Mycobiology

The Korean Society of Mycology (한국균학회)
권호 표지
DOI QR코드

DOI QR Code

Mechanisms of Uniparental Mitochondrial DNA Inheritance in Cryptococcus neoformans

  • Received : 2011.10.31
  • Accepted : 2011.11.01
  • Published : 2011.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

In contrast to the nuclear genome, the mitochondrial genome does not follow Mendelian laws of inheritance. The nuclear genome of meiotic progeny comes from the recombination of both parental genomes, whereas the meiotic progeny could inherit mitochondria from one, the other, or both parents. In fact, one fascinating phenomenon is that mitochondrial DNA in the majority of eukaryotes is inherited from only one particular parent. Typically, such unidirectional and uniparental inheritance of mitochondrial DNA can be explained by the size of the gametes involved in mating, with the larger gamete contributing towards mitochondrial DNA inheritance. However, in the human fungal pathogen Cryptococcus neoformans, bisexual mating involves the fusion of two isogamous cells of mating type (MAT) a and MAT${\alpha}$, yet the mitochondrial DNA is inherited predominantly from the MATa parent. Although the exact mechanism underlying such uniparental mitochondrial inheritance in this fungus is still unclear, various hypotheses have been proposed. Elucidating the mechanism of mitochondrial inheritance in this clinically important and genetically amenable eukaryotic microbe will yield insights into general mechanisms that are likely conserved in higher eukaryotes. In this review, we highlight studies on Cryptococcus mitochondrial inheritance and point out some important questions that need to be addressed in the future.

