Accumulation of retrotransposons contributes to W chromosome differentiation in the willow beauty Peribatodes rhomboidaria (Lepidoptera: Geometridae)
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
36631492
PubMed Central
PMC9834309
DOI
10.1038/s41598-023-27757-3
PII: 10.1038/s41598-023-27757-3
Knihovny.cz E-zdroje
- MeSH
- hybridizace in situ fluorescenční MeSH
- můry * genetika MeSH
- pohlavní chromozomy genetika MeSH
- retroelementy genetika MeSH
- Salix * genetika MeSH
- srovnávací genomová hybridizace MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- retroelementy MeSH
The W chromosome of Lepidoptera is typically gene-poor, repeat-rich and composed of heterochromatin. Pioneering studies investigating this chromosome reported an abundance of mobile elements. However, the actual composition of the W chromosome varies greatly between species, as repeatedly demonstrated by comparative genomic hybridization (CGH) or fluorescence in situ hybridization (FISH). Here we present an analysis of repeats on the W chromosome in the willow beauty, Peribatodes rhomboidaria (Geometridae), a species in which CGH predicted an abundance of W-enriched or W-specific sequences. Indeed, comparative analysis of male and female genomes using RepeatExplorer identified ten putative W chromosome-enriched repeats, most of which are LTR or LINE mobile elements. We analysed the two most abundant: PRW LINE-like and PRW Bel-Pao. The results of FISH mapping and bioinformatic analysis confirmed their enrichment on the W chromosome, supporting the hypothesis that mobile elements are the driving force of W chromosome differentiation in Lepidoptera. As the W chromosome is highly underrepresented in chromosome-level genome assemblies of Lepidoptera, this recently introduced approach, combining bioinformatic comparative genome analysis with molecular cytogenetics, provides an elegant tool for studying this elusive and rapidly evolving part of the genome.
Department of Experimental Biology Genetics Area University of Jaén Jaén Spain
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
Charlesworth B. The evolution of chromosomal sex determination and dosage compensation. Curr. Biol. 1996;6:149–162. doi: 10.1016/S0960-9822(02)00448-7. PubMed DOI
Abbott JK, Nordén AK, Hansson B. Sex chromosome evolution: historical insights and future perspectives. Proc. R. Soc. B. 2017;284:20162806. doi: 10.1098/rspb.2016.2806. PubMed DOI PMC
Charlesworth B. The evolution of sex chromosomes. Science. 1991;251:1030–1033. doi: 10.1126/science.1998119. PubMed DOI
Furman BLS, et al. Sex chromosome evolution: So many exceptions to the rules. Genome Biol. Evol. 2020;12:750–763. doi: 10.1093/gbe/evaa081. PubMed DOI PMC
Traut W, Sahara K, Marec F. Sex chromosomes and sex determination in Lepidoptera. Sex. Dev. 2007;1:332–346. doi: 10.1159/000111765. PubMed DOI
Kiuchi T, et al. A single female-specific piRNA is the primary determiner of sex in the silkworm. Nature. 2014;509:633–636. doi: 10.1038/nature13315. PubMed DOI
Abe H, Mita K, Yasukochi Y, Oshiki T, Shimada T. Retrotransposable elements on the W chromosome of the silkworm, Bombyx mori. Cytogenet. Genome Res. 2005;110:144–151. doi: 10.1159/000084946. PubMed DOI
Sahara K, Yoshido A, Traut W. Sex chromosome evolution in moths and butterflies. Chromosome Res. 2012;20:83–94. doi: 10.1007/s10577-011-9262-z. PubMed DOI
Traut W, Vogel H, Glöckner G, Hartmann E, Heckel DG. High-throughput sequencing of a single chromosome: A moth W chromosome. Chromosome Res. 2013;21:491–505. doi: 10.1007/s10577-013-9376-6. PubMed DOI
