Skip to main content
SpringerLink
Log in

The Meiotic Drive System on Maize Abnormal Chromosome 10 Contains Few Essential Genes

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

In maize, a distal portion of abnormal chromosome 10 (Ab10) causes the meiotic drive of itself as well as many unlinked heterochromatic regions known as knobs. The Ab10 drive system, which encodes trans- as well as cis-acting components, occupies a large region of chromosome 10L equivalent to ∼3% of the genome. Here we describe five new structural mutations of Ab10 (five deletions and a duplication) that arose from a screen for meiotic drive mutants. The high frequency of breakage events, detected both genetically and cytologically, suggest that the chromosome may be especially unstable. Very large deletions within the drive system are female-transmissible and plants homozygous for deficiencies lacking much of this interval can be grown to maturity. The data suggest that few genes required for normal growth and development lie within the portion of Ab10 responsible for meiotic drive. These and other published data suggest that meiotic drive systems tend to evolve in gene-sparse or otherwise information-poor regions of the genome where they are less likely to negatively affect individual fitness.

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

Similar content being viewed by others

References

  • Ananiev, E.V., R.L. Phillips & H.W. Rines, 1998. A knob-associated tandem repeat in maize capable of forming fold-back DNA segments: are chromosome knobs megatransposons? Proc. Nat. Acad. Sci. USA 95: 10785–10790.

    Google Scholar 

  • Arabidopsis Genome Initiative, 2000. Analysis of the genome sequence of the flowering plant Arabidopisis thaliana. Nature 408: 796–815.

    Google Scholar 

  • Ardlie, K.G., 1998. Putting the brake on drive: meiotic drive of t haplotypes in natural populations of mice. Trends Genet. 14: 189–193.

    Google Scholar 

  • Bass, H.W., W.F. Marshall, J.W. Sedat, D.A. Agard & W.Z. Cande, 1997. Telomeres cluster de novo before the initiation of synapsis: a three-dimensional spatial analysis of telomere positions before and during meiotic prophase. J. Cell Biol. 137: 5–18.

    Google Scholar 

  • Buckler, E.S.I., T.L. Phelps-Durr, C.S.K. Buckler, R.K. Dawe, J.F. Doebley & T.P. Holtsford, 1999. Meiotic drive of chromosomal knobs reshaped the maize genome. Genetics 153: 415–426.

    Google Scholar 

  • Cameron, D. & R. Moav, 1957. Inheritance in Nicotiana tabacum XXVI. Pollen killer, an alien genetic locus inducing abortion of microspores not carrying it. Genetics 42: 327–355.

    Google Scholar 

  • Carlson, W., 1988. The cytogenetics of corn, pp. 259–343 in Corn and Corn Improvement, edited by G. Sprague & J. Dudley. Academic Press, New York.

    Google Scholar 

  • Chao, S., J. Gardiner, S. Melia-Hancock & E.H. Coe Jr., 1996. Physical and genetic mapping of chromosome 9S in maize using mutations with terminal deficiencies. Genetics 143: 1785–1794.

    Google Scholar 

  • Davis, G., M. McMullen, C. Baysdorfer, T. Musket, D. Grant, M. Staebell, G. Xu, M. Polacco, L. Koster, S. Melia-Hancock, K. Houchins, S. Chao & E.H. Coe Jr., 1999. 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 152: 1137–1172.

    Google Scholar 

  • Dawe, R.K. & W.Z. Cande, 1996. Induction of centromeric activity in maize by suppressor of meiotic drive 1. Proc. Nat. Acad. Sci. USA 93: 8512–8517.

    Google Scholar 

  • Dawe, R.K., J.W. Sedat, D.A. Agard & W.Z. Cande, 1994. Meiotic chromosome pairing in maize is associated with a novel chromatin organization. Cell 76: 901–912.

    Google Scholar 

  • Emmerling, M., 1959. Preferential segregation of structurally modified chromosomes in maize. Genetics 44: 625–645.

    Google Scholar 

  • Fluminhan, A. &T. Kameya, 1997. Involvement of knob heterochromatin in mitotic abnormalities in germinating seeds of maize. Genome 40: 91–98.

    Google Scholar 

  • Fluminhan, A., M. Aguiar-Perecin & J. Santos, 1996. Evidence for heterochromatin involvement in chromosome breakage in maize callus culture. Ann. Bot. 78: 73–81.

    Google Scholar 

  • Hiatt, E.N., E.K. Kentner & R.K. Dawe, 2002. Independently regulated neocentromere activity of two classes of tandem repeat arrays. Plant Cell 14: 407–420.

    Google Scholar 

  • Hu, J. & C. Quiros, 1991. Molecular and cytological evidence of deletions in alien chromosomes for two monosomic addition lines. Theor. Appl. Genet. 81: 221–226.

    Google Scholar 

  • International Human Genome Sequencing Consortium, 2001. Initial sequencing and analysis of the human genome. Nature 409: 860–921.

    Google Scholar 

  • John, U., C.L. & J. Timmis, 1991. A sequence specific to B chromosomes of Brachycome dichromosomatica. Genome 34: 739–744.

    Google Scholar 

  • Longley, A.E., 1945. Abnormal segregation during megasporogenesis in maize. Genetics 30: 100–113.

    Google Scholar 

  • Lyttle, T., 1991. Segregation distorters. Ann. Rev. Genet. 25: 511–557.

    Google Scholar 

  • Maguire, M., 1963. High transmission frequency of a Tripsacum chromosome in corn. Genetics 48: 1185–1194.

    Google Scholar 

  • Mascarenhas, J., 1989. The male gametophyte of flowering plants. Plant Cell 1: 657–664.

