The Role of Repetitive Sequences in Repatterning of Major Ribosomal DNA Clusters in Lepidoptera
Jazyk angličtina Země Velká Británie, Anglie Médium print
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
37226278
PubMed Central
PMC10257491
DOI
10.1093/gbe/evad090
PII: 7179266
Knihovny.cz E-zdroje
- Klíčová slova
- Lepidoptera, major ribosomal RNA genes, mobile elements, satellite,
- MeSH
- chromozomy MeSH
- můry * genetika MeSH
- repetitivní sekvence nukleových kyselin * MeSH
- ribozomální DNA genetika MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- ribozomální DNA MeSH
Genes for major ribosomal RNAs (rDNA) are present in multiple copies mainly organized in tandem arrays. The number and position of rDNA loci can change dynamically and their repatterning is presumably driven by other repetitive sequences. We explored a peculiar rDNA organization in several representatives of Lepidoptera with either extremely large or numerous rDNA clusters. We combined molecular cytogenetics with analyses of second- and third-generation sequencing data to show that rDNA spreads as a transcription unit and reveal association between rDNA and various repeats. Furthermore, we performed comparative long read analyses among the species with derived rDNA distribution and moths with a single rDNA locus, which is considered ancestral. Our results suggest that satellite arrays, rather than mobile elements, facilitate homology-mediated spread of rDNA via either integration of extrachromosomal rDNA circles or ectopic recombination. The latter arguably better explains preferential spread of rDNA into terminal regions of lepidopteran chromosomes as efficiency of ectopic recombination depends on the proximity of homologous sequences to telomeres.
Department of Biology Tufts University
European Molecular Biology Laboratory Heidelberg Germany
Faculty of Science University of South Bohemia České Budějovice Czech Republic
Institute of Entomology Biology Centre CAS České Budějovice Czech Republic
Zobrazit více v PubMed
Ahola V, et al. 2014. The Glanville fritillary genome retains an ancient karyotype and reveals selective chromosomal fusions in Lepidoptera. Nat Commun. 5:4737. PubMed PMC
Barbosa P, et al. 2015. Identification and chromosome mapping of repetitive elements in the Astyanax scabripinnis (Teleostei: Characidae) species complex. Genetica. 143:55–62. PubMed
Baumgärtner L, Paiz LM, Zawadzki CH, Margarido VP, Portela Castro ALB. 2014. Heterochromatin polymorphism and physical mapping of 5S and 18S ribosomal DNA in four populations of Hypostomus strigaticeps (Regan, 1907) from the Paraná River basin, Brazil: evolutionary and environmental correlation. Zebrafish. 11:479–487. PubMed
Bedo DG. 1984. Karyotypic and chromosome banding studies of the potato tuber moth, Phthorimaea operculella (Zeller) (Lepidoptera, Gelechiidae). Can J Genet Cytol. 26:141–145.
Belser C, et al. 2021. Telomere-to-telomere gapless chromosomes of banana using nanopore sequencing. Commun Biol. 4:1047. PubMed PMC
Bishop G, et al. 2021. The genome sequence of the small tortoiseshell butterfly, Aglais urticae (linnaeus, 1758). Wellcome Open Res. 6:233. PubMed PMC
Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 30:2114–2120. PubMed PMC
Bueno D, Palacios-Gimenez OM, Cabral-de-Mello DC. 2013. Chromosomal mapping of repetitive DNAs in the grasshopper Abracris flavolineata reveal possible ancestry of the B chromosome and H3 histone spreading. PLoS ONE. 8:e66532. PubMed PMC
Cabral-de-Mello DC, Oliveira SG, de Moura RC, Martins C. 2011. Chromosomal organization of the 18S and 5S rRNAs and histone H3 genes in Scarabaeinae coleopterans: insights into the evolutionary dynamics of multigene families and heterochromatin. BMC Genet. 12:88. PubMed PMC
Cabral-de-Mello DC, Zrzavá M, Kubíčková S, Rendón P, Marec F. 2021. The role of satellite DNAs in genome architecture and sex chromosome evolution in Crambidae moths. Front Genet. 12:661417. PubMed PMC