Cabral-de-Mello DC, Zrzavá M, Kubíčková S, Rendón P, Marec F. The role of satellite DNAs in genome architecture and sex chromosome evolution in Crambidae moths. Front. Genet. 2021;12:661417. doi: 10.3389/fgene.2021.661417. PubMed DOI PMC
Dalíková M, Zrzavá M, Kubíčková S, Marec F. W-enriched satellite sequence in the Indian meal moth, Plodia interpunctella (Lepidoptera, Pyralidae) Chromosome Res. 2017;25:241–252. doi: 10.1007/s10577-017-9558-8. PubMed DOI
Fuková I, et al. Probing the W chromosome of the codling moth, Cydia pomonella, with sequences from microdissected sex chromatin. Chromosoma. 2007;116:135–145. doi: 10.1007/s00412-006-0086-0. PubMed DOI
Kejnovský E, Hobza R, Čermák T, Kubat Z, Vyskot B. The role of repetitive DNA in structure and evolution of sex chromosomes in plants. Heredity. 2009;102:533–541. doi: 10.1038/hdy.2009.17. PubMed DOI
Hood ME. Repetitive DNA in the automictic fungus Microbotryum violaceum. Genetica. 2005;124:1–10. doi: 10.1007/s10709-004-6615-y. PubMed DOI
Erlandsson R, Wilson JF, Pääbo S. Sex chromosomal transposable element accumulation and male-driven substitutional evolution in humans. Mol. Biol. Evol. 2000;17:804–812. doi: 10.1093/oxfordjournals.molbev.a026359. PubMed DOI
Toder R, Wakefield MJ, Graves JAM. The minimal mammalian Y chromosome—The marsupial Y as a model system. Cytogenet. Cell Genet. 2000;91:285–292. doi: 10.1159/000056858. PubMed DOI
Peona V, et al. The avian W chromosome is a refugium for endogenous retroviruses with likely effects on female-biased mutational load and genetic incompatibilities. Philos. Trans. R. Soc. B. 2021;376:20200186. doi: 10.1098/rstb.2020.0186. PubMed DOI PMC
Junakovic N, Terrinoni A, Di Franco C, Vieira C, Loevenbruck C. Accumulation of transposable elements in the heterochromatin and on the Y chromosome of Drosophila simulans and Drosophila melanogaster. J. Mol. Evol. 1998;46:661–668. doi: 10.1007/PL00006346. PubMed DOI
Rosolen LAM, Vicari MR, Almeida MC. Accumulation of transposable elements in autosomes and giant sex chromosomes of Omophoita (Chrysomelidae: Alticinae) Cytogenet. Genome Res. 2019;156:215–222. doi: 10.1159/000495199. PubMed DOI
Śliwińska EB, Martyka R, Tryjanowski P. Evolutionary interaction between W/Y chromosome and transposable elements. Genetica. 2016;144:267–278. doi: 10.1007/s10709-016-9895-0. PubMed DOI PMC
Zhu Y, Dai J, Fuerst PG, Voytas DF. Controlling integration specificity of a yeast retrotransposon. Proc. Natl. Acad. Sci. USA. 2003;100:5891–5895. doi: 10.1073/pnas.1036705100. PubMed DOI PMC
Bourque G, et al. Ten things you should know about transposable elements. Genome Biol. 2018;19:199. doi: 10.1186/s13059-018-1577-z. PubMed DOI PMC
Charlesworth B, Langley CH. The evolution of self-regulated transposition of transposable elements. Genetics. 1986;112:359–383. doi: 10.1093/genetics/112.2.359. PubMed DOI PMC
Ostertag EM, Kazazian J. Biology of mammalian L1 retrotransposons. Annu. Rev. Genet. 2001;35:501–538. doi: 10.1146/annurev.genet.35.102401.091032. PubMed DOI
Fugmann SD. The origins of the Rag genes—From transposition to V(D)J recombination. Semin. Immunol. 2010;22:10–16. doi: 10.1016/j.smim.2009.11.004. PubMed DOI PMC
Belfort M, Curcio MJ, Lued NF. Telomerase and retrotransposons: Reverse transcriptases that shaped genomes. Proc. Natl. Acad. Sci. USA. 2011;108:20304–20310. doi: 10.1073/pnas.1100269109. PubMed DOI PMC
Kazazian HH. Mobile elements: Drivers of genome evolution. Science. 2004;303:1626–1632. doi: 10.1126/science.1089670. PubMed DOI
Lyon MF. LINE-1 elements and X chromosome inactivation: A function for ‘junk’ DNA? Proc. Natl. Acad. Sci. USA. 2000;97:6248–6249. doi: 10.1073/pnas.97.12.6248. PubMed DOI PMC
Dechaud C, Volff JN, Schartl M, Naville M. Sex and the TEs: Transposable elements in sexual development and function in animals. Mob. DNA. 2019;10:42. doi: 10.1186/s13100-019-0185-0. PubMed DOI PMC
Hejníčková M, et al. Degenerated, undifferentiated, rearranged, lost: High variability of sex chromosomes in Geometridae (Lepidoptera) identified by sex chromatin. Cells. 2021;10:2230. doi: 10.3390/cells10092230. PubMed DOI PMC
Vítková M, Fuková I, Kubíčková S, Marec F. Molecular divergence of the W chromosomes in pyralid moths (Lepidoptera) Chromosome Res. 2007;15:917–930. doi: 10.1007/s10577-007-1173-7. PubMed DOI
Zrzavá M, et al. Sex chromosomes of the iconic moth Abraxas grossulariata (Lepidoptera, Geometridae) and its congener A. sylvata. Genes. 2018;9:279. doi: 10.3390/genes9060279. PubMed DOI PMC
Novák P, Neumann P, Pech J, Steinhaisl J, Macas J. RepeatExplorer: A galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics. 2013;29:792–793. doi: 10.1093/bioinformatics/btt054. PubMed DOI
Hejníčková M, et al. Absence of W chromosome in Psychidae moths and implications for the theory of sex chromosome evolution in Lepidoptera. Genes. 2019;10:1016. doi: 10.3390/genes10121016. PubMed DOI PMC
Winnepenninckx B, Backeljau T, De Wachter R. Extraction of high molecular weight DNA from molluscs. Trends Genet. 1993;9:407. doi: 10.1016/0168-9525(93)90102-N. PubMed DOI
Bolger AM, Lohse M, Usadel B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC
Andrews, S. FastQC.AQualityControlToolforHighThroughputSequenceData. (Babraham Bioinformatics, 2010).
Smit, A., Hubley, R. & Grenn, P. RepeatMaskerOpen-4.0.RepeatMaskerOpen-4.0.7. (2015).
Palomeque T, Muñoz-López M, Carrillo JA, Lorite P. Characterization and evolutionary dynamics of a complex family of satellite DNA in the leaf beetle Chrysolina carnifex (Coleoptera, Chrysomelidae) Chromosome Res. 2005;13:795–807. doi: 10.1007/s10577-005-1013-6. PubMed DOI
Montiel EE, Panzera F, Palomeque T, Lorite P, Pita S. Satellitome analysis of Rhodnius prolixus, one of the main chagas disease vector species. Int. J. Mol. Sci. 2021;22:6052. doi: 10.3390/ijms22116052. PubMed DOI PMC
Cabral-de-Mello DC, Marec F. Universal fluorescence in situ hybridization (FISH) protocol for mapping repetitive DNAs in insects and other arthropods. Mol. Genet. Genomics. 2021;296:513–526. doi: 10.1007/s00438-021-01765-2. PubMed DOI
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J. Mol. Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI
Maddison DR, Schulz KS, Maddison WP. The tree of life web project. Zootaxa. 2007;1668:19–40. doi: 10.11646/zootaxa.1668.1.4. DOI
Derks MFL, et al. The genome of winter moth (Operophtera brumata) provides a genomic perspective on sexual dimorphism and phenology. Genome Biol. Evol. 2015;7:2321–2332. doi: 10.1093/gbe/evv145. PubMed DOI PMC
Gregory TR, et al. Eukaryotic genome size databases. Nucleic Acids Res. 2007;35:D332–D338. doi: 10.1093/nar/gkl828. PubMed DOI PMC
Gage LP. The Bombyx mori genome: Analysis by DNA reassociation kinetics. Chromosoma. 1974;45:27–42. doi: 10.1007/BF00283828. PubMed DOI
Zhan S, Reppert SM. MonarchBase: The monarch butterfly genome database. Nucleic Acids Res. 2013;41:D758–763. doi: 10.1093/nar/gks1057. PubMed DOI PMC
Kawamoto M, et al. High-quality genome assembly of the silkworm, Bombyx mori. Insect Biochem. Mol. Biol. 2019;107:53–62. doi: 10.1016/j.ibmb.2019.02.002. PubMed DOI
