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. 2003 Apr;163(4):1315–1325. doi: 10.1093/genetics/163.4.1315

Mitochondria are inherited from the MATa parent in crosses of the basidiomycete fungus Cryptococcus neoformans.

Zhun Yan 1, Jianping Xu 1
PMCID: PMC1462512  PMID: 12702677

Abstract

Previous studies demonstrated that mitochondrial DNA (mtDNA) was uniparentally transmitted in laboratory crosses of the pathogenic yeast Cryptococcus neoformans. To begin understanding the mechanisms, this study examined the potential role of the mating-type locus on mtDNA inheritance in C. neoformans. Using existing isogenic strains (JEC20 and JEC21) that differed only at the mating-type locus and a clinical strain (CDC46) that possessed a mitochondrial genotype different from JEC20 and JEC21, we constructed strains that differed only in mating type and mitochondrial genotype. These strains were then crossed to produce hyphae and sexual spores. Among the 206 single spores analyzed from six crosses, all but one inherited mtDNA from the MATa parents. Analyses of mating-type alleles and mtDNA genotypes of natural hybrids from clinical and natural samples were consistent with the hypothesis that mtDNA is inherited from the MATa parent in C. neoformans. To distinguish two potential mechanisms, we obtained a pair of isogenic strains with different mating-type alleles, mtDNA types, and auxotrophic markers. Diploid cells from mating between these two strains were selected and 29 independent colonies were genotyped. These cells did not go through the hyphal stage or the meiotic process. All 29 colonies contained mtDNA from the MATa parent. Because no filamentation, meiosis, or spore formation was involved in generating these diploid cells, our results suggest a selective elimination of mtDNA from the MATalpha parent soon after mating. To our knowledge, this is the first demonstration that mating type controls mtDNA inheritance in fungi.

