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. 1999 Sep;153(1):415–426. doi: 10.1093/genetics/153.1.415

Meiotic drive of chromosomal knobs reshaped the maize genome.

E S Buckler 4th 1, T L Phelps-Durr 1, C S Buckler 1, R K Dawe 1, J F Doebley 1, T P Holtsford 1
PMCID: PMC1460728  PMID: 10471723

Abstract

Meiotic drive is the subversion of meiosis so that particular genes are preferentially transmitted to the progeny. Meiotic drive generally causes the preferential segregation of small regions of the genome; however, in maize we propose that meiotic drive is responsible for the evolution of large repetitive DNA arrays on all chromosomes. A maize meiotic drive locus found on an uncommon form of chromosome 10 [abnormal 10 (Ab10)] may be largely responsible for the evolution of heterochromatic chromosomal knobs, which can confer meiotic drive potential to every maize chromosome. Simulations were used to illustrate the dynamics of this meiotic drive model and suggest knobs might be deleterious in the absence of Ab10. Chromosomal knob data from maize's wild relatives (Zea mays ssp. parviglumis and mexicana) and phylogenetic comparisons demonstrated that the evolution of knob size, frequency, and chromosomal position agreed with the meiotic drive hypothesis. Knob chromosomal position was incompatible with the hypothesis that knob repetitive DNA is neutral or slightly deleterious to the genome. We also show that environmental factors and transposition may play a role in the evolution of knobs. Because knobs occur at multiple locations on all maize chromosomes, the combined effects of meiotic drive and genetic linkage may have reshaped genetic diversity throughout the maize genome in response to the presence of Ab10. Meiotic drive may be a major force of genome evolution, allowing revolutionary changes in genome structure and diversity over short evolutionary periods.

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Selected References

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  1. Alfenito M. R., Birchler J. A. Molecular characterization of a maize B chromosome centric sequence. Genetics. 1993 Oct;135(2):589–597. doi: 10.1093/genetics/135.2.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ananiev E. V., Phillips R. L., Rines H. W. A knob-associated tandem repeat in maize capable of forming fold-back DNA segments: are chromosome knobs megatransposons? Proc Natl Acad Sci U S A. 1998 Sep 1;95(18):10785–10790. doi: 10.1073/pnas.95.18.10785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ananiev E. V., Phillips R. L., Rines H. W. Complex structure of knob DNA on maize chromosome 9. Retrotransposon invasion into heterochromatin. Genetics. 1998 Aug;149(4):2025–2037. doi: 10.1093/genetics/149.4.2025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Buckler E. S., 4th, Holtsford T. P. Zea systematics: ribosomal ITS evidence. Mol Biol Evol. 1996 Apr;13(4):612–622. doi: 10.1093/oxfordjournals.molbev.a025621. [DOI] [PubMed] [Google Scholar]
  5. Burr B., Burr F. A., Matz E. C., Romero-Severson J. Pinning down loose ends: mapping telomeres and factors affecting their length. Plant Cell. 1992 Aug;4(8):953–960. doi: 10.1105/tpc.4.8.953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dawe R. K., Cande W. Z. Induction of centromeric activity in maize by suppressor of meiotic drive 1. Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8512–8517. doi: 10.1073/pnas.93.16.8512. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fluminhan A., Kameya T. Involvement of knob heterochromatin in mitotic abnormalities in germinating aged seeds of maize. Genome. 1997 Feb;40(1):91–98. doi: 10.1139/g97-012. [DOI] [PubMed] [Google Scholar]
  8. Kikudome G Y. Studies on the Phenomenon of Preferential Segregation in Maize. Genetics. 1959 Sep;44(5):815–831. doi: 10.1093/genetics/44.5.815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Lin Y. R., Schertz K. F., Paterson A. H. Comparative analysis of QTLs affecting plant height and maturity across the Poaceae, in reference to an interspecific sorghum population. Genetics. 1995 Sep;141(1):391–411. doi: 10.1093/genetics/141.1.391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Longley A E. Abnormal Segregation during Megasporogenesis in Maize. Genetics. 1945 Jan;30(1):100–113. doi: 10.1093/genetics/30.1.100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lyttle T. W. Segregation distorters. Annu Rev Genet. 1991;25:511–557. doi: 10.1146/annurev.ge.25.120191.002455. [DOI] [PubMed] [Google Scholar]
  12. McClintock B. CHROMOSOME MORPHOLOGY IN ZEA MAYS. Science. 1929 Jun 14;69(1798):629–629. doi: 10.1126/science.69.1798.629. [DOI] [PubMed] [Google Scholar]
  13. Pagel M., Johnstone R. A. Variation across species in the size of the nuclear genome supports the junk-DNA explanation for the C-value paradox. Proc Biol Sci. 1992 Aug 22;249(1325):119–124. doi: 10.1098/rspb.1992.0093. [DOI] [PubMed] [Google Scholar]
  14. Peacock W. J., Dennis E. S., Rhoades M. M., Pryor A. J. Highly repeated DNA sequence limited to knob heterochromatin in maize. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4490–4494. doi: 10.1073/pnas.78.7.4490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Pryor A., Faulkner K., Rhoades M. M., Peacock W. J. Asynchronous replication of heterochromatin in maize. Proc Natl Acad Sci U S A. 1980 Nov;77(11):6705–6709. doi: 10.1073/pnas.77.11.6705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Purvis A., Rambaut A. Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Comput Appl Biosci. 1995 Jun;11(3):247–251. doi: 10.1093/bioinformatics/11.3.247. [DOI] [PubMed] [Google Scholar]
  17. Rhoades M M. Preferential Segregation in Maize. Genetics. 1942 Jul;27(4):395–407. doi: 10.1093/genetics/27.4.395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Rhoades M. M., Dempsey E. On the mechanism of chromatin loss induced by the B chromosome of maize. Genetics. 1972 May;71(1):73–96. doi: 10.1093/genetics/71.1.73. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rhoades M. M., Dempsey E. The Effect of Abnormal Chromosome 10 on Preferential Segregation and Crossing over in Maize. Genetics. 1966 May;53(5):989–1020. doi: 10.1093/genetics/53.5.989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Stephan W. Quantitative variation and chromosomal location of satellite DNAs. Genet Res. 1987 Aug;50(1):41–52. doi: 10.1017/s0016672300023326. [DOI] [PubMed] [Google Scholar]
  21. Stephan W. Recombination and the evolution of satellite DNA. Genet Res. 1986 Jun;47(3):167–174. doi: 10.1017/s0016672300023089. [DOI] [PubMed] [Google Scholar]
  22. Yu H. G., Hiatt E. N., Chan A., Sweeney M., Dawe R. K. Neocentromere-mediated chromosome movement in maize. J Cell Biol. 1997 Nov 17;139(4):831–840. doi: 10.1083/jcb.139.4.831. [DOI] [PMC free article] [PubMed] [Google Scholar]

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