Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2002 Nov;162(3):1401–1413. doi: 10.1093/genetics/162.3.1401

Patterns of diversity and recombination along chromosome 1 of maize (Zea mays ssp. mays L.).

Maud I Tenaillon 1, Mark C Sawkins 1, Lorinda K Anderson 1, Stephen M Stack 1, John Doebley 1, Brandon S Gaut 1
PMCID: PMC1462344  PMID: 12454083

Abstract

We investigate the interplay between genetic diversity and recombination in maize (Zea mays ssp. mays). Genetic diversity was measured in three types of markers: single-nucleotide polymorphisms, indels, and microsatellites. All three were examined in a sample of previously published DNA sequences from 21 loci on maize chromosome 1. Small indels (1-5 bp) were numerous and far more common than large indels. Furthermore, large indels (>100 bp) were infrequent in the population sample, suggesting they are slightly deleterious. The 21 loci also contained 47 microsatellites, of which 33 were polymorphic. Diversity in SNPs, indels, and microsatellites was compared to two measures of recombination: C (=4Nc) estimated from DNA sequence data and R based on a quantitative recombination nodule map of maize synaptonemal complex 1. SNP diversity was correlated with C (r = 0.65; P = 0.007) but not with R (r = -0.10; P = 0.69). Given the lack of correlation between R and SNP diversity, the correlation between SNP diversity and C may be driven by demography. In contrast to SNP diversity, microsatellite diversity was correlated with R (r = 0.45; P = 0.004) but not C (r = -0.025; P = 0.55). The correlation could arise if recombination is mutagenic for microsatellites, or it may be consistent with background selection that is apparent only in this class of rapidly evolving markers.

Full Text

The Full Text of this article is available as a PDF (150.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Andolfatto P., Przeworski M. Regions of lower crossing over harbor more rare variants in African populations of Drosophila melanogaster. Genetics. 2001 Jun;158(2):657–665. doi: 10.1093/genetics/158.2.657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bachtrog D., Agis M., Imhof M., Schlötterer C. Microsatellite variability differs between dinucleotide repeat motifs-evidence from Drosophila melanogaster. Mol Biol Evol. 2000 Sep;17(9):1277–1285. doi: 10.1093/oxfordjournals.molbev.a026411. [DOI] [PubMed] [Google Scholar]
  3. Barakat A., Carels N., Bernardi G. The distribution of genes in the genomes of Gramineae. Proc Natl Acad Sci U S A. 1997 Jun 24;94(13):6857–6861. doi: 10.1073/pnas.94.13.6857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baudry E., Kerdelhué C., Innan H., Stephan W. Species and recombination effects on DNA variability in the tomato genus. Genetics. 2001 Aug;158(4):1725–1735. doi: 10.1093/genetics/158.4.1725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Begun D. J., Aquadro C. F. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature. 1992 Apr 9;356(6369):519–520. doi: 10.1038/356519a0. [DOI] [PubMed] [Google Scholar]
  6. Bennetzen J. L. Transposable element contributions to plant gene and genome evolution. Plant Mol Biol. 2000 Jan;42(1):251–269. [PubMed] [Google Scholar]
  7. Bergman C. M., Kreitman M. Analysis of conserved noncoding DNA in Drosophila reveals similar constraints in intergenic and intronic sequences. Genome Res. 2001 Aug;11(8):1335–1345. doi: 10.1101/gr.178701. [DOI] [PubMed] [Google Scholar]
  8. Braverman J. M., Hudson R. R., Kaplan N. L., Langley C. H., Stephan W. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics. 1995 Jun;140(2):783–796. doi: 10.1093/genetics/140.2.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chakraborty R., Kimmel M., Stivers D. N., Davison L. J., Deka R. Relative mutation rates at di-, tri-, and tetranucleotide microsatellite loci. Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):1041–1046. doi: 10.1073/pnas.94.3.1041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Charlesworth B., Morgan M. T., Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993 Aug;134(4):1289–1303. doi: 10.1093/genetics/134.4.1289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Charlesworth B. The effect of background selection against deleterious mutations on weakly selected, linked variants. Genet Res. 1994 Jun;63(3):213–227. doi: 10.1017/s0016672300032365. [DOI] [PubMed] [Google Scholar]
