Skip to main content
Genetics logoLink to Genetics
. 2004 Apr;166(4):1751–1759. doi: 10.1534/genetics.166.4.1751

Mating within the meiotic tetrad and the maintenance of genomic heterozygosity.

Michael E Hood 1, Janis Antonovics 1
PMCID: PMC1470809  PMID: 15126395

Abstract

Mating among the products of a single meiosis (automixis or meiotic parthenogenesis) is found in diverse groups of plant, animal, and fungal taxa. Restoration of the diploid stage is often strictly controlled and brings together products separated at the first meiotic division. Despite apparent similarities to diploid selfing, the theoretical prediction is that heterozygosity should be maintained on all chromosomes when it is linked to the centromeres and thus also segregates at the first meiotic division. Using the fungus Microbotryum, we directly test this prediction by linear tetrad analysis. The patterns of meiotic segregation for chromosome size variation (electrophoretic karyotypes) and PCR products (AFLP procedures) were determined for Microbotryum lineages native to North America and Europe. Our data reveal a surprisingly dynamic genome that is rich in heterozygosity and where size-dimorphic autosomes are common. The genetic variation agrees with the prediction of centromere-linked heterozygosity. This was observed to the greatest extent in the lineage of Microbotryum native to North America where there was consistent first-division segregation and independent assortment of multiple linkage groups. The data also show properties that distinguish the fungal sex chromosomes from the autosomes in both lineages of Microbotryum. We describe a scenario where the mating system of automixis with first-division restitution is the result of feedback mechanisms to control exposure of genetic load.

Full Text

The Full Text of this article is available as a PDF (187.3 KB).

