The Dynamic Interplay Between Ribosomal DNA and Transposable Elements: A Perspective From Genomics and Cytogenetics
Jazyk angličtina Země Spojené státy americké Médium print
Typ dokumentu časopisecké články
Grantová podpora
PID2020-119163GB-I00
Agencia Estatal de Investigación
Bundesministerium für Bildung und Forschung
German Research Foundation
Graduate Academy of the TU Dresden
22-16826S
Czech Science Foundation
PubMed
38306580
PubMed Central
PMC10946416
DOI
10.1093/molbev/msae025
PII: 7597089
Knihovny.cz E-zdroje
- Klíčová slova
- concerted evolution, genome size, genome stability, homogenization, housekeeping genes, long-read sequencing, molecular cytogenetics, recombination, repetitive DNA, ribosomal DNA, transposable elements, transposition,
- MeSH
- cytogenetické vyšetření MeSH
- genomika * MeSH
- metylace DNA MeSH
- molekulární evoluce MeSH
- ribozomální DNA MeSH
- transpozibilní elementy DNA * MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- ribozomální DNA MeSH
- transpozibilní elementy DNA * MeSH
Although both are salient features of genomes, at first glance ribosomal DNAs and transposable elements are genetic elements with not much in common: whereas ribosomal DNAs are mainly viewed as housekeeping genes that uphold all prime genome functions, transposable elements are generally portrayed as selfish and disruptive. These opposing characteristics are also mirrored in other attributes: organization in tandem (ribosomal DNAs) versus organization in a dispersed manner (transposable elements); evolution in a concerted manner (ribosomal DNAs) versus evolution by diversification (transposable elements); and activity that prolongs genomic stability (ribosomal DNAs) versus activity that shortens it (transposable elements). Re-visiting relevant instances in which ribosomal DNA-transposable element interactions have been reported, we note that both repeat types share at least four structural and functional hallmarks: (1) they are repetitive DNAs that shape genomes in evolutionary timescales, (2) they exchange structural motifs and can enter co-evolution processes, (3) they are tightly controlled genomic stress sensors playing key roles in senescence/aging, and (4) they share common epigenetic marks such as DNA methylation and histone modification. Here, we give an overview of the structural, functional, and evolutionary characteristics of both ribosomal DNAs and transposable elements, discuss their roles and interactions, and highlight trends and future directions as we move forward in understanding ribosomal DNA-transposable element associations.
Faculty of Biology Technische Universität Dresden D 01069 Dresden Germany
Institut Botànic de Barcelona CSIC CMCNB 08038 Barcelona Catalonia Spain
Institute of Biology NAWI Graz Karl Franzens Universität A 8010 Graz Austria
Institute of Biophysics Academy of Sciences of the Czech Republic 61265 Brno Czech Republic
Zobrazit více v PubMed
Abascal-Palacios G, Jochem L, Pla-Prats C, Beuron F, Vannini A. Structural basis of Ty3 retrotransposon integration at RNA polymerase III-transcribed genes. Nat Commun. 2021:12(1):6992. 10.1038/s41467-021-27338-w. PubMed DOI PMC
Almeida MV, Vernaz G, Putman ALK, Miska EA. Taming transposable elements in vertebrates: from epigenetic silencing to domestication. Trends Genet. 2022:38(6):529–553. 10.1016/j.tig.2022.02.009. PubMed DOI
Altinkut A, Raskina O, Nevo E, Belyayev A. En/Spm-like transposons in Poaceae species: transposase sequence variability and chromosomal distribution. Cell Mol Biol Lett. 2006:11(2):214–229. 10.2478/s11658-006-0017-3. PubMed DOI PMC
Arkhipova IR. Neutral theory, transposable elements, and eukaryotic genome evolution. Mol Biol Evol. 2018:35(6):1332–1337. 10.1093/molbev/msy083. PubMed DOI PMC
Baeza C, Schrader O, Budahn H. Characterization of geographically isolated accessions in five Alstroemeria L. species (Chile) using FISH of tandemly repeated DNA sequences and RAPD analysis. Plant Syst Evol. 2007:269(1–2):1–14. 10.1007/s00606-007-0591-5. 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(6):908–915. 10.1007/s004380000265. PubMed DOI
Bendich AJ, Rogers SO. Ribosomal intergenic spacers are filled with transposon remnants. Genome Biol Evol. 2023:15(7):evad114. 10.1093/gbe/evad114. PubMed DOI PMC
Bhattacharyya MK, Smith AM, Ellis THN, Hedley C, Martin C. The wrinkled-seed character of pea described by Mendel is caused by a transposon-like insertion in a gene encoding starch-branching enzyme. Cell. 1990:60(1):115–122. 10.1016/0092-8674(90)90721-P. PubMed DOI
Bigot Y, Lutcher F, Hamelin MH, Périquet G. The 28S ribosomal RNA-encoding gene of Hymenoptera: inserted sequences in the retrotransposon-rich regions. Gene. 1992:121(2):347–352. 10.1016/0378-1119(92)90142-C. PubMed DOI
Bloom SE, Goodpasture C. An improved technique for selective silver staining of nucleolar organizer regions in human chromosomes. Hum Genet. 1976:34(2):199–206. 10.1007/BF00278889. PubMed DOI
Blum H, Beier H, Gross HJ. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis. 1987:8(2):93–99. 10.1002/elps.1150080203. DOI
Blumenstiel JP. Birth, school, work, death, and resurrection: the life stages and dynamics of transposable element proliferation. Genes (Basel). 2019:10(5):336. 10.3390/genes10050336. PubMed DOI PMC
Brewer TE, Albertsen M, Edwards A, Kirkegaard RH, Rocha EP, Fierer N. Unlinked rRNA genes are widespread among bacteria and archaea. ISME J. 2020:14(2):597–608. 10.1038/s41396-019-0552-3. PubMed DOI PMC
Brown DD, Wensink PC, Jordan E. A comparison of the ribosomal DNA's of Xenopus laevis and Xenopus mulleri: the evolution of tandem genes. J Mol Biol. 1972:63(1):57–73. 10.1016/0022-2836(72)90521-9. PubMed DOI
Bueno D, Palacios-Gimenez OM, Cabral-de-Mello DC. Chromosomal mapping of repetitive DNAs in the grasshopper Abracris flavolineata reveal possible ancestry of the B chromosome and H3 histone spreading. PLoS One. 2013:8(6):e66532. 10.1371/journal.pone.0066532. PubMed DOI PMC
Burke WD, Calalang CC, Eickbush TH. The site-specific ribosomal insertion element type II of Bombyx mori (R2Bm) contains the coding sequence for a reverse transcriptase-like enzyme. Mol Cell Biol. 1987:7(6):2221–2230. 10.1128/mcb.7.6.2221-2230.1987. PubMed DOI PMC
Burke WD, Eickbush DG, Xiong Y, Jakubczak J, Eickbush TH. Sequence relationship of retrotransposable elements R1 and R2 within and between divergent insect species. Mol Biol Evol. 1993:10(1):163–185. 10.1093/oxfordjournals.molbev.a039990. PubMed DOI
Burke WD, Malik HS, Lathe WC III, Eickbush TH. Are retrotransposons long-term hitchhikers? Nature. 1998:392(6672):141–142. 10.1038/32330. PubMed DOI
Carleton KL, Conte MA, Malinsky M, Nandamuri SP, Sandkam BA, Meier JI, Mwaiko S, Seehausen O, Kocher TD. Movement of transposable elements contributes to cichlid diversity. Mol Ecol. 2020:29(24):4956–4969. 10.1111/mec.15685. PubMed DOI
Chester M, Sykorova E, Fajkus J, Leitch AR. Single integration and spread of a Copia-like sequence nested in rDNA intergenic spacers of Allium cernuum (Alliaceae). Cytogenet Genome Res. 2010:129(1–3):35–46. 10.1159/000312959. PubMed DOI
Chuong EB, Elde NC, Feschotte C. Regulatory activities of transposable elements: from conflicts to benefits. Nat Rev Genet. 2017:18(2):71–86. 10.1038/nrg.2016.139. PubMed DOI PMC
Cioffi MB, Martins C, Bertollo LAC. Chromosome spreading of associated transposable elements and ribosomal DNA in the fish Erythrinus erythrinus. Implications for genome change and karyoevolution in fish. BMC Evol Biol. 2010:10:271. 10.1186/1471-2148-10-271. PubMed DOI PMC
Coen E, Strachan T, Dover G. Dynamics of concerted evolution of ribosomal DNA and histone gene families in the melanogaster species subgroup of Drosophila. J Mol Biol. 1982:158(1):17–35. 10.1016/0022-2836(82)90448-X. PubMed DOI
Cohen S, Houben A, Segal D. Extrachromosomal circular DNA derived from tandemly repeated genomic sequences in plants. Plant J. 2008:53(6):1027–1034. 10.1111/j.1365-313X.2007.03394.x. PubMed DOI
Cohen S, Yacobi K, Segal D. Extrachromosomal circular DNA of tandemly repeated genomic sequences in Drosophila. Genome Res. 2003:13(6a):1133–1145. 10.1101/gr.907603. PubMed DOI PMC
Condon C, French S, Squires C, Squires CL. Depletion of functional ribosomal RNA operons in Escherichia coli causes increased expression of the remaining intact copies. EMBO J. 1993:12(11):4305–4315. 10.1002/j.1460-2075.1993.tb06115.x. PubMed DOI PMC
Cosby RL, Chang NC, Feschotte C. Host–transposon interactions: conflict, cooperation, and cooption. Genes Dev. 2019:33(17–18):1098–1116. 10.1101/gad.327312.119. PubMed DOI PMC
Dalíková M, Provazníková I, Provazník J, Grof-Tisza P, Pepi A, Nguyen P. The role of repetitive sequences in repatterning of major ribosomal DNA clusters in Lepidoptera. Gen Biol Evol. 2023:15(6):evad090. 10.1093/gbe/evad090. PubMed DOI PMC
da Silva M, Barbosa P, Artoni RF, Feldberg E. Evolutionary dynamics of 5S rDNA and recurrent association of transposable elements in electric fish of the family Gymnotidae (Gymnotiformes): the case of Gymnotus mamiraua. Cytogenet Genome Res. 2016:149(4):297–303. 10.1159/000449431. PubMed DOI
Devos KM, Brown JKM, Bennetzen JL. Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res. 2002:12(7):1075–1079. 10.1101/gr.132102. PubMed DOI PMC
Drouin G, De Sa MM. The concerted evolution of 5S ribosomal genes linked to the repeat units of other multigene families. Mol Biol Evol. 1995:12(3):481–493. 10.1093/oxfordjournals.molbev.a040223. PubMed DOI
Eagle SHC, Crease TJ. Copy number variation of ribosomal DNA and Pokey transposons in natural populations of Daphnia. Mob DNA. 2012:3(1):4. 10.1186/1759-8753-3-4. PubMed DOI PMC
Eaves LA, Gardner AJ, Fry RC. Tools for the assessment of epigenetic regulation. In: Fry RC, editor. Environmental epigenetics in toxicology and public health. Amsterdam: Elsevier; 2020. p. 33–64.
Eickbush DG, Burke WD, Eickbush TH. Evolution of the R2 retrotransposon ribozyme and its self-cleavage site. PLoS One. 2013:8(9):e66441. 10.1371/journal.pone.0066441. PubMed DOI PMC
Eickbush DG, Eickbush TH. Vertical transmission of the retrotransposable elements R1 and R2 during the evolution of the Drosophila melanogaster species subgroup. Genetics. 1995:139(2):671–684. 10.1093/genetics/139.2.671. PubMed DOI PMC
Eickbush DG, Eickbush TH. Transcription of endogenous and exogenous R2 elements in the rRNA gene locus of Drosophila melanogaster. Mol Cell Biol. 2003:23(11):3825–3836. 10.1128/MCB.23.11.3825-3836.2003. PubMed DOI PMC
Eickbush DG, Eickbush TH. R2 and R2/R1 hybrid non-autonomous retrotransposons derived by internal deletions of full-length elements. Mob DNA. 2012:3(1):10. 10.1186/1759-8753-3-10. PubMed DOI PMC
Eickbush DG, Ye J, Zhang X, Burke WD, Eickbush TH. Epigenetic regulation of retrotransposons within the nucleolus of Drosophila. Mol Cell Biol. 2008:28(20):6452–6461. 10.1128/MCB.01015-08. PubMed DOI PMC
Elliott TA, Stage DE, Crease TJ, Eickbush TH. In and out of the rRNA genes: characterization of Pokey elements in the sequenced Daphnia genome. Mob DNA. 2013:4(1):20. 10.1186/1759-8753-4-20. PubMed DOI PMC
Ellison CE, Bachtrog D. Non-allelic gene conversion enables rapid evolutionary change at multiple regulatory sites encoded by transposable elements. Elife. 2015:4:e05899. 10.7554/eLife.05899. PubMed DOI PMC
Fan W, Eklund E, Sherman RM, Liu H, Pitts S, Ford B, Rajeshkumar NV, Laiho M. Widespread genetic heterogeneity of human ribosomal RNA genes. RNA. 2022:28(4):478–492. 10.1261/rna.078925.121. PubMed DOI PMC
Fawcett JA, Innan H. The role of gene conversion between transposable elements in rewiring regulatory networks. Genome Biol Evol. 2019:11(7):1723–1729. 10.1093/gbe/evz124. PubMed DOI PMC
Fefelova EA, Pleshakova IM, Mikhaleva EA, Pirogov SA, Poltorachenko VA, Abramov YA, Romashin DD, Shatskikh AS, Blokh RS, Gvozdev VA, et al. Impaired function of rDNA transcription initiation machinery leads to derepression of ribosomal genes with insertions of R2 retrotransposon. Nucleic Acids Res. 2022:50(2):867–884. 10.1093/nar/gkab1276. PubMed DOI PMC
Ferretti ABSM, Ruiz-Ruano FJ, Milani D, Loreto V, Martí DA, Ramos E, Martins C, Cabral-de-Mello DC. How dynamic could be the 45S rDNA cistron? An intriguing variability in a grasshopper species revealed by integration of chromosomal and genomic data. Chromosoma. 2019:128(2):165–175. 10.1007/s00412-019-00706-8. PubMed DOI
Finnegan DJ. Eukaryotic transposable elements and genome evolution. Trends Genet. 1989:5(4):103–107. 10.1016/0168-9525(89)90039-5. PubMed DOI
Flavell AJ, Ish-Horowicz D. Extrachromosomal circular copies of the eukaryotic transposable element Copia in cultured Drosophila cells. Nature. 1981:292(5824):591–595. 10.1038/292591a0. PubMed DOI
Flavell RB, Bennett MD, Smith JB, Smith DB. Genome size and the proportion of repeated nucleotide sequence DNA in plants. Biochem Genet. 1974:12(4):257–269. 10.1007/BF00485947. PubMed DOI
Fujisawa M, Yamagata H, Kamiya K, Nakamura M, Saji S, Kanamori H, Wu J, Matsumoto T, Sasaki T. Sequence comparison of distal and proximal ribosomal DNA arrays in rice (Oryza sativa L.) chromosome 9S and analysis of their flanking regions. Theor Appl Genet. 2006:113(3):419–428. 10.1007/s00122-006-0307-1. PubMed DOI
Fujiwara H, Ogura T, Takada N, Miyajima N, Ishikawa H, Maekawa H. Introns and their flanking sequences of Bombyx mori rDNA. Nucleic Acids Res. 1984:12(17):6861–6869. 10.1093/nar/12.17.6861. PubMed DOI PMC
Ganley ARD, Kobayashi T. Ribosomal DNA and cellular senescence: new evidence supporting the connection between rDNA and aging. FEMS Yeast Res. 2014:14(1):49–59. 10.1111/1567-1364.12133. PubMed DOI
Gao D, Li Y, Kim KD, Abernathy B, Jackson SA. Landscape and evolutionary dynamics of terminal repeat retrotransposons in miniature in plant genomes. Genome Biol. 2016:17(1):7. 10.1186/s13059-015-0867-y. PubMed DOI PMC
Gao X, Hou Y, Ebina H, Levin H, Voytas DF. Chromodomains direct integration of retrotransposons to heterochromatin. Genome Res. 2008:18(3):359–369. 10.1101/gr.7146408. PubMed DOI PMC
Garcia S, Crhák Khaitová L, Kovařík A. Expression of 5 S rRNA genes linked to 35 S rDNA in plants, their epigenetic modification and regulatory element divergence. BMC Plant Biol. 2012:12:95. 10.1186/1471-2229-12-95. PubMed DOI PMC
Garcia S, Kovařík A, Leitch A, Garnatje T. Cytogenetic features of rRNA genes across land plants: analysis of the plant rDNA database. Plant J. 2017:89(5):1020–1030. 10.1111/tpj.13442. PubMed DOI
Garcia S, Lim KY, Chester M, Garnatje T, Pellicer J, Vallès J, Leitch AR, Kovařík A. Linkage of 35S and 5S rRNA genes in Artemisia (family Asteraceae): first evidence from angiosperms. Chromosoma. 2009:118(1):85–97. 10.1007/s00412-008-0179-z. PubMed DOI
Garcia S, Panero JL, Siroky J, Kovarik A. Repeated reunions and splits feature the highly dynamic evolution of 5S and 35S ribosomal RNA genes (rDNA) in the Asteraceae family. BMC Plant Biol. 2010:10:176. 10.1186/1471-2229-10-176. PubMed DOI PMC
Garcia S, Pascual-Díaz JP, Krumpolcová A, Kovařík A. Analysis of 5S rDNA genomic organization through the RepeatExplorer2 pipeline: a simplified protocol. In: Heitkam T, Garcia S, editors. Plant cytogenetics and cytogenomics. Methods in molecular biology. 1st ed. Vol. 2672. New York (NY): Humana; 2023. p. 501–512. 10.1007/978-1-0716-3226-0_30. PubMed DOI
Garcia S, Wendel JF, Borowska-Zuchowska N, Aïnouche M, Kuderova A, Kovarik A. The utility of graph clustering of 5S ribosomal DNA homoeologs in plant allopolyploids, homoploid hybrids, and cryptic introgressants. Front Plant Sci. 2020:11:41. 10.3389/fpls.2020.00041. PubMed DOI PMC
Gibbons JG, Branco AT, Godinho SA, Yu S, Lemos B. Concerted copy number variation balances ribosomal DNA dosage in human and mouse genomes. Proc Natl Acad Sci U S A. 2015:112(8):2485–2490. 10.1073/pnas.1416878112. PubMed DOI PMC
Gibbons JG, Branco AT, Yu S, Lemos B. Ribosomal DNA copy number is coupled with gene expression variation and mitochondrial abundance in humans. Nat Commun. 2014:5:4850. 10.1038/ncomms5850. PubMed DOI
Glass SK, Moszczynska A, Crease TJ. The effect of transposon Pokey insertions on sequence variation in the 28S rRNA gene of Daphnia pulex. Genome. 2008:51(12):988–1000. 10.1139/G08-092. PubMed DOI
Glugoski L, Giuliano-Caetano L, Moreira-Filho O, Vicari MR, Nogaroto V. Co-located hAT transposable element and 5S rDNA in an interstitial telomeric sequence suggest the formation of Robertsonian fusion in armored catfish. Gene. 2018:650:49–54. 10.1016/j.gene.2018.01.099. PubMed DOI
Goffová I, Fajkus J. The rDNA loci—intersections of replication, transcription, and repair pathways. Int J Mol Sci. 2021:22(3):1302. 10.3390/ijms22031302. PubMed DOI PMC
Gogolevsky KP, Vassetzky NS, Kramerov DA. 5S rRNA-derived and tRNA-derived SINEs in fruit bats. Genomics. 2009:93(5):494–500. 10.1016/j.ygeno.2009.02.001. PubMed DOI
Gonzalez IL, Tugendreich S, Hieter P, Sylvester JE. Fixation times of retroposons in the ribosomal DNA spacer of human and other primates. Genomics. 1993:18(1):29–36. 10.1006/geno.1993.1423. PubMed DOI
Gorbunova V, Seluanov A, Mita P, McKerrow W, Fenyö D, Boeke JD, Linker SB, Gage FH, Kreiling JA, Petrashen AP, et al. The role of retrotransposable elements in ageing and age-associated diseases. Nature. 2021:596(7870):43–53. 10.1038/s41586-021-03542-y. PubMed DOI PMC
Hall AN, Morton E, Queitsch C. First discovered, long out of sight, finally visible: ribosomal DNA. Trends Genet. 2022:38(6):587–597. 10.1016/j.tig.2022.02.005. PubMed DOI PMC
Handa H, Kanamori H, Tanaka T, Murata K, Kobayashi F, Robinson SJ, Koh CS, Pozniak CJ, Sharpe AG, Paux E, et al. Structural features of two major nucleolar organizer regions (NORs), Nor-B1 and Nor-B2, and chromosome-specific rRNA gene expression in wheat. Plant J. 2018:96(6):1148–1159. 10.1111/tpj.14094. PubMed DOI
Harasawa R, Pitcher DG, Ramírez AS, Bradbury JM. A putative transposase gene in the 16S–23S rRNA intergenic spacer region of Mycoplasma imitans. Microbiology (Reading). 2004:150(Pt 4):1023–1029. 10.1099/mic.0.26629-0. PubMed DOI
Hassan M, Das S, Adhya S. Mini-exon derived RNA gene of Leishmania donovani: structure, organization and expression. J Biosci. 1992:17(1):55–66. 10.1007/BF02716774. DOI
Havlová K, Dvořáčková M, Peiro R, Abia D, Mozgová I, Vansáčová L, Gutierrez C, Fajkus J. Variation of 45S rDNA intergenic spacers in Arabidopsis thaliana. Plant Mol Biol. 2016:92(4–5):457–471. 10.1007/s11103-016-0524-1. PubMed DOI
Heitkam T, Garcia S. Plant cytogenetics and cytogenomics: methods in molecular biology. 1st ed. Vol. 2672. New York (NY): Humana; 2023. p. 1–568. 10.1007/978-1-0716-3226-0. PubMed DOI
Heitkam T, Schmidt T. BNR—a LINE family from Beta vulgaris—contains a RRM domain in open reading frame 1 and defines a L1 sub-clade present in diverse plant genomes. Plant J. 2009:59(6):872–882. 10.1111/j.1365-313X.2009.03923.x. PubMed DOI
Heitkam T, Weber B, Walter I, Liedtke S, Ost C, Schmidt T. Satellite DNA landscapes after allotetraploidization of quinoa (Chenopodium quinoa) reveal unique A and B subgenomes. Plant J. 2020:103(1):32–52. 10.1111/tpj.14705. PubMed DOI
Hemleben V, Grierson D, Borisjuk N, Volkov RA, Kovarik A. Personal perspectives on plant ribosomal RNA genes research: from precursor-rRNA to molecular evolution. Front Plant Sci. 2021:12:797348. 10.3389/fpls.2021.797348. PubMed DOI PMC
Hemleben V, Zentgraf U. Structural organization and regulation of transcription by RNA polymerase I of plant nuclear ribosomal RNA genes. Results Probl Cell Differ. 1994:20:3–24. 10.1007/978-3-540-48037-2_1. PubMed DOI
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. 10.1186/1471-2229-10-204. PubMed DOI PMC
Ingle J, Timmis JN, Sinclair J. The relationship between satellite deoxyribonucleic acid, ribosomal ribonucleic acid gene redundancy, and genome size in plants. Plant Physiol. 1975:55(3):496–501. 10.1104/pp.55.3.496. PubMed DOI PMC
Jakubczak JL, Xiong Y, Eickbush TH. Type I (R1) and type II (R2) ribosomal DNA insertions of Drosophila melanogaster are retrotransposable elements closely related to those of Bombyx mori. J Mol Biol. 1990:212(1):37–52. 10.1016/0022-2836(90)90303-4. PubMed DOI
Jakubczak JL, Zenni MK, Woodruff RC, Eickbush TH. Turnover of R1 (type I) and R2 (type II) retrotransposable elements in the ribosomal DNA of Drosophila melanogaster. Genetics. 1992:131(1):129–142. 10.1093/genetics/131.1.129. PubMed DOI PMC
Jamrich M, Miller OL. The rare transcripts of interrupted rRNA genes in Drosophila melanogaster are processed or degraded during synthesis. EMBO J. 1984:3(7):1541–1545. 10.1002/j.1460-2075.1984.tb02008.x. PubMed DOI PMC
Jiang N, Bao Z, Zhang X, Eddy SR, Wessler SR. Pack-MULE transposable elements mediate gene evolution in plants. Nature. 2004:431(7008):569–573. 10.1038/nature02953. PubMed DOI
Jo S-H, Koo D-H, Kim JF, Hur C-G, Lee S, Yang TJ, Kwon SY, Choi D. Evolution of ribosomal DNA-derived satellite repeat in tomato genome. BMC Plant Biol. 2009:9(1):1–14. 10.1186/1471-2229-9-42. PubMed DOI PMC
Kalendar R, Raskina O, Belyayev A, Schulman AH. Long tandem arrays of Cassandra retroelements and their role in genome dynamics in plants. Int J Mol Sci. 2020:21(8):2931. 10.3390/ijms21082931. PubMed DOI PMC
Kalendar R, Tanskanen J, Chang W, Antonius K, Sela H, Peleg O, Schulman AH. Cassandra retrotransposons carry independently transcribed 5S RNA. Proc Natl Acad Sci U S A. 2008:105(15):5833–5838. 10.1073/pnas.0709698105. PubMed DOI PMC
Kamstra SA, Kuipers AGJ, De Jeu MJ, Ramanna MS, Jacobsen E. Physical localisation of repetitive DNA sequences in Alstroemeria: karyotyping of two species with species-specific and ribosomal DNA. Genome. 1997:40(5):652–658. 10.1139/g97-086. PubMed DOI
Kapitonov VV, Jurka J. A novel class of SINE elements derived from 5S rRNA. Mol Biol Evol. 2003:20(5):694–702. 10.1093/molbev/msg075. PubMed DOI
Kasselimi E, Pefani DE, Taraviras S, Lygerou Z. Ribosomal DNA and the nucleolus at the heart of aging. Trends Biochem Sci. 2022:47(4):328–341. 10.1016/j.tibs.2021.12.007. PubMed DOI
Kazazian HH. Mobile DNA transposition in somatic cells. BMC Biol. 2011:9(1):1–4. 10.1186/1741-7007-9-62. PubMed DOI PMC
Kejnovsky E, Hobza R, Kubat Z, Widmer A, Marais GAB, Vyskot B. High intrachromosomal similarity of retrotransposon long terminal repeats: evidence for homogenization by gene conversion on plant sex chromosomes? Gene. 2007:390(1–2):92–97. 10.1016/j.gene.2006.10.007. PubMed DOI
Kempken F. Hideaway, a repeated element from Ascobolus immersus, is rDNA-associated and may resemble a retrotransposon. Curr Genet. 2001:40(3):179–185. 10.1007/s002940100253. PubMed DOI
Kerrebrock AW, Srivastava R, Gerbi SA. Isolation and characterization of ribosomal DNA variants from Sciara coprophila. J Mol Biol. 1989:210(1):1–13. 10.1016/0022-2836(89)90286-6. PubMed DOI
Kimura M. Evolutionary rate at the molecular level. Nature. 1968:217(5129):624–626. 10.1038/217624a0. PubMed DOI
Kobayashi T. Strategies to maintain the stability of the ribosomal RNA gene repeats—collaboration of recombination, cohesion, and condensation. Genes Genet Syst. 2006:81(3):155–161. 10.1266/ggs.81.155. PubMed DOI
Kojima KK, Fujiwara H. Cross-genome screening of novel sequence specific non-LTR retrotransposons: various multicopy RNA genes and microsatellites are selected as targets. Mol Biol Evol. 2004:21(2):207–217. 10.1093/molbev/msg235. PubMed DOI
Kojima KK, Fujiwara H. Long-term inheritance of the 28S rDNA-specific retrotransposon R2. Mol Biol Evol. 2005:22(11):2157–2165. 10.1093/molbev/msi210. PubMed DOI
Kojima KK. Helenus and Ajax, Two groups of non-autonomous LTR retrotransposons, represent a new type of small rna gene-derived mobile elements. Biology. 2024:13(2):119. 10.3390/biology13020119 PubMed DOI PMC
Kuroki-Kami A, Nichuguti N, Yatabe H, Mizuno S, Kawamura S, Fujiwara H. Targeted gene knockin in zebrafish using the 28S rDNA-specific non-LTR-retrotransposon R2Ol. Mob DNA. 2019:10(1):23. 10.1186/s13100-019-0167-2. PubMed DOI PMC
Lan T, Albert VA. Dynamic distribution patterns of ribosomal DNA and chromosomal evolution in Paphiopedilum, a lady's slipper orchid. BMC Plant Biol. 2011:11(1):126. 10.1186/1471-2229-11-126. PubMed DOI PMC
Lanciano S, Carpentier MC, Llauro C, Jobet E, Robakowska-Hyzorek D, Lasserre E, Ghesquière A, Panaud O, Mirouze M. Sequencing the extrachromosomal circular mobilome reveals retrotransposon activity in plants. PLoS Genet. 2017:13(2):e1006630. 10.1371/journal.pgen.1006630. PubMed DOI PMC
Lathe WC, Burke WD, Eickbush DG, Eickbush TH. Evolutionary stability of the R1 retrotransposable element in the genus Drosophila. Mol Biol Evol. 1995:12(6):1094–1105. 10.1093/oxfordjournals.molbev.a040283. PubMed DOI
Lavrinienko A, Jernfors T, Koskimäki JJ, Pirttilä AM, Watts PC. Does intraspecific variation in rDNA copy number affect analysis of microbial communities? Trends Microbiol. 2021:29(1):19–27. 10.1016/j.tim.2020.05.019. PubMed DOI
Lecanidou R, Eickbush TH, Kafatos FC. Ribosomal DNA genes of Bombyx mori: a minor fraction of the repeating units contain insertions. Nucleic Acids Res. 1984:12(11):4703–4713. 10.1093/nar/12.11.4703. PubMed DOI PMC
LeRiche K, Eagle SHC, Crease TJ. Copy number of the transposon, Pokey, in rDNA is positively correlated with rDNA copy number in Daphnia obtuse. PLoS ONE. 2014:9(12):e114773. 10.1371/journal.pone.0114773. PubMed DOI PMC
Lim K, Furuta Y, Kobayashi I. Large variations in bacterial ribosomal RNA genes. Mol Biol Evol. 2012:29(10):2937–2948. 10.1093/molbev/mss101. PubMed DOI PMC
Liu H, Pan G, Dang X, Li T, Zhou Z. Characterization of active ribosomal RNA harboring MITEs insertion in microsporidian Nosema bombycis genome. Parasitol Res. 2013:112(3):1011–1020. 10.1007/s00436-012-3223-0. PubMed DOI
Locati MD, Pagano JFB, Girard G, Ensink WA, van Olst M, van Leeuwen S, Nehrdich U, Spaink HP, Rauwerda H, Jonker MJ, et al. Expression of distinct maternal and somatic 5.8S, 18S, and 28S rRNA types during zebrafish development. RNA. 2017:23(8):1188–1199. 10.1261/rna.061515.117. PubMed DOI PMC
Long EO, Dawid IB. Expression of ribosomal DNA insertions in Drosophila melanogaster. Cell. 1979:18(4):1185–1196. 10.1016/0092-8674(79)90231-9. PubMed DOI
Longo MS, Brown JD, Zhang C, O’Neill MJ, O’Neill RJ. Identification of a recently active mammalian SINE derived from ribosomal RNA. Genome Biol Evol. 2015:7(3):775–788. 10.1093/gbe/evv015. PubMed DOI PMC
Lopez FB, Fort A, Tadini L, Probst AV, McHale M, Friel J, Ryder P, Pontvianne F, Pesaresi P, Sulpice R, et al. Gene dosage compensation of rRNA transcript levels in Arabidopsis thaliana lines with reduced ribosomal gene copy number. Plant Cell. 2021:33(4):1135–1150. 10.1093/plcell/koab020. PubMed DOI PMC
Luo Y, Fefelova E, Ninova M, Chen YCA, Aravin AA. Repression of interrupted and intact rDNA by the sumo pathway in Drosophila melanogaster. Elife. 2020:9:e52416. 10.7554/eLife.52416. PubMed DOI PMC
Maeda M, Shimada T, Ishihama A. Strength and regulation of seven rRNA promoters in Escherichia coli. PLoS One. 2015:10(12):e0144697. 10.1371/journal.pone.0144697. PubMed DOI PMC
Mahelka V, Krak K, Kopecký D, Fehrer J, Šafář J, Bartoš J, Hobza R, Blavet N, Blattner FR. Multiple horizontal transfers of nuclear ribosomal genes between phylogenetically distinct grass lineages. Proc Natl Acad Sci U S A. 2017:114(7):1726–1731. 10.1073/pnas.1613375114. PubMed DOI PMC
Maiwald S, Mann L, Garcia S, Heitkam T. Evolving together: Cassandra retrotransposons gradually mirror promoter mutations of the 5S rRNA genes. Mol Biol Evol. 2024:41(2):msae010. 10.1093/molbev/msae010. PubMed DOI PMC
Maiwald S, Weber B, Seibt KM, Schmidt T, Heitkam T. The Cassandra retrotransposon landscape in sugar beet (Beta vulgaris) and related Amaranthaceae: recombination and re-shuffling lead to a high structural variability. Ann Bot. 2021:127(1):91–109. 10.1093/aob/mcaa176. PubMed DOI PMC
Malik HS, Eickbush TH. Modular evolution of the integrase domain in the Ty3/Gypsy class of LTR retrotransposons. J Virol. 1999:73(6):5186–5190. 10.1128/JVI.73.6.5186-5190.1999. PubMed DOI PMC
Malone JH. Balancing copy number in ribosomal DNA. Proc Natl Acad Sci U S A. 2015:112(9):2635–2636. 10.1073/pnas.1500054112. PubMed DOI PMC
Mann L, Seibt KM, Weber B, Heitkam T. ECCsplorer: a pipeline to detect extrachromosomal circular DNA (eccDNA) from next-generation sequencing data. BMC Bioinformatics. 2022:23(1):1–15. 10.1186/s12859-021-04545-2. PubMed DOI PMC
Mansisidor A, Molinar T, Srivastava P, Dartis DD, Pino Delgado A, Blitzblau HG, Klein H, Hochwagen A. Genomic copy-number loss is rescued by self-limiting production of DNA circles. Mol Cell. 2018:72(3):583–593.e4. 10.1016/j.molcel.2018.08.036. PubMed DOI PMC
Marx V. Method of the year: long-read sequencing. Nat Methods. 2023:20(1):6–11. 10.1038/s41592-022-01730-w. PubMed DOI
Matveev V, Okada N. Retroposons of salmonoid fishes (Actinopterygii: Salmonoidei) and their evolution. Gene. 2009:434(1-2):16–28. 10.1016/j.gene.2008.04.022. PubMed DOI
McClintock B. The relation of a particular chromosomal element to the development of the nucleoli in Zea mays. Zeitschrift für Zellforschung und Mikroskopische Anatomie. 1934:21(2):294–326. 10.1007/BF00374060. DOI
McClintock B. The origin and behavior of mutable loci in maize. Proc Natl Acad Sci U S A. 1950:36(6):344–355. 10.1073/pnas.36.6.344. PubMed DOI PMC
McClintock B. Chromosome organization and genic expression. Cold Spring Harb Symp Quant Biol. 1951:16:13–47. 10.1101/SQB.1951.016.01.004. PubMed DOI
McKinlay A, Fultz D, Wang F, Pikaard CS. Targeted enrichment of rRNA gene tandem arrays for ultra-long sequencing by selective restriction endonuclease digestion. Front Plant Sci. 2021:12:762. 10.3389/fpls.2021.656049. PubMed DOI PMC
Merkulov P, Egorova E, Kirov I. Composition and structure of Arabidopsis thaliana extrachromosomal circular DNAs revealed by nanopore sequencing. Plants (Basel). 2023:12(11):2178. 10.3390/plants12112178. PubMed DOI PMC
Merlo MA, Cross I, Rodríguez-Rúa A, Manchado M, Rebordinos L. First approach to studying the genetics of the meagre (Argyrosomus regius; Asso, 1801) using three multigene families. Aquacult Res. 2013:44(6):974–984. 10.1111/j.1365-2109.2012.03103.x. DOI
Mizuochi H, Marasek A, Okazaki K. Molecular cloning of Tulipa fosteriana rDNA and subsequent FISH analysis yields cytogenetic organization of 5S rDNA and 45S rDNA in T. gesneriana and T. fosteriana. Euphytica. 2007:155(1–2):235–248. 10.1007/s10681-006-9325-y. DOI
Morgan EA. Insertions of Tn10 into an E. coli ribosomal RNA operon are incompletely polar. Cell. 1980:21(1):257–265. 10.1016/0092-8674(80)90133-6. PubMed DOI
Moss T, Stefanovsky V, Langlois F, Gagnon-Kugler T. A new paradigm for the regulation of the mammalian ribosomal RNA genes. Biochem Soc Trans. 2006:34(6):1079–1081. 10.1042/BST0341079. PubMed DOI
Muscarella DE, Vogt VM. A mobile group I intron in the nuclear rDNA of Physarum polycephalum. Cell. 1989:56(3):443–454. 10.1016/0092-8674(89)90247-x. PubMed DOI
Naish M, Alonge M, Wlodzimierz P, Tock AJ, Abramson BW, Schmücker A, Mandáková T, Jamge B, Lambing C, Kuo P, et al. The genetic and epigenetic landscape of the Arabidopsis centromeres. Science. 2021:374(6569):eabi7489. 10.1126/science.abi7489. PubMed DOI PMC
Nakajima RT, Cabral-de-Mello DC, Valente GT, Venere PC, Martins C. Evolutionary dynamics of rRNA gene clusters in cichlid fish. BMC Evol Biol. 2012:12:198. 10.1186/1471-2148-12-198. PubMed DOI PMC
Nei M, Hughes AL. Balanced polymorphism and evolution by the birth-and-death process in the MHC loci. In: Tsuji K, Aizawa M, Sasazuki T, editors. 11th Histocompatibility workshop and conference. Oxford: Oxford University Press; 1992. p. 27–38.
Nei M, Rooney AP. Concerted and birth-and-death evolution of multigene families. Ann Rev Genet. 2005:39(1):121–152. 10.1146/annurev.genet.39.073003.112240. PubMed DOI PMC
Nelson JO, Slicko A, Yamashita YM. The retrotransposon R2 maintains Drosophila ribosomal DNA repeats. Proc Natl Acad Sci U S A. 2023:120(23):e2221613120. 10.1073/pnas.2221613120. PubMed DOI PMC
Neuhaus H, Müller F, Etter A, Tobler H. Type I-like Intervening sequences are found in the rDNA of the nematode Ascaris lumbricoides. Nucleic Acids Res. 1987:15(19):7689–7707. 10.1093/nar/15.19.7689. PubMed DOI PMC
Neumann P, Navrátilová A, Koblížková A, Kejnovsk E, Hřibová E, Hobza R, Widmer A, Doležel J, Macas J. Plant centromeric retrotransposons: a structural and cytogenetic perspective. Mob DNA. 2011:2(1):4. 10.1186/1759-8753-2-4. PubMed DOI PMC
Nieto-Feliner G, Rosato M, Alegre G, San Segundo P, Rosselló JA, Garnatje T, Garcia S. Dissimilar molecular and morphological patterns in an introgressed peripheral population of a sand dune species (Armeria pungens, Plumbaginaceae). Plant Biol. 2019:21(6):1072–1082. 10.1111/plb.13035. PubMed DOI
Nieto-Feliner G, Rosselló JA. Better the devil you know? Guidelines for insightful utilization of nrDNA ITS in species-level evolutionary studies in plants. Mol Phylogenet Evol. 2007:44(2):911–919. 10.1016/j.ympev.2007.01.013. PubMed DOI
Nisen P, Shapiro L. E. coli ribosomal RNA contains sequences homologous to insertion sequences IS1 and IS2. Nature. 1979:282(5741):872–874. 10.1038/282872a0. PubMed DOI
Nishihara H, Smit AFA, Okada N. Functional noncoding sequences derived from SINEs in the mammalian genome. Genome Res. 2006:16(7):864–874. 10.1101/gr.5255506. PubMed DOI PMC
Novák P, Guignard MS, Neumann P, Kelly LJ, Mlinarec J, Koblížková A, Dodsworth S, Kovařík A, Pellicer J, Wang W, et al. Repeat-sequence turnover shifts fundamentally in species with large genomes. Nat Plants. 2020:6(11):1325–1329. 10.1038/s41477-020-00785-x. PubMed DOI
Novák P, Neumann P, Macas J. Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinformatics. 2010:11:378. 10.1186/1471-2105-11-378. PubMed DOI PMC
Novikova O. Chromodomains and LTR retrotransposons in plants. Commun Integr Biol. 2009:2(2):158–162. 10.4161/cib.7702. PubMed DOI PMC
O’Connor C, Adams JU. Essentials of cell biology. Cambridge (MA): NPG Education; 2010.
Orgel LE, Crick FHC. Selfish DNA: the ultimate parasite. Nature. 1980:284(5757):604–607. 10.1038/284604a0. PubMed DOI
Oyun NY, Zagoskina AS, Mukha DV. Inheritance of 5′-truncated copies of R2 retrotransposon in a series of generations of German cockroach, Blattella germanica. Russ J Genet. 2018:54(12):1438–1444. 10.1134/S1022795418120116. DOI
Paço A, Freitas R, Vieira-da-Silva A. Conversion of DNA sequences: from a transposable element to a tandem repeat or to a gene. Genes (Basel). 2019:10(12):1014. 10.3390/genes10121014. PubMed DOI PMC
Pedrosa-Harand A, de Almeida CCS, Mosiolek M, Blair MW, Schweizer D, Guerra M. Extensive ribosomal DNA amplification during Andean common bean (Phaseolus vulgaris L.) evolution. Theor Appl Genet. 2006:112(5):924–933. 10.1007/s00122-005-0196-8. PubMed DOI
Peng H, Mirouze M, Bucher E. Extrachromosomal circular DNA: a neglected nucleic acid molecule in plants. Curr Opin Plant Biol. 2022:69:102263. 10.1016/j.pbi.2022.102263. PubMed DOI
Penton EH, Crease TJ. Evolution of the transposable element Pokey in the ribosomal DNA of species in the subgenus Daphnia (Crustacea: Cladocera). Mol Biol Evol. 2004:21(9):1727–1739. 10.1093/molbev/msh189. PubMed DOI
Penton EH, Sullender BW, Crease TJ. Pokey, a new DNA transposon in Daphnia (Cladocera: Crustacea). J Mol Evol. 2002:55(6):664–673. 10.1007/s00239-002-2362-9. PubMed DOI
Pérez-González CE, Burke WD, Eickbush TH. R1 and R2 retrotransposition and deletion in the rDNA loci on the X and Y chromosomes of Drosophila melanogaster. Genetics. 2003:165(2):675–685. 10.1093/genetics/165.2.675. PubMed DOI PMC
Pérez-González CE, Eickbush TH. Dynamics of R1 and R2 elements in the rDNA locus of Drosophila simulans. Genetics. 2001:158(4):1557–1567. 10.1093/genetics/158.4.1557. PubMed DOI PMC
Pinhal D, Yoshimura TS, Araki CS, Martins C. The 5S rDNA family evolves through concerted and birth-and-death evolution in fish genomes: an example from freshwater stingrays. BMC Evol Biol. 2011:11:151. 10.1186/1471-2148-11-151. PubMed DOI PMC
Piskurek O, Nishihara H, Okada N. The evolution of two partner LINE/SINE families and a full-length chromodomain-containing Ty3/Gypsy LTR element in the first reptilian genome of Anolis carolinensis. Gene. 2009:441(1-2):111–118. 10.1016/j.gene.2008.11.030. PubMed DOI
Platt RN, Vandewege MW, Ray DA. Mammalian transposable elements and their impacts on genome evolution. Chromosome Res. 2018:26(1–2):25–43. 10.1007/s10577-017-9570-z. PubMed DOI PMC
Pont G, Degroote F, Picard G. Some extrachromosomal circular DNAs from Drosophila embryos are homologous to tandemly repeated genes. J Mol Biol. 1987:195(2):447–451. 10.1016/0022-2836(87)90665-6. PubMed DOI
Prokopowich CD, Gregory TR, Crease TJ. The correlation between rDNA copy number and genome size in eukaryotes. Genome. 2003:46(1):48–50. 10.1139/g02-103. PubMed DOI
Raskina O, Barber JC, Nevo E, Belyayev A. Repetitive DNA and chromosomal rearrangements: speciation-related events in plant genomes. Cytogenet Genome Res. 2008:120(3–4):351–357. 10.1159/000121084. PubMed DOI
Redd PS, Payero L, Gilbert DM, Page CA, King R, McAssey EV, Bodie D, Diaz S, Hancock CN. Transposase expression, element abundance, element size, and DNA repair determine the mobility and heritability of PIF/Pong/Harbinger transposable elements. Front Cell Dev Biol. 2023:11:1184046. 10.3389/fcell.2023.1184046. PubMed DOI PMC
Renkawitz-Pohl R, Matsumoto L, Gerbi SA. Structure of the ribosomal DNA repeat of Sciara coprophila. Nucleic Acids Res. 1981:9(15):3747–3764. 10.1093/nar/9.15.3747. PubMed DOI PMC
Robicheau BM, Susko E, Harrigan AM, Snyder M. Ribosomal RNA genes contribute to the formation of pseudogenes and junk DNA in the human genome. Genome Biol Evol. 2017:9(2):380–397. 10.1093/gbe/evw307. PubMed DOI PMC
Rodríguez-González R, Gutiérrez ML, Fuentes I, Gálvez-Prada F, Sochorová J, Kovařík A, Garcia S. Release 4.0 of the plant rDNA database: a database on plant ribosomal DNA loci number, their position, and organization: an information source for comparative cytogenetics. In: Garcia S, Nualart N, editors. Plant genomic and cytogenetic databases: methods in molecular biology. Vol. 2703. New York (NY): Humana; 2023. p. 237–245. 10.1007/978-1-0716-3389-2_18. PubMed DOI
Saifitdinova A, Galkina S, Kulak M, Fillon V, Volodkina V, Pavlova O, Gaginskaya E. The dispersal of ribosomal gene sequences in the karyotype of Coturnix japonica. Biopolym Cell. 2019:35(3):229–230. 10.7124/bc.0009F5. DOI
Sampath P, Yang T-J. Miniature inverted-repeat transposable elements (MITEs) as valuable genomic resources for the evolution and breeding of Brassica crops. Plant Breed Biotechnol. 2014:2(4):322–333. 10.9787/PBB.2014.2.4.322. DOI
Schmidt C, Fransz P, Rönspies M, Dreissig S, Fuchs J, Heckmann S, Houben A, Puchta H. Changing local recombination patterns in Arabidopsis by CRISPR/Cas mediated chromosome engineering. Nat Commun. 2020:11(1):4418. 10.1038/s41467-020-18277-z. PubMed DOI PMC
Schmidt N, Seibt KM, Weber B, Schwarzacher T, Schmidt T, Heitkam T. Broken, silent, and in hiding: tamed endogenous pararetroviruses escape elimination from the genome of sugar beet (Beta vulgaris). Ann Bot. 2021:128(3):281–299. 10.1093/aob/mcab042. PubMed DOI PMC
Schmidt T, Heitkam T, Liedtke S, Schubert V, Menzel G. Adding color to a century-old enigma: multi-color chromosome identification unravels the autotriploid nature of saffron (Crocus sativus) as a hybrid of wild Crocus cartwrightianus cytotypes. New Phytol. 2019:222(4):1965–1980. 10.1111/nph.15715. PubMed DOI
Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, et al. The B73 maize genome: complexity, diversity, and dynamics. Science. 2009:326(5956):1112–1115. 10.1126/science.1178534. PubMed DOI
Schrader L, Schmitz J. The impact of transposable elements in adaptive evolution. Mol Ecol. 2019:28(6):1537–1549. 10.1111/mec.14794. PubMed DOI
Schubert I. Mobile nucleolus organizing regions (NORs) in Allium (Liliaceae s. lat.)?—inferences from the specifity of silver staining. Plant Syst Evol. 1984:144(3–4):291–305. 10.1007/BF00984139. DOI
Schubert I, Wobus U. In situ hybridization confirms jumping nucleolus organizing regions in Allium. Chromosoma. 1985:92(2):143–148. 10.1007/BF00328466. DOI
Seibt KM, Schmidt T, Heitkam T. FlexiDot: highly customizable, ambiguity-aware dotplots for visual sequence analyses. Bioinformatics. 2018:34(20):3575–3577. 10.1093/bioinformatics/bty395. PubMed DOI
Seibt KM, Schmidt T, Heitkam T. The conserved 3′ Angio-domain defines a superfamily of short interspersed nuclear elements (SINEs) in higher plants. Plant J. 2020:101(3):681–699. 10.1111/tpj.14567. PubMed DOI
Setiawan AB, Teo CH, Kikuchi S, Sassa H, Kato K, Koba T. Chromosomal locations of a non-LTR retrotransposon, Menolird18, in Cucumis melo and Cucumis sativus, and its implication on genome evolution of Cucumis species. Cytogenet Genome Res. 2020:160(9):554–564. 10.1159/000511119. PubMed DOI
Shahid S, Slotkin RK. The current revolution in transposable element biology enabled by long reads. Curr Opin Plant Biol. 2020:54:49–56. 10.1016/j.pbi.2019.12.012. PubMed DOI
Shibata F, Hizume M. Evolution of 5S rDNA units and their chromosomal localization in Allium cepa and Allium schoenoprasum revealed by microdissection and FISH. Theor Appl Genet. 2002:105(2):167–172. 10.1007/s00122-002-0950-0. PubMed DOI
Silva-Sousa R, López-Panadès E, Casacuberta E. Drosophila telomeres: an example of co-evolution with transposable elements. Genome Dyn. 2012:7:46–67. 10.1159/000337127. PubMed DOI
Sinclair DA, Guarente L. Extrachromosomal rDNA circles—a cause of aging in yeast. Cell. 1997:91(7):1033–1042. 10.1016/S0092-8674(00)80493-6. PubMed DOI
Smith CJ, Castanon O, Said K, Volf V, Khoshakhlagh P, Hornick A, Ferreira R, Wu CT, Güell M, Garg S, et al. Enabling large-scale genome editing at repetitive elements by reducing DNA nicking. Nucleic Acids Res. 2020:48(9):5183–5195. 10.1093/nar/gkaa239. PubMed DOI PMC
Sochorová J, Garcia S, Gálvez F, Symonová R, Kovařík A. Evolutionary trends in animal ribosomal DNA loci: introduction to a new online database. Chromosoma. 2018:127(1):141–150. 10.1007/s00412-017-0651-8. PubMed DOI PMC
Sultana T, Zamborlini A, Cristofari G, Lesage P. Integration site selection by retroviruses and transposable elements in eukaryotes. Nat Rev Genet. 2017:18(5):292–308. 10.1038/nrg.2017.7. PubMed DOI
Sultanov D, Hochwagen A. Varying strength of selection contributes to the intragenomic diversity of rRNA genes. Nat Commun. 2022:13(1):7245. 10.1038/s41467-022-34989-w. PubMed DOI PMC
Symonová R, Majtánová Z, Sember A, Staaks GBO, Bohlen J, Freyhof J, Rábová M, Ráb P. Genome differentiation in a species pair of coregonine fishes: an extremely rapid speciation driven by stress-activated retrotransposons mediating extensive ribosomal DNA multiplications. BMC Evol Biol. 2013:13:42. 10.1186/1471-2148-13-42. PubMed DOI PMC
Symonová R, Ocalewicz K, Kirtiklis L, Delmastro GB, Pelikánová Š, Garcia S, Kovařík A. Higher-order organisation of extremely amplified, potentially functional and massively methylated 5S rDNA in European pikes (Esox sp.). BMC Genomics. 2017:18(1):391. 10.1186/s12864-017-3774-7. PubMed DOI PMC
Tamayo-Ordóñez YJ, Narváez-Zapata JA, Tamayo-Ordóñez MC, Sánchez-Teyer LF. Retroelements and DNA methylation could contribute to diversity of 5S rDNA in Agave L. J Mol Evol. 2018:86(6):404–423. 10.1007/s00239-018-9856-6. PubMed DOI
TE Hub Consortium, Elliot TA, Heitkam T, Hubley R, Quesneville H, Suh A, Wheeler TJ. TE Hub: a community-oriented space for sharing and connecting tools, data, resources, and methods for transposable element annotation. Mob DNA. 2021:12(1):16. 10.1186/s13100-021-00244-0. PubMed DOI PMC
Tulpová Z, Kovařík A, Toegelová H, Navrátilová P, Kapustová V, Hřibová E, Vrána J, Macas J, Doležel J, Šimková H. Fine structure and transcription dynamics of bread wheat ribosomal DNA loci deciphered by a multi-omics approach. Plant Genome. 2022:15(1):e20191. 10.1002/tpg2.20191. PubMed DOI
van’t Hof AE, Campagne P, Rigden DJ, Yung CJ, Lingley J, Quail MA, Hall N, Darby AC, Saccheri IJ. The industrial melanism mutation in British peppered moths is a transposable element. Nature. 2016:534(7605):102–105. 10.1038/nature17951. PubMed DOI
Vassetzky NS, Kramerov DA. SINEBase: a database and tool for SINE analysis. Nucleic Acids Res. 2013:41(D1):83–89. 10.1093/nar/gks1263. PubMed DOI PMC
Vincent A, Petes TD. Isolation and characterization of a Ty element inserted into the ribosomal DNA of the yeast Saccharomyces cerevisiae. Nucleic Acids Res. 1986:14(7):2939–2949. 10.1093/nar/14.7.2939. PubMed DOI PMC
Wang J, Han G-Z. Unearthing LTR retrotransposon gag genes co-opted in the deep evolution of eukaryotes. Mol Biol Evol. 2021:38(8):3267–3278. 10.1093/molbev/msab101. PubMed DOI PMC
Wang J, Wang A, Han Z, Zhang Z, Li F, Li X. Characterization of three novel SINE families with unusual features in Helicoverpa armigera. PLoS ONE. 2012:7(2):e31355. 10.1371/journal.pone.0031355. PubMed DOI PMC
Wang W, Zhang X, Garcia S, Leitch AR, Kovařík A. Intragenomic rDNA variation-the product of concerted evolution, mutation, or something in between? Heredity (Edinb). 2023:131(3):179–188. 10.1038/s41437-023-00634-5. PubMed DOI PMC
Watada E, Li S, Hori Y, Fujiki K, Shirahige K, Inada T, Kobayashi T. Age-dependent ribosomal DNA variations in mice. Mol Cell Biol. 2020:40(22):e00368-20. 10.1128/MCB.00368-20. PubMed DOI PMC
Weber B, Heitkam T, Holtgräwe D, Weisshaar B, Minoche AE, Dohm JC, Himmelbauer H, Schmidt T. Highly diverse chromoviruses of Beta vulgaris are classified by chromodomains and chromosomal integration. Mob DNA. 2013:4(1):8. 10.1186/1759-8753-4-8. PubMed DOI PMC
Wells JN, Feschotte C. A field guide to eukaryotic transposable elements. Annu Rev Genet. 2020:54(1):539–561. 10.1146/annurev-genet-040620-022145. PubMed DOI PMC
Williams SM, Robbins LG, Cluster PD, Allard RW, Strobeck C. Superstructure of the Drosophila ribosomal gene family. Proc Natl Acad Sci U S A. 1990:87(8):3156–3160. 10.1073/pnas.87.8.3156. PubMed DOI PMC
Wollrab C, Heitkam T, Holtgräwe D, Weisshaar B, Minoche AE, Dohm JC, Himmelbauer H, Schmidt T. Evolutionary reshuffling in the Errantivirus lineage Elbe within the Beta vulgaris genome. Plant J. 2012:72(4):636–651. 10.1111/j.1365-313X.2012.05107.x. PubMed DOI
Xiong Y, Eickbush TH. The site-specific ribosomal DNA insertion element R1Bm belongs to a class of non-long-terminal-repeat retrotransposons. Mol Cell Biol. 1988:8(1):114–123. 10.1128/mcb.8.1.114-123.1988. PubMed DOI PMC
Yang N, Srivastav SP, Rahman R, Ma Q, Dayama G, Li S, Chinen M, Lei EP, Rosbash M, Lau NC. Transposable element landscapes in aging Drosophila. PLoS Genet. 2022:18(3):e1010024. 10.1371/journal.pgen.1010024. PubMed DOI PMC
Yang F, Su W, Chung OW, Tracy L, Wang L, Ramsden DA, Zhang ZZ. Retrotransposons hijack alt-EJ for DNA replication and eccDNA biogenesis. Nature. 2023:620(7972):218–225. 10.1038/s41586-023-06327-7. PubMed DOI PMC
Yano CF, Merlo MA, Portela-Bens S, Cioffi MDB, Bertollo LAC, Santos-Júnior CD, Rebordinos L. Evolutionary dynamics of multigene families in Triportheus (Characiformes, Triportheidae): a transposon mediated mechanism? Front Mar Sci. 2020:7:6. 10.3389/fmars.2020.00006. DOI
Yin H, Du J, Li L, Jin C, Fan L, Li M, Wu J, Zhang S. Comparative genomic analysis reveals multiple long terminal repeats, lineage-specific amplification, and frequent interelement recombination for Cassandra retrotransposon in pear (Pyrus bretschneideri Rehd.). Genome Biol Evol. 2014:6(6):1423–1436. 10.1093/gbe/evu114. PubMed DOI PMC
Yushkova E, Moskalev A. Transposable elements and their role in aging. Ageing Res Rev. 2023:86:101881. 10.1016/j.arr.2023.101881. PubMed DOI
Zhang X, Eickbush TH. Characterization of active R2 retrotransposition in the rDNA locus of Drosophila simulans. Genetics. 2005:170(1):195–205. 10.1534/genetics.104.038703. PubMed DOI PMC
Zhang M, Tang Y-W, Xu Y, Yonezawa T, Shao Y, Wang Y-G, Song Z-P, Yang J, Zhang W-J. Concerted and birth-and-death evolution of 26S ribosomal DNA in Camellia L. Ann Bot. 2021:127(1):63–73. 10.1093/aob/mcaa169. PubMed DOI PMC