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Selected References

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  1. Bertrand Helmut. ROLE OF MITOCHONDRIAL DNA IN THE SENESCENCE AND HYPOVIRULENCE OF FUNGI AND POTENTIAL FOR PLANT DISEASE CONTROL. Annu Rev Phytopathol. 2000;38(NaN):397–422. doi: 10.1146/annurev.phyto.38.1.397. [DOI] [PubMed] [Google Scholar]
  2. Birky C. W., Jr Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci U S A. 1995 Dec 5;92(25):11331–11338. doi: 10.1073/pnas.92.25.11331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boekhout T., Theelen B., Diaz M., Fell J. W., Hop W. C., Abeln E. C., Dromer F., Meyer W. Hybrid genotypes in the pathogenic yeast Cryptococcus neoformans. Microbiology. 2001 Apr;147(Pt 4):891–907. doi: 10.1099/00221287-147-4-891. [DOI] [PubMed] [Google Scholar]
  4. Boynton J. E., Harris E. H., Burkhart B. D., Lamerson P. M., Gillham N. W. Transmission of mitochondrial and chloroplast genomes in crosses of Chlamydomonas. Proc Natl Acad Sci U S A. 1987 Apr;84(8):2391–2395. doi: 10.1073/pnas.84.8.2391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Currie B. P., Freundlich L. F., Casadevall A. Restriction fragment length polymorphism analysis of Cryptococcus neoformans isolates from environmental (pigeon excreta) and clinical sources in New York City. J Clin Microbiol. 1994 May;32(5):1188–1192. doi: 10.1128/jcm.32.5.1188-1192.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Forche A., Xu J., Vilgalys R., Mitchell T. G. Development and characterization of a genetic linkage map of Cryptococcus neoformans var. neoformans using amplified fragment length polymorphisms and other markers. Fungal Genet Biol. 2000 Dec;31(3):189–203. doi: 10.1006/fgbi.2000.1240. [DOI] [PubMed] [Google Scholar]
  7. Franzot S. P., Salkin I. F., Casadevall A. Cryptococcus neoformans var. grubii: separate varietal status for Cryptococcus neoformans serotype A isolates. J Clin Microbiol. 1999 Mar;37(3):838–840. doi: 10.1128/jcm.37.3.838-840.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ikeda R., Shinoda T., Fukazawa Y., Kaufman L. Antigenic characterization of Cryptococcus neoformans serotypes and its application to serotyping of clinical isolates. J Clin Microbiol. 1982 Jul;16(1):22–29. doi: 10.1128/jcm.16.1.22-29.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kabasawa K., Itagaki H., Ikeda R., Shinoda T., Kagaya K., Fukazawa Y. Evaluation of a new method for identification of Cryptococcus neoformans which uses serologic tests aided by selected biological tests. J Clin Microbiol. 1991 Dec;29(12):2873–2876. doi: 10.1128/jcm.29.12.2873-2876.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kwon-Chung K. J., Bennett J. E., Rhodes J. C. Taxonomic studies on Filobasidiella species and their anamorphs. Antonie Van Leeuwenhoek. 1982;48(1):25–38. doi: 10.1007/BF00399484. [DOI] [PubMed] [Google Scholar]
  11. Kwon-Chung K. J., Edman J. C., Wickes B. L. Genetic association of mating types and virulence in Cryptococcus neoformans. Infect Immun. 1992 Feb;60(2):602–605. doi: 10.1128/iai.60.2.602-605.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kwon-Chung K. J. Morphogenesis of Filobasidiella neoformans, the sexual state of Cryptococcus neoformans. Mycologia. 1976 Jul-Aug;68(4):821–833. [PubMed] [Google Scholar]
  13. Lengeler K. B., Cox G. M., Heitman J. Serotype AD strains of Cryptococcus neoformans are diploid or aneuploid and are heterozygous at the mating-type locus. Infect Immun. 2001 Jan;69(1):115–122. doi: 10.1128/IAI.69.1.115-122.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. May G., Taylor J. W. Patterns of mating and mitochondrial DNA inheritance in the agaric Basidiomycete Coprinus cinereus. Genetics. 1988 Feb;118(2):213–220. doi: 10.1093/genetics/118.2.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Mirfakhrai M., Tanaka Y., Yanagisawa K. Evidence for mitochondrial DNA polymorphism and uniparental inheritance in the cellular slime mold Polysphondylium pallidum: effect of intraspecies mating on mitochondrial DNA transmission. Genetics. 1990 Mar;124(3):607–613. doi: 10.1093/genetics/124.3.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Monteiro-Vitorello C. B., Baidyaroy D., Bell J. A., Hausner G., Fulbright D. W., Bertrand H. A circular mitochondrial plasmid incites hypovirulence in some strains of Cryphonectria parasitica. Curr Genet. 2000 Apr;37(4):242–256. doi: 10.1007/s002940050526. [DOI] [PubMed] [Google Scholar]
  17. Sia R. A., Lengeler K. B., Heitman J. Diploid strains of the pathogenic basidiomycete Cryptococcus neoformans are thermally dimorphic. Fungal Genet Biol. 2000 Apr;29(3):153–163. doi: 10.1006/fgbi.2000.1192. [DOI] [PubMed] [Google Scholar]
  18. Wickes B. L., Mayorga M. E., Edman U., Edman J. C. Dimorphism and haploid fruiting in Cryptococcus neoformans: association with the alpha-mating type. Proc Natl Acad Sci U S A. 1996 Jul 9;93(14):7327–7331. doi: 10.1073/pnas.93.14.7327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Wilch G., Ward S., Castle A. Transmission of mitochondrial DNA in Ustilago violacea. Curr Genet. 1992 Aug;22(2):135–140. doi: 10.1007/BF00351473. [DOI] [PubMed] [Google Scholar]
  20. Xu J., Ali R. Y., Gregory D. A., Amick D., Lambert S. E., Yoell H. J., Vilgalys R. J., Mitchell T. G. Uniparental mitochondrial transmission in sexual crosses in Cryptococcus neoformans. Curr Microbiol. 2000 Apr;40(4):269–273. doi: 10.1007/s002849910053. [DOI] [PubMed] [Google Scholar]
  21. Xu J., Ramos A. R., Vilgalys R., Mitchell T. G. Clonal and spontaneous origins of fluconazole resistance in Candida albicans. J Clin Microbiol. 2000 Mar;38(3):1214–1220. doi: 10.1128/jcm.38.3.1214-1220.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Xu J., Vilgalys R., Mitchell T. G. Multiple gene genealogies reveal recent dispersion and hybridization in the human pathogenic fungus Cryptococcus neoformans. Mol Ecol. 2000 Oct;9(10):1471–1481. doi: 10.1046/j.1365-294x.2000.01021.x. [DOI] [PubMed] [Google Scholar]
  23. Xu Jianping. Estimating the spontaneous mutation rate of loss of sex in the human pathogenic fungus Cryptococcus neoformans. Genetics. 2002 Nov;162(3):1157–1167. doi: 10.1093/genetics/162.3.1157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Xu Jianping. Mitochondrial DNA polymorphisms in the human pathogenic fungus Cryptococcus neoformans. Curr Genet. 2002 Apr 3;41(1):43–47. doi: 10.1007/s00294-002-0282-2. [DOI] [PubMed] [Google Scholar]

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