Skip to main content
SpringerLink
Log in

Factors affecting polymorphism at microsatellite loci in bread wheat [Triticum aestivum (L.) Thell]: effects of mutation processes and physical distance from the centromere

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

Abstract

The effects of factors known to influence the level of polymorphism at microsatellite loci were studied using 99 markers and seven lines of bread wheat. Mutational factors as well as indirect selective events shape diversity at these loci. Theory predicts that the selection of favorable alleles should reduce polymorphism at neutral neighboring loci in genomic areas with low recombination rates. In wheat, local recombination rate is positively correlated with physical distance from the centromere. Seventy four loci among the 99 used could be physically located on the chromosome. We studied how the following affected the diversity among a set of inbred lines: the length of the alleles, the motif (CA versus CT), the structure of the loci (perfect versus imperfect) and the chromosomal position of the loci. For each locus, we determined whether the polymorphism observed at a locus was compatible with the Stepwise Mutation Model (SMM) or the Two-Phase Model (TPM). Both the mutation rate and the compatibility with the SMM or the TPM were shown to be variable between loci. Wheat microsatellite loci were found to be more variable when segregating alleles were perfect and had long motifs (composed of many repetitions). Diversity observed at 19 loci was not compatible with the SMM. Loci located in distal regions, with presumably high recombination rates, had longer allele sizes and were more polymorphic than loci located in proximal regions. We conclude that both mutation factors and indirect selective events vary according to the local recombination rate and therefore jointly influence the level of polymorphism at microsatellite loci in wheat.

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

Fig. 1

Similar content being viewed by others

References

  • Akhunov ED, Goodyear JA, Geng S, Qi L, Echalier B, Gill BS, Lazo G, Chao S, Anderson OD, Linkiewicz AM, Dubcovsky J, La Rota M, Sorrells ME, Miftahudin, Zhang D, Nguyen HT, Gustafson PJ, Khwaja Hossain VK, Kianian SF, Peng J, Lapitan NLV, Gonzalez-Hernandez JL, Anderson JA, Choi DW, Close TJ, Dilbirligi M, Gill KS, Walker-Simmons KM, Steber C, McGuire PE, Qualset CO, Dvorak J (2003) The organization and rate of evolution of wheat genomes are correlated with recombination rates along chromosome arms. Genome Res 13:753–763

    Article  CAS  PubMed  Google Scholar 

  • Baudry E, Kerdelhue C, Innan H, Stephan W (2001) Species and recombination effects on DNA variability in the tomato genus. Genetics 158:1725–1735

    CAS  PubMed  Google Scholar 

  • Begun DJ, Aquadro CF (1992) Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356:519–520

    CAS  PubMed  Google Scholar 

  • Biagetti M, Vitellozzi F, Ceoloni C (1999) Physical mapping of wheat-Aegilops longissima breakpoints in mildew-resistant recombinant lines using FISH with highly repeated and low-copy DNA probes. Genome 42:1013–1019

    Article  CAS  Google Scholar 

  • Boyko EV, Gill KS, Mickelson-Young L, Nasuda S, Raupp WJ, Ziegle JN, Singh J, Hassawi DS, Fritz AK, Namuth D, Lapitan NLV, Gill BS (1999) A high-density genetic linkage map of Aegilops tauschii, the D-genome progenitor of bread wheat. Theor Appl Genet 99:16–26

    CAS  Google Scholar 

  • Brinkmann B, Klintschar M, Neuhuber F, Huhne J, Rolf B (1998) Mutation rate in human microsatellites: influence of the structure and length of the tandem repeat. Am J Hum Genet 62:1408–1415

    CAS  PubMed  Google Scholar 

  • Cabrera A, Martin A, Barro F (2002) In-situ comparative mapping (ISCM) of Glu-1 loci in Triticum and Hordeum. Chrom Res 10:49–54

    CAS  PubMed  Google Scholar 

  • Chakraborty R, Kimmel M, Stivers DN, Davison LJ, Deka R (1997) Relative mutation rates at di-, tri- and tetra-nucleotides microsatellite loci. Proc Natl Acad Sci USA 94:1041–1046

