An Interspecific Fungal Hybrid Reveals Cross-Kingdom Rules for Allopolyploid Gene Expression Patterns

English version České info

Organisms are complex biological systems that must continue to function even as their genomes evolve. While evolution is usually gradual, the formation of new species by the hybridization of different parents—allopolyploidization—occurs nearly instantaneously. A key question is what happens to expression of the two parental gene copies following genome merger. To determine this, we focused on a fungal allopolyploid from a group that dominates many of the world's pastoral economies. To investigate the fate of gene expression in this system, we developed a novel pipeline to assign high throughput RNA sequence reads to the two parental gene copies, thus allowing quantification of expression. We found transcriptional responses to be predominantly conservative: most gene copies either inherit parental expression patterns, or if differentially expressed in the parents, that difference is lost in the hybrid. Moreover, we identified an extraordinary level of concordance in the fate of genome-wide allopolyploid gene expression with that seen in cotton. The very different nature of these two allopolyploids suggests that there is a set of universal rules for the transcriptional response to genome merger. We propose a mechanistic model whereby this conserved response reflects similarities in mutational processes that underlie gene regulatory evolution.

Vyšlo v časopise: An Interspecific Fungal Hybrid Reveals Cross-Kingdom Rules for Allopolyploid Gene Expression Patterns. PLoS Genet 10(3): e32767. doi:10.1371/journal.pgen.1004180
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004180

Souhrn

Zdroje

1. SémonM, WolfeKH (2007) Consequences of genome duplication. Curr Opin Genet Dev 17: 505–512.

2. DoyleJJ, FlagelLE, PatersonAH, RappRA, SoltisDE, et al. (2008) Evolutionary genetics of genome merger and doubling in plants. Annu Rev Genet 42: 443–461.

3. MableBK, AlexandrouMA, TaylorMI (2011) Genome duplication in amphibians and fish: an extended synthesis. J Zool 284: 151–182.

4. JiaoY, WickettNJ, AyyampalayamS, ChanderbaliAS, LandherrL, et al. (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97–100.

5. MoonCD, CravenKD, LeuchtmannA, ClementSL, SchardlCL (2004) Prevalence of interspecific hybrids amongst asexual fungal endophytes of grasses. Mol Ecol 13: 1455–1467.

6. OsbornTC, PiresJC, BirchlerJA, AugerDL, ChenZJ, et al. (2003) Understanding mechanisms of novel gene expression in polyploids. Trends Genet 19: 141–147.

7. AdamsKL, WendelJF (2005) Novel patterns of gene expression in polyploid plants. Trends Genet 21: 539–543.

8. HittingerCT (2013) Saccharomyces diversity and evolution: A budding model genus. Trends in Genetics 29: 309–317.

9. SoltisPS, SoltisDE (2009) The role of hybridization in plant speciation. Ann Rev Plant Biol 60: 561–588.

10. DonovanLA, RosenthalDR, Sanchez-VelenosiM, RiesebergLH, LudwigF (2010) Are hybrid species more fit than ancestral parent species in the current hybrid species habitats? J Evol Biol 23: 805–816.

11. MadlungA (2013) Polyploidy and its effect on evolutionary success: Old questions revisited with new tools. Heredity 110: 99–104.

12. BirchlerJA, YaoH, ChudalayandiS, VaimanD, VeitiaRA (2010) Heterosis. Plant Cell 22: 2105–2112.

13. ChenZJ (2013) Genomic and epigenetic insights into the molecular bases of heterosis. Nat Rev Genet 14: 471–482.

14. McClintockB (1984) The significance of responses of the genome to challenge. Science 226: 792–801.

15. ParisodC, AlixK, JustJ, PetitM, SarilarV, et al. (2010) Impact of transposable elements on the organization and function of allopolyploid genomes. New Phytol 186: 37–45.

16. O'NeillRJW, O'NeillMJ, GravesJAM (1998) Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature 393: 68–72.

17. HegartyMJ, BatstoneT, BarkerGL, EdwardsKJ, AbbottRJ, et al. (2011) Nonadditive changes to cytosine methylation as a consequence of hybridization and genome duplication in Senecio (Asteraceae). Mol Ecol 20: 105–113.

