Boom-Bust Turnovers of Megabase-Sized Centromeric DNA in Solanum Species: Rapid Evolution of DNA Sequences Associated with Centromeres

. 2014 Apr ; 26 (4) : 1436-1447. [epub] 20140411

Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid24728646

Centromeres are composed of long arrays of satellite repeats in most multicellular eukaryotes investigated to date. The satellite repeat-based centromeres are believed to have evolved from "neocentromeres" that originally contained only single- or low-copy sequences. However, the emergence and evolution of the satellite repeats in centromeres has been elusive. Potato (Solanum tuberosum) provides a model system for studying centromere evolution because each of its 12 centromeres contains distinct DNA sequences, allowing comparative analysis of homoeologous centromeres from related species. We conducted genome-wide analysis of the centromeric sequences in Solanum verrucosum, a wild species closely related to potato. Unambiguous homoeologous centromeric sequences were detected in only a single centromere (Cen9) between the two species. Four centromeres (Cen2, Cen4, Cen7, and Cen10) in S. verrucosum contained distinct satellite repeats that were amplified from retrotransposon-related sequences. Strikingly, the same four centromeres in potato contain either different satellite repeats (Cen2 and Cen7) or exclusively single- and low-copy sequences (Cen4 and Cen10). Our sequence comparison of five homoeologous centromeres in two Solanum species reveals rapid divergence of centromeric sequences among closely related species. We propose that centromeric satellite repeats undergo boom-bust cycles before a favorable repeat is fixed in the population.

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Albert P.S., Gao Z., Danilova T.V., Birchler J.A. (2010). Diversity of chromosomal karyotypes in maize and its relatives. Cytogenet. Genome Res. 129: 6–16 PubMed

Altschul S.F., Madden T.L., Schäffer A.A., Zhang J.H., Zhang Z., Miller W., Lipman D.J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389–3402 PubMed PMC

Ammiraju J.S.S., et al. (2008). Dynamic evolution of oryza genomes is revealed by comparative genomic analysis of a genus-wide vertical data set. Plant Cell 20: 3191–3209 PubMed PMC

Ananiev E.V., Phillips R.L., Rines H.W. (1998). Chromosome-specific molecular organization of maize (Zea mays L.) centromeric regions. Proc. Natl. Acad. Sci. USA 95: 13073–13078 PubMed PMC

Bensasson D. (2011). Evidence for a high mutation rate at rapidly evolving yeast centromeres. BMC Evol. Biol. 11: 211. PubMed PMC

Cheng Z.K., Buell C.R., Wing R.A., Jiang J. (2002a). Resolution of fluorescence in-situ hybridization mapping on rice mitotic prometaphase chromosomes, meiotic pachytene chromosomes and extended DNA fibers. Chromosome Res. 10: 379–387 PubMed

Cheng Z.K., Dong F.G., Langdon T., Ouyang S., Buell C.R., Gu M.H., Blattner F.R., Jiang J.M. (2002b). Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell 14: 1691–1704 PubMed PMC

Dong F., Song J., Naess S.K., Helgeson J.P., Gebhardt C., Jiang J. (2000). Development and applications of a set of chromosome-specific cytogenetic DNA markers in potato. Theor. Appl. Genet. 101: 1001–1007

Dong F.G., Miller J.T., Jackson S.A., Wang G.L., Ronald P.C., Jiang J.M. (1998). Rice (Oryza sativa) centromeric regions consist of complex DNA. Proc. Natl. Acad. Sci. USA 95: 8135–8140 PubMed PMC

Du J.C., Tian Z.X., Hans C.S., Laten H.M., Cannon S.B., Jackson S.A., Shoemaker R.C., Ma J.X. (2010). Evolutionary conservation, diversity and specificity of LTR-retrotransposons in flowering plants: insights from genome-wide analysis and multi-specific comparison. Plant J. 63: 584–598 PubMed

Gao D.Y., et al. (2009). A lineage-specific centromere retrotransposon in Oryza brachyantha. Plant J. 60: 820–831 PubMed

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

Hasson D., Panchenko T., Salimian K.J., Salman M.U., Sekulic N., Alonso A., Warburton P.E., Black B.E. (2013). The octamer is the major form of CENP-A nucleosomes at human centromeres. Nat. Struct. Mol. Biol. 20: 687–695 PubMed PMC

Hawkes, J.G. (1990). The Potato: Evolution, Biodiversity and Genetic Resources. (London: Smithsonian Institution Press).

He L., Liu J., Torres G.A., Zhang H.Q., Jiang J.M., Xie C.H. (2013). Interstitial telomeric repeats are enriched in the centromeres of chromosomes in Solanum species. Chromosome Res. 21: 5–13 PubMed

Henikoff S., Ahmad K., Malik H.S. (2001). The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293: 1098–1102 PubMed

Horvath J.E., Willard H.F. (2007). Primate comparative genomics: lemur biology and evolution. Trends Genet. 23: 173–182 PubMed

Ishii K., Ogiyama Y., Chikashige Y., Soejima S., Masuda F., Kakuma T., Hiraoka Y., Takahashi K. (2008). Heterochromatin integrity affects chromosome reorganization after centromere dysfunction. Science 321: 1088–1091 PubMed

Iwata A., et al. (2013). Identification and characterization of functional centromeres of the common bean. Plant J. 76: 47–60 PubMed

Jackson S.A., Wang M.L., Goodman H.M., Jiang J.M. (1998). Application of fiber-FISH in physical mapping of Arabidopsis thaliana. Genome 41: 566–572 PubMed

Jiang J.M., Birchler J.A., Parrott W.A., Dawe R.K. (2003). A molecular view of plant centromeres. Trends Plant Sci. 8: 570–575 PubMed

Kalitsis P., Choo K.H.A. (2012). The evolutionary life cycle of the resilient centromere. Chromosoma 121: 327–340 PubMed

Ketel C., Wang H.S.W., 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

Langmead B., Trapnell C., Pop M., Salzberg S.L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10: R25. PubMed PMC

Lee H.R., Zhang W.L., Langdon T., Jin W.W., Yan H.H., Cheng Z.K., Jiang J.M. (2005). Chromatin immunoprecipitation cloning reveals rapid evolutionary patterns of centromeric DNA in Oryza species. Proc. Natl. Acad. Sci. USA 102: 11793–11798 PubMed PMC

Lou Q.F., Iovene M., Spooner D.M., Buell C.R., Jiang J.M. (2010). Evolution of chromosome 6 of Solanum species revealed by comparative fluorescence in situ hybridization mapping. Chromosoma 119: 435–442 PubMed

Macas J., Neumann P., Navrátilová A. (2007). Repetitive DNA in the pea (Pisum sativum L.) genome: comprehensive characterization using 454 sequencing and comparison to soybean and Medicago truncatula. BMC Genomics 8: 427. PubMed PMC

Marshall O.J., Chueh A.C., Wong L.H., Choo K.H.A. (2008). Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. Am. J. Hum. Genet. 82: 261–282 PubMed PMC

Melters D.P., et al. (2013). Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution. Genome Biol. 14: R10. PubMed PMC

Nagaki K., Neumann P., Zhang D., Ouyang S., Buell C.R., Cheng Z.K., Jiang J.M. (2005). Structure, divergence, and distribution of the CRR centromeric retrotransposon family in rice. Mol. Biol. Evol. 22: 845–855 PubMed

Neumann P., Navrátilová A., Koblížková A., Kejnovský E., Hřibová E., Hobza R., Widmer A., Doležel J., Macas J. (2011). Plant centromeric retrotransposons: a structural and cytogenetic perspective. Mob. DNA 2: 4. PubMed PMC

Neumann P., Navrátilová A., Schroeder-Reiter E., Koblížková A., Steinbauerová V., Chocholová E., Novák P., Wanner G., Macas J. (2012). Stretching the rules: monocentric chromosomes with multiple centromere domains. PLoS Genet. 8: e1002777. PubMed PMC

Novák P., Neumann P., Macas J. (2010). Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinformatics 11: 378. PubMed PMC

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

Pendinen G., Spooner D.M., Jiang J.M., Gavrilenko T. (2012). Genomic in situ hybridization reveals both auto- and allopolyploid origins of different North and Central American hexaploid potato (Solanum sect. Petota) species. Genome 55: 407–415 PubMed

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

Sanetomo R., Hosaka K. (2013). A recombination-derived mitochondrial genome retained stoichiometrically only among Solanum verrucosum Schltdl. and Mexican polyploid wild potato species. Genet. Resour. Crop Evol. 60: 2391–2404

Shang W.-H., et al. (2013). Chromosome engineering allows the efficient isolation of vertebrate neocentromeres. Dev. Cell 24: 635–648 PubMed PMC

Shang W.H., Hori T., Toyoda A., Kato J., Popendorf K., Sakakibara Y., Fujiyama A., Fukagawa T. (2010). Chickens possess centromeres with both extended tandem repeats and short non-tandem-repetitive sequences. Genome Res. 20: 1219–1228 PubMed PMC

Tek A.L., Jiang J.M. (2004). The centromeric regions of potato chromosomes contain megabase-sized tandem arrays of telomere-similar sequence. Chromosoma 113: 77–83 PubMed

Xu X., et al. Potato Genome Sequencing Consortium (2011). Genome sequence and analysis of the tuber crop potato. Nature 475: 189–195 PubMed

Vafa O., Sullivan K.F. (1997). Chromatin containing CENP-A and alpha-satellite DNA is a major component of the inner kinetochore plate. Curr. Biol. 7: 897–900 PubMed

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

Wang L.S., Zeng Z.X., Zhang W.L., Jiang J.M. (2014). Three potato centromeres are associated with distinct haplotypes with or without megabase-sized satellite repeat arrays. Genetics 196: 397–401 PubMed PMC

Willard H.F. (1991). Evolution of alpha satellite. Curr. Opin. Genet. Dev. 1: 509–514 PubMed

Willard H.F., Waye J.S. (1987). Hierarchical order in chromosome-specific human alpha satellite DNA. Trends Genet. 3: 192–198

Yan H.H., Talbert P.B., Lee H.R., Jett J., Henikoff S., Chen F., Jiang J.M. (2008). Intergenic locations of rice centromeric chromatin. PLoS Biol. 6: e286. PubMed PMC

Yan H.H., et al. (2006). Genomic and genetic characterization of rice Cen3 reveals extensive transcription and evolutionary implications of a complex centromere. Plant Cell 18: 2123–2133 PubMed PMC

Yi C.D., Zhang W.L., Dai X.B., Li X., Gong Z.Y., Zhou Y., Liang G.H., Gu M.H. (2013). Identification and diversity of functional centromere satellites in the wild rice species Oryza brachyantha. Chromosome Res. 21: 725–737 PubMed

Zhang T., Talbert P.B., Zhang W.L., Wu Y.F., Yang Z.J., Henikoff J.G., Henikoff S., Jiang J.M. (2013). The CentO satellite confers translational and rotational phasing on cenH3 nucleosomes in rice centromeres. Proc. Natl. Acad. Sci. USA 110: E4875–E4883 PubMed PMC

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