    CAS  PubMed  Google Scholar 

  • Charlesworth B, Morgan MT, Charlesworth D (1993) The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289–1303

    CAS  PubMed  Google Scholar 

  • Chigagure NN, Baxter GD, Barker SC (2000) Microsatellite loci of the cattle tick Boophilus microplus (Acari: Ixodidae). Exp Appl Acarology 24:951–956

    Article  CAS  Google Scholar 

  • Christiansen MJ, Andersen SB, Ortiz R (2002) Diversity changes in an intensively bred wheat germplasm during the 20th century. Mol Breed 9:1–11

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Delaney DE, Nasuda S, Endo TR, Gill BS, Hulbert SH (1995b) Cytologically based physical maps of the group-2 chromosomes of wheat. Theor Appl Genet 91:568 573

    CAS  Google Scholar 

  • Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91:3166–3170

    PubMed  Google Scholar 

  • Donini P, Law JR, Koebner RMD, Reeves JC, Cooke RJ (2000) Temporal trends in the diversity of UK wheat. Theor Appl Genet 100:912–917

    Article  Google Scholar 

  • Donnelly P, Tavaré S (1995) Coalescents and genealogical structure under neutrality. Annu Rev Genet 29:401–421

    Article  CAS  PubMed  Google Scholar 

  • Dvorak J, Luo M, Yang Z (1998a) Restriction fragment length polymorphism and divergence in the genomic regions of high and low recombination in self-fertilizing and cross-fertilizing Aegilops species. Genetics 148:423–434

    PubMed  Google Scholar 

  • Dvorak J,·Luo MC, Yang ZL, Zhang HB (1998b) The structure of the Aegilops tauschii genepool and the evolution of hexaploid wheat. Theor Appl Genet 97:657–670

    CAS  Google Scholar 

  • Ellegren H (1995) Mutation rates at porcine microsatellite loci. Mammal Genome 6:376–377

    CAS  Google Scholar 

  • Ellegren H (2000a) Heterogeneous mutation processes in human microsatellite DNA sequences. Nature Genet 24:400–402

    Article  CAS  PubMed  Google Scholar 

  • Endo TR, Gill BS (1996) The deletion stocks of common wheat. J Hered 87:295–307

    CAS  Google Scholar 

  • Ewens WJ (1972) The sampling theory of selectively neutral alleles. Theor Pop Biol 3:87–112

    CAS  Google Scholar 

  • Faris JD, Gill BS (2002) Genomic targeting and high-resolution mapping of the domestication gene Q in wheat. Genome 45:706–718

    Article  CAS  PubMed  Google Scholar 

  • Feldman MW, Kumm J, Pritchard J (1999) Mutation and migration in models of microsatellite evolution. In: Goldstein DB, Schlötterer C (eds) Microsatellite evolution: inferences from population data. Oxford University Press, Oxford, pp 98–115

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    CAS  PubMed  Google Scholar 

  • Gill KS, Gill BS, Endo TR (1993) A chromosome region-specific mapping strategy reveals gene-rich telomeric ends in wheat. Chromosoma 102:374–381

    CAS  Google Scholar 

  • Gill KS, Gill BS, Endo TR, Boyko EV (1996a) Identification and high-density mapping of gene-rich regions in chromosome group 5 of wheat. Genetics 143:1001–1012

    CAS  PubMed  Google Scholar 

  • Gill KS, Gill BS, Endo TR, Taylor T (1996b) Identification and high-density mapping of gene-rich regions in chromosome group 1 of wheat. Genetics 144:1883–1891

    CAS  PubMed  Google Scholar 

  • Hohmann U, Endo TR, Gill KS, Gill BS (1994) Comparison of genetic and physical maps of group-7 chromosomes from Triticum aestivum L. Mol Gen Genet 245:644–653

    CAS  PubMed  Google Scholar 

  • Huang XQ, Börner A, Röder M, Ganal MW (2002) Assessing genetic diversity of wheat (Triticum aestivum L.) germplasm using microsatellite markers. Theor Appl Genet 105:699–707

