Unisexual Reproduction Drives Meiotic Recombination and Phenotypic and Karyotypic Plasticity in

English version České info

Unisexual reproduction has been reported in several fungal species that have been traditionally thought to undergo bisexual reproduction, including major human fungal pathogens such as Cryptococcus neoformans and Candida albicans. While it has been well characterized qualitatively, quantitative description of unisexual reproduction, and detailed comparisons between unisexual and bisexual reproduction, are lacking. Here, by analyzing meiotic progeny generated from both α-α unisexual and a-α bisexual reproduction in C. neoformans, we find that the progeny collected from the two modes of sexual reproduction show similar phenotypic segregation, with transgressive segregation of several phenotypes being observed in both. Additionally, the two modes of sexual reproduction are similar in all the aspects of meiotic recombination that we have examined, providing definitive evidence that α-α unisexual reproduction is a meiotic process that operates similarly as in a-α bisexual reproduction. The ability to undergo both unisexual and bisexual reproduction may provide evolutionary advantages in environments where suitable mating partners are scarce, or where sexual reproduction is favored over asexual reproduction by mixing genetic materials and producing spores that are more tolerant of harsh environments. We discuss the implications of these findings in the context of the evolution of pathogenesis, mating types, and mating systems.

Vyšlo v časopise: Unisexual Reproduction Drives Meiotic Recombination and Phenotypic and Karyotypic Plasticity in. PLoS Genet 10(12): e32767. doi:10.1371/journal.pgen.1004849
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004849

Souhrn

Zdroje

1. Heitman J, Kozel TR, Kwon-Chung JK, Perfect JR, Casadevall A (2011) Cryptococcus: from human pathogen to model yeast.; Heitman J, Kozel TR, Kwon-Chung JK, Perfect JR, Casadevall A, editors. Washington, D. C.: ASM Press.

2. ParkBJ, WannemuehlerKA, MarstonBJ, GovenderN, PappasPG, et al. (2009) Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS 23: 525–530.

3. McClellandCM, ChangYC, VarmaA, Kwon-ChungKJ (2004) Uniqueness of the mating system in Cryptococcus neoformans. Trends Microbiol 12: 208–212.

4. HullCM, HeitmanJ (2002) Genetics of Cryptococcus neoformans. Annual Review of Genetics 36: 557–615.

5. Kwon-ChungKJ (1976) Morphogenesis of Filobasidiella neoformans, the sexual state of Cryptococcus neoformans. Mycologia 68: 821–833.

6. NielsenK, De ObaldiaAL, HeitmanJ (2007) Cryptococcus neoformans mates on pigeon guano: implications for the realized ecological niche and globalization. Eukaryot Cell 6: 949–959.

7. XueC, TadaY, DongX, HeitmanJ (2007) The human fungal pathogen Cryptococcus can complete its sexual cycle during a pathogenic association with plants. Cell Host Microbe 1: 263–273.

8. LengelerKB, FoxDS, FraserJA, AllenA, ForresterK, et al. (2002) Mating-type locus of Cryptococcus neoformans: a step in the evolution of sex chromosomes. Eukaryotic Cell 1: 704–718.

9. IdnurmA (2010) A tetrad analysis of the basidiomycete fungus Cryptococcus neoformans. Genetics 185: 153–163.

10. GilesSS, DagenaisTRT, BottsMR, KellerNP, HullCM (2009) Elucidating the pathogenesis of spores from the human fungal pathogen Cryptococcus neoformans. Infection and Immunity 77: 3491–3500.

11. HsuehYP, IdnurmA, HeitmanJ (2006) Recombination hotspots flank the Cryptococcus mating-type locus: implications for the evolution of a fungal sex chromosome. PLoS Genet 2: e184.

12. SunS, HsuehY-P, HeitmanJ (2012) Gene conversion occurs within the mating-type locus of Cryptococcus neoformans during sexual reproduction. PLoS Genet 8: e1002810.

13. MarraRE, HuangJC, FungE, NielsenK, HeitmanJ, et al. (2004) A genetic linkage map of Cryptococcus neoformans variety neoformans serotype D (Filobasidiella neoformans). Genetics 167: 619–631.

14. Kwon-ChungKJ, BennettJE (1978) Distribution of α and a mating types of Cryptococcus neoformans among natural and clinical isolates. Am J Epidemiol 108: 337–340.

15. XuJ (2005) Cost of interacting with sexual partners in a facultative sexual microbe. Genetics 171: 1597–1604.

16. LinX, HullCM, HeitmanJ (2005) Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature 434: 1017–1021.

17. FeretzakiM, HeitmanJ (2013) Genetic circuits that govern bisexual and unisexual reproduction in Cryptococcus neoformans. PLoS Genet 9: e1003688.

18. LinX, LitvintsevaAP, NielsenK, PatelS, FloydA, et al. (2007) αADα hybrids of Cryptococcus neoformans: evidence of same-sex mating in nature and hybrid fitness. PLoS Genet 3: 1975–1990.

19. LinX, PatelS, LitvintsevaAP, FloydA, MitchellTG, et al. (2009) Diploids in the Cryptococcus neoformans serotype A population homozygous for the α mating type originate via unisexual mating. PLoS Pathogens 5: e1000283.

20. ChowdharyA, HiremathSS, SunS, KowshikT, RandhawaHS, et al. (2011) Genetic differentiation, recombination and clonal expansion in environmental populations of Cryptococcus gattii in India. Environmental Microbiology 13: 1875–1888.

21. SaulN, KrockenbergerM, CarterD (2008) Evidence of recombination in mixed-mating-type and alpha-only populations of Cryptococcus gattii sourced from single eucalyptus tree hollows. Eukaryot Cell 7: 727–734.

22. HiremathSS, ChowdharyA, KowshikT, RandhawaHS, SunS, et al. (2008) Long-distance dispersal and recombination in environmental populations of Cryptococcus neoformans var. grubii from India. Microbiology 154: 1513–1524.

23. BuiT, LinX, MalikR, HeitmanJ, CarterD (2008) Isolates of Cryptococcus neoformans from infected animals reveal genetic exchange in unisexual, alpha mating type populations. Eukaryot Cell 7: 1771–1780.

24. AlbyK, SchaeferD, BennettRJ (2009) Homothallic and heterothallic mating in the opportunistic pathogen Candida albicans. Nature 460: 890–893.

25. ForcheA, AlbyK, SchaeferD, JohnsonAD, BermanJ, et al. (2008) The parasexual cycle in Candida albicans provides an alternative pathway to meiosis for the formation of recombinant strains. PLoS Biol 6: e110.

26. NiM, FeretzakiM, LiW, Floyd-AveretteA, MieczkowskiP, et al. (2013) Unisexual and heterosexual meiotic reproduction generate aneuploidy and phenotypic diversity de novo in the yeast Cryptococcus neoformans. PLoS Biol 11: e1001653.

27. ZhaiB, ZhuP, FoyleD, UpadhyayS, IdnurmA, et al. (2013) Congenic strains of the filamentous form of Cryptococcus neoformans for studies of fungal morphogenesis and virulence. Infection and Immunity 81: 2626–2637.

28. SunS, XuJ (2007) Genetic analyses of a hybrid cross between serotypes A and D strains of the human pathogenic fungus Cryptococcus neoformans. Genetics 177: 1475–1486.

29. RockmillB, Voelkel-MeimanK, RoederGS (2006) Centromere-proximal crossovers are associated with precocious separation of sister chromatids during meiosis in Saccharomyces cerevisiae. Genetics 174: 1745–1754.

30. YangS, YuanY, WangL, LiJ, WangW, et al. (2012) Great majority of recombination events in Arabidopsis are gene conversion events. PNAS 109: 20992–20997.

31. ShiJ, WolfSE, BurkeJM, PrestingGG, Ross-IbarraJ, et al. (2010) Widespread gene conversion in centromere cores. PLoS Biol 8: e1000327.

32. FraserJA, DiezmannS, SubaranRL, AllenA, LengelerKB, et al. (2004) Convergent evolution of chromosomal sex-determining regions in the animal and fungal kingdoms. PLoS Biology 2: e384.

33. SunS, XuJ (2009) Chromosomal rearrangements between serotype A and D strains in Cryptococcus neoformans. PLoS ONE 4: e5524.

34. VoganAA, KhankhetJ, XuJ (2013) Evidence for mitotic recombination within the basidia of a hybrid cross of Cryptococcus neoformans. PLoS ONE 8: e62790.

35. ZörgöE, ChwialkowskaK, GjuvslandAB, GarréE, SunnerhagenP, et al. (2013) Ancient evolutionary trade-offs between yeast ploidy states. PLoS Genet 9: e1003388.

36. SchoustraSE, DebetsAJM, SlakhorstM, HoekstraRF (2007) Mitotic recombination accelerates adaptation in the fungus Aspergillus nidulans. PLoS Genet 3: e68.

37. SongW, DominskaM, GreenwellPW, PetesTD (2014) Genome-wide high-resolution mapping of chromosome fragile sites in Saccharomyces cerevisiae. PNAS 111: E2210–E2218.

38. SiaRA, LengelerKB, HeitmanJ (2000) Diploid strains of the pathogenic basidiomycete Cryptococcus neoformans are thermally dimorphic. Fungal Genet Biol 29: 153–163.

39. HullCM, DavidsonRC, HeitmanJ (2002) Cell identity and sexual development in Cryptococcus neoformans are controlled by the mating-type-specific homeodomain protein Sxi1α. Genes Dev 16: 3046–3060.

40. FindleyK, SunS, FraserJA, HsuehY-P, AveretteAF, et al. (2012) Discovery of a modified tetrapolar sexual cycle in Cryptococcus amylolentus and the evolution of MAT in the Cryptococcus species complex. PLoS Genet 8: e1002528.

41. LoftusBJ, FungE, RoncagliaP, RowleyD, AmedeoP, et al. (2005) The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 307: 1321–1324.

42. LiH, DurbinR (2009) Fast and accurate short read alignment with Burrows - Wheeler transform. Bioinformatics 25: 1754–1760.

43. McKennaA, HannaM, BanksE, SivachenkoA, CibulskisK, et al. (2010) The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research 20: 1297–1303.

44. LiH, HandsakerB, WysokerA, FennellT, RuanJ, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079.

45. García-AlcaldeF, OkonechnikovK, CarbonellJ, CruzLM, GötzS, et al. (2012) Qualimap: evaluating next-generation sequencing alignment data. Bioinformatics 28: 2678–2679.

46. ThorvaldsdóttirH, RobinsonJT, MesirovJP (2013) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Briefings in Bioinformatics 14: 178–192.

47. Wu Y, Bhat P, Close TJ, Lonardi S (2007) Efficient and accurate construction of genetic linkage maps from noisy and missing genotyping data. Workshop on Algorithms in Bioinformatics (WABI) 2007, Lecture Notes in Bioinformatics (LNBI) 4645. Philadelphia PA. pp. 395–406.

48. SkosirevaI, JamesT, SunS, XuJ (2010) Mitochondrial inheritance in haploid x non-haploid crosses in Cryptococcus neoformans. Current Genetics 56: 163–176.