JR, Stefansson K (2002) A high-resolution recombination map of the human genome. Nat Genet 31:241–247

    CAS  PubMed  Google Scholar 

  • Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Google Scholar 

  • Lagercrantz U, Lydiate DJ (1995) RFLP mapping in Brassica nigra indicates differing recombination rates in male and female meioses. Genome 38:255–264

    CAS  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Lincoln SE, Newburg L, Green P (1987) mapmaker: an interactive package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  CAS  PubMed  Google Scholar 

  • Lashermes P, Combes MC, Prakash NS, Trouslot P, Lorieux M, Charrier A (2001) Genetic linkage map of Coffea canephora: effect of segregation distortion and analysis of recombination rate in male and female meioses. Genome 44:589–596

    Article  CAS  PubMed  Google Scholar 

  • Lydiate DJ, Ikeda H, Hopwood DA (1986) A 2.6-kb sequence of Streptomyces coelicolor A3(2) which functions as a transposable element. Mol Gen Genet 203:79–88

    Article  CAS  PubMed  Google Scholar 

  • Maliepaard C, Alston FH, van Arkel G, Brown LM, Chevreau E, Dunemann F, Evans KM, Gardiner S, Guilford P, van Heusden AW, Janse J, Laurens F, Lynn JR, Manganaris AG, den Nijs APM, Periam N, Rikkerink E, Roche P, Ryder C, Sansavini S, Schmidt H, Tertarini S, Verhaegh JJ, Vrielink-van Ginkel M, King, GJ (1998) Aligning male and female linkage maps of apple (Malus pumila Mill) using multi-allelic markers. Theor Appl Genet 97:60–73

    Article  CAS  Google Scholar 

  • Morgan TH (1912) Complete linkage in the second chromosome of the male of Drosophila. Science 36:719–720

    Google Scholar 

  • Morgan TH (1914) No crossing over in the male of Drosophila of genes in the second and third pairs of chromosomes. Biol Bull 26:195–204

    Google Scholar 

  • Nelson MN (2000) Genetic analysis of Sinapis alba. PhD thesis, University of East Anglia, UK

  • Olsson G (1974) Continuous selection for seed number per pod and oil content in white mustard. Hereditas 77:197–204

    CAS  PubMed  Google Scholar 

  • Ooijen JW van, Sandbrink JM, Vrielink M, Verkerk R, Zabel P, Lindhout P (1994) An RFLP linkage map of Lycopersicon peruvianum. Theor Appl Genet 89:1007–1013

    CAS  Google Scholar 

  • Parkin IAP, Sharpe AG, Keith DJ, Lydiate DJ (1995) Identification of the A and C genomes of amphidiploid Brassica napus (oilseed rape). Genome 38:1122–1131

    CAS  Google Scholar 

  • Plomion C, O’Malley DM (1996) Recombination rate differences for pollen parents and seed parents in Pinus pinaster. Heredity 77:341–350

    CAS  Google Scholar 

  • Pratt JW, Gibbons JD (1981) Concepts of nonparametric theory. Springer, Berlin Heidelberg New York, pp 318–336

    Google Scholar 

  • Rakow G, Potts D, Raney P, Katepa-Mupondwa F (2000). Designing oilseed crops for the Canadian dry prairie. In: 3rd Int Crop Sci Congr. Book of Abstracts, p 221, session 4C, poster no. 34. Hamburg, Germany

  • Rivard SR, Cappadocia M, Landry BS (1996) A comparison of RFLP maps based on anther culture derived, selfed, and hybrid progenies of Solanum chacoense. Genome 39:611–621

    CAS  Google Scholar 

  • Rockmill B, Roeder GS (1998) Telomere-mediated chromosome pairing during meiosis in budding yeast. Genes Dev 12:2574–2586

    CAS  PubMed  Google Scholar 

  • Sakamoto T, Danzmann RG, Gharbi K, Howard P, Ozaki A, Khoo SK, Woram RA, Okamoto N, Ferguson MM, Holm L-E, Guyomard R, Hoyheim B (2000) A microsatellite linkage map of rainbow trout (Oncorhynchus mykiss) characterized by large sex-specific differences in recombination rates. Genetics 155:1331–1345

    CAS  PubMed  Google Scholar 

  • Samollow PB, Kammerer CM, Mahaney SM, Schneider JL, Westenberger SJ, VandeBerg JL, Robinson ES (2004) First-generation linkage map of the gray, short-tailed opossum, Monodelphis domestica, reveals genome-wide reduction in female recombination rates. Genetics 166:307–329

    Article  CAS  PubMed  Google Scholar 

  • Schnable PS, Hsia A-N, Nikolau BJ (1998) Genetic recombination in plants. Curr Opin Plant Biol 1:123–129

    Article  CAS  PubMed  Google Scholar 

  • Sewell MM, Sherman BK, Neale DB (1999) A consensus map for loblolly pine (Pinus taeda L) I Construction and integration of individual linkage maps from two outbred three-generation pedigrees. Genetics 151:321–330

    CAS  PubMed  Google Scholar 

  • Sharpe AG, Parkin IAP, Keith DJ, Lydiate DJ (1995) Frequent nonreciprocal translocations in the amphidiploid genome of oilseed rape (Brassica napus). Genome 38:1112–1121

    CAS  Google Scholar 

  • Singer A, Perlman H, Yan HY, Walker C, Corley-Smith G, Brandhorst B, Postlethwait J (2002) Sex-specific recombination rates in zebrafish (Danio rerio). Genetics 160:649–657

    CAS  PubMed  Google Scholar 

  • Thormann CE, Ferreira ME, Camargo LEA, Tivang JG, Osborn TC (1994) Comparison of RFLP and RAPD markers to estimating genetic-relationships within and among cruciferous species. Theor Appl Genet 88:973–980

    Article  Google Scholar 

  • Trelles-Sticken E, Dresser ME, Scherthan H (2000) Meiotic telomere protein Ndj1p is required for meiosis-specific telomere distribution, bouquet formation and efficient homologue pairing. J Cell Biol 151:95–106

    Article  CAS  PubMed  Google Scholar 

  • Vicente MC de, 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

    Article  Google Scholar 

  • Warwick SI, Black LD (1991) Molecular systematics of Brassica and allied genera (Subtribe Brassicinae, Brassiceae) - chloroplast genome and cytodeme congruence. Theor Appl Genet 82:81–92

    Article  CAS  Google Scholar 

  • Weber DF, Schneerman MC, Bowen B, Arbuckle J, Nunes R, Sowinski S, Brown E, Falzone J, Gizzarelli P (1999) Comparative recombination distances among varieties of Zea mays L. In: 41st Maize Genet Conf. Abstr no. 41, poster no.143. Lake Geneva, Wis.

  • Zetka M-C, Rose AM (1990) Sex-related differences in crossing over in Caenorhabditis elegans. Genetics 126:355–363

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Dr. Gerhard Rakow and Mr. Todd Olsen for formative discussions and for developing plant materials. The work was supported by Agriculture and Agri-Food Canada and by the Federal-Provincial AgriFood Innovation Fund. M.N.N. was supported by a John Innes Foundation studentship.

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Correspondence to Matthew N. Nelson.

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Communicated by C. Möllers

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Nelson, M.N., Nixon, J. & Lydiate, D.J. Genome-wide analysis of the frequency and distribution of crossovers at male and female meiosis in Sinapis alba L. (white mustard). Theor Appl Genet 111, 31–43 (2005). https://doi.org/10.1007/s00122-005-1961-4

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  • DOI: https://doi.org/10.1007/s00122-005-1961-4

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