Keywords

References

  1. Chen XJ, Butow RA. The organization and inheritance of the mitochondrial genome. Nat Rev Genet 2005;6:815-25. https://doi.org/10.1038/nrg1708
  2. Westermann B. Mitochondrial fusion and fission in cell life and death. Nat Rev Mol Cell Biol 2010;11:872-84. https://doi.org/10.1038/nrm3013
  3. Basse CW. Mitochondrial inheritance in fungi. Curr Opin Microbiol 2010;13:712-9. https://doi.org/10.1016/j.mib.2010.09.003
  4. Schapira AH. Mitochondrial disease. Lancet 2006;368:70-82. https://doi.org/10.1016/S0140-6736(06)68970-8
  5. Birky CW Jr. Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci U S A 1995;92:11331-8. https://doi.org/10.1073/pnas.92.25.11331
  6. Birky CW Jr. Transmission genetics of mitochondria and chloroplasts. Annu Rev Genet 1978;12:471-512. https://doi.org/10.1146/annurev.ge.12.120178.002351
  7. Ephrussi B, Hottinguer H. On an unstable cell state in yeast. Cold Spring Harb Symp Quant Biol 1951;16:75-85. https://doi.org/10.1101/SQB.1951.016.01.007
  8. Mitchell MB, Mitchell HK. A Case of "Maternal" Inheritance in Neurospora Crassa. Proc Natl Acad Sci U S A 1952; 38:442-9. https://doi.org/10.1073/pnas.38.5.442
  9. Akins RA, Lambowitz AM. The [poky] mutant of Neurospora contains a 4-base-pair deletion at the 5' end of the mitochondrial small rRNA. Proc Natl Acad Sci U S A 1984;81:3791-5. https://doi.org/10.1073/pnas.81.12.3791
  10. Xu J. The inheritance of organelle genes and genomes: patterns and mechanisms. Genome 2005;48:951-8. https://doi.org/10.1139/g05-082
  11. Reboud X, Zeyl C. Organelle inheritance in plants. Heredity 1994;72:132-40. https://doi.org/10.1038/hdy.1994.19
  12. Casadevall A, Perfect JR. Cryptococcus neoformans. Washington, DC: ASM Press; 1998.
  13. Heitman J, Kozel TR, Kwon-Chung KJ, Perfect JR, Casadevall A. Cryptococcus: from human pathogen to model yeast. Washington, DC: ASM Press; 2011.
  14. Lin X, Heitman J. The biology of the Cryptococcus neoformans species complex. Annu Rev Microbiol 2006;60:69-105. https://doi.org/10.1146/annurev.micro.60.080805.142102
  15. Lin X. Cryptococcus neoformans: morphogenesis, infection, and evolution. Infect Genet Evol 2009;9:401-16. https://doi.org/10.1016/j.meegid.2009.01.013
  16. McClelland CM, Chang YC, Varma A, Kwon-Chung KJ. Uniqueness of the mating system in Cryptococcus neoformans. Trends Microbiol 2004;12:208-12. https://doi.org/10.1016/j.tim.2004.03.003
  17. Lin X, Hull CM, Heitman J. Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature 2005;434:1017-21. https://doi.org/10.1038/nature03448
  18. Kwon-Chung KJ. A new genus, Filobasidiella, the perfect state of Cryptococcus neoformans. Mycologia 1975;67:1197-200. https://doi.org/10.2307/3758842
  19. Wang L, Lin X. Mechanisms of unisexual mating in Cryptococcus neoformans. Fungal Genet Biol 2011;48:651-60. https://doi.org/10.1016/j.fgb.2011.02.001
  20. Lin X, Jackson JC, Feretzaki M, Xue C, Heitman J. Transcription factors Mat2 and Znf2 operate cellular circuits orchestrating opposite- and same-sex mating in Cryptococcus neoformans. PLoS Genet 2010;6:e1000953. https://doi.org/10.1371/journal.pgen.1000953
  21. Hull CM, Davidson RC, Heitman J. Cell identity and sexual development in Cryptococcus neoformans are controlled by the mating-type-specific homeodomain protein Sxi1alpha. Genes Dev 2002;16:3046-60. https://doi.org/10.1101/gad.1041402
  22. Hull CM, Boily MJ, Heitman J. Sex-specific homeodomain proteins Sxi1alpha and Sxi2a coordinately regulate sexual development in Cryptococcus neoformans. Eukaryot Cell 2005;4:526-35. https://doi.org/10.1128/EC.4.3.526-535.2005
  23. Davidson RC, Nichols CB, Cox GM, Perfect JR, Heitman J. A MAP kinase cascade composed of cell type specific and non-specific elements controls mating and differentiation of the fungal pathogen Cryptococcus neoformans. Mol Microbiol 2003;49:469-85. https://doi.org/10.1046/j.1365-2958.2003.03563.x
  24. Yan Z, Hull CM, Sun S, Heitman J, Xu J. The mating type-specific homeodomain genes Sxi1$\alpha$ and Sxi2$\alpha$ coordinately control uniparental mitochondrial inheritance in Cryptococcus neoformans. Curr Genet 2007;51:187-95. https://doi.org/10.1007/s00294-006-0115-9
  25. Xu J, Ali RY, Gregory DA, Amick D, Lambert SE, Yoell HJ, Vilgalys RJ, Mitchell TG. Uniparental mitochondrial transmission in sexual crosses in Cryptococcus neoformans. Curr Microbiol 2000;40:269-73. https://doi.org/10.1007/s002849910053
  26. Yan Z, Xu J. Mitochondria are inherited from the MATa parent in crosses of the basidiomycete fungus Cryptococcus neoformans. Genetics 2003;163:1315-25.
  27. Yan Z, Sun S, Shahid M, Xu J. Environment factors can influence mitochondrial inheritance in the fungus Cryptococcus neoformans. Fungal Genet Biol 2007;44:315-22. https://doi.org/10.1016/j.fgb.2006.10.002
  28. Skosireva I, James TY, Sun S, Xu J. Mitochondrial inheritance in haploid x non-haploid crosses in Cryptococcus neoformans. Curr Genet 2010;56:163-76. https://doi.org/10.1007/s00294-010-0289-z
  29. Yan Z, Hull CM, Heitman J, Sun S, Xu J. Sxi1$\alpha$ controls uniparental mitochondrial inheritance in Cryptococcus neoformans. Curr Biol 2004;14:R743-4. https://doi.org/10.1016/j.cub.2004.09.008
  30. Idnurm A, Bahn YS, Nielsen K, Lin X, Fraser JA, Heitman J. Deciphering the model pathogenic fungus Cryptococcus neoformans. Nat Rev Microbiol 2005;3:753-64. https://doi.org/10.1038/nrmicro1245
  31. Fraser JA, Diezmann S, Subaran RL, Allen A, Lengeler KB, Dietrich FS, Heitman J. Convergent evolution of chromosomal sex-determining regions in the animal and fungal kingdoms. PLoS Biol 2004;2:e384. https://doi.org/10.1371/journal.pbio.0020384
  32. Kozubowski L, Heitman J. Profiling a killer, the development of Cryptococcus neoformans. FEMS Microbiol Rev 2011 Jun 9 [Epub]. http://dx.doi.org/ 10.1111/j.1574-6976.2011.00286.x.
  33. Xue C, Bahn YS, Cox GM, Heitman J. G protein-coupled receptor Gpr4 senses amino acids and activates the cAMP-PKA pathway in Cryptococcus neoformans. Mol Biol Cell 2006;17:667-79.
  34. Lin X, Nielsen K, Patel S, Heitman J. Impact of mating type, serotype, and ploidy on the virulence of Cryptococcus neoformans. Infect Immun 2008;76:2923-38. https://doi.org/10.1128/IAI.00168-08
  35. Giles RE, Blanc H, Cann HM, Wallace DC. Maternal inheritance of human mitochondrial DNA. Proc Natl Acad Sci U S A 1980;77:6715-9. https://doi.org/10.1073/pnas.77.11.6715
  36. Hutchison CA 3rd, Newbold JE, Potter SS, Edgell MH. Maternal inheritance of mammalian mitochondrial DNA. Nature 1974;251:536-8. https://doi.org/10.1038/251536a0
  37. Shalgi R, Magnus A, Jones R, Phillips DM. Fate of sperm organelles during early embryogenesis in the rat. Mol Reprod Dev 1994;37:264-71. https://doi.org/10.1002/mrd.1080370304
  38. Sutovsky P, Moreno RD, Ramalho-Santos J, Dominko T, Simerly C, Schatten G. Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos. Biol Reprod 2000;63: 582-90. https://doi.org/10.1095/biolreprod63.2.582
  39. Ankel-Simons F, Cummins JM. Misconceptions about mitochondria and mammalian fertilization: implications for theories on human evolution. Proc Natl Acad Sci U S A 1996;93:13859-63. https://doi.org/10.1073/pnas.93.24.13859
  40. Allen JF. Separate sexes and the mitochondrial theory of ageing. J Theor Biol 1996;180:135-40. https://doi.org/10.1006/jtbi.1996.0089
  41. Mogensen HL. Exclusion of male mitochondria and plastids during syngamy in barley as a basis for maternal inheritance. Proc Natl Acad Sci U S A 1988;85:2594-7. https://doi.org/10.1073/pnas.85.8.2594
  42. Nunnari J, Marshall WF, Straight A, Murray A, Sedat JW, Walter P. Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA. Mol Biol Cell 1997;8:1233-42. https://doi.org/10.1091/mbc.8.7.1233
  43. Strausberg RL, Perlman PS. The effect of zygotic bud position on the transmission of mitochondrial genes in Saccharomyces cerevisiae. Mol Gen Genet 1978;163:131-44. https://doi.org/10.1007/BF00267404
  44. Yaffe MP. The machinery of mitochondrial inheritance and behavior. Science 1999;283:1493-7. https://doi.org/10.1126/science.283.5407.1493
  45. Aoyama H, Hagiwara Y, Misumi O, Kuroiwa T, Nakamura S. Complete elimination of maternal mitochondrial DNA during meiosis resulting in the paternal inheritance of the mitochondrial genome in Chlamydomonas species. Protoplasma 2006;228:231-42. https://doi.org/10.1007/s00709-006-0155-5
  46. Boynton JE, Harris EH, Burkhart BD, Lamerson PM, Gillham NW. Transmission of mitochondrial and chloroplast genomes in crosses of Chlamydomonas. Proc Natl Acad Sci U S A 1987;84:2391-5. https://doi.org/10.1073/pnas.84.8.2391
  47. Baptista-Ferreira JL, Economou A, Casselton LA. Mitochondrial genetics of Coprinus: recombination of mitochondrial genomes. Curr Genet 1983;7:405-7. https://doi.org/10.1007/BF00445883
  48. Sia RA, Lengeler KB, Heitman J. Diploid strains of the pathogenic basidiomycete Cryptococcus neoformans are thermally dimorphic. Fungal Genet Biol 2000;29:153-63. https://doi.org/10.1006/fgbi.2000.1192