Interspecific introgression mediates adaptation to whole genome duplication

. 2019 Nov 18 ; 10 (1) : 5218. [epub] 20191118

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid31740675

Grantová podpora
BB/P013511/1 RCUK | Biotechnology and Biological Sciences Research Council (BBSRC) - International
BB/M01973X/1 RCUK | Biotechnology and Biological Sciences Research Council (BBSRC) - International

Odkazy

PubMed 31740675
PubMed Central PMC6861236
DOI 10.1038/s41467-019-13159-5
PII: 10.1038/s41467-019-13159-5
Knihovny.cz E-zdroje

Adaptive gene flow is a consequential phenomenon across all kingdoms. Although recognition is increasing, there is no study showing that bidirectional gene flow mediates adaptation at loci that manage core processes. We previously discovered concerted molecular changes among interacting members of the meiotic machinery controlling crossover number upon adaptation to whole-genome duplication (WGD) in Arabidopsis arenosa. Here we conduct a population genomic study to test the hypothesis that adaptation to WGD has been mediated by adaptive gene flow between A. arenosa and A. lyrata. We find that A. lyrata underwent WGD more recently than A. arenosa, suggesting that pre-adapted alleles have rescued nascent A. lyrata, but we also detect gene flow in the opposite direction at functionally interacting loci under the most extreme levels of selection. These data indicate that bidirectional gene flow allowed for survival after WGD, and that the merger of these species is greater than the sum of their parts.

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Abbott R, et al. Hybridization and speciation. J. Evolution Biol. 2013;26:229–246. doi: 10.1111/j.1420-9101.2012.02599.x. PubMed DOI

Selmecki AM, et al. Polyploidy can drive rapid adaptation in yeast. Nature. 2015;519:349–351. doi: 10.1038/nature14187. PubMed DOI PMC

Doyle JJ, Coate JE. Polyploidy, the nucleotype, and novelty: The impact of genome doubling on the biology of the cell. Int. J. Plant Sci. 2019;180:1–52. doi: 10.1086/700636. DOI

Cui L, et al. Widespread genome duplications throughout the history of flowering plants. Genome Res. 2006;16:738–749. doi: 10.1101/gr.4825606. PubMed DOI PMC

Schmickl R, Marburger S, Bray S, Yant L. Hybrids and horizontal transfer: Introgression allows adaptive allele discovery. J. Exp. Bot. 2017;68:5453–5470. doi: 10.1093/jxb/erx297. PubMed DOI

Mallet J, Besansky N, Hahn MW. How reticulated are species? Bioessays. 2015;38:140–149. doi: 10.1002/bies.201500149. PubMed DOI PMC

Yant L, Bomblies K. Genomic studies of adaptive evolution in outcrossing Arabidopsis species. Curr. Opin. Plant Biol. 2017;36:9–14. doi: 10.1016/j.pbi.2016.11.018. PubMed DOI

Schmickl R, Koch MA. Arabidopsis hybrid speciation processes. Proc. Natl Acad. Sci. USA. 2011;108:14192–14197. doi: 10.1073/pnas.1104212108. PubMed DOI PMC

Arnold B, Kim ST, Bomblies K. Single geographic origin of a widespread autotetraploid Arabidopsis arenosa lineage followed by interploidy admixture. Mol. Biol. Evol. 2015;32:1382–1395. doi: 10.1093/molbev/msv089. PubMed DOI

Kolář F, et al. Northern glacial refugia and altitudinal niche divergence shape genome-wide differentiation in the emerging plant model Arabidopsis arenosa. Mol. Ecol. 2016;25:3929–3949. doi: 10.1111/mec.13721. PubMed DOI

Baduel P, Hunter B, Yeola S, Bomblies K. Genetic basis and evolution of rapid cycling in railway populations of tetraploid Arabidopsis arenosa. PLoS Genet. 2018;14:e1007510–e1007526. doi: 10.1371/journal.pgen.1007510. PubMed DOI PMC

Hollister JD, et al. Genetic adaptation associated with genome-doubling in autotetraploid Arabidopsis arenosa. PLoS Genet. 2012;8:e1003093. doi: 10.1371/journal.pgen.1003093. PubMed DOI PMC

Yant L, et al. Meiotic adaptation to genome duplication in Arabidopsis arenosa. Curr. Biol. 2013;23:2151–2156. doi: 10.1016/j.cub.2013.08.059. PubMed DOI PMC

Bomblies K, Madlung A. Polyploidy in the Arabidopsis genus. Chromosome Res. 2014;22:117–134. doi: 10.1007/s10577-014-9416-x. PubMed DOI

