Dominance of transposable element-related satDNAs results in great complexity of “satDNA library” and invokes the extension towards “repetitive DNA library”

Monika Tunjić-Cvitanić, Daniel García-Souto, Juan J. Pasantes, Eva Šatović-Vukšić

Marine Life Science & Technology ›› 2024, Vol. 6 ›› Issue (2) : 236-251. DOI: 10.1007/s42995-024-00218-0
Research Paper

Dominance of transposable element-related satDNAs results in great complexity of “satDNA library” and invokes the extension towards “repetitive DNA library”

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Abstract

Research on bivalves is fast-growing, including genome-wide analyses and genome sequencing. Several characteristics qualify oysters as a valuable model to explore repetitive DNA sequences and their genome organization. Here we characterize the satellitomes of five species in the family Ostreidae (Crassostrea angulata, C. virginica, C. hongkongensis, C. ariakensis, Ostrea edulis), revealing a substantial number of satellite DNAs (satDNAs) per genome (ranging between 33 and 61) and peculiarities in the composition of their satellitomes. Numerous satDNAs were either associated to or derived from transposable elements, displaying a scarcity of transposable element-unrelated satDNAs in these genomes. Due to the non-conventional satellitome constitution and dominance of Helitron-associated satDNAs, comparative satellitomics demanded more in-depth analyses than standardly employed. Comparative analyses (including C. gigas, the first bivalve species with a defined satellitome) revealed that 13 satDNAs occur in all six oyster genomes, with Cg170/HindIII satDNA being the most abundant in all of them. Evaluating the “satDNA library model” highlighted the necessity to adjust this term when studying tandem repeat evolution in organisms with such satellitomes. When repetitive sequences with potential variation in the organizational form and repeat-type affiliation are examined across related species, the introduction of the terms “TE library” and “repetitive DNA library” becomes essential.

Keywords

Satellitome / Comparative satellitomics / Helitron / Bivalves / “Dark matter of the genome”

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Monika Tunjić-Cvitanić, Daniel García-Souto, Juan J. Pasantes, Eva Šatović-Vukšić. Dominance of transposable element-related satDNAs results in great complexity of “satDNA library” and invokes the extension towards “repetitive DNA library”. Marine Life Science & Technology, 2024, 6(2): 236‒251 https://doi.org/10.1007/s42995-024-00218-0

