Genome Evolution in Arabideae Was Marked by Frequent Centromere Repositioning

. 2020 Mar ; 32 (3) : 650-665. [epub] 20200109

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid31919297

Centromere position may change despite conserved chromosomal collinearity. Centromere repositioning and evolutionary new centromeres (ENCs) were frequently encountered during vertebrate genome evolution but only rarely observed in plants. The largest crucifer tribe, Arabideae (∼550 species; Brassicaceae, the mustard family), diversified into several well-defined subclades in the virtual absence of chromosome number variation. Bacterial artificial chromosome-based comparative chromosome painting uncovered a constancy of genome structures among 10 analyzed genomes representing seven Arabideae subclades classified as four genera: Arabis, Aubrieta, Draba, and Pseudoturritis Interestingly, the intra-tribal diversification was marked by a high frequency of ENCs on five of the eight homoeologous chromosomes in the crown-group genera, but not in the most ancestral Pseudoturritis genome. From the 32 documented ENCs, at least 26 originated independently, including 4 ENCs recurrently formed at the same position in not closely related species. While chromosomal localization of ENCs does not reflect the phylogenetic position of the Arabideae subclades, centromere seeding was usually confined to long chromosome arms, transforming acrocentric chromosomes to (sub)metacentric chromosomes. Centromere repositioning is proposed as the key mechanism differentiating overall conserved homoeologous chromosomes across the crown-group Arabideae subclades. The evolutionary significance of centromere repositioning is discussed in the context of possible adaptive effects on recombination and epigenetic regulation of gene expression.

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Al-Shehbaz I.A. (2012). A generic and tribal synopsis of the Brassicaceae (Cruciferae). Taxon 61: 931–954.

Ávila Robledillo L., Koblížková A., Novák P., Böttinger K., Vrbová I., Neumann P., Schubert I., Macas J. (2018). Satellite DNA in Vicia faba is characterized by remarkable diversity in its sequence composition, association with centromeres, and replication timing. Sci. Rep. 8: 5838. PubMed PMC

Andrews S. (2010). FastQC: A quality control tool for high throughput sequence data. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc.

Bao W., Kojima K.K., Kohany O. (2015). Repbase update, a database of repetitive elements in eukaryotic genomes. Mob. DNA 6: 11. PubMed PMC

Bracewell R., Chatla K., Nalley M.J., Bachtrog D. (2019). Dynamic turnover of centromeres drives karyotype evolution in Drosophila. eLife 8: e49002. PubMed PMC

Carbone L., et al. (2006). Evolutionary movement of centromeres in horse, donkey, and zebra. Genomics 87: 777–782. PubMed

Cardone M.F., et al. (2006). Independent centromere formation in a capricious, gene-free domain of chromosome 13q21 in Old World monkeys and pigs. Genome Biol. 7: R91. PubMed PMC

Cheng F., Wu J., Fang L., Wang X. (2012). Syntenic gene analysis between Brassica rapa and other Brassicaceae species. Front. Plant Sci. 3: 198. PubMed PMC

Chiatante G., Capozzi O., Svartman M., Perelman P., Centrone L., Romanenko S.S., Ishida T., Valeri M., Roelke-Parker M.E., Stanyon R. (2017). Centromere repositioning explains fundamental number variability in the New World monkey genus Saimiri. Chromosoma 126: 519–529. PubMed

Comai L., Maheshwari S., Marimuthu M.P.A. (2017). Plant centromeres.​ Curr. Opin. Plant Biol. 36: 158–167. PubMed

Delcher A.L., Phillippy A., Carlton J., Salzberg S.L. (2002). Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res. 30: 2478–2483. PubMed PMC

Drouaud J., Camilleri C., Bourguignon P.Y., Canaguier A., Bérard A., Vezon D., Giancola S., Brunel D., Colot V., Prum B., Quesneville H., Mézard C. (2006). Variation in crossing-over rates across chromosome 4 of Arabidopsis thaliana reveals the presence of meiotic recombination “hot spots”. Genome Res. 16: 106–114. PubMed PMC

Geiser C., Mandáková T., Arrigo N., Lysak M.A., Parisod C. (2016). Repeated whole-genome duplication, karyotype reshuffling, and biased retention of stress-responding genes in Buckler mustard. Plant Cell 28: 17–27. PubMed PMC

Gong Z., Wu Y., Koblízková A., Torres G.A., Wang K., Iovene M., Neumann P., Zhang W., Novák P., Buell C.R., Macas J., Jiang J. (2012). Repeatless and repeat-based centromeres in potato: Implications for centromere evolution. Plant Cell 24: 3559–3574. PubMed PMC

Grant V. (1981). Plant Speciation. (New York: Columbia University Press; ).