    CAS  Google Scholar 

  • Hudson RR (1990) Gene genealogies and the coalescent process. Oxford Surveys Evolution Biol 7:1–44

    Google Scholar 

  • Jankowski C, Nag K (2002) Most meiotic CAG repeat tract-length alterations in yeast are SPO11 dependent. Mol Gen Genet 267:64–70

    Article  CAS  Google Scholar 

  • Jarne P, Lagoda P (1996) Microsatellites: from molecules to populations and back. Trends Ecol Evol 11:424–429

    Article  Google Scholar 

  • Kauer M, Zangerl B, Dieringer D, Schlotterer C (2002) Chromosomal patterns of microsatellite variability contrast sharply in African and non-African populations of Drosophila melanogaster. Genetics 160:247–256

    CAS  PubMed  Google Scholar 

  • Kimura M, Otha T (1978) Stepwise mutation model and distribution of allelic frequencies in a finite population. Proc Natl Acad Sci USA 75:2868–2872

    CAS  PubMed  Google Scholar 

  • Kraft T, Sall T, Magnusson-Rading I, Nilsson NO, Hallden C (1998) Positive correlation between recombination rates and levels of genetic variation in natural populations of sea beet (Beta vulgaris subsp. maritima). Genetics 150:1239–1244

    CAS  PubMed  Google Scholar 

  • Kruglyak S, Durrett RT, Schug MD, Aquadro CF (1998) Equilibrium distributions of microsatellite repeat length resulting from a balance between slippage events and point mutations. Proc Natl Acad Sci USA 95:10774–10778

    Article  CAS  PubMed  Google Scholar 

  • Lercher MJ, Hurst LD (2002) Human SNP variability and mutation rate are higher in regions of high recombination. Trends Genet 18:337–340

    Article  CAS  PubMed  Google Scholar 

  • Li YC, Korol AB, Fahima T, Beiles A, Nevo E (2002) Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol Biol Evol 11:2453–2465

    Article  CAS  Google Scholar 

  • Lukaszewski AJ, Curtis CA (1993) Physical distribution of recombination in B-genome chromosomes of tetraploid wheat. Theor Appl Genet 85:121–127

    Google Scholar 

  • Marais G, Mouchiroud D, Duret L (2001) Does recombination improve selection on codon usage? Lessons from nematode and fly complete-genomes. Proc Natl Acad Sci USA 90:5688–5692

    Article  Google Scholar 

  • Marino CL, Nelson JC, Lu YH, Sorrells ME, Leroy P, Tuleen NA, Lopes CR, Hart GE (1996) Molecular genetic maps of the group-6 chromosomes of hexaploid wheat (Triticum aestivum L. em. Thell). Genome 3:359–366

    Google Scholar 

  • Maynard-Smith J, Haig D (1974) The hitchicking effect of a favourable gene. Genetic Res 23:23–35

    Google Scholar 

  • Michalakis Y, Veuille M (1996) Length variation of CAG/CAA trinucleotide repeats in natural populations of Drosophila melanogaster and its relation to the recombination rate. Genetics 143:1713–1725

    CAS  PubMed  Google Scholar 

  • Mickelson-Young L, Endo TR, Gill BS (1995) A cytological ladder-map of the wheat homeologous group-4 chromosomes. Theor Appl Genet 90:1007–1011

    CAS  Google Scholar 

  • Moran PA (1975) Wandering distributions and the electrophoretic profile. Theor Pop Biol 8:318–330

    CAS  Google Scholar 

  • Nachman MW, Bauer VL, Cromwell SL, Aquadro CF (1998) DNA variability and recombination rates at X-linked loci in humans. Genetics 150:1133–1141

    CAS  PubMed  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

  • Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10

    Google Scholar 

  • Nelson JC, Van Deynze AE, Autrique E, Sorrells ME, Lu YH, Nègre S, Bernard M, Leroy P (1995a) Molecular mapping of wheat. Homoeologous group 3. Genome 38:525–533

    CAS  Google Scholar 

  • Nelson JC, Sorrells ME, Van Deynze AE, Lu YH, Atkinson M, Bernard M, Leroy P, Faris JD, Anderson JA (1995b) Molecular mapping of wheat. Major genes and rearrangements in homoeologous groups 4, 5 and 7. Genetics 141:721–731

    CAS  PubMed  Google Scholar 

  • Nelson JC, Van Deynze AE, Autrique E, Sorrells ME, Lu YH, Merlino M, Atkinson M, Leroy P (1995c) Molecular mapping of wheat. Homoeologous group 2. Genome 38:516–524

    CAS  Google Scholar 

  • Nordborg M, Charlesworth B, Charlesworth D (1996) The effect of recombination on background selection. Genet Res 67:159–174

    CAS  PubMed  Google Scholar 

  • Pal C, Hurst RD (2003) Evidence for co-evolution and gene order and recombination rate. Nature Genet 33:392–395

    Article  CAS  PubMed  Google Scholar 

  • Payseur BA, Nachman MW (2000) Microsatellite variation and recombination rate in the human genome. Genetics 156:1285–1298

    CAS  PubMed  Google Scholar 

  • Przeworski M, Hudson RR, DiRienzo A (2000) Adjusting the focus on human variation. Trends Genet 16:296–302

    CAS  PubMed  Google Scholar 

  • Qi LL, Gill BS (2001) High-density physical maps reveal that the dominant male-sterile gene Ms3 is located in a genomic region of low recombination in wheat and is not amenable to map-based cloning. Theor Appl Genet 103:998–1006

    CAS  Google Scholar 

  • Röder MS, Korzun V, Wendehake K, Plaschke J, Tixier MH, Leroy P, Ganal MW (1998a) A microsatellite map of wheat. Genetics 149:2007–2023

    PubMed  Google Scholar 

  • Röder MS, Korzun V, Gill BS, Ganal MW (1998b) The physical mapping of microsatellite markers in wheat. Genome 41:278–283

    Article  Google Scholar 

  • Sarma RN, Fish L, Gill BS, Snape JW (2000) Physical characterization of the homoeologous Group-5 chromosomes of wheat in terms of rice linkage blocks, and physical mapping of some important genes. Genome 43:191–198

    Article  CAS  PubMed  Google Scholar 

  • SAS (1999) SAS/STAT user’s guide, version 8.1. Cary, North California

  • Schlötterer C, Ritter R, Harr B, Brem G (1998) High mutation rate of a long microsatellite allele in Drosophila melanogaster provides evidence for allele-specific mutation rates. Mol Biol Evol 15:1269–1274

    PubMed  Google Scholar 

  • Schlötterer C, Vogl C, Tautz D (1997) Polymorphism and locus-specific effects on polymorphism at microsatellite loci in natural Drosophila melanogaster populations. Genetics 146:309–320

    PubMed  Google Scholar 

  • Schug MD, Mackay TF, Aquadro CF (1997) Low mutation rates of microsatellite loci in Drosophila melanogaster. Nature Genet 15:99–102

    CAS  PubMed  Google Scholar 

  • Schug MD, Wetterstrand KA, Gaudette MS, Lim RH, Hutter CM, Aquadro CF (1998) The distribution and frequency of microsatellite loci in Drosophila melanogaster. Mol Ecol 7:57–70

    CAS  PubMed  Google Scholar 

  • Stephan W, Langley CH (1998) DNA polymorphism in Lycopersicon and crossing-over per physical length. Genetics 150:1585–1593

    CAS  PubMed  Google Scholar 

  • Tachida W, Iizuka M (1992) Persistence of repeated sequences that evolve by replication slippage. Genetics 131:471–478

    CAS  PubMed  Google Scholar 

  • Timmermans MCP, Prem DO, Messing J (1996) Characterization of a meiotic crossover in Maize identified by a restriction fragment length polymorphism-based method. Genetics 143:1771–1783

    CAS  PubMed  Google Scholar 

  • Thuillet AC, Bru D, David JL, Roumet P, Santoni S, Sourdille P, Bataillon T (2002) Direct estimation of mutation rate for ten microsatellite loci in durum wheat, Triticum turgidum (L.) Thell. ssp durum desf. Mol Biol Evol 19:122–125

    CAS  PubMed  Google Scholar 

  • Van Deynze AE, Dubcovsky J, Gill KS, Nelson JC, Sorrells ME, Dvorak J, Gill BS, Lagudah ES, McCouch SR, Appels R (1995) Molecular-genetic maps for group-1 chromosomes of Triticeae species and their relation to chromosomes in rice and oat. Genome 38:45–59

    Google Scholar 

  • Varshney RK, Prasad M, Roy JK, Roder MS, Balyan HS, Gupta PK (2001) Integrated physical maps of 2DL, 6 BS and 7DL carrying loci for grain protein content and pre-harvest sprouting tolerance in bread wheat. Cereal Res Commun 29:33–40

    CAS  Google Scholar 

  • Vigouroux Y, Jaqueth JS, Matsuoka Y, Smith OS, Beavis WD, Smith JS, Doebley J (2002) Rate and pattern of mutation at microsatellite loci in maize. Mol Biol Evol 19:1251–60

    CAS  PubMed  Google Scholar 

  • Weber JL, Wong C (1993) Mutation of human short tandem repeats. Human Mol Genet 2:1123–1128

    CAS  Google Scholar 

  • Weng Y, Lazar MD (2002) Comparison of homeologous group-6 short arm physical maps of wheat and barley reveals a similar distribution of recombinogenic and gene-rich regions. Theor Appl Genet 104:1078–1085

    Article  Google Scholar 

  • Wiehe T (1998) The effect of selective sweeps on the variance of the allele distribution of a linked multiallele locus: hitch-hiking of microsatellites. Theor Pop Biol 53:272–283

    Article  CAS  Google Scholar 

  • Wierdl M, Dominska M, Petes TD (1997) Microsatellite instability in yeast: dependence on the length of the microsatellite. Genetics 146:769–779

    CAS  PubMed  Google Scholar 

  • Xu X, Peng M, Fang Z (2000) The direction of microsatellite mutations is dependent upon allele length. Nature Genet 24:396–399

    CAS  PubMed  Google Scholar 

  • Zhang XY, Li CW,·Wang LF, Wang·HM, You GX, Dong YS (2002) An estimation of the minimum number of SSR alleles needed to reveal genetic relationships in wheat varieties. I. Information from large-scale planted varieties and cornerstone breeding parents in Chinese wheat improvement and production. Theor Appl Genet 106:112–117

    CAS  PubMed  Google Scholar 

  • Zhou WC, Kolb FL, Bai GH, Shaner G, Domier LL (2002) Genetic analysis of scab resistance QTL in wheat with microsatellite and AFLP markers. Genome 45:719–727

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Eduard Akhunov, Karyn Deal and Jan Dvorak for helpful comments on the paper. This work was supported by a grant from the Bureau des Ressources Génétiques.

Author information

Authors and Affiliations

  1. INRA-UMR Diversité et Génomes des Plantes Cultivées, Domaine de Melgueil, 34130, Mauguio, France

    A.-C. Thuillet, T. Bataillon & J. L. David

  2. Station d’Amélioration des Plantes Domaine de Crouël, INRA, Unité Génome, 63039, Clermont-Ferrand Cedex, France

    P. Sourdille

Authors
  1. A.-C. Thuillet
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. Bataillon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. Sourdille
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. L. David
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. L. David.

Additional information

Communicated by J. Dvorak

Rights and permissions

Reprints and permissions

About this article

Cite this article

Thuillet, AC., Bataillon, T., Sourdille, P. et al. Factors affecting polymorphism at microsatellite loci in bread wheat [Triticum aestivum (L.) Thell]: effects of mutation processes and physical distance from the centromere. Theor Appl Genet 108, 368–377 (2004). https://doi.org/10.1007/s00122-003-1443-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-003-1443-5

Keywords

Search

Navigation