Novák P, et al. Repeat-sequence turnover shifts fundamentally in species with large genomes. Nat. Plants. 2020;6:1325–1329. doi: 10.1038/s41477-020-00785-x. PubMed DOI
Gasparotto AE, et al. A step forward in the genome characterization of the sugarcane borer, Diatraea saccharalis: Karyotype analysis, sex chromosome system and repetitive DNAs through a cytogenomic approach. Chromosoma. 2022 doi: 10.1007/s00412-022-00781-4. PubMed DOI
Dechaud C, et al. Sex and the TEs: Transposable elements in sexual development and function in animals. Mob. DNA. 2019;10:42. doi: 10.1186/s13100-019-0185-0. PubMed DOI PMC
Schemberger MO, et al. DNA transposon invasion and microsatellite accumulation guide W chromosome differentiation in a Neotropical fish genome. Chromosoma. 2019;128:547–560. doi: 10.1007/s00412-019-00721-9. PubMed DOI
Srikulnath K, Ahmad SF, Singchat W, Panthum T. Do Ty3/Gypsy transposable elements play preferential roles in sex chromosome differentiation? Life. 2022;12:522. doi: 10.3390/life12040522. PubMed DOI PMC
Mawaribuchi S, et al. Sex chromosome differentiation and the W- and Z-specific loci in Xenopus laevis. Dev Biol. 2017;426:393–400. doi: 10.1016/j.ydbio.2016.06.015. PubMed DOI
Kudoh T, et al. Molecular insights into the non-recombining nature of the spinach male-determining region. Mol. Genet. Genomics. 2018;293:557–568. doi: 10.1007/s00438-017-1405-2. PubMed DOI
Na JK, Wang J, Ming R. Accumulation of interspersed and sex-specific repeats in the non-recombining region of papaya sex chromosomes. BMC Genomics. 2014;15:335. doi: 10.1186/1471-2164-15-335. PubMed DOI PMC
Conte MA, et al. Origin of a giant sex chromosome. Mol. Biol. Evol. 2021;38:1554–1569. doi: 10.1093/molbev/msaa319. PubMed DOI PMC
Tennessen JA, et al. Repeated translocation of a gene cassette drives sex-chromosome turnover in strawberries. PLoS Biol. 2018;16:e2006062. doi: 10.1371/journal.pbio.2006062. PubMed DOI PMC
Kabir A, et al. Repeated translocation of a supergene underlying rapid sex chromosome turnover in Takifugu pufferfish. Proc. Natl. Acad. Sci. 2022;119:e2121469119. doi: 10.1073/pnas.2121469119. PubMed DOI PMC
Martin A, et al. A transposon-induced epigenetic change leads to sex determination in melon. Nature. 2009;461:1135–1138. doi: 10.1038/nature08498. PubMed DOI
Bachtrog D. Sex chromosome evolution: Molecular aspects of Y-chromosome degeneration in Drosophila. Genome Res. 2005;15:1393–1401. doi: 10.1101/gr.3543605. PubMed DOI PMC
Bachtrog D. Y-chromosome evolution: Emerging insights into processes of Y-chromosome degeneration. Nat. Rev. Genet. 2013;14:113–124. doi: 10.1038/nrg3366. PubMed DOI PMC
Nokkala S. Cytological characteristics of chromosome behaviour during female meiosis in Sphinx ligustri L. (Sphingidae, Lepidoptera) Hereditas. 1987;106:69–179.
Traut W. A study of recombination, formation of chiasmata and synaptonemal complexes in female and male meiosis of Ephestia kuehniella (Lepidoptera) Genetica. 1977;47:135–142. doi: 10.1007/BF00120178. DOI
Marec F. Synaptonemal complexes in insects. Int. J. Insect Morphol. Embryol. 1996;25:205–233. doi: 10.1016/0020-7322(96)00009-8. DOI
Abe H, Fujii T, Shimada T, Mita K. Novel non-autonomous transposable elements on W chromosome of the silkworm, Bombyx mori. J. Genet. 2010;89:375–387. doi: 10.1007/s12041-010-0049-3. PubMed DOI
Macas J, Neumann P, Požárková D. Zaba: A novel miniature transposable element present in genomes of legume plants. Mol. Genet. Genomics. 2003;269:624–631. doi: 10.1007/s00438-003-0869-4. PubMed DOI