18. PetitM, GuidatC, DanielJ, DenisE, MontoriolE, et al. (2010) Mobilization of retrotransposons in synthetic allotetraploid tobacco. New Phytol 186: 135–147.

19. SongK, LuP, TangK, OsbornTC (1995) Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. Proc Natl Acad Sci USA 92: 7719–7723.

20. GaetaRT, PiresJC, Iniguez-LuyF, LeonE, OsbornTC (2007) Genomic changes in resynthesized Brassica napus and their effect on gene expression and phenotype. Plant Cell 19: 3403–3417.

21. KashkushK, FeldmanM, LevyAA (2003) Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet 33: 102–106.

22. WolfeKH, ShieldsDC (1997) Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387: 708–713.

23. GordonJL, ByrneKP, WolfeKH (2009) Additions, losses, and rearrangements on the evolutionary route from a reconstructed ancestor to the modern Saccharomyces cerevisiae genome. PLoS Genet 5: e1000485.

24. ScannellDR, ByrneKP, GordonJL, WongS, WolfeKH (2006) Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts. Nature 440: 341–345.

25. ThomasBC, PedersenB, FreelingM (2006) Following tetraploidy in an Arabidopsis ancestor, genes were removed preferentially from one homeolog leaving clusters enriched in dose-sensitive genes. Genome Res 16: 934–946.

26. BuggsRJA, ChamalaS, WuW, TateJA, SchnablePS, et al. (2012) Rapid, repeated, and clustered loss of duplicate genes in allopolyploid plant populations of independent origin. Curr Biol 22: 248–252.

27. SchnableJC, SpringerNM, FreelingM (2011) Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proc Natl Acad Sci USA 108: 4069–4074.

28. BaumelA, AinoucheM, KalendarR, SchulmanAH (2002) Retrotransposons and genomic stability in populations of the young allopolyploid species Spartina anglica C.E. Hubbard (Poaceae). Mol Biol Evol 19: 1218–1227.

29. LiuB, BrubakerCL, MergeaiG, CronnRC, WendelJF (2001) Polyploid formation in cotton is not accompanied by rapid genomic changes. Genome 44: 321–330.

30. PatersonAH, ChapmanBA, KissingerJC, BowersJE, FeltusFA, et al. (2006) Many gene and domain families have convergent fates following independent whole-genome duplication events in Arabidopsis, Oryza, Saccharomyces and Tetraodon. Trends Genet 22: 597–602.

31. AdamsKL (2007) Evolution of duplicate gene expression in polyploid and hybrid plants. J Hered 98: 136–141.

32. ChaudharyB, FlagelL, StuparRM, UdallJA, VermaN, et al. (2009) Reciprocal silencing, transcriptional bias and functional divergence of homeologs in polyploid cotton (Gossypium). Genetics 182: 503–517.

33. FlagelL, WendelJ, UdallJ (2012) Duplicate gene evolution, homoeologous recombination, and transcriptome characterization in allopolyploid cotton. BMC Genom 13: 302.

34. CombesMC, CenciA, BarailleH, BertrandB, LashermesP (2012) Homeologous gene expression in response to growing temperature in a recent Allopolyploid (Coffea arabica L.). J Hered 103: 36–46.

35. VidalRO, MondegoJM, PotD, AmbrosioAB, AndradeAC, et al. (2010) A high-throughput data mining of single nucleotide polymorphisms in Coffea species expressed sequence tags suggests differential homeologous gene expression in the allotetraploid Coffea arabica. Plant Physiol 154: 1053–1066.

36. HegartyMJ, BarkerGL, WilsonID, AbbottRJ, EdwardsKJ, et al. (2006) Transcriptome shock after interspecific hybridization in Senecio is ameliorated by genome duplication. Curr Biol 16: 1652–1659.

37. ChelaifaH, MonnierA, AinoucheM (2010) Transcriptomic changes following recent natural hybridization and allopolyploidy in the salt marsh species Spartina x townsendii and Spartina anglica (Poaceae). New Phytol 186: 161–174.

38. HeP, FriebeBR, GillBS, ZhouJM (2003) Allopolyploidy alters gene expression in the highly stable hexaploid wheat. Plant Mol Biol 52: 401–414.

39. BuggsRJA, ZhangL, MilesN, TateJA, GaoL, et al. (2011) Transcriptomic shock generates evolutionary novelty in a newly formed, natural allopolyploid plant. Curr Biol 21: 551–556.

40. TateJA, NiZ, ScheenAC, KohJ, GilbertCA, et al. (2006) Evolution and expression of homeologous loci in Tragopogon miscellus (Asteraceae), a recent and reciprocally formed allopolyploid. Genetics 173: 1599–1611.

41. RappR, UdallJ, WendelJ (2009) Genomic expression dominance in allopolyploids. BMC Biol 7: 18.

42. BardilA, de AlmeidaJD, CombesMC, LashermesP, BertrandB (2011) Genomic expression dominance in the natural allopolyploid Coffea arabica is massively affected by growth temperature. New Phytol 192: 760–774.

43. GroverCE, GallagherJP, SzadkowskiEP, YooMJ, FlagelLE, et al. (2012) Homoeolog expression bias and expression level dominance in allopolyploids. New Phytol 196: 966–971.

44. CoxMP, EatonCJ, ScottDB (2010) Exploring molecular signaling in plant-fungal symbioses using high throughput RNA sequencing. Plant Signal Behav 5: 1353–1358.

45. BuggsRJA, Renny-ByfieldS, ChesterM, Jordon-ThadenIE, VicciniLF, et al. (2012) Next-generation sequencing and genome evolution in allopolyploids. Am J Bot 99: 372–382.

46. YooMJ, SzadkowskiE, WendelJF (2013) Homoeolog expression bias and expression level dominance in allopolyploid cotton. Heredity 110: 171–180.

47. AuryJM, JaillonO, DuretL, NoelB, JubinC, et al. (2006) Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444: 171–178.

48. KasaharaM, NaruseK, SasakiS, NakataniY, QuW, et al. (2007) The medaka draft genome and insights into vertebrate genome evolution. Nature 447: 714–719.

49. SchardlCL, CravenKD (2003) Interspecific hybridization in plant-associated fungi and oomycetes: A review. Mol Ecol 12: 2861–2873.

50. SchardlCL, LeuchtmannA, TsaiHF, CollettMA, WattDM, et al. (1994) Origin of a fungal symbiont of perennial ryegrass by interspecific hybridization of a mutualist with the ryegrass choke pathogen, Epichloë typhina. Genetics 136: 1307–1317.

51. SchardlCL (2010) The Epichloae, symbionts of the grass subfamily Poöideae. Ann Missouri Bot Gard 97: 646–665.

52. TsaiH-F, LiuJ-S, StabenC, ChristensenMJ, LatchGC, et al. (1994) Evolutionary diversification of fungal endophytes of tall fescue grass by hybridization with Epichloë species. Proc Natl Acad Sci USA 91: 2542–2546.

53. GlazkoGV, NeiM (2003) Estimation of divergence times for major lineages of primate species. Mol Biol Evol 20: 424–434.

54. CollettMA, BradshawRE, ScottDB (1995) A mutualistic fungal symbiont of perennial ryegrass contains two different pyr4 genes, both expressing orotidine-5′-monophosphate decarboxylase. Gene 158: 31–39.

55. GanleyARD, ScottB (1998) Extraordinary ribosomal spacer length heterogeneity in a Neotyphodium endophyte hybrid: Implications for concerted evolution. Genetics 150: 1625–1637.

56. SchardlCL, YoungCA, PanJ, FloreaS, TakachJE, et al. (2013) Currencies of mutualisms: Sources of alkaloid genes in vertically transmitted epichloae. Toxins 5: 1064–1088.

57. GanleyARD, ScottB (2002) Concerted evolution in the ribosomal RNA genes of an Epichloë endophyte hybrid: Comparison between tandemly arranged rDNA and dispersed 5S rrn genes. Fungal Genet Biol 35: 39–51.

58. ColemanM, HenricotB, ArnauJ, OliverRP (1997) Starvation-induced genes of the tomato pathogen Cladosporium fulvum are also induced during growth in planta. Mol Plant Microbe Interact 10: 1106–1109.

59. SchardlCL, YoungCA, HesseU, AmyotteSG, AndreevaK, et al. (2013) Plant-symbiotic fungi as chemical engineers: Multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid loci. PLoS Genet 9: e1003323.