Selected References

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

  1. Antonovics Janis, Hood Michael, Partain Jessica. The ecology and genetics of a host shift: microbotryum as a model system. Am Nat. 2002 Oct;160 (Suppl 4):S40–S53. doi: 10.1086/342143. [DOI] [PubMed] [Google Scholar]
  2. Belshaw Robert, Quicke Donald L. J. The cytogenetics of thelytoky in a predominantly asexual parasitoid wasp with covert sex. Genome. 2003 Feb;46(1):170–173. doi: 10.1139/g02-112. [DOI] [PubMed] [Google Scholar]
  3. Beukeboom L. W., Pijnacker L. P. Automictic parthenogenesis in the parasitoid Venturia canescens (Hymenoptera: Ichneumonidae) revisited. Genome. 2000 Dec;43(6):939–944. doi: 10.1139/g00-061. [DOI] [PubMed] [Google Scholar]
  4. Charlesworth B., Langley C. H. The population genetics of Drosophila transposable elements. Annu Rev Genet. 1989;23:251–287. doi: 10.1146/annurev.ge.23.120189.001343. [DOI] [PubMed] [Google Scholar]
  5. Delmotte F, Bucheli E, Shykoff JA. Host and parasite population structure in a natural plant-pathogen system . Heredity (Edinb) 1999 Apr;82(Pt 3):300–308. doi: 10.1038/sj.hdy.6884850. [DOI] [PubMed] [Google Scholar]
  6. Freeman Angela B., Duong K. Kellye, Shi Tie-Liu, Hughes Carolyn F., Perlin Michael H. Isolates of Microbotryum violaceum from North American host species are phylogenetically distinct from their European host-derived counterparts. Mol Phylogenet Evol. 2002 May;23(2):158–170. doi: 10.1016/S1055-7903(02)00003-9. [DOI] [PubMed] [Google Scholar]
  7. Gallegos A., Jacobson D. J., Raju N. B., Skupski M. P., Natvig D. O. Suppressed recombination and a pairing anomaly on the mating-type chromosome of Neurospora tetrasperma. Genetics. 2000 Feb;154(2):623–633. doi: 10.1093/genetics/154.2.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Garber E. D., Ruddat M. Transmission genetics of Microbotryum violaceum (Ustilago violacea): a case history. Adv Appl Microbiol. 2002;51:107–127. doi: 10.1016/s0065-2164(02)51003-0. [DOI] [PubMed] [Google Scholar]
  9. Hood M. E., Antonovics J. Intratetrad mating, heterozygosity, and the maintenance of deleterious alleles in Microbotryum violaceum (=Ustilago violacea). Heredity (Edinb) 2000 Sep;85(Pt 3):231–241. doi: 10.1046/j.1365-2540.2000.00748.x. [DOI] [PubMed] [Google Scholar]
  10. Hood M. E., Antonovics J. Intratetrad mating, heterozygosity, and the maintenance of deleterious alleles in Microbotryum violaceum (=Ustilago violacea). Heredity (Edinb) 2000 Sep;85(Pt 3):231–241. doi: 10.1046/j.1365-2540.2000.00748.x. [DOI] [PubMed] [Google Scholar]
  11. Hood M. E. Dynamics of multiple infection and within-host competition by the anther-smut pathogen. Am Nat. 2003 Jun 27;162(1):122–133. doi: 10.1086/375539. [DOI] [PubMed] [Google Scholar]
  12. Hood Michael E., Antonovics Janis, Heishman Hilary. Karyotypic similarity identifies multiple host-shifts of a pathogenic fungus in natural populations. Infect Genet Evol. 2003 Feb;2(3):167–172. doi: 10.1016/s1567-1348(02)00154-5. [DOI] [PubMed] [Google Scholar]
  13. Hood Michael E. Dimorphic mating-type chromosomes in the fungus Microbotryum violaceum. Genetics. 2002 Feb;160(2):457–461. doi: 10.1093/genetics/160.2.457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kerrigan R. W., Royer J. C., Baller L. M., Kohli Y., Horgen P. A., Anderson J. B. Meiotic behavior and linkage relationships in the secondarily homothallic fungus Agaricus bisporus. Genetics. 1993 Feb;133(2):225–236. doi: 10.1093/genetics/133.2.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kistler H. C., Miao V. P. New modes of genetic change in filamentous fungi. Annu Rev Phytopathol. 1992;30:131–153. doi: 10.1146/annurev.py.30.090192.001023. [DOI] [PubMed] [Google Scholar]
  16. Laport Ginna G., Levine Bruce L., Stadtmauer Edward A., Schuster Stephen J., Luger Selina M., Grupp Stephan, Bunin Nancy, Strobl Frank J., Cotte Julio, Zheng Zhaohui. Adoptive transfer of costimulated T cells induces lymphocytosis in patients with relapsed/refractory non-Hodgkin lymphoma following CD34+-selected hematopoietic cell transplantation. Blood. 2003 May 22;102(6):2004–2013. doi: 10.1182/blood-2003-01-0095. [DOI] [PubMed] [Google Scholar]
  17. Lonnig Wolf-Ekkehard, Saedler Heinz. Chromosome rearrangements and transposable elements. Annu Rev Genet. 2002 Jun 11;36:389–410. doi: 10.1146/annurev.genet.36.040202.092802. [DOI] [PubMed] [Google Scholar]
  18. Marescalchi O., Scali V. Chromosomal and NOR patterns in the polyclonal stick insect Bacillus atticus atticus (Insecta; Phasmatodea). Genome. 1997 Apr;40(2):261–270. doi: 10.1139/g97-037. [DOI] [PubMed] [Google Scholar]
  19. McCluskey K., Russell B. W., Mills D. Electrophoretic karyotyping without the need for generating protoplasts. Curr Genet. 1990 Nov;18(4):385–386. doi: 10.1007/BF00318221. [DOI] [PubMed] [Google Scholar]
  20. Merino S. T., Nelson M. A., Jacobson D. J., Natvig D. O. Pseudohomothallism and evolution of the mating-type chromosome in Neurospora tetrasperma. Genetics. 1996 Jun;143(2):789–799. doi: 10.1093/genetics/143.2.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Powell A. J., Jacobson D. J., Natvig D. O. Allelic diversity at the het-c locus in Neurospora tetrasperma confirms outcrossing in nature and reveals an evolutionary dilemma for pseudohomothallic ascomycetes. J Mol Evol. 2001 Jan;52(1):94–102. doi: 10.1007/s002390010138. [DOI] [PubMed] [Google Scholar]
  22. Saenz G. S., Stam J. G., Jacobson D. J., Natvig D. O. Heteroallelism at the het-c locus contributes to sexual dysfunction in outcrossed strains of Neurospora tetrasperma. Fungal Genet Biol. 2001 Nov;34(2):123–129. doi: 10.1006/fgbi.2001.1294. [DOI] [PubMed] [Google Scholar]
  23. Summerbell R. C., Castle A. J., Horgen P. A., Anderson J. B. Inheritance of restriction fragment length polymorphisms in Agaricus brunnescens. Genetics. 1989 Oct;123(2):293–300. doi: 10.1093/genetics/123.2.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Van Putten Wilhelmus F., Biere Arjen, Van Damme Jos M. M. Intraspecific competition and mating between fungal strains of the anther smut Microbotryum violaceum from the host plants Silene latifolia and S. dioica. Evolution. 2003 Apr;57(4):766–776. [PubMed] [Google Scholar]
  25. Zakharov I. A. Nekotorye zakonomernosti raspolozheniia genov v khromosomakh éukariot. Postanovka problemy i analiz nesluchainosti raspolozheniia lokusov tipa sparivaniia u gribov. Genetika. 1986 Nov;22(11):2620–2624. [PubMed] [Google Scholar]
  26. Zolan M. E. Chromosome-length polymorphism in fungi. Microbiol Rev. 1995 Dec;59(4):686–698. doi: 10.1128/mr.59.4.686-698.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES