Genetic Adaptation Associated with Genome-Doubling in Autotetraploid
Genome duplication, which results in polyploidy, is disruptive to fundamental biological processes. Genome duplications occur spontaneously in a range of taxa and problems such as sterility, aneuploidy, and gene expression aberrations are common in newly formed polyploids. In mammals, genome duplication is associated with cancer and spontaneous abortion of embryos. Nevertheless, stable polyploid species occur in both plants and animals. Understanding how natural selection enabled these species to overcome early challenges can provide important insights into the mechanisms by which core cellular functions can adapt to perturbations of the genomic environment. Arabidopsis arenosa includes stable tetraploid populations and is related to well-characterized diploids A. lyrata and A. thaliana. It thus provides a rare opportunity to leverage genomic tools to investigate the genetic basis of polyploid stabilization. We sequenced the genomes of twelve A. arenosa individuals and found signatures suggestive of recent and ongoing selective sweeps throughout the genome. Many of these are at genes implicated in genome maintenance functions, including chromosome cohesion and segregation, DNA repair, homologous recombination, transcriptional regulation, and chromatin structure. Numerous encoded proteins are predicted to interact with one another. For a critical meiosis gene, ASYNAPSIS1, we identified a non-synonymous mutation that is highly differentiated by cytotype, but present as a rare variant in diploid A. arenosa, indicating selection may have acted on standing variation already present in the diploid. Several genes we identified that are implicated in sister chromatid cohesion and segregation are homologous to genes identified in a yeast mutant screen as necessary for survival of polyploid cells, and also implicated in genome instability in human diseases including cancer. This points to commonalities across kingdoms and supports the hypothesis that selection has acted on genes controlling genome integrity in A. arenosa as an adaptive response to genome doubling.
Vyšlo v časopise:
Genetic Adaptation Associated with Genome-Doubling in Autotetraploid. PLoS Genet 8(12): e32767. doi:10.1371/journal.pgen.1003093
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1003093
Souhrn
Genome duplication, which results in polyploidy, is disruptive to fundamental biological processes. Genome duplications occur spontaneously in a range of taxa and problems such as sterility, aneuploidy, and gene expression aberrations are common in newly formed polyploids. In mammals, genome duplication is associated with cancer and spontaneous abortion of embryos. Nevertheless, stable polyploid species occur in both plants and animals. Understanding how natural selection enabled these species to overcome early challenges can provide important insights into the mechanisms by which core cellular functions can adapt to perturbations of the genomic environment. Arabidopsis arenosa includes stable tetraploid populations and is related to well-characterized diploids A. lyrata and A. thaliana. It thus provides a rare opportunity to leverage genomic tools to investigate the genetic basis of polyploid stabilization. We sequenced the genomes of twelve A. arenosa individuals and found signatures suggestive of recent and ongoing selective sweeps throughout the genome. Many of these are at genes implicated in genome maintenance functions, including chromosome cohesion and segregation, DNA repair, homologous recombination, transcriptional regulation, and chromatin structure. Numerous encoded proteins are predicted to interact with one another. For a critical meiosis gene, ASYNAPSIS1, we identified a non-synonymous mutation that is highly differentiated by cytotype, but present as a rare variant in diploid A. arenosa, indicating selection may have acted on standing variation already present in the diploid. Several genes we identified that are implicated in sister chromatid cohesion and segregation are homologous to genes identified in a yeast mutant screen as necessary for survival of polyploid cells, and also implicated in genome instability in human diseases including cancer. This points to commonalities across kingdoms and supports the hypothesis that selection has acted on genes controlling genome integrity in A. arenosa as an adaptive response to genome doubling.
Zdroje
1. ComaiL (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6: 836–846.
2. OsbornTC, PiresJC, BirchlerJA, AugerDL, ChenZJ, et al. (2003) Understanding mechanisms of novel gene expression in polyploids. Trends Genet 19: 141–147.
3. OttoSP (2007) The evolutionary consequences of polyploidy. Cell 131: 452–462.
4. ParisodC, HoldereggerR, BrochmannC (2010) Evolutionary consequences of autopolyploidy. New Phytol 186: 5–17.
5. RamseyJ, SchemskeDW (2002) Neopolyploidy in flowering plants. Ann Rev Ecol Systemat 33: 589–639.
6. AdamsKL, WendelJF (2005) Novel patterns of gene expression in polyploid plants. Trends Genet 21: 539–543.
7. ChenZJ, NiZ (2006) Mechanisms of genomic rearrangements and gene expression changes in plant polyploids. Bioessays 28: 240–252.
8. ChenZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol 58: 377–406.
9. StorchovaZ, PellmanD (2004) From polyploidy to aneuploidy, genome instability and cancer. Nat Rev Mol Cell Biol 5: 45–54.
10. WoodTE, TakebayashiN, BarkerMS, MayroseI, GreenspoonPB, et al. (2009) The frequency of polyploid speciation in vascular plants. Proc Natl Acad Sci U S A 106: 13875–13879.
11. GregoryTR, MableBK (2005) Polyploidy in animals. The Evolution of the Genome 171: 427–517.
12. StorchováS, BrenemanA, CandeJ, DunnJ, BurbankK, et al. (2006) Genome-wide genetic analysis of polyploidy in yeast. Nature 443: 541–547.
13. GriffithsS, SharpR, FooteTN, BertinI, WanousM, et al. (2006) Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat. Nature 439: 749–752.
14. SoltisDE, SoltisPS, SchemskeDW, HancockJF, ThompsonJN, et al. (2007) Autopolyploidy in angiosperms: Have we grossly underestimated the number of species? Taxon 56: 13–30.
15. HuTT, PattynP, BakkerEG, CaoJ, ChengJ-F, et al. (2011) The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nature Genet 43: 476–481.
16. Al-ShehbazIA, O'KaneSL (2002) Taxonomy and phylogeny of Arabidopsis (Brassicaceae). Arabidopsis Book 1: e0001.
17. KochMA, MatschingerM (2007) Evolution and genetic differentiation among relatives of Arabidopsis thaliana. Proc Natl Acad Sci U S A 104: 6272–6277.
18. CarvalhoA, DelgadoM, BarãoA, FrescatadaM, RibeiroE, et al. (2010) Chromosome and DNA methylation dynamics during meiosis in the autotetraploid Arabidopsis arenosa. Sex Plant Reprod 23: 29–37.
19. JørgensenMH, EhrichD, SchmicklR, KochMA, BrystingAK (2011) Interspecific and interploidal gene flow in Central European Arabidopsis (Brassicaceae). BMC Evol Biol 11: 346.
20. SchmicklR, KochMA (2011) Arabidopsis hybrid speciation processes. Proc Natl Acad Sci U S A 108: 14192–14197.
21. Ross-IbarraJ, WrightSI, FoxeJP, KawabeA, DeRose-WilsonL, et al. (2008) Patterns of polymorphism and demographic history in natural populations of Arabidopsis lyrata. PLoS ONE 3: e2411 doi:10.1371/journal.pone.0002411..
22. WrightSI, LaugaB, CharlesworthD (2003) Subdivision and haplotype structure in natural populations of Arabidopsis lyrata.. Mol Ecol 12: 1247–1263.
23. MoodyME, MuellerLD, SoltisDE (1993) Genetic variation and random drift in autotetraploid populations. Genetics 134: 649–657.
24. ArnoldB, BombliesK, WakeleyJ (2012) Extending coalescent theory to autotetraploids. Genetics 192: 195–204.
25. Arabidopsis genome initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.
26. Weir BS (1996) Genetic Data Analysis II. Sunderland, MA: Sinauer Associates.
27. NielsenR, WilliamsonS, KimY, HubiszMJ, ClarkAG, et al. (2005) Genomic scans for selective sweeps using SNP data. Genome Res 15: 1566–1575.
28. HahnS (2004) Structure and mechanism of the RNA polymerase II transcription machinery. Nat Struct Mol Biol 18: 2437–2468.
29. WangW, ChenX (2004) HUA ENHANCER3 reveals a role for a cyclin-dependent protein kinase in the specification of floral organ identity in Arabidopsis.. Development 131: 3147–3156.
30. AutranD, JonakC, BelcramK, BeemsterGTS, KronenbergerJ, et al. (2002) Cell numbers and leaf development in Arabidopsis: a functional analysis of the STRUWWELPETER gene. EMBO J 21: 6036–6049.
31. GillmorCS, ParkMY, SmithMR, PepitoneR, KerstetterRA, et al. (2010) The MED12-MED13 module of mediator regulates the timing of embryo patterning in Arabidopsis.. Development 137: 113–122.
32. SebastianJ, RaviM, AndreuzzaS, PanoliAP, MarimuthuMPA, et al. (2009) The plant adherin AtSCC2 is required for embryogenesis and sister-chromatid cohesion during meiosis in Arabidopsis. Plant J 59: 1–13.
33. LamWS, YangX, MakaroffCA (2005) Characterization of Arabidopsis thaliana SMC1 and SMC3: evidence that AtSMC3 may function beyond chromosome cohesion. J Cell Sci 118: 3037–3048 (2005).
34. SchubertV, WeißlederA, AliH, FuchsJ, LermontovaI, et al. (2009) Cohesin gene defects may impair sister chromatid alignment and genome stability in Arabidopsis thaliana. Chromosoma 118: 591–605.
35. WatanabeK, PacherM, DukowicS, SchubertV, PuchtaH, et al. (2009) The STRUCTURAL MAINTENANCE OF CHROMOSOMES 5/6 Complex Promotes Sister Chromatid Alignment and Homologous Recombination after DNA Damage in Arabidopsis thaliana.. Plant Cell 21: 2688–2699.
36. BickelJS, ChenL, HaywardJ, YeapSL, AlkersAE, et al. (2010) Structural Maintenance of Chromosomes (SMC) proteins promote homolog-independent recombination repair in meiosis crucial for germ cell genomic stability. PLoS Genet 6: e1001028 doi:10.1371/journal.pgen.1001028..
37. CarylAP, ArmstrongSJ, JonesGH, FranklinFCH (2000) A homologue of the yeast HOP1 gene is inactivated in the Arabidopsis meiotic mutant asy1. Chromosoma 109: 62–71.
38. BrandãoMM, DantasLL, Siva-FilhoMC (2009) AtPIN: Arabidopsis thaliana protein interaction network. BMC Bioinformatics 10: 454.
39. HaraK, MarukiY, LongX, YoshinoK-I, OshiroN, et al. (2002) Raptor, a binding partner of Target of Rapamycin (TOR), mediates TOR action. Cell 110: 177–189.
40. MenandB, DesnosT, NussameL, BergerF, BouchezD, et al. (2002) Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene. Proc Natl Acad Sci U S A 99: 6422–6427.
41. AndersonGH, VeitB, HansonMR (2005) The Arabidopsis AtRaptor genes are esssential for post-embryonic plant growth. BMC Biology 3: 12.
42. ParkHJ, ParkHC, LeeSY, BohnertHJ, YunD-J (2011) Ubiquitin and ubiquitin-like modifiers in plants. J Plant Biol 54: 275–285.
43. LagoC, ClericiE, MizziL, ColomboL, KaterMM (2004) TBP-associated factors in Arabidopsis. Gene 342: 231–241.
44. EarleyKW, ShookMS, Brower-TolandB, HicksL, PikaardCS (2007) In vitro specificities of Arabidopsis co-activator histone acetyltransferases: implications for histone hyperacetylation in gene activation. Plant J 52: 615–626.
45. KhannaKK, JacksonSP (2001) DNA double-strand breaks: signaling, repair and the cancer connection. Nature Genet 27: 247–254.
46. MatsudaM, MiyagawaK, TakahashiM, FukudaT, KataokaT, et al. (1999) Mutations in the RAD54 recombination gene in primary cancers. Oncogene 18: 3427–3430.
47. LiuJ, KrantzID (2008) Cohesin and human disease. Ann Rev Genom Human Genet 9: 303–320.
48. ManniniL, MengaS, MusioA (2010) The expanding universe of cohesin functions: a new stability caretaker involved in human disease and cancer. Human Mut 31: 623–630.
49. JohnsonFB, LombardDB, NeffNF, MastrangeloM-A, DewolfW, et al. (2000) Association of the Bloom Syndrome protein with Topoisomerase IIIa in somatic and meiotic cells. Cancer Res 60: 1162–1167.
50. MeyerR, FofanovV, PanigrahiAK, MerchantF, ZhangN, et al. (2009) Overexpression and mislocalization of the chromosomal segregation protein separase in multiple human cancers. Clin Cancer Res 15: 2703–2710.
51. MartelottoLG, OrtizJPA, SteinJ, EspinozaF, QuarinCL, et al. (2005) A comprehensive analysis of gene expression alterations in a newly synthesized Paspalum notatum autotetraploid. Plant Science 169: 211–220.
52. WangJ, TianL, LeeHS, WeiNE, JiangH, et al. (2006) Genome-wide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172: 507–517.
53. StuparRM, BhaskarPB, YandellBS, RensinkWA, HartAL, et al. (2007) Phenotypic and transcriptomic changes associated with potato autopolyploidization. Genetics 176: 2055–2067..
54. PignattaD, DilkesBP, YooS-Y, HenryIM, MadlungA, et al. (2010) Differential sensitivity of the Arabidopsis thaliana transcriptome and enhancers to the effects of genome doubling. New Phytologist 186: 194–206..
55. YuZ, HabererG, MatthesM, RatteiT, MayerKFX, et al. (2010) Impact of natural genetic variation on the transcriptome of autotetraploid Arabidopsis thaliana.. Proc Natl Acad U S A 107: 17809–17814.
56. NgDW-K, ZhangC, MillerM, ShenZ, BriggsSP, et al. (2012) Proteomic divergence in Arabidopsis autopolyploids and allopolyploids and their progenitors. Heredity 108: 419–430.
57. WangJ, TianL, MadlungA, LeeH-S, ChenM, et al. (2004) Stochastic and epigenetic changes of gene expression in Arabidopsis polyploids. Genetics 167: 1961–1973.
58. ShakedH, Avivi-RagolskyN, LevyAA (2006) Involvement of the Arabidopsis SWI2/SNF2 chromatin remodeling gene family in DNA damage response and recombination. Genetics 173: 985–994.
59. OsakabeK, AbeK, YoshiokaT, OsakabeY, TodorikiS, et al. (2006) Isolation and characterization of the RAD54 gene from Arabidopsis thaliana. Plant J 48: 827–842.
60. ØstmanB, HintzeA, AdamiC (2012) Impact of epistasis and pleiotropy on evolutionary adaptation. Proc R Soc B 279: 247–256.
61. TakahasiKR (2009) Coalescent under the evolution of coadaptation. Mol Ecol 18: 5018–5029.
62. HittingerCT, GonçalvesP, SampaioJP, DoverJ, JohnstonM, et al. (2010) Remarkably ancient balanced polymorphisms in a multi-locus gene network. Nature 464: 54–58.
63. BremRB, StoreyJD, WhittleJ, KruglyakL (2005) Genetic interactions between polymorphisms that affect gene expression in yeast. Nature 436: 701–703.
64. SteinerCC, WeberJN, HoekstraHE (2007) Adaptive variation in beach mice produced by two interacting pigmentation genes. PLoS Biol 5: e219 doi:10.1371/journal.pbio.0050219..
65. GerkeJ, LorenzK, CohenB (2009) Genetic interactions between transcription factors cause natural variation in yeast. Science 323: 498–501.
66. KarlowskiWM, ZielezinskiA, CarrèreJ, PontierD, LagrangeT, et al. (2010) Genome-wide computational identification of WG/GW Argonaute-binding proteins in Arabidopsis. Nucl Acids Res 38: 4231–4245.
67. ObbardDJ, JigginsFM, BradshawNJ, LittleTJ (2011) Recent and recurrent selective sweeps of the antiviral RNAi gene Argonaute-2 in three species of Drosophila. Mol Biol Evol 28: 1043–1056.
68. LeeH-C, ChangS-S, ChoudharyS, AaltoAP, MaitiM, et al. (2009) qiRNA is a new type of small interfering RNA induced by DNA damage. Nature 459: 274–278.
69. WeiW, BaZ, GaoM, WuY, MaY, et al. (2012) A role for small RNAs in DNA double-strand break repair. Cell 149: 101–112.
70. DingD-Q, OkamasaK, YamaneM, TsutsumiC, HaraguchiT, et al. (2012) Meiosis-specific noncoding RNA mediates robust pairing of homologous chromosomes in meiosis. Science 336: 732–736.
71. Durand-DubiefM, BastinP (2003) TbAGO1, an Argonaute protein required for RNA interference, is involved in mitosis and chromosome segregation in Trypanosoma brucei. BMC Biol 1: 2.
72. HallIM, NomaK-I, GrewalSI (2003) RNA interference machinery regulates chromosome dynamics during mitosis and meiosis in fission yeast. Proc Natl Acad Sci U S A 100: 193–198.
73. LeeDW, PrattRJ, McLaughlinM, AramayoR (2003) An Argonaute-like protein is required for meiotic silencing. Genetics 164: 821–828.
74. HollingsworthNM, ByersB (1989) HOP1: a yeast meiotic pairing gene. Genetics 121: 445–462.
75. NonomuraK, NakanoM, EiguchiM, SuzukiT, KurataN (2006) PAIR2 is essential for homologous chromosome synapsis in rice meiosis. J Cell Sci 119: 217–225.
76. BodenSA, LangridgeP, SpangenbergG, AbleJA (2009) TaASY1 promotes homologous chromosome interactions and is affected by deletion of Ph1. Plant J 57: 487–497.
77. AviviL (1976) The effect of genes controlling different degrees of homoeologous pairing on quadrivalent frequency in induced autotetraploid lines of Triticum longissimum. Can J Genet Cytol 18: 357–364.
78. OssowskiS, SchneebergerK, ClarkRM, LanzC, WarthmannN, et al. (2008) Sequencing of natural strains of Arabidopsis thaliana with short reads. Genome Res 18: 2024–2033.
79. GreenRE, KrauseJ, BriggsAW, MaricicT, StenzelU, et al. (2010) A draft sequence of the Neandertal genome. Science 328: 710–722.
80. McKennaA, HannaM, BanksE, SivachenkoA, CibulskisK, et al. (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20: 1297–1303.
81. ThorntonK (2003) libsequence: a C++ class library for evolutionary genetic analysis. Bioinformatics 19: 2325–2327.
82. HudsonRR (2002) Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 18: 337–338.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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