Guo X., Liu J., Hao G., Zhang L., Mao K., Wang X., Zhang D., Ma T., Hu Q., Al-Shehbaz I.A., Koch M.A. (2017). Plastome phylogeny and early diversification of Brassicaceae. BMC Genomics 18: 176. PubMed PMC

Han Y., Zhang Z., Liu C., Liu J., Huang S., Jiang J., Jin W. (2009). Centromere repositioning in cucurbit species: Implication of the genomic impact from centromere activation and inactivation. Proc. Natl. Acad. Sci. USA 106: 14937–14941. PubMed PMC

Hohmann N., Wolf E.M., Lysak M.A., Koch M.A. (2015). A time-calibrated road map of Brassicaceae species radiation and evolutionary history. Plant Cell 27: 2770–2784. PubMed PMC

Hu T.T., et al. (2011). The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat. Genet. 43: 476–481. PubMed PMC

Huang J., Zhao Y., Bai D., Shiraigol W., Li B., Yang L., Wu J., Bao W., Ren X., Jin B., Zhao Q., Li A., et al. (2015). Donkey genome and insight into the imprinting of fast karyotype evolution. Sci. Rep. 5: 14106. PubMed PMC

Huang X.-C., German D.A., Koch M.A. (2019). Temporal patterns of diversification in Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization events. Ann. Bot. 125: 29–47. PubMed PMC

Jordon-Thaden I., Hase I., Al-Shehbaz I., Koch M.A. (2010). Molecular phylogeny and systematics of the genus Draba (Brassicaceae) and identification of its most closely related genera. Mol. Phylogenet. Evol. 55: 524–540. PubMed

Jordon-Thaden I.E., Al-Shehbaz I.A., Koch M.A. (2013). Species richness of the globally distributed, arctic–alpine genus Draba L. (Brassicaceae). Alp. Bot. 123: 97–106.

Karl R., Koch M.A. (2013). A world-wide perspective on crucifer speciation and evolution: Phylogenetics, biogeography and trait evolution in tribe Arabideae. Ann. Bot. 112: 983–1001. PubMed PMC

Karl R., Koch M.A. (2014). Phylogenetic signatures of adaptation: The Arabis hirsuta species aggregate (Brassicaceae) revisited. Perspect. Plant Ecol. Evol. Syst. 16: 247–264.

Karl R., Kiefer C., Ansell S.W., Koch M.A. (2012). Systematics and evolution of Arctic-Alpine Arabis alpina (Brassicaceae) and its closest relatives in the eastern Mediterranean. Am. J. Bot. 99: 778–794. PubMed

Katoh K., Standley D.M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 30: 772–780. PubMed PMC

Kearse M., et al. (2012). Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649. PubMed PMC

Ketel C., Wang H.S., McClellan M., Bouchonville K., Selmecki A., Lahav T., Gerami-Nejad M., Berman J. (2009). Neocentromeres form efficiently at multiple possible loci in Candida albicans. PLoS Genet. 5: e1000400. PubMed PMC

Kiefer C., Severing E., Karl R., Bergonzi S., Koch M., Tresch A., Coupland G. (2017). Divergence of annual and perennial species in the Brassicaceae and the contribution of cis-acting variation at FLC orthologues. Mol. Ecol. 26: 3437–3457. PubMed PMC

Kiefer C., Willing E.-M., Jiao W.-B., Sun H., Piednoël M., Hümann U., Hartwig B., Koch M.A., Schneeberger K. (2019). Interspecies association mapping links reduced CG to TG substitution rates to the loss of gene-body methylation. Nat. Plants 5: 846–855. PubMed

Koch M.A., Karl R., German D.A., Al-Shehbaz I.A. (2012). Systematics, taxonomy and biogeography of three new Asian genera of Brassicaceae tribe Arabideae: An ancient distribution circle around the Asian high mountains. Taxon 61: 955–969.

Koch M.A., Karl R., German D.A. (2017). Underexplored biodiversity of eastern Mediterranean biota: Systematics and evolutionary history of the genus Aubrieta (Brassicaceae). Ann. Bot. 119: 39–57. PubMed PMC

Kocsis E., Trus B.L., Steer C.J., Bisher M.E., Steven A.C. (1991). Image averaging of flexible fibrous macromolecules: The clathrin triskelion has an elastic proximal segment. J. Struct. Biol. 107: 6–14. PubMed

Kohany O., Gentles A.J., Hankus L., Jurka J. (2006). Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinformatics 7: 474. PubMed PMC

Kozlov A.M., Darriba D., Flouri T., Morel B., Stamatakis A. (2019). RAxML-NG: A fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35: 4453–4455. PubMed PMC

Lamb J.C., Meyer J.M., Birchler J.A. (2007). A hemicentric inversion in the maize line knobless Tama flint created two sites of centromeric elements and moved the kinetochore-forming region. Chromosoma 116: 237–247. PubMed

Leinonen R., Sugawara H., Shumway M. (2011) International Nucleotide Sequence Database Collaboration. (2011). The sequence read archive. Nucleic Acids Res. 39: D19–D21. PubMed PMC

Levin D.A. (2002). The Role of Chromosomal Change in Plant Evolution. (New York: Oxford University Press; ).

Liao Y., Zhang X., Li B., Liu T., Chen J., Bai Z., Wang M., Shi J., Walling J.G., Wing R.A., Jiang J., Chen M. (2018). Comparison of Oryza sativa and Oryza brachyantha genomes reveals selection-driven gene escape from the centromeric regions. Plant Cell 30: 1729–1744. PubMed PMC

Liu Y., Su H., Pang J., Gao Z., Wang X.J., Birchler J.A., Han F. (2015). Sequential de novo centromere formation and inactivation on a chromosomal fragment in maize. Proc. Natl. Acad. Sci. USA 112: E1263–E1271. PubMed PMC

Locke D.P., et al. (2011). Comparative and demographic analysis of orang-utan genomes. Nature 469: 529–533. PubMed PMC

Lomiento M., Jiang Z., D’Addabbo P., Eichler E.E., Rocchi M. (2008). Evolutionary-new centromeres preferentially emerge within gene deserts. Genome Biol. 9: R173. PubMed PMC

López E., Pradillo M., Oliver C., Romero C., Cuñado N., Santos J.L. (2012). Looking for natural variation in chiasma frequency in Arabidopsis thaliana. J. Exp. Bot. 63: 887–894. PubMed

Lu M., He X. (2019). Centromere repositioning causes inversion of meiosis and generates a reproductive barrier. Proc. Natl. Acad. Sci. USA 116: 21580–21591. PubMed PMC

Lysak M.A., Berr A., Pecinka A., Schmidt R., McBreen K., Schubert I. (2006). Mechanisms of chromosome number reduction in Arabidopsis thaliana and related Brassicaceae species. Proc. Natl. Acad. Sci. USA 103: 5224–5229. PubMed PMC

Lysak M.A., Mandáková T., Schranz M.E. (2016). Comparative paleogenomics of crucifers: Ancestral genomic blocks revisited. Curr. Opin. Plant Biol. 30: 108–115. PubMed

Mandáková T., Lysak M.A. (2008). Chromosomal phylogeny and karyotype evolution in x=7 crucifer species (Brassicaceae). Plant Cell 20: 2559–2570. PubMed PMC

Mandáková T., Lysak M.A. (2016a). Painting of Arabidopsis chromosomes with chromosome-specific BAC clones. Curr. Protoc. Plant Biol. 1: 359–371. PubMed

Mandáková T., Lysak M.A. (2016b). Chromosome preparation for cytogenetic analyses in Arabidopsis. Curr. Protoc. Plant Biol. 1: 43–51. PubMed

Mandáková T., Kovarík A., Zozomová-Lihová J., Shimizu-Inatsugi R., Shimizu K.K., Mummenhoff K., Marhold K., Lysak M.A. (2013). The more the merrier: Recent hybridization and polyploidy in cardamine. Plant Cell 25: 3280–3295. PubMed PMC

Mandáková T., Hloušková P., German D.A., Lysak M.A. (2017). Monophyletic origin and evolution of the largest crucifer genomes. Plant Physiol. 174: 2062–2071. PubMed PMC

Mandáková T., Zozomová-Lihová J., Kudoh H., Zhao Y., Lysak M.A., Marhold K. (2019a). The story of promiscuous crucifers: Origin and genome evolution of an invasive species, Cardamine occulta (Brassicaceae), and its relatives. Ann. Bot. 124: 209–220. PubMed PMC

Mandáková T., Pouch M., Brock J.R., Al-Shehbaz I.A., Lysak M.A. (2019b). Origin and evolution of diploid and allopolyploid Camelina genomes were accompanied by chromosome shattering. Plant Cell 31: 2596–2612. PubMed PMC

Montefalcone G., Tempesta S., Rocchi M., Archidiacono N. (1999). Centromere repositioning. Genome Res. 9: 1184–1188. PubMed PMC

Neumann P., Novák P., Hoštáková N., Macas J. (2019). Systematic survey of plant LTR-retrotransposons elucidates phylogenetic relationships of their polyprotein domains and provides a reference for element classification. Mob. DNA 10: 1. PubMed PMC

Nikolov L.A., Shushkov P., Nevado B., Gan X., Al-Shehbaz I.A., Filatov D., Bailey C.D., Tsiantis M. (2019). Resolving the backbone of the Brassicaceae phylogeny for investigating trait diversity. New Phytol. 222: 1638–1651. PubMed

Novák P., Neumann P., Pech J., Steinhaisl J., Macas J. (2013). RepeatExplorer: A Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics 29: 792–793. PubMed

Novák P., Ávila Robledillo L., Koblížková A., Vrbová I., Neumann P., Macas J. (2017). TAREAN: A computational tool for identification and characterization of satellite DNA from unassembled short reads. Nucleic Acids Res. 45: e111. PubMed PMC

Piras F.M., Nergadze S.G., Magnani E., Bertoni L., Attolini C., Khoriauli L., Raimondi E., Giulotto E. (2010). Uncoupling of satellite DNA and centromeric function in the genus Equus. PLoS Genet. 6: e1000845. PubMed PMC

Rieseberg L.H. (2001). Chromosomal rearrangements and speciation. Trends Ecol. Evol. (Amst.) 16: 351–358. PubMed

Ritz K.R., Noor M.A.F., Singh N.D. (2017). Variation in recombination rate: Adaptive or not? Trends Genet. 33: 364–374. PubMed

Rocchi M., Archidiacono N., Schempp W., Capozzi O., Stanyon R. (2012). Centromere repositioning in mammals. Heredity 108: 59–67. PubMed PMC

Schneider K.L., Xie Z., Wolfgruber T.K., Presting G.G. (2016). Inbreeding drives maize centromere evolution. Proc. Natl. Acad. Sci. USA 113: E987–E996. PubMed PMC

Schranz M.E., Lysak M.A., Mitchell-Olds T. (2006). The ABC’s of comparative genomics in the Brassicaceae: Building blocks of crucifer genomes. Trends Plant Sci. 11: 535–542. PubMed

Schubert I. (2018). What is behind “centromere repositioning”? Chromosoma 127: 229–234. PubMed

Sharma A., Wolfgruber T.K., Presting G.G. (2013). Tandem repeats derived from centromeric retrotransposons. BMC Genomics 14: 142. PubMed PMC

Tolomeo D., et al. (2017). Epigenetic origin of evolutionary novel centromeres. Sci. Rep. 7: 41980. PubMed PMC

Ventura M., et al. (2004). Recurrent sites for new centromere seeding. Genome Res. 14: 1696–1703. PubMed PMC

Ventura M., Antonacci F., Cardone M.F., Stanyon R., D’Addabbo P., Cellamare A., Sprague L.J., Eichler E.E., Archidiacono N., Rocchi M. (2007). Evolutionary formation of new centromeres in macaque. Science 316: 243–246. PubMed

Wang H., Bennetzen J.L. (2012). Centromere retention and loss during the descent of maize from a tetraploid ancestor. Proc. Natl. Acad. Sci. USA 109: 21004–21009. PubMed PMC

Wang K., Wu Y., Zhang W., Dawe R.K., Jiang J. (2014). Maize centromeres expand and adopt a uniform size in the genetic background of oat. Genome Res. 24: 107–116. PubMed PMC

White M.J.D. (1978). Modes of Speciation. (San Francisco: W.H. Freeman & Co.).

Willing E.-M., et al. (2015). Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation. Nat. Plants 1: 14023. PubMed

Wolfgruber T.K., Nakashima M.M., Schneider K.L., Sharma A., Xie Z., Albert P.S., Xu R., Bilinski P., Dawe R.K., Ross-Ibarra J., Birchler J.A., Presting G.G. (2016). High quality maize centromere 10 sequence reveals evidence of frequent recombination events. Front. Plant Sci. 7: 308. PubMed PMC

Yang L., et al. (2014). Next-generation sequencing, FISH mapping and synteny-based modeling reveal mechanisms of decreasing dysploidy in Cucumis. Plant J. 77: 16–30. PubMed

Zhao H., Zeng Z., Koo D.H., Gill B.S., Birchler J.A., Jiang J. (2017). Recurrent establishment of de novo centromeres in the pericentromeric region of maize chromosome 3. Chromosome Res. 25: 299–311. PubMed

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