References

[1]
Athanasopoulou K, Boti MA, Adamopoulos PG, Skourou PC, Scorilas A. Third-generation sequencing: the spearhead towards the radical transformation of modern genomics. Life, 2022, 12: 30,
CrossRef Google scholar
[2]
Bao W, Kojima KK, Kohany O. Repbase update, a database of repetitive elements in eukaryotic genomes. Mob DNA, 2015, 6: 11,
CrossRef Google scholar
[3]
Belyayev A, Josefiová J, Jandová M, Mahelka V, Krak K, Mandák B. Transposons and satellite DNA: on the origin of the major satellite DNA family in the Chenopodium genome. Mob DNA, 2020, 11: 20,
CrossRef Google scholar
[4]
Biscotti MA, Barucca M, Capriglione T, Odierna G, Olmo E, Canapa A. Molecular and cytogenetic characterization of repetitive DNA in the Antarctic polyplacophoran Nuttallochiton mirandus. Chromosom Res, 2008, 16: 907-916,
CrossRef Google scholar
[5]
Biscotti MA, Olmo E, Heslop-Harrison JS. Repetitive DNA in eukaryotic genomes. Chromosom Res, 2015, 23: 415-420,
CrossRef Google scholar
[6]
Boštjančić LL, Bonassin L, Anušić L, Lovrenčić L, Besendorfer V, Maguire I, Grandjean F, Austin CM, Greve C, Hamadou AB, Mlinarec J. The Pontastacus leptodactylus (Astacidae) repeatome provides insight into genome evolution and reveals remarkable diversity of satellite DNA. Front Genet, 2021, 11,
CrossRef Google scholar
[7]
Bouilly K, Chaves R, Leitao A, Benabdelmouna A, Guedes-Pinto H. Chromosomal organization of simple sequence repeats in chromosome patterns. J Genet, 2008, 87: 119-125,
CrossRef Google scholar
[8]
Boutet I, Alves Monteiro HJ, Baudry L, Takeuchi T, Bonnivard E, Billoud B, Farhat S, Gonzales-Araya R, Salaun B, Andersen AC, Toullec JY, Lallier FH, Flot JF, Guiglielmoni N, Guo X, Li C, Allam B, Pales-Espinosa E, Hemmer-Hansen J, Moreau P, et al.. Chromosomal assembly of the flat oyster (Ostrea edulis L.) genome as a new genetic resource for aquaculture. Evol Appl, 2022, 15: 1730-1748,
CrossRef Google scholar
[9]
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: 1-15,
CrossRef Google scholar
[10]
Cabral-de-Mello DC, Mora P, Rico-Porras JM, Ferretti ABSM, Palomeque T, Lorite P. The spread of satellite DNAs in euchromatin and insights into the multiple sex chromosome evolution in Hemiptera revealed by repeatome analysis of the bug Oxycarenus hyalinipennis. Insect Mol Biol, 2023, 6: 725-737,
CrossRef Google scholar
[11]
Camacho JPM, Cabrero J, López-León MD, Martín-Peciña M, Perfectti F, Garrido-Ramos MA, Ruiz-Ruano FJ. Satellitome comparison of two oedipodine grasshoppers highlights the contingent nature of satellite DNA evolution. BMC Biol, 2022, 20: 36,
CrossRef Google scholar
[12]
Charlesworth B, Sniegowski P, Stephan W. The evolutionary dynamics of repetitive DNA in eukaryotes. Nature, 1994, 371: 215-220,
CrossRef Google scholar
[13]
Clabby C, Goswami U, Flavin F, Wilkins NP, Houghton JA, Powell R. Cloning, characterization and chromosomal location of a satellite DNA from the Pacific oyster, Crassostrea gigas. Gene, 1996, 168: 205-209,
CrossRef Google scholar
[14]
Cohen S, Agmon N, Sobol O, Segal D. Extrachromosomal circles of satellite repeats and 5S ribosomal DNA in human cells. Mob DNA, 2010, 1: 11,
CrossRef Google scholar
[15]
Dias GB, Svartman M, Delprat A, Ruiz A, Kuhn GCSS. Tetris is a foldback transposon that provided the building blocks for an emerging satellite DNA of Drosophila virilis. Genome Biol Evol, 2014, 6: 1302-1313,
CrossRef Google scholar
[16]
Dover GA. Molecular drive in multigene families: how biological novelties arise, spread and are assimilated. Trends Genet, 1986, 2: 159-165,
CrossRef Google scholar
[17]
Fry K, Salser W. Nucleotide sequences of HS-α satellite DNA from kangaroo rat Dipodomys ordii and characterization of similar sequences in other rodents. Cell, 1977, 12: 1069-1084,
CrossRef Google scholar
[18]
Gaffney PM, Pierce JC, Mackinley AG, Titchen DA, Glenn WK. Pearl, a novel family of putative transposable elements in bivalve mollusks. J Mol Evol, 2003, 56: 308-316,
CrossRef Google scholar
[19]