  12. Cheng Z., Presting G. G., Buell C. R., Wing R. A., Jiang J. High-resolution pachytene chromosome mapping of bacterial artificial chromosomes anchored by genetic markers reveals the centromere location and the distribution of genetic recombination along chromosome 10 of rice. Genetics. 2001 Apr;157(4):1749–1757. doi: 10.1093/genetics/157.4.1749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Davis G. L., McMullen M. D., Baysdorfer C., Musket T., Grant D., Staebell M., Xu G., Polacco M., Koster L., Melia-Hancock S. A maize map standard with sequenced core markers, grass genome reference points and 932 expressed sequence tagged sites (ESTs) in a 1736-locus map. Genetics. 1999 Jul;152(3):1137–1172. doi: 10.1093/genetics/152.3.1137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dooner H. K. Genetic Fine Structure of the BRONZE Locus in Maize. Genetics. 1986 Aug;113(4):1021–1036. doi: 10.1093/genetics/113.4.1021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dvorák J., Luo M. C., Yang Z. L. Restriction fragment length polymorphism and divergence in the genomic regions of high and low recombination in self-fertilizing and cross-fertilizing aegilops species. Genetics. 1998 Jan;148(1):423–434. doi: 10.1093/genetics/148.1.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fearnhead P., Donnelly P. Estimating recombination rates from population genetic data. Genetics. 2001 Nov;159(3):1299–1318. doi: 10.1093/genetics/159.3.1299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Fernando Vázquez J., Pérez T., Albornoz J., Domínguez A. Estimation of microsatellite mutation rates in Drosophila melanogaster. Genet Res. 2000 Dec;76(3):323–326. doi: 10.1017/s0016672300004791. [DOI] [PubMed] [Google Scholar]
  18. Frisse L., Hudson R. R., Bartoszewicz A., Wall J. D., Donfack J., Di Rienzo A. Gene conversion and different population histories may explain the contrast between polymorphism and linkage disequilibrium levels. Am J Hum Genet. 2001 Aug 29;69(4):831–843. doi: 10.1086/323612. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Fu Huihua, Zheng Zhenwei, Dooner Hugo K. Recombination rates between adjacent genic and retrotransposon regions in maize vary by 2 orders of magnitude. Proc Natl Acad Sci U S A. 2002 Jan 15;99(2):1082–1087. doi: 10.1073/pnas.022635499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gaut B. S., Clegg M. T. Molecular evolution of the Adh1 locus in the genus Zea. Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):5095–5099. doi: 10.1073/pnas.90.11.5095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Gaut B. S., Morton B. R., McCaig B. C., Clegg M. T. Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10274–10279. doi: 10.1073/pnas.93.19.10274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gill K. S., Gill B. S., Endo T. R., Taylor T. Identification and high-density mapping of gene-rich regions in chromosome group 1 of wheat. Genetics. 1996 Dec;144(4):1883–1891. doi: 10.1093/genetics/144.4.1883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Glenn T. C., Stephan W., Dessauer H. C., Braun M. J. Allelic diversity in alligator microsatellite loci is negatively correlated with GC content of flanking sequences and evolutionary conservation of PCR amplifiability. Mol Biol Evol. 1996 Oct;13(8):1151–1154. doi: 10.1093/oxfordjournals.molbev.a025678. [DOI] [PubMed] [Google Scholar]
  24. Gu X., Li W. H. The size distribution of insertions and deletions in human and rodent pseudogenes suggests the logarithmic gap penalty for sequence alignment. J Mol Evol. 1995 Apr;40(4):464–473. doi: 10.1007/BF00164032. [DOI] [PubMed] [Google Scholar]
  25. Hey J., Wakeley J. A coalescent estimator of the population recombination rate. Genetics. 1997 Mar;145(3):833–846. doi: 10.1093/genetics/145.3.833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hudson R. R. Estimating the recombination parameter of a finite population model without selection. Genet Res. 1987 Dec;50(3):245–250. doi: 10.1017/s0016672300023776. [DOI] [PubMed] [Google Scholar]
  27. Hudson R. R. Two-locus sampling distributions and their application. Genetics. 2001 Dec;159(4):1805–1817. doi: 10.1093/genetics/159.4.1805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Iltis H. H. From teosinte to maize: the catastrophic sexual transmutation. Science. 1983 Nov 25;222(4626):886–894. doi: 10.1126/science.222.4626.886. [DOI] [PubMed] [Google Scholar]
