Species and Population Level Molecular Profiling Reveals Cryptic Recombination and Emergent Asymmetry in the Dimorphic Mating Locus of

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Heteromorphic sex-determining regions or mating-type loci can contain large regions of non-recombining sequence where selection operates under different constraints than in freely recombining autosomal regions. Detailed studies of these non-recombining regions can provide insights into how genes are gained and lost, and how genetic isolation is maintained between mating haplotypes or sex chromosomes. The Chlamydomonas reinhardtii mating-type locus (MT) is a complex polygenic region characterized by sequence rearrangements and suppressed recombination between its two haplotypes, MT+ and MT−. We used new sequence information to redefine the genetic contents of MT and found repeated translocations from autosomes as well as sexually controlled expression patterns for several newly identified genes. We examined sequence diversity of MT genes from wild isolates of C. reinhardtii to investigate the impacts of recombination suppression. Our population data revealed two previously unreported types of genetic exchange in Chlamydomonas MT—gene conversion in the rearranged domains, and crossover exchanges in flanking domains—both of which contribute to maintenance of genetic homogeneity between haplotypes. To investigate the cause of blocked recombination in MT we assessed recombination rates in crosses where the parents were homozygous at MT. While normal recombination was restored in MT+×MT+ crosses, it was still suppressed in MT−×MT− crosses. These data revealed an underlying asymmetry in the two MT haplotypes and suggest that sequence rearrangements are insufficient to fully account for recombination suppression. Together our findings reveal new evolutionary dynamics for mating loci and have implications for the evolution of heteromorphic sex chromosomes and other non-recombining genomic regions.

Vyšlo v časopise: Species and Population Level Molecular Profiling Reveals Cryptic Recombination and Emergent Asymmetry in the Dimorphic Mating Locus of. PLoS Genet 9(8): e32767. doi:10.1371/journal.pgen.1003724
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003724

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Zdroje

1. CharlesworthD (2013) Plant sex chromosome evolution. J Exp Bot doi: 10.1093/jxb/ers322

2. FraserJA, HeitmanJ (2005) Chromosomal sex-determining regions in animals, plants and fungi. Curr Opin Genet Dev 15: 645–651 doi:10.1016/j.gde.2005.09.002

3. BachtrogD, KirkpatrickM, MankJE, McDanielSF, PiresJC, et al. (2011) Are all sex chromosomes created equal? Trends in Genetics 27: 350–357 doi:10.1016/j.tig.2011.05.005

4. CharlesworthD, CharlesworthB, MaraisG (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95: 118–128 doi:10.1038/sj.hdy.6800697

5. BellottDW, SkaletskyH, PyntikovaT, MardisER, GravesT, et al. (2010) Convergent evolution of chicken Z and human X chromosomes by expansion and gene acquisition. Nature 466: 612–616 doi:10.1038/nature09172

6. LeeSC, NiM, LiW, ShertzC, HeitmanJ (2010) The evolution of sex: a perspective from the fungal kingdom. Microbiol Mol Biol Rev 74: 298–340 doi:10.1128/MMBR.00005-10

7. EllisonCE, StajichJE, JacobsonDJ, NatvigDO, LapidusA, et al. (2011) Massive changes in genome architecture accompany the transition to self-fertility in the filamentous fungus Neurospora tetrasperma. Genetics 189: 55–69 doi:10.1534/genetics.111.130690

8. FraserJA, DiezmannS, SubaranRL, AllenA, LengelerKB, et al. (2004) Convergent Evolution of Chromosomal Sex-Determining Regions in the Animal and Fungal Kingdoms. PLoS Biol 2: e384 doi:10.1371/journal.pbio.0020384

9. HoodME (2002) Dimorphic mating-type chromosomes in the fungus Microbotryum violaceum. Genetics 160: 457–461.

10. LeeN, BakkerenG, WongK, SherwoodJE, KronstadJW (1999) The mating-type and pathogenicity locus of the fungus Ustilago hordei spans a 500-kb region. Proc Natl Acad Sci USA 96: 15026–15031.

11. FerrisP, OlsonBJSC, De HoffPL, DouglassS, CaseroD, et al. (2010) Evolution of an expanded sex-determining locus in Volvox. Science 328: 351–354 doi:10.1126/science.1186222

12. AllenCE (1945) The genetics of bryophytes. II. The Botanical Review 11: 260–287.

13. YamatoKT, IshizakiK, FujisawaM, OkadaS, NakayamaS, et al. (2007) Gene organization of the liverwort Y chromosome reveals distinct sex chromosome evolution in a haploid system. Proc Natl Acad Sci USA 104: 6472–6477 doi:10.1073/pnas.0609054104

14. UmenJG (2011) Evolution of sex and mating loci: An expanded view from Volvocine algae. Curr Opin Microbiol 14: 634–641 doi:10.1016/j.mib.2011.10.005

15. NozakiH, MisawaK, KajitaT, KatoM, NoharaS, et al. (2000) Origin and evolution of the colonial volvocales (Chlorophyceae) as inferred from multiple, chloroplast gene sequences. Mol Phylogenet Evol 17: 256–268 doi:10.1006/mpev.2000.0831

16. ColemanA (2012) A Comparative Analysis of the Volvocaceae (Chlorophyta). J Phycol 48: 491–513.

17. NozakiH (1996) Morphology and evolution of sexual reproduction in the Volvocaceae (Chlorophyta). J Plant Res 109: 353–361.

18. GoodenoughU, LinH, LeeJ-H (2007) Sex determination in Chlamydomonas. Seminars in Cell & Developmental Biology 18: 350–361 doi:10.1016/j.semcdb.2007.02.006

19. FerrisPJ, ArmbrustEV, GoodenoughUW (2002) Genetic structure of the mating-type locus of Chlamydomonas reinhardtii. Genetics 160: 181–200.

20. MerchantSS, ProchnikSE, VallonO, HarrisEH, KarpowiczSJ, et al. (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245–250 doi:10.1126/science.1143609

21. CharlesworthD, CharlesworthB (2010) Evolutionary Biology: The Origins of Two Sexes. Current Biology 20: R519–R521 doi:10.1016/j.cub.2010.05.015

22. FerrisPJ, GoodenoughUW (1994) The mating-type locus of Chlamydomonas reinhardtii contains highly rearranged DNA sequences. Cell 76: 1135–1145.

23. GoodsteinDM, ShuS, HowsonR, NeupaneR, HayesRD, et al. (2011) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40: D1178–D1186 doi:10.1093/nar/gkr944

24. WheelerGL, Miranda-SaavedraD, BartonGJ (2008) Genome Analysis of the Unicellular Green Alga Chlamydomonas reinhardtii Indicates an Ancient Evolutionary Origin for Key Pattern Recognition and Cell-Signaling Protein Families. Genetics 179: 193–197 doi:10.1534/genetics.107.085936

25. LahnBT, PageDC (1999) Four evolutionary strata on the human X chromosome. Science 286: 964–967.

26. BergeroR, CharlesworthD (2009) The evolution of restricted recombination in sex chromosomes. Trends Ecol Evol (Amst) 24: 94–102 doi:10.1016/j.tree.2008.09.010

27. VotintsevaAA, FilatovDA (2009) Evolutionary strata in a small mating-type-specific region of the smut fungus Microbotryum violaceum. Genetics 182: 1391–1396 doi:10.1534/genetics.109.103192

28. MenkisA, JacobsonDJ, GustafssonT, JohannessonH (2008) The mating-type chromosome in the filamentous ascomycete Neurospora tetrasperma represents a model for early evolution of sex chromosomes. PLoS Genet 4: e1000030 doi:10.1371/journal.pgen.1000030

29. PetitE, GiraudT, de VienneDM, CoelhoMA, AguiletaG, et al. (2012) Linkage to the mating-type locus across the genus Microbotryum: insights into nonrecombining chromosomes. Evolution; International Journal of Organic Evolution 66: 3519–3533 doi:10.1111/j.1558-5646.2012.01703.x

30. SharpPM, LiWH (1987) The codon Adaptation Index–a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15: 1281–1295.

31. WhittleCA, SunY, JohannessonH (2011) Degeneration in codon usage within the region of suppressed recombination in the mating-type chromosomes of Neurospora tetrasperma. Eukaryotic Cell 10: 594–603 doi:10.1128/EC.00284-10

32. Merchant S, Pellegrini M (2010) Chlamydomonas 454 Reads. genomes-merchantmcdbuclaedu. Available: http://genomes-merchant.mcdb.ucla.edu/. Accessed 21 January 2013.

33. BullJ (1978) Sex Chromosomes in Haploid Dioecy: A Unique Contrast to Muller's Theory for Diploid Dioecy. The American Naturalist 112: 245–250.

34. CharlesworthB, CharlesworthD (2000) The degeneration of Y chromosomes. Philos Trans R Soc Lond, B, Biol Sci 355: 1563–1572 doi:10.1098/rstb.2000.0717

35. BachtrogD (2006) A dynamic view of sex chromosome evolution. Curr Opin Genet Dev 16: 578–585 doi:10.1016/j.gde.2006.10.007

36. StöckM, HornA, GrossenC, LindtkeD, SermierR, et al. (2011) Ever-young sex chromosomes in European tree frogs. PLoS Biol 9: e1001062 doi:10.1371/journal.pbio.1001062

37. SmithDR, LeeRW (2008) Nucleotide diversity in the mitochondrial and nuclear compartments of Chlamydomonas reinhardtii: investigating the origins of genome architecture. BMC Evol Biol 8: 156 doi:10.1186/1471-2148-8-156

38. Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press. 1 pp.

39. EllegrenH (2009) The different levels of genetic diversity in sex chromosomes and autosomes. Trends Genet 25: 278–284 doi:10.1016/j.tig.2009.04.005

40. NeiM, MillerJC (1990) A simple method for estimating average number of nucleotide substitutions within and between populations from restriction data. Genetics 125: 873–879.

41. HudsonRR, SlatkinM, MaddisonWP (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132: 583–589.

42. HusonDH, BryantD (2006) Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23: 254–267 doi:10.1093/molbev/msj030

43. BetránE, RozasJ, NavarroA, BarbadillaA (1997) The estimation of the number and the length distribution of gene conversion tracts from population DNA sequence data. Genetics 146: 89–99.

44. UyenoyamaMK (2005) Evolution under tight linkage to mating type. New Phytol 165: 63–70 doi:10.1111/j.1469-8137.2004.01246.x

45. IronsideJE (2010) No amicable divorce? Challenging the notion that sexual antagonism drives sex chromosome evolution. BioEssays 32: 718–726 doi:10.1002/bies.200900124

46. FerrisPJ, GoodenoughUW (1997) Mating type in Chlamydomonas is specified by mid, the minus-dominance gene. Genetics 146: 859–869.

47. FerrisPJ (1995) Localization of the Nic-7, Ac-29 and THI-10 Genes within the Mating-Type Locus of Chlamydomonas Reinhardtii. Genetics 141: 543.

48. SmythRD, MartinekGW, EbersoldWT (1975) Linkage of six genes in Chlamydomonas reinhardtii and the construction of linkage test strains. J Bacteriol 124: 1615–1617.

49. RymarquisLA, HandleyJM, ThomasM, SternDB (2005) Beyond complementation. Map-based cloning in Chlamydomonas reinhardtii. PLANT PHYSIOLOGY 137: 557–566 doi:10.1104/pp.104.054221

50. JacobsonDJ (2005) Blocked recombination along the mating-type chromosomes of Neurospora tetrasperma involves both structural heterozygosity and autosomal genes. Genetics 171: 839–843 doi:10.1534/genetics.105.044040

51. KathirP, LaVoieM, BrazeltonW, HaasN (2003) Molecular Map of the Chlamydomonas reinhardtii Nuclear Genome. Eukaryotic Cell 2: 362–379.

52. ArmbrustEV, FerrisPJ, GoodenoughUW (1993) A mating type-linked gene cluster expressed in Chlamydomonas zygotes participates in the uniparental inheritance of the chloroplast genome. Cell 74: 801–811.

53. SmaczniakC, ImminkRGH, AngenentGC, KaufmannK (2012) Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development 139: 3081–3098 doi:10.1242/dev.074674

54. BalakirevMY, TcherniukSO, JaquinodM, ChroboczekJ (2003) Otubains: a new family of cysteine proteases in the ubiquitin pathway. EMBO Rep 4: 517–522 doi:10.1038/sj.embor.embor824

55. AdamsCR, StamerKA, MillerJK, McNallyJG, KirkMM, et al. (1990) Patterns of organellar and nuclear inheritance among progeny of two geographically isolated strains of Volvox carteri. Curr Genet 18: 141–153.

56. FerrisPJ, WaffenschmidtS, UmenJG, LinH, LeeJ-H, et al. (2005) Plus and minus sexual agglutinins from Chlamydomonas reinhardtii. The Plant Cell 17: 597–615 doi:10.1105/tpc.104.028035

57. HwangCJ, MonkBC, GoodenoughUW (1981) Linkage of Mutations Affecting minus Flagellar Membrane Agglutinability to the mt Mating-Type Locus of Chlamydomonas. Genetics 99: 41–47.

58. SunS, HsuehY-P, HeitmanJ (2012) Gene Conversion Occurs within the Mating-Type Locus of Cryptococcus neoformans during Sexual Reproduction. PLoS Genet 8: e1002810 doi:10.1371/journal.pgen.1002810.t004

59. MenkisA, WhittleCA, JohannessonH (2010) Gene genealogies indicates abundant gene conversions and independent evolutionary histories of the mating-type chromosomes in the evolutionary history of Neurospora tetrasperma. BMC Evol Biol 10: 234 doi:10.1186/1471-2148-10-234

60. Pecon SlatteryJ, Sanner-WachterL, O'BrienSJ (2000) Novel gene conversion between X-Y homologues located in the nonrecombining region of the Y chromosome in Felidae (Mammalia). Proc Natl Acad Sci USA 97: 5307–5312.

61. IwaseM, SattaY, HiraiH, HiraiY, TakahataN (2010) Frequent gene conversion events between the X and Y homologous chromosomal regions in primates. BMC Evol Biol 10: 225 doi:10.1186/1471-2148-10-225

62. LinH, GoodenoughUW (2007) Gametogenesis in the Chlamydomonas reinhardtii minus mating type is controlled by two genes, MID and MTD1. Genetics 176: 913–925 doi:10.1534/genetics.106.066167

63. HoodME, PetitE, GiraudT (2013) Extensive divergence between mating-type chromosomes of the anther-smut fungus. Genetics 193: 309–315 doi:10.1534/genetics.112.146266

64. BellafioreS (2002) Loss of Albino3 Leads to the Specific Depletion of the Light-Harvesting System. The Plant Cell 14: 2303–2314 Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=12215522&retmode=ref&cmd=prlinks.

65. DebuchyR, PurtonS, RochaixJD (1989) The argininosuccinate lyase gene of Chlamydomonas reinhardtii: an important tool for nuclear transformation and for correlating the genetic and molecular maps of the ARG7 locus. EMBO J 8: 2803–2809.

66. Harris EH (1989) The Chlamydomonas Sourcebook: A Comprehensive Guide to Biology and Laboratory Use. Academic Press. 1 pp.

67. RiceP, LongdenI, BleasbyA (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16: 276–277 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=10827456.

68. EdgarRC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113 doi:10.1186/1471-2105-5-113

69. TamuraK, PetersonD, PetersonN, StecherG, NeiM, et al. (2011) MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Molecular Biology and Evolution 28: 2731–2739 Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=21546353&retmode=ref&cmd=prlinks.

70. YangZ (2007) PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24: 1586–1591 doi:10.1093/molbev/msm088

71. YangZ, NielsenR (2000) Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Molecular Biology and Evolution 17: 32–43.

72. PuigbòP, BravoI, Garcia-VallveS (2008) CAIcal: A combined set of tools to assess codon usage adaptation. Biology Direct 3: 38.

73. FangS-C, de los ReyesC, UmenJG (2006) Cell size checkpoint control by the retinoblastoma tumor suppressor pathway. PLoS Genet 2: e167 doi:10.1371/journal.pgen.0020167

74. WeeksDP, BeermanN, GriffithOM (1986) A small-scale five-hour procedure for isolating multiple samples of CsCl-purified DNA: application to isolations from mammalian, insect, higher plant, algal, yeast, and bacterial sources. Analytical Biochemistry 152: 376–385 Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=3963370&retmode=ref&cmd=prlinks.

75. LarkinMA, BlackshieldsG, BrownNP, ChennaR, McGettiganPA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948 doi:10.1093/bioinformatics/btm404

76. LibradoP, RozasJ (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452 doi:10.1093/bioinformatics/btp187

77. TamuraK (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Molecular Biology and Evolution 9: 678–687.

78. KuboT, AbeJ, SaitoT, MatsudaY (2002) Genealogical relationships among laboratory strains of Chlamydomonas reinhardtii as inferred from matrix metalloprotease genes. Curr Genet 41: 115–122 Available: http://www.springerlink.com/openurl.asp?genre=article&id=doi:10.1007/s00294-002-0284-0.

79. LissM, KirkD, BeyserK, FabryS (1997) Intron sequences provide a tool for high-resolution phylogenetic analysis of volvocine algae. Curr Genet 31: 214–27.