    Google Scholar 

  • McClintock, B., 1941a. The association of mutants with homozygous deficiencies in Zea mays. Genetics 25: 542–571.

    Google Scholar 

  • McClintock, B., 1941b. The stability of broken ends of chromosomes in Zea mays. Genetics 26: 234–282.

    Google Scholar 

  • McClintock, B., 1944. The relation of homozygous deficiencies to mutations and allelic series in maize. Genetics 29: 478–502.

    Google Scholar 

  • Miles, J., 1970. Influence of modified K10 chromosomes on preferential segregation and crossing over in Zea mays. PhD Thesis, University of Indiana, Bloomington.

    Google Scholar 

  • Nel, P., 1973. The modification of crossing over in maize by extraneous chromosomal elements. Theor. Appl. Genet. 43: 196–202.

    Google Scholar 

  • Östergren, G., 1945. Parasitic nature of extra fragment chromosomes. Bot. Notiser. 2: 157–163.

    Google Scholar 

  • Peacock, W.J., E.S. Dennis, M.M. Rhoades & A.J. Pryor, 1981. Highly repeated DNA sequence limited to knob heterochromatin in maize. Proc. Natl. Acad. Sci. USA 78: 4490–4494.

    Google Scholar 

  • Pryor, A., F. Faulkner, M.M. Rhoades & W.J. Peacock, 1980. Asynchronous replication of heterochromatin in maize. Proc. Nat. Acad. Sci. 77: 6705–6709.

    Google Scholar 

  • Rhoades, M.M., 1952. Preferential segregation in maize. pp. 66–80 in Heterosis, edited by J.W. Gowen. Iowa State College Press, Ames, IA.

    Google Scholar 

  • Rhoades, M.M. & E. Dempsey, 1953. Cytogenetic studies of deficient-duplicate chromosomes derived from inversion heterozygotes in maize. Am. J. Bot. 40: 405–424.

    Google Scholar 

  • Rhoades, M.M. & E. Dempsey, 1966. The effect of abnormal chromosome 10 on preferential segregation and crossing over in maize. Genetics 53: 989–1020.

    Google Scholar 

  • Rhoades, M.M. & E. Dempsey, 1985. Structural heterogeneity of chromosome 10 in races of maize and teosinte. pp. 1–18 in Plant Genetics, edited by M. Freeling. Alan R. Liss, New York.

  • Rhoades, M.M. & E. Dempsey, 1986. Evidence that the K10 knob is not responsible for preferential segregation and neocentromere activity. Maize Genet. Coop. Newslett. 60: 26–27.

    Google Scholar 

  • Rhoades, M.M. & E. Dempsey, 1989. Further studies on K10-I and K10-II. Maize Genet. Coop. Newslett. 63: 42–43.

    Google Scholar 

  • Rhoades, M.M. & H. Vilkomerson, 1942. On the anaphase movement of chromosomes. Proc. Natl. Acad. Sci. USA 28: 433–443.

    Google Scholar 

  • Robertson, D., 1968. Increased crossing over in chromosome 5 in the presence of abnormal chromosome 10. Maize Genet. Coop. Newslett. 42: 89.

    Google Scholar 

  • Robertson, D., P. Stinard & M. Maguire, 1994. Genetic evidence of Mutator-induced deletions in the short arm of chromosome 9 in maize. II. wd deletions. Genetics 136: 1143–1149.

    Google Scholar 

  • Silver, L.M., 1985. Mouse t haplotypes. Ann. Rev. Genet. 19: 179–208.

    Google Scholar 

  • Sokal, R.R. & F.J. Rohlf, 1969. Biometry: The Principles and Practice of Statistics in Biological Research. W.H. Freeman and Company, San Francisco, CA, pp. 575–585.

    Google Scholar 

  • Stadler, L.J. & H. Roman, 1948. The effect of X-rays upon mutation of the gene A in maize. Genetics 33: 273–303.

    Google Scholar 

  • Tsujimoto, H., T. Yamada & T. Sasakuma, 1997. Molecular structure of a wheat chromosome end healed after gametocidal gene-induced breakage. Proc. Nat. Acad. Sci. USA 94: 3140–3144.

    Google Scholar 

  • Walbot, V., 1992. Strategies for mutategenesis and gene cloning using transposon tagging and T-DNA insertional mutagenesis. Ann. Rev. Plant Phys. Mol. Biol. 43: 49–82.

    Google Scholar 

  • Werner, J., R. Kota, B. Gill & T. Endo, 1992. Distribution of telomeric repeats and their role in the healing of broken chromosome ends in wheat. Genome 35: 844–848.

    Google Scholar 

  • Yu, H.-G., E.N. Hiatt, A. Chan, M. Sweeney & R.K. Dawe, 1997. Neocentromere-mediated chromosome movement in maize. J. Cell Biol. 139: 831–840.

    Google Scholar 

  • Zimmering, S., L. Sandler & B. Nicoletti, 1970. Mechanisms of meiotic drive. Ann. Rev. Genet. 4: 409–436.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Genetics, University of Georgia, Athens, GA, 30602, USA

    Evelyn N. Hiatt & R. Kelly Dawe

  2. Department of Plant Biology, University of Georgia, Athens, GA, 30602, USA

    R. Kelly Dawe

Authors
  1. Evelyn N. Hiatt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Kelly Dawe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to R. Kelly Dawe.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hiatt, E.N., Kelly Dawe, R. The Meiotic Drive System on Maize Abnormal Chromosome 10 Contains Few Essential Genes. Genetica 117, 67–76 (2003). https://doi.org/10.1023/A:1022316716682

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1022316716682

Search

Navigation