60. ChesterM, GallagherJP, SymondsVV, da SilvaAVC, MavrodievEV, et al. (2012) Extensive chromosomal variation in a recently formed natural allopolyploid species, Tragopogon miscellus (Asteraceae). Proc Natl Acad Sci USA 109: 1176–1181.

61. ChenZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol 58: 377–406.

62. SchlöttererC, TautzD (1994) Chromosomal homogeneity of Drosophila ribosomal DNA arrays suggests intrachromosomal exchanges drive concerted evolution. Curr Biol 4: 777–783.

63. DadejováM, LimKY, Soucková-SkalickáK, MatyásekR, GrandbastienMA, et al. (2007) Transcription activity of rRNA genes correlates with a tendency towards intergenomic homogenization in Nicotiana allotetraploids. New Phytol 174: 658–668.

64. RiddleNC, BirchlerJA (2003) Effects of reunited diverged regulatory hierarchies in allopolyploids and species hybrids. Trends Genet 19: 597–600.

65. ChenZJ, NiZ (2006) Mechanisms of genomic rearrangements and gene expression changes in plant polyploids. Bioessays 28: 240–252.

66. RooseML, GottliebLD (1980) Biochemical properties and level of expression of alcohol dehydrogenases in the allotetraploid plant Tragopogon miscellus and its diploid progenitors. Biochem Genet 18: 1065–1085.

67. TiroshI, ReikhavS, LevyAA, BarkaiN (2009) A yeast hybrid provides insight into the evolution of gene expression regulation. Science 324: 659–662.

68. WittkoppPJ, HaerumBK, ClarkAG (2004) Evolutionary changes in cis and trans gene regulation. Nature 430: 85–88.

69. HegartyMJ, HiscockSJ (2008) Genomic clues to the evolutionary success of polyploid plants. Curr Biol 18: R435–444.

70. FlagelL, UdallJ, NettletonD, WendelJ (2008) Duplicate gene expression in allopolyploid Gossypium reveals two temporally distinct phases of expression evolution. BMC Biology 6: 16.

71. BakerCR, Hanson-SmithV, JohnsonAD (2013) Following gene duplication, paralog interference constrains transcriptional circuit evolution. Science 342: 104–108.

72. ChristensenMJ, LeuchtmannA, RowanDD, TapperBA (1993) Taxonomy of Acremonium endophytes of tall fescue (Festuca arundinacea), meadow fescue (F. pratensis) and perennial ryegrass (Lolium perenne). Mycolog Res 97: 1083–1092.

73. YoungCA, BryantMK, ChristensenMJ, TapperBA, BryanGT, et al. (2005) Molecular cloning and genetic analysis of a symbiosis-expressed gene cluster for lolitrem biosynthesis from a mutualistic endophyte of perennial ryegrass. Mol Genet Genom 274: 13–29.

74. CoxMP, PetersonDA, BiggsPJ (2010) SolexaQA: At-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinf 11: 485.

75. FisherRA (1922) On the interpretation of χ2 from contingency tables, and the calculation of P. J R Statist Soc 85: 87–94.

76. R Development Core Team (2013) R: A Language and Environment for Statistical Computing.

77. WangL, FengZ, WangX, WangX, ZhangX (2010) DEGseq: An R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26: 136–138.

78. StoreyJD, TibshiraniR (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100: 9440–9445.

79. RobinsonJT, ThorvaldsdóttirH, WincklerW, GuttmanM, LanderES, et al. (2011) Integrative genomics viewer. Nat Biotech 29: 24–26.

80. PeintnerU, BougherNL, CastellanoMA, MoncalvoJM, MoserMM, et al. (2001) Multiple origins of sequestrate fungi related to Cortinarius (Cortinariaceae). Am J Bot 88: 2168–2179.

81. KasugaT, WhiteTJ, TaylorJW (2002) Estimation of nucleotide substitution rates in eurotiomycete fungi. Mol Biol Evol 19: 2318–2324.

82. CharltonND, CravenKD, MittalS, HopkinsAA, YoungCA (2012) Epichloë canadensis, a new interspecific epichloid hybrid symbiotic with Canada wildrye (Elymus canadensis). Mycologia 104: 1187–1199.