  29. Innan H., Terauchi R., Miyashita N. T. Microsatellite polymorphism in natural populations of the wild plant Arabidopsis thaliana. Genetics. 1997 Aug;146(4):1441–1452. doi: 10.1093/genetics/146.4.1441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Jones G. H. The control of chiasma distribution. Symp Soc Exp Biol. 1984;38:293–320. [PubMed] [Google Scholar]
  31. Kaplan N. L., Hudson R. R., Langley C. H. The "hitchhiking effect" revisited. Genetics. 1989 Dec;123(4):887–899. doi: 10.1093/genetics/123.4.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Kliman R. M., Andolfatto P., Coyne J. A., Depaulis F., Kreitman M., Berry A. J., McCarter J., Wakeley J., Hey J. The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics. 2000 Dec;156(4):1913–1931. doi: 10.1093/genetics/156.4.1913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kraft T., Säll T., Magnusson-Rading I., Nilsson N. O., Halldén C. Positive correlation between recombination rates and levels of genetic variation in natural populations of sea beet (Beta vulgaris subsp. maritima). Genetics. 1998 Nov;150(3):1239–1244. doi: 10.1093/genetics/150.3.1239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Künzel G., Korzun L., Meister A. Cytologically integrated physical restriction fragment length polymorphism maps for the barley genome based on translocation breakpoints. Genetics. 2000 Jan;154(1):397–412. doi: 10.1093/genetics/154.1.397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Machado Carlos A., Kliman Richard M., Markert Jeffrey A., Hey Jody. Inferring the history of speciation from multilocus DNA sequence data: the case of Drosophila pseudoobscura and close relatives. Mol Biol Evol. 2002 Apr;19(4):472–488. doi: 10.1093/oxfordjournals.molbev.a004103. [DOI] [PubMed] [Google Scholar]
  36. Nachman M. W., Bauer V. L., Crowell S. L., Aquadro C. F. DNA variability and recombination rates at X-linked loci in humans. Genetics. 1998 Nov;150(3):1133–1141. doi: 10.1093/genetics/150.3.1133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Nei M. Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3321–3323. doi: 10.1073/pnas.70.12.3321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Nurminsky D. I. Genes in sweeping competition. Cell Mol Life Sci. 2001 Jan;58(1):125–134. doi: 10.1007/PL00000772. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Okagaki R. J., Weil C. F. Analysis of recombination sites within the maize waxy locus. Genetics. 1997 Oct;147(2):815–821. doi: 10.1093/genetics/147.2.815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Payseur B. A., Nachman M. W. Microsatellite variation and recombination rate in the human genome. Genetics. 2000 Nov;156(3):1285–1298. doi: 10.1093/genetics/156.3.1285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Przeworski M., Hudson R. R., Di Rienzo A. Adjusting the focus on human variation. Trends Genet. 2000 Jul;16(7):296–302. doi: 10.1016/s0168-9525(00)02030-8. [DOI] [PubMed] [Google Scholar]
  42. Przeworski Molly. The signature of positive selection at randomly chosen loci. Genetics. 2002 Mar;160(3):1179–1189. doi: 10.1093/genetics/160.3.1179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Reeves A. MicroMeasure: a new computer program for the collection and analysis of cytogenetic data. Genome. 2001 Jun;44(3):439–443. [PubMed] [Google Scholar]
  44. Remington D. L., Thornsberry J. M., Matsuoka Y., Wilson L. M., Whitt S. R., Doebley J., Kresovich S., Goodman M. M., Buckler E. S., 4th Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci U S A. 2001 Sep 18;98(20):11479–11484. doi: 10.1073/pnas.201394398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Richard G. F., Pâques F. Mini- and microsatellite expansions: the recombination connection. EMBO Rep. 2000 Aug;1(2):122–126. doi: 10.1093/embo-reports/kvd031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Rozas J., Rozas R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics. 1999 Feb;15(2):174–175. doi: 10.1093/bioinformatics/15.2.174. [DOI] [PubMed] [Google Scholar]
  47. SanMiguel P., Tikhonov A., Jin Y. K., Motchoulskaia N., Zakharov D., Melake-Berhan A., Springer P. S., Edwards K. J., Lee M., Avramova Z. Nested retrotransposons in the intergenic regions of the maize genome. Science. 1996 Nov 1;274(5288):765–768. doi: 10.1126/science.274.5288.765. [DOI] [PubMed] [Google Scholar]
  48. Schlötterer C., Ritter R., Harr B., Brem G. High mutation rate of a long microsatellite allele in Drosophila melanogaster provides evidence for allele-specific mutation rates. Mol Biol Evol. 1998 Oct;15(10):1269–1274. doi: 10.1093/oxfordjournals.molbev.a025855. [DOI] [PubMed] [Google Scholar]
  49. Schlötterer C., Tautz D. Slippage synthesis of simple sequence DNA. Nucleic Acids Res. 1992 Jan 25;20(2):211–215. doi: 10.1093/nar/20.2.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Schug M. D., Hutter C. M., Wetterstrand K. A., Gaudette M. S., Mackay T. F., Aquadro C. F. The mutation rates of di-, tri- and tetranucleotide repeats in Drosophila melanogaster. Mol Biol Evol. 1998 Dec;15(12):1751–1760. doi: 10.1093/oxfordjournals.molbev.a025901. [DOI] [PubMed] [Google Scholar]
  51. Schug M. D., Mackay T. F., Aquadro C. F. Low mutation rates of microsatellite loci in Drosophila melanogaster. Nat Genet. 1997 Jan;15(1):99–102. doi: 10.1038/ng0197-99. [DOI] [PubMed] [Google Scholar]
  52. Sherman J. D., Stack S. M. Two-dimensional spreads of synaptonemal complexes from solanaceous plants. VI. High-resolution recombination nodule map for tomato (Lycopersicon esculentum). Genetics. 1995 Oct;141(2):683–708. doi: 10.1093/genetics/141.2.683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Slatkin M. Hitchhiking and associative overdominance at a microsatellite locus. Mol Biol Evol. 1995 May;12(3):473–480. doi: 10.1093/oxfordjournals.molbev.a040222. [DOI] [PubMed] [Google Scholar]
  54. Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
  55. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989 Nov;123(3):585–595. doi: 10.1093/genetics/123.3.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Tenaillon M. I., Sawkins M. C., Long A. D., Gaut R. L., Doebley J. F., Gaut B. S. Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc Natl Acad Sci U S A. 2001 Jul 24;98(16):9161–9166. doi: 10.1073/pnas.151244298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Thornsberry J. M., Goodman M. M., Doebley J., Kresovich S., Nielsen D., Buckler E. S., 4th Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet. 2001 Jul;28(3):286–289. doi: 10.1038/90135. [DOI] [PubMed] [Google Scholar]
  58. Udupa S. M., Baum M. High mutation rate and mutational bias at (TAA)n microsatellite loci in chickpea (Cicer arietinum L.). Mol Genet Genomics. 2001 Aug;265(6):1097–1103. doi: 10.1007/s004380100508. [DOI] [PubMed] [Google Scholar]
  59. Vigouroux Yves, Jaqueth Jennifer S., Matsuoka Yoshihiro, Smith Oscar S., Beavis William D., Smith J. Stephen C., Doebley John. Rate and pattern of mutation at microsatellite loci in maize. Mol Biol Evol. 2002 Aug;19(8):1251–1260. doi: 10.1093/oxfordjournals.molbev.a004186. [DOI] [PubMed] [Google Scholar]
  60. Wall J. D. A comparison of estimators of the population recombination rate. Mol Biol Evol. 2000 Jan;17(1):156–163. doi: 10.1093/oxfordjournals.molbev.a026228. [DOI] [PubMed] [Google Scholar]
  61. Wang R. L., Stec A., Hey J., Lukens L., Doebley J. The limits of selection during maize domestication. Nature. 1999 Mar 18;398(6724):236–239. doi: 10.1038/18435. [DOI] [PubMed] [Google Scholar]
  62. Wang R. L., Wakeley J., Hey J. Gene flow and natural selection in the origin of Drosophila pseudoobscura and close relatives. Genetics. 1997 Nov;147(3):1091–1106. doi: 10.1093/genetics/147.3.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Weber J. L., Wong C. Mutation of human short tandem repeats. Hum Mol Genet. 1993 Aug;2(8):1123–1128. doi: 10.1093/hmg/2.8.1123. [DOI] [PubMed] [Google Scholar]
  64. Wiehe T. The effect of selective sweeps on the variance of the allele distribution of a linked multiallele locus: hitchhiking of microsatellites. Theor Popul Biol. 1998 Jun;53(3):272–283. doi: 10.1006/tpbi.1997.1346. [DOI] [PubMed] [Google Scholar]
  65. Xu X., Peng M., Fang Z. The direction of microsatellite mutations is dependent upon allele length. Nat Genet. 2000 Apr;24(4):396–399. doi: 10.1038/74238. [DOI] [PubMed] [Google Scholar]
  66. Zhang Liqing, Peek Andrew S., Dunams Detiger, Gaut Brandon S. Population genetics of duplicated disease-defense genes, hm1 and hm2, in maize (Zea mays ssp. mays L.) and its wild ancestor (Zea mays ssp. parviglumis). Genetics. 2002 Oct;162(2):851–860. doi: 10.1093/genetics/162.2.851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Zickler D., Kleckner N. Meiotic chromosomes: integrating structure and function. Annu Rev Genet. 1999;33:603–754. doi: 10.1146/annurev.genet.33.1.603. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES