Inversion of the Chromosomal Region between Two Mating Type Loci Switches the Mating Type in
The mating system of Saccharomycotina has evolved from the ancestral heterothallic system as seen in Yarrowia lipolytica to homothallism as seen in Saccharomyces cerevisiae. The acquisition of silent cassettes was an important step towards homothallism. However, some Saccharomycotina species that diverged from the common ancestor before the acquisition of silent cassettes are also homothallic, including Hansenula polymorpha. We investigated the structure and functions of the mating type locus (MAT) in H. polymorpha, and found two MAT loci, MAT1 and MAT2. Although MAT1 contains both a and α information, the results suggest that it functions as MATα. MATa is represented by MAT2, which is located at a distance of 18 kb from MAT1. The functional repression of MAT1 or MAT2 was required to establish a or α mating type identity in individual cells. The chromosomal location of MAT1 and MAT2 was found to influence their transcriptional status, with only one locus maintained in an active state. An inversion of the MAT intervening region resulted in the switching of the two MAT loci and hence of mating type identity, which was required for homothallism. This chromosomal inversion-based mechanism represents a novel form of mating type switching that requires two MAT loci, of which only one is expressed.
Vyšlo v časopise:
Inversion of the Chromosomal Region between Two Mating Type Loci Switches the Mating Type in. PLoS Genet 10(11): e32767. doi:10.1371/journal.pgen.1004796
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004796
Souhrn
The mating system of Saccharomycotina has evolved from the ancestral heterothallic system as seen in Yarrowia lipolytica to homothallism as seen in Saccharomyces cerevisiae. The acquisition of silent cassettes was an important step towards homothallism. However, some Saccharomycotina species that diverged from the common ancestor before the acquisition of silent cassettes are also homothallic, including Hansenula polymorpha. We investigated the structure and functions of the mating type locus (MAT) in H. polymorpha, and found two MAT loci, MAT1 and MAT2. Although MAT1 contains both a and α information, the results suggest that it functions as MATα. MATa is represented by MAT2, which is located at a distance of 18 kb from MAT1. The functional repression of MAT1 or MAT2 was required to establish a or α mating type identity in individual cells. The chromosomal location of MAT1 and MAT2 was found to influence their transcriptional status, with only one locus maintained in an active state. An inversion of the MAT intervening region resulted in the switching of the two MAT loci and hence of mating type identity, which was required for homothallism. This chromosomal inversion-based mechanism represents a novel form of mating type switching that requires two MAT loci, of which only one is expressed.
Zdroje
1. HerskowitzI (1989) A regulatory hierarchy for cell specialization in yeast. Nature 342: 749–757.
2. LeeSC, NiM, LiW, ShertzC, HeitmanJ (2010) The Evolution of Sex: a Perspective from the Fungal Kingdom. Microbiology and Molecular Biology Reviews 74: 298–340 doi:10.1128/MMBR.00005-10
3. HaberJE (2012) Mating-Type Genes and MAT Switching in Saccharomyces cerevisiae. Genetics 191: 33–64 doi:10.1534/genetics.111.134577
4. ReedyJL, FloydAM, HeitmanJ (2009) Mechanistic Plasticity of Sexual Reproduction and Meiosis in the Candida Pathogenic Species Complex. Current Biology 19: 891–899 doi:10.1016/j.cub.2009.04.058
5. JonesSKJr, BennettRJ (2011) Fungal mating pheromones: Choreographing the dating game. Fungal Genetics and Biology 48: 668–676 doi:10.1016/j.fgb.2011.04.001
6. NakayamaN, MiyajimaA, AraiK (1987) Common signal transduction system shared by STE2 and STE3 in haploid cells of Saccharomyces cerevisiae: autocrine cell-cycle arrest results from forced expression of STE2. EMBO J 6: 249–254.
7. HerskowitzI (1995) MAP Kinase Pathways in Yeast: Review For Mating and More. Cell 80: 187–197.
8. MerliniL, DudinO, MartinSG (2013) Mate and fuse: how yeast cells do it. Open Biology 3: 130008 doi:10.1007/BF00312769
9. RaudaskoskiM, KotheE (2010) Basidiomycete Mating Type Genes and Pheromone Signaling. Eukaryotic Cell 9: 847–859 doi:10.1128/EC.00319-09
10. Poggeler S (2007) MAT and Its Role in the Homothallic Ascomycete Sordaria macrospora. In: Heitman J, Kronstad J, Taylor J, Casselton L, editors. Sex in Fungi. American Society for Microbiology. pp. 171–188. doi:10.1128/9781555815837.ch10.
11. HicksJB, HerskowitzI (1977) Interconversion Of Yeast Mating Types Ii. Restoration Of Mating Ability To Sterile Mutants In Homothallic And Heterothallic Strains.Genetics 85: 373–393.
12. Klar AJS, Fogel S, Radin DN (1979) Switching Of A Mating-Type a Mutant Allele In Budding Yeast Saccharomyces cerevisiae. Genetics: 759–776.
13. ButlerG, KennyC, FaganA, KurischkoC, GaillardinC, et al. (2004) Evolution of the MAT locus and its Ho endonuclease in yeast species. Proceedings of the National Academy of Sciences 101: 1632–1637 doi:10.1073/pnas.0304170101
14. HermanA, RomanH (1966) Allele specific determinants of homothallism in Saccharomyces lactis. Genetics 53: 727–740.
15. BarsoumE, MartinezP, AstromSU (2010) Alpha3, a transposable element that promotes host sexual reproduction. Genes & Development 24: 33–44 doi:10.1101/gad.557310
16. Hansen H, Hollenberg CP (1996) Hansenula polymorpha (Pichia angusta). In: Wolf K, editor. Nonconventional Yeasts in Biotechnology. Berlin, Heidelberg: Springer Berlin Heidelberg. pp. 293–311. doi:10.1007/978-3-642-79856-6_9.
17. Lahtchev K (2002) Basic genetics of Hansenula polymorpha. In: Gellissen G, editor. Hansenula polymorpha. wiley-vch. pp. 8–20.
18. RavinNV, EldarovMA, KadnikovVV, BeletskyAV, SchneiderJ, et al. (2013) Genome sequence and analysis of methylotrophic yeast Hansenula polymorpha DL1. BMC Genomics 14: 837 doi:10.1186/1471-2164-14-837
19. BurkholderAC, HartwellLH (1985) The yeast a-factor receptor: structural properties deduced from the sequence of the STE2 gene. Nucleic Acids Res 13: 8463–8475.
20. HagenDC, McCaffreyG, SpragueGJ (1986) Evidence the yeast STE3 gene encodes a receptor for the peptide pheromone a factor: Gene sequence and implicationsfor the structure of the presumed receptor. Proceedings of the National Academy of Sciences 83: 1418–1422.
21. KielJAKW, TitorenkoVI, van der KleiIJ, VeenhuisM (2007) Overproduction of translation elongation factor 1-alpha (eEF1A) suppresses the peroxisome biogenesis defect in a Hansenula polymorpha pex3 mutant via translational read-through. FEMS Yeast Research 7: 1114–1125 doi:10.1111/j.1567-1364.2007.00232.x
22. SangwallekJ, KanekoY, SugiyamaM, OnoH, BambaT, et al. (2013) for fatty acyl chain length in Saccharomyces cerevisiae. Arch Microbiol 195: 843–852 doi:10.1007/s00203-013-0933-3
23. HaberJE, GeorgeJP (1979) A mutation that permits the expression of normally silent copies of mating-type information in Saccharomyces cerevisiae. Genetics 93: 13–35.
24. RineJ, StrathernJN, HicksJB, HerskowitzI (1979) A suppressor of mating-type locus mutations in Saccharomyces cerevisiae: evidence for and identification of cryptic mating-type loci. Genetics 93: 877–901.
25. RineJ, HerskowitzI (1987) Four Genes Responsible for a position effect on expressio from HML and HMR in Saccharomyces cerevisiae. Genetics 116: 9–22.
26. LorentzA, OstermannK, FleckO, SchmidtH (1994) Switching gene swi6, involved in repression of silent mating-type loci in fission yeast, encodes a homologue of chromatin-associated proteins from. Gene 143: 139–143.
27. HickmanMA, RuscheLN (2010) Transcriptional silencing functions of the yeastprotein Orc1/Sir3 subfunctionalizedaftergene duplication. Proceedings of the National Academy of Sciences 107: 19384–19389 doi:10.1073/pnas.1006436107/-/DCSupplemental
28. AströmSU, RineJ (1998) Theme and Variation Among Silencing Proteins in Saccharomyces cerevisiae and Kluyveromyces lactis. Genetics 148: 1021–1029.
29. SherwoodRK, ScadutoCM, TorresSE, BennettRJ (2014) Convergent evolution of a fused sexual cycle promotes the haploid lifestyle. Nature 506: 387–390 doi:10.1038/nature12891
30. KitamuraK, ShimodaC (1991) The Schizosaccharomyces pombe mam2 gene encodes a putative pheromone receptor which has a significant homology with the Saccharomyces cerevisiae Ste2 protein. EMBO J 10: 3743–3751.
31. TanakaK, DaveyJ, ImaiY, YamamotoM (1993) Schizosaccharomyces pombe map3+ encodes the putative M-factor receptor. Molecular and Cellular Biology 13: 80–88.
32. TodaT, ShimanukiM, YanagidaM (1991) Fission yeast genes that confer resistance to staurosporine encode an AP-1-like transcription factor and a protein kinase related to the mammalian ERK1/MAP2 and budding yeast FUS3 and KSS1 kinases. Genes & Development 5: 60–73 doi:10.1101/gad.5.1.60
33. Arcangioli B, Thon G (2004) Mating-Type Cassettes: Structure, Switching and Silencing. In: Egel R, editor. The Molecular Biology of Schizosaccharomyces pombe. Berlin, Heidelberg: Springer Berlin Heidelberg. pp. 129–147. doi:10.1007/978-3-662-10360-9_9.
34. YunS-H, BerbeeML, YoderOC, TurgeonBG (1999) Evolution of the fungal self-fertile reproductive life style from self-sterile ancestors. Proceedings of the National Academy of Sciences 96: 5592–5597.
35. YunS-H, ArieT, KanekoI, YoderOC, TurgeonBG (2000) Molecular Organization of Mating Type Loci in Heterothallic, Homothallic, and Asexual Gibberella/Fusarium Species. Fungal Genetics and Biology 31: 7–20 doi:10.1006/fgbi.2000.1226
36. ChitrampalamP, InderbitzinP, MaruthachalamK, WuB-M, SubbaraoKV (2013) The Sclerotinia sclerotiorum Mating Type Locus (MAT) Contains a 3.6-kb Region That Is Inverted in Every Meiotic Generation. PLoS ONE 8: e56895 doi:10.1371/journal.pone.0056895.s022
37. SilvermanM, SimonM (1980) Phase Variation: Genetic Analysis of Switching Mutants. Cell 19: 845–854.
38. van der WoudeMW, BäumlerAJ (2004) Phase and antigenic variation in bacteria. Clinical Microbiology Reviews 17: 581–611 doi:10.1128/CMR.17.3.581-611.2004
39. AndrewsBJ, ProteauGA, BeattyLG, SadowskiPD (1985) The FLP Recombinase of the 2∼ Circle DNA of Yeast: Interaction with Its Target Sequences. Cell 40: 759–803.
40. BarsoumE, RajaeiN, AstromSU (2011) RAS/cyclic AMP and transcription factor Msn2 regulate mating and mating-type switching in the yeast Kluyveromyces lactis. Eukaryotic Cell 10: 1545–1552 doi:10.1128/EC.05158-11
41. LuSF, TolstorukovII, AnamnartS, KanekoY, HarashimaS (2000) Cloning, sequencing, and functional analysis of H-OLE1 gene encoding delta9-fatty acid desaturase in Hansenula polymorpha. Appl Microbiol Biotechnol 54: 499–509.
42. JankeC, MagieraMM, RathfelderN, TaxisC, ReberS, et al. (2004) A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21: 947–962 doi:10.1002/yea.1142
43. SarayaR, KrikkenAM, KielJAKW, BaerendsRJS, VeenhuisM, et al. (2012) Novel genetic tools for Hansenula polymorpha. FEMS Yeast Research 12: 271–278 doi:10.1111/j.1567-1364.2011.00772.x
44. FaberKN, HaimaP, HarderW, VeenhuisM, GeertAB (1994) Highly-efficient electrotransformation of the yeast Hansenulapolymorpha. Current Genetics 25: 305–310.
45. ShermanF (1991) Getting started with yeast. Meth Enzymol 194: 3–21.
46. Sambrook J, Russell DW (2001) Molecular Cloning. CSHL Press. 1 pp.
47. van ZutphenT, BaerendsRJ, SusannaKA, de JongA, KuipersOP, et al. (2010) Adaptation of Hansenula polymorpha to methanol: a transcriptome analysis. BMC Genomics 11: 1 doi:10.1186/1471-2164-11-1
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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