BACKGROUND: The centromeric and pericentromeric regions of plant chromosomes are colonized by Ty3/gypsy retrotransposons, which, on the basis of their reverse transcriptase sequences, form the chromovirus CRM clade. Despite their potential importance for centromere evolution and function, they have remained poorly characterized. In this work, we aimed to carry out a comprehensive survey of CRM clade elements with an emphasis on their diversity, structure, chromosomal distribution and transcriptional activity. RESULTS: We have surveyed a set of 190 CRM elements belonging to 81 different retrotransposon families, derived from 33 host species and falling into 12 plant families. The sequences at the C-terminus of their integrases were unexpectedly heterogeneous, despite the understanding that they are responsible for targeting to the centromere. This variation allowed the division of the CRM clade into the three groups A, B and C, and the members of each differed considerably with respect to their chromosomal distribution. The differences in chromosomal distribution coincided with variation in the integrase C-terminus sequences possessing a putative targeting domain (PTD). A majority of the group A elements possess the CR motif and are concentrated in the centromeric region, while members of group C have the type II chromodomain and are dispersed throughout the genome. Although representatives of the group B lack a PTD of any type, they appeared to be localized preferentially in the centromeres of tested species. All tested elements were found to be transcriptionally active. CONCLUSIONS: Comprehensive analysis of the CRM clade elements showed that genuinely centromeric retrotransposons represent only a fraction of the CRM clade (group A). These centromeric retrotransposons represent an active component of centromeres of a wide range of angiosperm species, implying that they play an important role in plant centromere evolution. In addition, their transcriptional activity is consistent with the notion that the transcription of centromeric retrotransposons has a role in normal centromere function.

Biology Centre of the Academy of Sciences of the Czech Republic Institute of Plant Molecular Biology Branišovská 31 České Budějovice CZ 37005 Czech Republic

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Arkhipova IR. Transposable elements in the animal kingdom. Mol Biol. 2001;35:157–167. doi: 10.1023/A:1010485915642. PubMed DOI

Bennetzen JL. The contributions of retroelements to plant genome organization, function and evolution. Trends Microbiol. 1996;4:347–353. doi: 10.1016/0966-842X(96)10042-1. PubMed DOI

Deininger PL, Batzer MA. Mammalian retroelements. Genome Res. 2002;12:1455–1465. doi: 10.1101/gr.282402. PubMed DOI

Hirochika H, Hirochika R. Ty1-copia group retrotransposons as ubiquitous components of plant genomes. Jpn J Genet. 1993;68:35–46. doi: 10.1266/jjg.68.35. PubMed DOI

Kumekawa N, Ohtsubo E, Ohtsubo H. Identification and phylogenetic analysis of gypsy-type retrotransposons in the plant kingdom. Genes Genetic Syst. 1999;74:299–307. doi: 10.1266/ggs.74.299. PubMed DOI

Suoniemi A, Tanskanen J, Schulman AH. Gypsy-like retrotransposons are widespread in the plant kingdom. Plant J. 1998;13:699–705. doi: 10.1046/j.1365-313X.1998.00071.x. PubMed DOI

Wöstemeyer J, Kreibich A. Repetitive DNA elements in fungi (Mycota): impact on genomic architecture and evolution. Curr Genet. 2002;41:189–198. PubMed

Feschotte C, Jiang N, Wessler SR. Plant transposable elements: where genetics meets genomics. Nat Rev Genet. 2002;3:329–341. doi: 10.1038/nrg793. PubMed DOI

Vitte C, Panaud O. LTR retrotransposons and flowering plant genome size: emergence of the increase/decrease model. Cytogenet Genome Res. 2005;110:91–107. doi: 10.1159/000084941. PubMed DOI

Balint-Kurti PJ, Clendennen SK, Doleželová M, Valárik M, Doležel J, Beetham PR, May GD. Identification and chromosomal localization of the monkey retrotransposon in Musa sp. Mol Gen Genet. 2000;263:908–915. doi: 10.1007/s004380000265. PubMed DOI

Kejnovský E, Kubát Z, Macas J, Hobza R, Mráček J, Vyskot B. Retand: a novel family of gypsy-like retrotransposons harboring an amplified tandem repeat. Mol Genet Genomics. 2006;276:254–263. PubMed

Jiang J. A molecular view of plant centromeres. Trends Plant Sci. 2003;8:570–575. doi: 10.1016/j.tplants.2003.10.011. PubMed DOI

Liu Z, Yue W, Li D, Wang R, Kong X, Lu K, Wang G, Dong Y, Jin W, Zhang X. Structure and dynamics of retrotransposons at wheat centromeres and pericentromeres. Chromosoma. 2008;117:445–456. doi: 10.1007/s00412-008-0161-9. PubMed DOI

Bao W, Zhang W, Yang Q, Zhang Y, Han B, Gu M, Xue Y, Cheng Z. Diversity of centromeric repeats in two closely related wild rice species, Oryza officinalis and Oryza rhizomatis. Mol Genet Genomics. 2006;275:421–430. doi: 10.1007/s00438-006-0103-2. PubMed DOI

Cheng ZK, Dong FG, Langdon T, Shu OY, Buell CR, Gu MH, Blattner FR, Jiang JM. Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell. 2002;14:1691–1704. doi: 10.1105/tpc.003079. PubMed DOI PMC

Kumekawa N, Ohmido N, Fukui K, Ohtsubo E, Ohtsubo H. A new gypsy-type retrotransposon, RIRE7: preferential insertion into the tandem repeat sequence TrsD in pericentromeric heterochromatin regions of rice chromosomes. Mol Genet Genomics. 2001;265:480–488. doi: 10.1007/s004380000436. PubMed DOI

Nagaki K, Neumann P, Zhang DF, Ouyang S, Buell CR, Cheng ZK, Jiang JM. Structure, divergence, and distribution of the CRR centromeric retrotransposon family in rice. Mol Biol Evol. 2005;22:845–855. doi: 10.1093/molbev/msi069. PubMed DOI

Nagaki K, Song J, Stupar RM, Parokonny AS, Yuan Q, Ouyang S, Liu J, Hsiao J, Jones KM, Dawe RK, Buell CR, Jiang J. Molecular and cytological analyses of large tracks of centromeric DNA reveal the structure and evolutionary dynamics of maize centromeres. Genetics. 2003;163:759–770. PubMed PMC

Zhong CX, Marshall JB, Topp C, Mroczek R, Kato A, Nagaki K, Birchler JA, Jiang JM, Dawe RK. Centromeric retroelements and satellites interact with maize kinetochore protein CENH3. Plant Cell. 2002;14:2825–2836. doi: 10.1105/tpc.006106. PubMed DOI PMC

Nagaki K, Murata M. Characterization of CENH3 and centromere-associated DNA sequences in sugarcane. Chromosome Res. 2005;13:195–203. doi: 10.1007/s10577-005-0847-2. PubMed DOI

Francki MG. Identification of Bilby, a diverged centromeric Ty1-copia retrotransposon family from cereal rye (Secale cereale L.) Genome. 2001;44:266–274. doi: 10.1139/gen-44-2-266. PubMed DOI

Hudakova S, Michalek W, Presting GG, ten Hoopen R, dos Santos K, Jasencakova Z, Schubert I. Sequence organization of barley centromeres. Nucleic Acids Res. 2001;29:5029–5035. doi: 10.1093/nar/29.24.5029. PubMed DOI PMC

Presting GG, Malysheva L, Fuchs J, Schubert I. A TY3/GYPSY retrotransposon-like sequence localizes to the centromeric regions of cereal chromosomes. Plant J. 1998;16:721–728. doi: 10.1046/j.1365-313x.1998.00341.x. PubMed DOI

Miller JT, Dong F, Jackson SA, Song J, Jiang J. Retrotransposon-related DNA sequences in the centromeres of grass chromosomes. Genetics. 1998;150:1615–1623. PubMed PMC

Gindullis F, Desel C, Galasso I, Schmidt T. The large-scale organization of the centromeric region in Beta species. Genome Res. 2001;11:253–265. doi: 10.1101/gr.162301. PubMed DOI PMC

Weber B, Schmidt T. Nested Ty3-gypsy retrotransposons of a single Beta procumbens centromere contain a putative chromodomain. Chromosome Res. 2009;17:379–396. doi: 10.1007/s10577-009-9029-y. PubMed DOI

Gorinsek B, Gubensek F, Kordis D. Evolutionary genomics of chromoviruses in eukaryotes. Mol Biol Evol. 2004;21:781–798. doi: 10.1093/molbev/msh057. PubMed DOI

Sharma A, Presting GG. Centromeric retrotransposon lineages predate the maize/rice divergence and differ in abundance and activity. Mol Genet Genomics. 2008;279:133–147. doi: 10.1007/s00438-007-0302-5. PubMed DOI

Gorinsek B, Gubensek F, Kordis D. Phylogenomic analysis of chromoviruses. Cytogenet Genome Res. 2005;110:543–552. doi: 10.1159/000084987. PubMed DOI

Kordis D. A genomic perspective on the chromodomain-containing retrotransposons: chromoviruses. Gene. 2005;347:161–173. doi: 10.1016/j.gene.2004.12.017. PubMed DOI

Gao X, Hou Y, Ebina H, Levin HL, Voytas DF. Chromodomains direct integration of retrotransposons to heterochromatin. Genome Res. 2008;18:359–369. doi: 10.1101/gr.7146408. PubMed DOI PMC

Ma J, Wing RA, Bennetzen JL, Jackson SA. Plant centromere organization: a dynamic structure with conserved functions. Trends Genet. 2007;23:134–139. doi: 10.1016/j.tig.2007.01.004. PubMed DOI

Wu J, Fujisawa M, Tian Z, Yamagata H, Kamiya K, Shibata M, Hosokawa S, Ito Y, Hamada M, Katagiri S, Kurita K, Yamamoto M, Kikuta A, Machita K, Karasawa W, Kanamori H, Namiki N, Mizuno H, Ma J, Sasaki T, Matsumoto T. Comparative analysis of complete orthologous centromeres from two subspecies of rice reveals rapid variation of centromere organization and structure. Plant J. 2009;60:805–819. doi: 10.1111/j.1365-313X.2009.04002.x. PubMed DOI

Topp CN, Zhong CX, Dawe RK. Centromere-encoded RNAs are integral components of the maize kinetochore. Proc Natl Acad Sci USA. 2004;101:15986–15991. doi: 10.1073/pnas.0407154101. PubMed DOI PMC

Neumann P, Yan H, Jiang J. The centromeric retrotransposons of rice are transcribed and differentially processed by RNA interference. Genetics. 2007;176:749–761. doi: 10.1534/genetics.107.071902. PubMed DOI PMC

Lloréns C, Fares MA, Moya A. Relationships of gag-pol diversity between Ty3/Gypsy and Retroviridae LTR retroelements and the three kings hypothesis. BMC Evol Biol. 2008;8:276. PubMed PMC

Malik HS, Eickbush TH. Modular evolution of the integrase domain in the Ty3/Gypsy class of LTR retrotransposons. J Virol. 1999;73:5186–5190. PubMed PMC

L'Homme Y, Séguin A, Tremblay FM. Different classes of retrotransposons in coniferous spruce species. Genome. 2000;43:1084–1089. PubMed

Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyère C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V. French-Italian Public Consortium for Grapevine Genome Characterization et al.The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature. 2007;449:463–467. doi: 10.1038/nature06148. PubMed DOI

Sarri V, Minelli S, Panara F, Morgante M, Jurman I, Zuccolo A, Cionini PG. Characterization and chromosomal organization of satellite DNA sequences in Picea abies. Genome. 2008;51:705–713. doi: 10.1139/G08-048. PubMed DOI

Bennett MD, Leitch IJ. Angiosperm DNA C-values database (release 7.0, Dec. 2010) http://www.kew.org/cvalues/

Macas J, Neumann P, Navrátilová A. Repetitive DNA in the pea (Pisum sativum L.) genome: comprehensive characterization using 454 sequencing and comparison to soybean and Medicago truncatula. BMC Genomics. 2007;8:427. doi: 10.1186/1471-2164-8-427. PubMed DOI PMC

Neumann P, Nouzová M, Macas J. Molecular and cytogenetic analysis of repetitive DNA in pea (Pisum sativum L.) Genome. 2001;44:716–728. doi: 10.1139/gen-44-4-716. PubMed DOI

Folco HD, Pidoux AL, Urano T, Allshire RC. Heterochromatin and RNAi are required to establish CENP-A chromatin at centromeres. Science. 2008;319:94–97. doi: 10.1126/science.1150944. PubMed DOI PMC

Wong LH, Brettingham-Moore KH, Chan L, Quach JM, Anderson MA, Northrop EL, Hannan R, Saffery R, Shaw ML, Williams E, Choo KHA. Centromere RNA is a key component for the assembly of nucleoproteins at the nucleolus and centromere. Genome Res. 2007;17:1146–1160. doi: 10.1101/gr.6022807. PubMed DOI PMC

Gustafson AM, Allen E, Givan S, Smith D, Carrington JC, Kasschau KD. ASRP: the Arabidopsis Small RNA Project Database. Nucleic Acids Res. 2005;33:D637–D640. doi: 10.1093/nar/gki127. PubMed DOI PMC

Szittya G, Moxon S, Santos DM, Jing R, Fevereiro MPS, Moulton V, Dalmay T. High-throughput sequencing of Medicago truncatula short RNAs identifies eight new miRNA families. BMC Genomics. 2008;9:593. doi: 10.1186/1471-2164-9-593. PubMed DOI PMC

Barakat A, Wall PK, DiLoreto S, dePamphilis CW, Carlson JE. Conservation and divergence of microRNAs in Populus. BMC Genomics. 2007;8:481. doi: 10.1186/1471-2164-8-481. PubMed DOI PMC

Čermák T, Kubát Z, Hobza R, Koblížková A, Widmer A, Macas J, Vyskot B, Kejnovský E. Survey of repetitive sequences in Silene latifolia with respect to their distribution on sex chromosomes. Chromosome Res. 2008;16:961–976. PubMed

Houben A, Schroeder-Reiter E, Nagaki K, Nasuda S, Wanner G, Murata M, Endo TR. CENH3 interacts with the centromeric retrotransposon cereba and GC-rich satellites and locates to centromeric substructures in barley. Chromosoma. 2007;116:275–283. doi: 10.1007/s00412-007-0102-z. PubMed DOI

Pereira V. Insertion bias and purifying selection of retrotransposons in the Arabidopsis thaliana genome. Genome Biol. 2004;5:R79. doi: 10.1186/gb-2004-5-10-r79. PubMed DOI PMC

Peterson-Burch BD, Nettleton D, Voytas DF. Genomic neighborhoods for Arabidopsis retrotransposons: a role for targeted integration in the distribution of the Metaviridae. Genome Biol. 2004;5:R78. doi: 10.1186/gb-2004-5-10-r78. PubMed DOI PMC

Hřibová E, Neumann P, Matsumoto T, Roux N, Macas J, Doležel J. Repetitive part of the banana (Musa acuminata) genome investigated by low-depth 454 sequencing. BMC Plant Biol. 2010;10:204. PubMed PMC

Neumann P, Požárková D, Koblížková A, Macas J. PIGY, a new plant envelope-class LTR retrotransposon. Mol Genet Genomics. 2005;273:43–53. doi: 10.1007/s00438-004-1092-7. PubMed DOI

Houben A, Demidov D, Gernand D, Meister A, Leach CR, Schubert I. Methylation of histone H3 in euchromatin of plant chromosomes depends on basic nuclear DNA content. Plant J. 2003;33:967–973. doi: 10.1046/j.1365-313X.2003.01681.x. PubMed DOI

Novikova O, Mayorov V, Smyshlyaev G, Fursov M, Adkison L, Pisarenko O, Blinov A. Novel clades of chromodomain-containing Gypsy LTR retrotransposons from mosses (Bryophyta) Plant J. 2008;56:562–574. doi: 10.1111/j.1365-313X.2008.03621.x. PubMed DOI

Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y, Tanahashi T, Sakakibara K, Fujita T, Oishi K, Shin-I T, Kuroki Y, Toyoda A, Suzuki Y, Hashimoto S, Yamaguchi K, Sugano S, Kohara Y, Fujiyama A, Anterola A, Aoki S, Ashton N, Barbazuk WB, Barker E, Bennetzen JL, Blankenship R. et al.The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science. 2008;319:64–69. doi: 10.1126/science.1150646. PubMed DOI

Friesen N, Brandes A, Heslop-Harrison JSP. Diversity, origin, and distribution of retrotransposons (gypsy and copia) in conifers. Mol Biol Evol. 2001;18:1176–1188. PubMed

Slotkin RK, Martienssen R. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet. 2007;8:272–285. doi: 10.1038/nrg2072. PubMed DOI

Hall AE, Keith KC, Hall SE, Copenhaver GP, Preuss D. The rapidly evolving field of plant centromeres. Curr Opin Plant Biol. 2004;7:108–114. doi: 10.1016/j.pbi.2004.01.008. PubMed DOI

Henikoff S, Ahmad K, Malik HS. The centromere paradox: stable inheritance with rapidly evolving DNA. Science. 2001;293:1098–1102. doi: 10.1126/science.1062939. PubMed DOI

Houben A, Schubert I. DNA and proteins of plant centromeres. Curr Opin Plant Biol. 2003;6:554–560. doi: 10.1016/j.pbi.2003.09.007. PubMed DOI

Nagaki K, Walling J, Hirsch C, Jiang J, Murata M. Structure and evolution of plant centromeres. Prog Mol Subcell Biol. 2009;48:153–179. full_text. PubMed

Dawe RK, Henikoff S. Centromeres put epigenetics in the driver's seat. Trends Biochem Sci. 2006;31:662–669. doi: 10.1016/j.tibs.2006.10.004. PubMed DOI

Carone DM, Longo MS, Ferreri GC, Hall L, Harris M, Shook N, Bulazel KV, Carone BR, Obergfell C, O'Neill MJ, O'Neill RJ. A new class of retroviral and satellite encoded small RNAs emanates from mammalian centromeres. Chromosoma. 2009;118:113–125. doi: 10.1007/s00412-008-0181-5. PubMed DOI

Maison C, Bailly D, Peters AHFM, Quivy JP, Roche D, Taddei A, Lachner M, Jenuwein T, Almouzni G. Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat Genet. 2002;30:329–334. doi: 10.1038/ng843. PubMed DOI

Muchardt C, Guillemé M, Seeler JS, Trouche D, Dejean A, Yaniv M. Coordinated methyl and RNA binding is required for heterochromatin localization of mammalian HP1α. EMBO Rep. 2002;3:975–981. doi: 10.1093/embo-reports/kvf194. PubMed DOI PMC

Kagansky A, Folco HD, Almeida R, Pidoux AL, Boukaba A, Simmer F, Urano T, Hamilton GL, Allshire RC. Synthetic heterochromatin bypasses RNAi and centromeric repeats to establish functional centromeres. Science. 2009;324:1716–1719. doi: 10.1126/science.1172026. PubMed DOI PMC

Cam HP, Sugiyama T, Chen ES, Chen X, FitzGerald PC, Grewal SIS. Comprehensive analysis of heterochromatin- and RNAi-mediated epigenetic control of the fission yeast genome. Nat Genet. 2005;37:809–819. doi: 10.1038/ng1602. PubMed DOI

Deshpande G, Calhoun G, Schedl P. Drosophila argonaute-2 is required early in embryogenesis for the assembly of centric/centromeric heterochromatin, nuclear division, nuclear migration, and germ-cell formation. Genes Dev. 2005;19:1680–1685. doi: 10.1101/gad.1316805. PubMed DOI PMC

Durand-Dubief M, Bastin P. TbAGO1, an Argonaute protein required for RNA interference, is involved in mitosis and chromosome segregation in Trypanosoma brucei. BMC Biol. 2003;1:2. doi: 10.1186/1741-7007-1-2. PubMed DOI PMC

Fukagawa T, Nogami M, Yoshikawa M, Ikeno M, Okazaki T, Takami Y, Nakayama T, Oshimura M. Dicer is essential for formation of the heterochromatin structure in vertebrate cells. Nat Cell Biol. 2004;6:784–791. doi: 10.1038/ncb1155. PubMed DOI

Kanellopoulou C, Muljo SA, Kung AL, Ganesan S, Drapkin R, Jenuwein T, Livingston DM, Rajewsky K. Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Gene Dev. 2005;19:489–501. doi: 10.1101/gad.1248505. PubMed DOI PMC

Pal-Bhadra M, Leibovitch BA, Gandhi SG, Rao M, Bhadra U, Birchler JA, Elgin SCR. Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science. 2004;303:669–672. doi: 10.1126/science.1092653. PubMed DOI

Pidoux AL, Allshire RC. The role of heterochromatin in centromere function. Philos Trans R Soc Lond B Biol Sci. 2005;360:569–579. doi: 10.1098/rstb.2004.1611. PubMed DOI PMC

Provost P, Silverstein RA, Dishart D, Walfridsson J, Djupedal I, Kniola B, Wright A, Samuelsson B, Rådmark O, Ekwall K. Dicer is required for chromosome segregation and gene silencing in fission yeast cells. Proc Natl Acad Sci USA. 2002;99:16648–16653. doi: 10.1073/pnas.212633199. PubMed DOI PMC

Volpe T, Schramke V, Hamilton GL, White SA, Teng G, Martienssen RA, Allshire RC. RNA interference is required for normal centromere function in fission yeast. Chromosome Res. 2003;11:137–146. doi: 10.1023/A:1022815931524. PubMed DOI

May BP, Lippman ZB, Fang Y, Spector DL, Martienssen RA. Differential regulation of strand-specific transcripts from Arabidopsis centromeric satellite repeats. PLoS Genet. 2005;1:e79. doi: 10.1371/journal.pgen.0010079. PubMed DOI PMC

Lloréns C, Futami R, Bezemer D, Moya A. The Gypsy Database (GyDB) of mobile genetic elements. Nucleic Acids Res. 2008;36:38–46. PubMed PMC

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–410. PubMed

Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–3402. doi: 10.1093/nar/25.17.3389. PubMed DOI PMC

Xu Z, Wang H. LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 2007;35:W265–W268. doi: 10.1093/nar/gkm286. PubMed DOI PMC

Durbin R, Eddy SR, Krogh A, Mitchison GJ. Biological Sequence Analysis: Probabilistic Models of Proteins and Nucleic Acids. Cambridge, UK: Cambridge University Press; 1998.

Eddy SR. A probabilistic model of local sequence alignment that simplifies statistical significance estimation. PLoS Comput Biol. 2008;4:e1000069. doi: 10.1371/journal.pcbi.1000069. PubMed DOI PMC

Bailey TL, Elkan C. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol. 1994;2:28–36. PubMed

Bailey TL, Gribskov M. Combining evidence using p-values: application to sequence homology searches. Bioinformatics. 1998;14:48–54. doi: 10.1093/bioinformatics/14.1.48. PubMed DOI

Rice P, Longden I, Bleasby A. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 2000;16:276–277. doi: 10.1016/S0168-9525(00)02024-2. PubMed DOI

Staden R. The Staden sequence analysis package. Mol Biotechnol. 1996;5:233–241. doi: 10.1007/BF02900361. PubMed DOI

Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23:2947–2948. doi: 10.1093/bioinformatics/btm404. PubMed DOI

Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1797. doi: 10.1093/nar/gkh340. PubMed DOI PMC

Myers EW, Miller W. Optimal alignments in linear space. Comput Appl Biosci. 1988;4:11–17. PubMed

Marchler-Bauer A, Anderson JB, DeWeese-Scott C, Fedorova ND, Geer LY, He S, Hurwitz DI, Jackson JD, Jacobs AR, Lanczycki CJ, Liebert CA, Liu C, Madej T, Marchler GH, Mazumder R, Nikolskaya AN, Panchenko AR, Rao BS, Shoemaker BA, Simonyan V, Song JS, Thiessen PA, Vasudevan S, Wang Y, Yamashita RA, Yin JJ, Bryant SH. CDD: a curated Entrez database of conserved domain alignments. Nucleic Acids Res. 2003;31:383–387. doi: 10.1093/nar/gkg087. PubMed DOI PMC

Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 2010;27:221–224. doi: 10.1093/molbev/msp259. PubMed DOI

Letunic I, Bork P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics. 2007;23:127–128. doi: 10.1093/bioinformatics/btl529. PubMed DOI

FigTree. http://tree.bio.ed.ac.uk/software/figtree/

Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res. 2004;14:1188–1190. doi: 10.1101/gr.849004. PubMed DOI PMC

Map viewer. http://www.ncbi.nlm.nih.gov/mapview/

Yang H, McLeese J, Weisbart M, Dionne JL, Lemaire I, Aubin RA. Simplified high throughput protocol for northern hybridization. Nucleic Acids Res. 1993;21:3337–3338. doi: 10.1093/nar/21.14.3337. PubMed DOI PMC

Huang X, Madan A. CAP3: a DNA sequence assembly program. Genome Res. 1999;9:868–877. doi: 10.1101/gr.9.9.868. PubMed DOI PMC

Lodhi MA, Reisch BI. Nuclear DNA content of Vitis species, cultivars, and other genera of the Vitaceae. Theor Appl Genet. 1995;90:11–16. doi: 10.1007/BF00220990. PubMed DOI

Siljak-Yakovlev S, Cerbah M, Coulaud J, Stoian V, Brown SC, Zoldos V, Jelenic S, Papes D. Nuclear DNA content, base composition, heterochromatin and rDNA in Picea omorika and Picea abies. Theor Appl Genet. 2002;104:505–512. doi: 10.1007/s001220100755. PubMed DOI

Doleželová M, Valárik M, Swennen R, Horry JP, Doležel J. Physical mapping of the 18S-25S and 5S ribosomal RNA genes in diploid bananas. Biol Plantarum. 1998;41:497–505.

Űberall I, Vrána J, Bartoš J, Šmerda J, Doležel J, Havel L. Isolation of chromosomes from Picea abies and their analysis by flow cytometry. Biol Plantarum. 2004;48:199–203.

Leitch AR, Schwarzacher T, Jackson D, Leitch IJ. In situ Hybridization. Oxford, UK: BIOS Scientific; 1994.

Chaw SM, Chang CC, Chen HL, Li WH. Dating the monocot-dicot divergence and the origin of core eudicots using whole chloroplast genomes. J Mol Evol. 2004;58:424–441. doi: 10.1007/s00239-003-2564-9. PubMed DOI

Repeat-based holocentromeres of the woodrush Luzula sylvatica reveal insights into the evolutionary transition to holocentricity

DANTE and DANTE_LTR: lineage-centric annotation pipelines for long terminal repeat retrotransposons in plant genomes

Celine, a long interspersed nuclear element retrotransposon, colonizes in the centromeres of poplar chromosomes

The Dynamic Interplay Between Ribosomal DNA and Transposable Elements: A Perspective From Genomics and Cytogenetics

Assembly of the 81.6 Mb centromere of pea chromosome 6 elucidates the structure and evolution of metapolycentric chromosomes

Draft Sequencing Crested Wheatgrass Chromosomes Identified Evolutionary Structural Changes and Genes and Facilitated the Development of SSR Markers

The Sister Chromatid Division of the Heteromorphic Sex Chromosomes in Silene Species and Their Transmissibility towards the Mitosis

Advances in the Molecular Cytogenetics of Bananas, Family Musaceae

Telomere-to-telomere gapless chromosomes of banana using nanopore sequencing

Comparative analyses of DNA repeats and identification of a novel Fesreba centromeric element in fescues and ryegrasses

Nested plant LTR retrotransposons target specific regions of other elements, while all LTR retrotransposons often target palindromes and nucleosome-occupied regions: in silico study

Chromosome Painting Facilitates Anchoring Reference Genome Sequence to Chromosomes In Situ and Integrated Karyotyping in Banana (Musa Spp.)

Systematic survey of plant LTR-retrotransposons elucidates phylogenetic relationships of their polyprotein domains and provides a reference for element classification

Satellite DNA and Transposable Elements in Seabuckthorn (Hippophae rhamnoides), a Dioecious Plant with Small Y and Large X Chromosomes

Repeat Composition of CenH3-chromatin and H3K9me2-marked heterochromatin in Sugar Beet (Beta vulgaris)

Holocentromeres in Rhynchospora are associated with genome-wide centromere-specific repeat arrays interspersed among euchromatin

Impact of repetitive DNA on sex chromosome evolution in plants

Characterization of repetitive DNA landscape in wheat homeologous group 4 chromosomes

LTR retrotransposon dynamics in the evolution of the olive (Olea europaea) genome

Genome-wide analysis of repeat diversity across the family Musaceae