Carabajal Paladino LZ, et al. 2019. Sex chromosome turnover in moths of the diverse superfamily Gelechioidea. Genome Biol Evol. 11:1307–1319. PubMed PMC
Carabajal Paladino LZ, Nguyen P, Šíchová J, Marec F. 2014. Mapping of single-copy genes by TSA-FISH in the codling moth, Cydia pomonella. BMC Genet. 15:S15. PubMed PMC
Cheng T, et al. 2017. Genomic adaptation to polyphagy and insecticides in a major East Asian noctuid pest. Nat Ecol Evol. 1:1747–1756. PubMed
Dalíková M, et al. 2017a. New insights into the evolution of the W chromosome in Lepidoptera. J Hered. 108:709–719. PubMed
Dalíková M, Provazníková I, Provazník J, Grof-Tisza P, Pepi A, Nguyen P. 2022. The role of repetitive DNA in re-patterning of major rDNA clusters in Lepidoptera, Dryad, Dataset. 10.5061/dryad.gmsbcc2qj PubMed DOI PMC
Dalíková M, Zrzavá M, Kubíčková S, Marec F. 2017b. W-enriched satellite sequence in the Indian meal moth, Plodia interpunctella (Lepidoptera, Pyralidae). Chromosome Res. 25:241–252. PubMed
da Silva M, Barbosa P, Artoni RF, Feldberg E. 2016. 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. 149:297–303. PubMed
De Coster W, D’Hert S, Schultz DT, Cruts M, Van Broeckhoven C. 2018. Nanopack: visualizing and processing long-read sequencing data. Bioinformatics. 34:2666–2669. PubMed PMC
de Sene VF, et al. 2015. Mapping of the retrotransposable elements Rex1 and Rex3 in chromosomes of Eigenmannia (Teleostei, Gymnotiformes, Sternopygidae). Cytogenet Genome Res. 146:319–324. PubMed
Eickbush TH, Eickbush DG. 2007. Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics. 175:477–485. PubMed PMC
Eickbush TH, Eickbush DG. 2015. Integration, regulation, and long-term stability of R2 retrotransposons. Microbiol Spectr. 3:2. PubMed PMC
Elliott TA, Stage DE, Crease TJ, Eickbush TH. 2013. In and out of the rRNA genes: characterization of Pokey elements in the sequenced Daphnia genome. Mob DNA. 4:20. PubMed PMC
Ferretti ABSM, et al. 2019. How dynamic could be the 45S rDNA cistron? An intriguing variability in a grasshopper species revealed by integration of chromosomal and genomic data. Chromosoma. 128:165–175. PubMed
Fiore-Donno AM, et al. 2012. 18S rDNA phylogeny of Lamproderma and allied genera (Stemonitales, Myxomycetes, Amoebozoa). PLoS ONE. 7:e35359. PubMed PMC
Fu L, Niu B, Zhu Z, Wu S, Li W. 2012. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics. 28:3150–3152. PubMed PMC
Fujiwara H, et al. 1984. Introns and their flanking sequences of Bombyx mori rDNA. Nucl Acids Res. 12:6861–6869. PubMed PMC
Fuková I, Nguyen P, Marec F. 2005. Codling moth cytogenetics: karyotype, chromosomal location of rDNA, and molecular differentiation of sex chromosomes. Genome. 48:1083–1092. PubMed
García-Souto D, Pérez-García C, Kendall J, Pasantes J. 2016. Molecular cytogenetics in trough shells (Mactridae, Bivalvia): divergent GC-rich heterochromatin content. Genes (Basel). 7:47. PubMed PMC
García S, Kovařík A, Leitch AR, Garnatje T. 2017. Cytogenetic features of rRNA genes across land plants: analysis of the Plant rDNA database. Plant J. 89:1020–1030. PubMed
Garrido-Ramos MA. 2017. Satellite DNA: An Evolving Topic. Genes (Basel). 8:230. PubMed PMC
Goldman ASH, Lichten M. 1996. The efficiency of meiotic recombination between dispersed sequences in Saccharomyces cerevisiae depends upon their chromosomal location. Genetics. 144:43–55. PubMed PMC
Grozdanov P, Georgiev O, Karagyozov L. 2003. Complete sequence of the 45-kb mouse ribosomal DNA repeat: analysis of the intergenic spacer. Genomics. 82:637–643. PubMed
Haq IU, et al. 2022. Satellitome analysis and transposable elements comparison in geographically distant populations of Spodoptera frugiperda. Life (Basel). 12:521. PubMed PMC
Havlová K, et al. 2016. Variation of 45S rDNA intergenic spacers in Arabidopsis thaliana. Plant Mol Biol. 92:457–471. PubMed
Ingle J, Timmis JN, Sinclair J. 1975. The relationship between satellite deoxyribonucleic acid, ribosomal ribonucleic acid gene redundancy, and genome size in plants. Plant Physiol. 55:496–501. PubMed PMC
Jakubczak JL, Burke WD, Eickbush TH. 1991. Retrotransposable elements RI and R2 interrupt the rRNA genes of most insects. Proc Natl Acad Sci U S A. 88:3295–3299. PubMed PMC
Jo SH, et al. 2009. Evolution of ribosomal DNA-derived satellite repeat in tomato genome. BMC Plant Biol. 9:42. PubMed PMC
Kato A, et al. 2006. Sensitive fluorescence in situ hybridization signal detection in maize using directly labeled probes produced by high concentration DNA polymerase nick translation. Biotechnic Histochem. 81:71–78. PubMed
Kierzek E, et al. 2009. Secondary structures for 5′ regions of R2 retrotransposon RNAs reveal a novel conserved pseudoknot and regions that evolve under different constraints. J Mol Biol. 390:428–442. PubMed PMC
Kobayashi T. 2011. Regulation of ribosomal RNA gene copy number and its role in modulating genome integrity and evolutionary adaptability in yeast. Cell Mol Life Sci. 68:1395–1403. PubMed PMC
Kojima KK, Fujiwara H. 2005. Long-term inheritance of the 28S rDNA-specific retrotransposon R2. Mol Biol Evol. 22:2157–2165. PubMed
Kolmogorov M, Yuan J, Lin Y. 2019. Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol. 37:540–546. PubMed
Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods. 9:357–359. PubMed PMC
Langmead B, Wilks C, Antonescu V, Charles R. 2019. Scaling read aligners to hundreds of threads on general-purpose processors. Bioinformatics. 35:421–432. PubMed PMC
Li H, et al. 2009. The sequence Alignment/Map format and SAMtools. Bioinformatics. 25:2078–2079. PubMed PMC
Li H. 2018. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 34:3094–3100. PubMed PMC
Lohe AR, Roberts PA. 2000. Evolution of DNA in heterochromatin: the Drosophila melanogaster sibling species subgroup as a resource. Genetica. 109:125–130. PubMed
Long EO, Dawid IB. 1979. Expression of ribosomal DNA insertions in Drosophila melanogaster. Cell. 18:1185–1196. PubMed
Long EO, Dawid IB. 1980. Repeated genes in eukaryotes. Annu Rev Biochem. 49:727–764. PubMed
Lu Y, Kochert GD, Isenhour DJ, Adang MJ. 1994. Molecular characterization of a strain-specific repeated DNA sequence in the fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). Insect Mol Biol. 3:123–130. PubMed
Lukhtanov V. 2015. The blue butterfly Polyommatus (Plebicula) atlanticus (Lepidoptera, Lycaenidae) holds the record of the highest number of chromosomes in the non-polyploid eukaryotic organisms. Comparat Cytogenet. 9:683–690. PubMed PMC
Macas J, Navrátilová A, Mészáros T. 2003. Sequence subfamilies of satellite repeats related to rDNA intergenic spacer are differentially amplified on Vicia sativa chromosomes. Chromosoma. 112:152–158. PubMed
Mahendran B, Acharya C, Dash R, Ghosh SK, Kundu SC. 2006. Repetitive DNA in tropical tasar silkworm Antheraea mylitta. Gene. 370:51–57. PubMed
Mandrioli M, Manicardi GC, Marec F. 2003. Cytogenetic and molecular characterization of the MBSAT1 satellite DNA in holokinetic chromosomes of the cabbage moth, Mamestra brassicae (Lepidoptera). Chromosome Res. 11:51–56. PubMed
Martí E, et al. 2021. Cytogenomic analysis unveils mixed molecular evolution and recurrent chromosomal rearrangements shaping the multigene families on Schistocerca grasshopper genomes. Evolution. 75:2027–2041. PubMed
McKinlay A, Fultz D, Wang F, Pikaard CS. 2021. Targeted enrichment of rRNA gene tandem arrays for ultra-long sequencing by selective restriction endonuclease digestion. Front Plant Sci. 12:656049. PubMed PMC
Mediouni J, Fuková I, Frydrychová R, Dhouibi MH, Marec F. 2004. Karyotype, sex chromatin and sex chromosome differentiation in the carob moth, Ectomyelois ceratoniae (Lepidoptera: Pyralidae). Caryologia. 57:184–194.
Muirhead CA, Presgraves DC. 2021. Satellite DNA-mediated diversification of a sex-ratio meiotic drive gene family in Drosophila. Nat Ecol Evol. 5:1604–1612. PubMed PMC
Nelson JO, Slicko A, Yamashita YM. 2023. The retrotransposon R2 maintains Drosophila ribosomal DNA repeats. Proc Natl Acad Sci U S A. 120:e2221613120. 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
Nguyen P, Sahara K, Yoshido A, Marec F. 2010. Evolutionary dynamics of rDNA clusters on chromosomes of moths and butterflies (lepidoptera). Genetica. 138:343–354. PubMed
Noller HF, Lancaster L, Mohan S, Zhou J. 2017. Ribosome structural dynamics in translocation: yet another functional role for ribosomal RNA. Quart Rev Biophys. 50:e12. PubMed
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
Palacios-Gimenez OM, Castillo ER, Martí DA, Cabral-de-Mello DC. 2013. Tracking the evolution of sex chromosome systems in Melanoplinae grasshoppers through chromosomal mapping of repetitive DNA sequences. BMC Evol Biol. 13:167. PubMed PMC
Perumal S, et al. 2017. Elucidating the major hidden genomic components of the A, C, and AC genomes and their influence on Brassica evolution. Sci Rep. 7:17986. PubMed PMC
Poletto AB, et al. 2010. Chromosome differentiation patterns during cichlid fish evolution. BMC Genet. 11:50. PubMed PMC
Prins JD, Saitoh K. 2003. Karyology and sex determination. In: Kükenthal W, editors. Band 4: Arthropoda, 2 Hälfte: Insecta, Lepidoptera, moths and butterflies, Teilband/part 36, vol 2: morphology, physiology, and development. Berlin, Boston: DE GRUYTER. p. 449–468.
Prokopowich CD, Gregory TR, Crease TJ. 2003. The correlation between rDNA copy number and genome size in eukaryotes. Genome. 46:48–50. PubMed
Proux-Wéra E, Byrne KP, Wolfe KH. 2013. Evolutionary mobility of the ribosomal DNA array in yeasts. Genome Biol Evol. 5:525–531. PubMed PMC
Provazníková I, et al. 2021. Large-scale comparative analysis of cytogenetic markers across Lepidoptera. Sci Rep. 11:12214. PubMed PMC
Raskina O, Barber JC, Nevo E, Belyayev A. 2008. Repetitive DNA and chromosomal rearrangements: speciation-related events in plant genomes. Cytogenet Genome Res. 120:351–357. PubMed
Raskina O, Belyayev A, Nevo E. 2004. Activity of the En/Spm-like transposons in meiosis as a base for chromosome repatterning in a small, isolated, peripheral population of Aegilops speltoides Tausch. Chromosome Res. 12:153–161. PubMed
Rego A, Marec F. 2003. Telomeric and interstitial telomeric sequences in holokinetic chromosomes of Lepidoptera: telomeric DNA mediates association between postpachytene bivalents in achiasmatic meiosis of females. Chromosome Res. 11:681–694. PubMed
Robinson R. 1971. Lepidoptera genetics. Oxford: Pergamon Press.
Roiha H, Miller J, Woods L. 1981. Arrangements and rearrangements of sequences flanking the two types of rDNA insertion in D. melanogaster. Nature. 290:749–754. PubMed
Ruiz-Herrera A, Nergadze SG, Santagostino M, Giulotto E. 2008. Telomeric repeats far from the ends: mechanisms of origin and role in evolution. Cytogenet Genome Res. 122:219–228. PubMed
Ruiz JC, Wahl GM. 1990. Chromosomal destabilization during gene amplification. Mol Cell Biol. 10:3056–3066. PubMed PMC
Scacchetti PC, et al. 2012. Molecular characterization and physical mapping of two classes of 5S rDNA in the genomes of Gymnotus sylvius and G. inaequilabiatus (Gymnotiformes, Gymnotidae). Cytogenet Genome Res. 136:131–137. PubMed
Scali V, et al. 2016. Co-localization of ribosomal and telomeric sequences in Leptynia (Insecta: Phasmatodea). Ital J Zool. 83:285–290.
Sember A, et al. 2018. Dynamics of tandemly repeated DNA sequences during evolution of diploid and tetraploid botiid loaches (Teleostei: Cobitoidea: Botiidae). PLoS ONE. 13:e0195054. PubMed PMC
Šíchová J, et al. 2015. Dynamic karyotype evolution and unique sex determination systems in Leptidea wood white butterflies. BMC Evol Biol. 15:89. PubMed PMC
Šíchová J, et al. 2016. Fissions, fusions, and translocations shaped the karyotype and multiple sex chromosome constitution of the northeast-Asian wood white butterfly, Leptidea amurensis. Biol J Linn Soc. 118:457–471.
Šíchová J, Nguyen P, Dalíková M, Marec F. 2013. Chromosomal evolution in tortricid moths: conserved karyotypes with diverged features. PLoS ONE. 8:e64520. PubMed PMC
Silva DMZ de A, et al. 2014. Delimiting the origin of a B chromosome by FISH mapping, chromosome painting and DNA sequence analysis in Astyanax paranae (Teleostei, Characiformes). PLoS ONE. 9:e94896. PubMed PMC
Sims J, Sestini G, Elgert C, von Haeseler A, Schlögelhofer P. 2021. Sequencing of the Arabidopsis NOR2 reveals its distinct organization and tissue-specific rRNA ribosomal variants. Nat Commun. 12:387. PubMed PMC
Smit AFA, Hubley R, Green P. 2013. RepeatMasker Open-4.0.
Sochorová J, Garcia S, Gálvez F, Symonová R, Kovařík A. 2018. Evolutionary trends in animal ribosomal DNA loci: introduction to a new online database. Chromosoma. 127:141–150. PubMed PMC
Sproul JS, Barton LM, Maddison DR. 2020. Repetitive DNA profiles reveal evidence of rapid genome evolution and reflect species boundaries in ground beetles. Syst Biol. 69:1137–1148. PubMed
Symonová R, et al. 2013. 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. 13:42. PubMed PMC
Symonová R. 2019. Integrative rDNAomics—importance of the oldest repetitive fraction of the eukaryote genome. Genes (Basel). 10:345. PubMed PMC
Van Nieukerken EJ, et al. 2011. Order Lepidoptera Linnaeus, 1758. In: Zhang, Z.-Q. (Ed.) animal biodiversity: an outline of higher-level classification and survey of taxonomic richness. Zootaxa. 3148:212. PubMed
Van’t Hof AE, et al. 2013. Linkage map of the peppered moth, Biston betularia (Lepidoptera, Geometridae): a model of industrial melanism. Heredity (Edinb). 110:283–295. PubMed PMC
Věchtová P, et al. 2016. CpSAT-1, a transcribed satellite sequence from the codling moth, Cydia pomonella. Genetica. 144:385–395. PubMed
Vershinina AO, Anokhin BA, Lukhtanov VA. 2015. Ribosomal DNA clusters and telomeric (TTAGG)n repeats in blue butterflies (Lepidoptera, Lycaenidae) with low and high chromosome numbers. Comp Cytogenet. 9:161–171. PubMed PMC
Vítková M, Fuková I, Kubíčková S, Marec F. 2007. Molecular divergence of the W chromosomes in pyralid moths (Lepidoptera). Chromosome Res. 15:917–930. PubMed
Vondrak T, et al. 2021. Complex sequence organization of heterochromatin in the holocentric plant Cuscuta europaea elucidated by the computational analysis of nanopore reads. Comput Struct Biotechnol. 19:2179–2189. PubMed PMC
Weber B, et al. 2013. Highly diverse chromoviruses of Beta vulgaris are classified by chromodomains and chromosomal integration. Mobile DNA. 4:8. PubMed PMC
Wolf KW, Novak K, Marec F. 1997. Kinetic organization of metaphase I bivalents in spermatogenesis of Lepidoptera and Trichoptera species with small chromosome numbers. Heredity (Edinb). 79:35–143.
Wu S, Xiong J, Yu Y. 2015. Taxonomic resolutions based on 18S rRNA genes: a case study of subclass Copepoda. PLoS ONE. 10:e0131498. PubMed PMC
Xiong Y, Burke WD, Jakubczak JL, Eickbush TH. 1988. Ribosomal DNA insertion elements R1Bm and R2Bm can transpose in a sequence specific manner to locations outside the 28S genes. Nucleic Acids Res. 16:10561–10573. PubMed PMC
Yano CF, et al. 2020. Evolutionary dynamics of multigene families in Triportheus (Characiformes, Triportheidae): a transposon mediated mechanism? Front Mar Sci. 7:6.
Yasukochi Y, et al. 2011. Isolation of BAC clones containing conserved genes from libraries of three distantly related moths: a useful resource for comparative genomics of Lepidoptera. J Biomed Biotechnol. 2011:1–6. PubMed PMC
Zhou J, Eickbush MT, Eickbush TH. 2013. A population genetic model for the maintenance of R2 retrotransposons in rRNA gene loci. PLoS Genet. 9:e1003179. PubMed PMC
Zrzavá M, et al. 2018. Sex chromosomes of the iconic moth Abraxas grossulariata (Lepidoptera, Geometridae) and its congener A. sylvata. Genes (Basel). 9:279. PubMed PMC
The Role of Repetitive Sequences in Repatterning of Major Ribosomal DNA Clusters in Lepidoptera