Bomblies K, Higgins JD, Yant L. Meiosis evolves: Adaptation to external and internal environments. New Phytol. 2015;208:306–323. doi: 10.1111/nph.13499. PubMed DOI

Clauss MJ, Mitchell-Olds T. Population genetic structure of Arabidopsis lyrata in Europe. Mol. Ecol. 2006;15:2753–2766. doi: 10.1111/j.1365-294X.2006.02973.x. PubMed DOI

Ross-Ibarra J, et al. Patterns of polymorphism and demographic history in natural populations of Arabidopsis lyrata. PLoS ONE. 2008;3:e2411. doi: 10.1371/journal.pone.0002411. PubMed DOI PMC

Ansell SW, et al. Population structure and historical biogeography of European Arabidopsis lyrata. Heredity. 2010;105:543–553. doi: 10.1038/hdy.2010.10. PubMed DOI

Jørgensen MH, Ehrich D, Schmickl R, Koch MA, Brysting AK. Interspecific and interploidal gene flow in Central European Arabidopsis (Brassicaceae) BMC Evol. Biol. 2011;11:346. doi: 10.1186/1471-2148-11-346. PubMed DOI PMC

Lafon-Placette CL, Köhler C. Endosperm-based postzygotic hybridization barriers: developmental mechanisms and evolutionary drivers. Mol. Ecol. 2016;25:2620–2629. doi: 10.1111/mec.13552. PubMed DOI

Monnahan P, et al. Pervasive population genomic consequences of genome duplication in Arabidopsis arenosa. Nat. Ecol. Evol. 2019;3:1–15. doi: 10.1038/s41559-019-0807-4. PubMed DOI

Hohmann N, Koch MA. An Arabidopsis introgression zone studied at high spatio-temporal resolution: interglacial and multiple genetic contact exemplified using whole nuclear and plastid genomes. BMC Genomics. 2017;18:1–18. doi: 10.1186/s12864-017-4220-6. PubMed DOI PMC

Excoffier L, Dupanloup I, Huerta-Sánchez E, Sousa VC, Foll M. Robust demographic inference from genomic and SNP data. PLoS Genet. 2013;9:e1003905. doi: 10.1371/journal.pgen.1003905. PubMed DOI PMC

Hohmann N, Wolf EM, Lysak MA, Koch MA. A time-calibrated road map of brassicaceae species radiation and evolutionary history. Plant Cell. 2015;27:2770–2784. PubMed PMC

Beilstein MA, Nagalingum NS, Clements MD, Manchester SR, Mathews S. Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. Proc. Natl Acad. Sci. USA. 2010;107:18724–18728. doi: 10.1073/pnas.0909766107. PubMed DOI PMC

Ehlers J., Gibbard P.L., Hughes P.D. Past Glacial Environments. 2018. Quaternary Glaciations and Chronology; pp. 77–101.

Li H, Durbin R. Inference of human population history from individual whole-genome sequences. Nature. 2011;475:493–496. doi: 10.1038/nature10231. PubMed DOI PMC

Cruickshank TE, Hahn MW. Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol. Ecol. 2014;23:3133–3157. doi: 10.1111/mec.12796. PubMed DOI

Weir B. S. Genetic Data Analysis II. Biometrics. 1997;53(1):392. doi: 10.2307/2533134. DOI

Ronfort J, Jenczewski E, Bataillon T, Rousset F. Analysis of population structure in autotetraploid species. Genetics. 1998;150:921–930. PubMed PMC

Arnold Brian J., Lahner Brett, DaCosta Jeffrey M., Weisman Caroline M., Hollister Jesse D., Salt David E., Bomblies Kirsten, Yant Levi. Borrowed alleles and convergence in serpentine adaptation. Proceedings of the National Academy of Sciences. 2016;113(29):8320–8325. doi: 10.1073/pnas.1600405113. PubMed DOI PMC

Novikova PY, et al. Sequencing of the genus Arabidopsis identifies a complex history of nonbifurcating speciation and abundant trans-specific polymorphism. Nat. Genet. 2016;48:1077–1082. doi: 10.1038/ng.3617. PubMed DOI

Barow M. Endopolyploidy in seed plants. Bioessays. 2006;28:271–281. doi: 10.1002/bies.20371. PubMed DOI

Breuer C, Braidwood L, Sugimoto K. Endocycling in the path of plant development. Curr. Opin. Plant Biol. 2014;17:78–85. doi: 10.1016/j.pbi.2013.11.007. PubMed DOI

Scholes DR, Paige KN. Plasticity in ploidy: a generalized response to stress. Trends Plant Sci. 2015;20:165–175. doi: 10.1016/j.tplants.2014.11.007. PubMed DOI

Albertin W, et al. Autopolyploidy in cabbage (Brassica oleracea L.) does not alter significantly the proteomes of green tissues. Proteomics. 2005;5:2131–2139. doi: 10.1002/pmic.200401092. PubMed DOI

Stupar RM, et al. Phenotypic and transcriptomic changes associated with potato autopolyploidization. Genetics. 2007;176:2055–2067. doi: 10.1534/genetics.107.074286. PubMed DOI PMC

del Pozo JC, Ramirez-Parra E. Deciphering the molecular bases for drought tolerance in Arabidopsis autotetraploids. Plant, Cell Environ. 2014;37:2722–2737. doi: 10.1111/pce.12344. PubMed DOI

Coate JE, Doyle JJ. Variation in transcriptome size: are we getting the message? Chromosoma. 2014;124:27–43. doi: 10.1007/s00412-014-0496-3. PubMed DOI

Martin SH, Van Belleghem SM. Exploring evolutionary relationships across the genome using topology weighting. Genetics. 2017;206:429–438. doi: 10.1534/genetics.116.194720. PubMed DOI PMC

Christe C, et al. Adaptive evolution and segregating load contribute to the genomic landscape of divergence in two tree species connected by episodic gene flow. Mol. Ecol. 2016;26:59–76. doi: 10.1111/mec.13765. PubMed DOI

Huerta-Sánchez E, et al. Altitude adaptation in Tibetans caused by introgression of Denisovan-like DNA. Nature. 2014;512:194–197. doi: 10.1038/nature13408. PubMed DOI PMC

Hamilton JA, la Torre De,AR, Aitken SN. Fine-scale environmental variation contributes to introgression in a three-species spruce hybrid complex. Tree Genet. Genomes. 2014;11:95–14.

Ronfort J. The mutation load under tetrasomic inheritance and its consequences for the evolution of the selfing rate in autotetraploid species. Genet. Res. 1999;74:31–42. doi: 10.1017/S0016672399003845. DOI

Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 2011;17:10–12. doi: 10.14806/ej.17.1.200. DOI

Bolger A, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC

Hu TT, et al. The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat. Genet. 2011;43:476–481. doi: 10.1038/ng.807. PubMed DOI PMC

Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv (2013) arXiv:1303.3997

Raj A, Stephens M, Pritchard JK. FastSTRUCTURE: Variational inference of population structure in large SNP data sets. Genetics. 2014;197:573–589. doi: 10.1534/genetics.114.164350. PubMed DOI PMC

Pritchard JK, Pickrell JK, Coop G. The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation. Curr. Biol. 2010;20:R208–R215. doi: 10.1016/j.cub.2009.11.055. PubMed DOI PMC

Jombart T, Ahmed I. adegenet 1.3-1: New tools for the analysis of genome-wide SNP data. Bioinformatics. 2011;27:3070–3071. doi: 10.1093/bioinformatics/btr521. PubMed DOI PMC

Higgins, J. D., Wright, K. M., Bomblies, K. & Franklin, F. C. H. Cytological techniques to analyze meiosis in Arabidopsis arenosa for investigating adaptation to polyploidy. Front. Plant Sci. 4, 546 (2014). PubMed PMC

Weir BS, Cockerham CC. Estimating F-statistics for the analysis of population structure. Evolution. 1984;38:1358–1370. PubMed

Cingolani P, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin) 2012;6:80–92. doi: 10.4161/fly.19695. PubMed DOI PMC

Rawat V, et al. Improving the annotation of Arabidopsis lyrata using RNA-Seq data. PLoS ONE. 2015;10:e0137391–12. doi: 10.1371/journal.pone.0137391. PubMed DOI PMC

Gascuel O. BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol. Biol. Evol. 1997;14:685–695. doi: 10.1093/oxfordjournals.molbev.a025808. PubMed DOI

Guindon S, et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 2010;59:307–321. doi: 10.1093/sysbio/syq010. PubMed DOI

Ewing G, Hermisson J. MSMS: A coalescent simulation program including recombination, demographic structure and selection at a single locus. Bioinformatics. 2010;26:2064–2065. doi: 10.1093/bioinformatics/btq322. PubMed DOI PMC

Rambaut A, Grassly NC. Seq-Gen: an application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic trees. Computer Appl. Biosci.: CABIOS. 1997;13:235–238. PubMed

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