Garrido-Ramos MA. Satellite DNA: an evolving topic. Genes, 2017, 8: 230,
CrossRef Google scholar
[20]
Gomes-dos-Santos A, Lopes-Lima M, Castro LFC, Froufe E. Molluscan genomics: the road so far and the way forward. Hydrobiologia, 2020, 847: 1705-1726,
CrossRef Google scholar
[21]
Grabundzija I, Messing SA, Thomas J, Cosby RL, Bilic I, Miskey C, Gogol-Döring A, Kapitonov V, Diem T, Dalda A, Jurka J, Pritham EJ, Dyda F, Izsvák Z, Ivics Z. A Helitron transposon reconstructed from bats reveals a novel mechanism of genome shuffling in eukaryotes. Nat Commun, 2016, 7: 10716,
CrossRef Google scholar
[22]
Hartley G, O’Neill R. Centromere repeats: hidden gems of the genome. Genes, 2019, 10: 223,
CrossRef Google scholar
[23]
Hikosaka A, Kawahara A. Lineage-specific tandem repeats riding on a transposable element of MITE in Xenopus evolution: a new mechanism for creating simple sequence repeats. J Mol Evol, 2004, 59: 738-746,
CrossRef Google scholar
[24]
Hofstatter PG, Thangavel G, Lux T, Neumann P, Vondrak T, Novak P, Zhang M, Costa L, Castellani M, Scott A, Toegelová H, Fuchs J, Mata-Sucre Y, Dias Y, Vanzela ALL, Huettel B, Almeida CCS, Šimková H, Souza G, Pedrosa-Harand A, et al.. Repeat-based holocentromeres influence genome architecture and karyotype evolution. Cell, 2022, 185: 3153-3168.e18,
CrossRef Google scholar
[25]
Jurka J, Kapitonov VV, Kohany O, Jurka MV. Repetitive sequences in complex genomes: structure and evolution. Annu Rev Genom Hum Genet, 2007, 8: 241-259,
CrossRef Google scholar
[26]
Kojima KK. Structural and sequence diversity of eukaryotic transposable elements. Genes Genet Syst, 2019, 94: 233-252,
CrossRef Google scholar
[27]
Kourtidis A, Drosopoulou E, Pantzartzi CN, Chintiroglou CC, Scouras ZG. Three new satellite sequences and a mobile element found inside HSP70 introns of the Mediterranean mussel (Mytilus galloprovincialis). Genome, 2006, 49: 1451-1458,
CrossRef Google scholar
[28]
Kuhn GCS, Heringer P, Dias GB. Ugarković Đ. Structure, organization, and evolution of satellite DNAs: insights from the Drosophila repleta and D. virilis species groups. Satellite DNAs in physiology and evolution, 2021 1 Cham Springer 27-56,
CrossRef Google scholar
[01]
Kumar S, Suleski M, Craig JM, Kasprowicz AE, Sanderford M, Li M, Stecher G, Hedges SB. TimeTree 5: an expanded resource for species divergence times. Mol Biol Evol, 2022, 39: 1-6,
CrossRef Google scholar
[29]
Langdon T, Seago C, Mende M, Leggett M, Thomas H, Forster JW, Jones RN, Jenkins G. Retrotransposon evolution in diverse plant genomes. Genetics, 2000, 156: 313-325,
CrossRef Google scholar
[30]
Li Y, Nong W, Baril T, Yip HY, Swale T, Hayward A, Ferrier DEK, Hui JHL. Reconstruction of ancient homeobox gene linkages inferred from a new high-quality assembly of the Hong Kong oyster (Magallana hongkongensis) genome. BMC Genom, 2020, 21: 1-17,
CrossRef Google scholar
[31]
Li C, Kou Q, Zhang Z, Hu L, Huang W, Cui Z, Liu Y, Ma P, Wang H. Reconstruction of the evolutionary biogeography reveal the origins and diversification of oysters (Bivalvia: Ostreidae). Mol Phylogenet Evol, 2021, 164,
CrossRef Google scholar
[32]
López-Flores I, Garrido-Ramos MA. Garrido-Ramos MA. The repetitive DNA content of eukaryotic genomes. Genome dynamics, 2012 1 Basel Karger 1-28
[33]
López-Flores I, de la Herrán R, Garrido-Ramos MA, Boudry P, Ruiz-Rejón C, Ruiz-Rejón M. The molecular phylogeny of oysters based on a satellite DNA related to transposons. Gene, 2004, 339: 181-188,
CrossRef Google scholar
[34]
Lower SS, McGurk MP, Clark AG, Barbash DA. Satellite DNA evolution: old ideas, new approaches. Curr Opin Genet Dev, 2018, 49: 70-78,
CrossRef Google scholar
[35]
Luchetti A. TerMITEs: miniature inverted-repeat transposable elements (MITEs) in the termite genome (Blattodea: Termitoidae). Mol Genet Genom, 2015, 290: 1499-1509,
CrossRef Google scholar
[36]
Macas J, Koblízková A, Navrátilová A, Neumann P. Hypervariable 3’ UTR region of plant LTR-retrotransposons as a source of novel satellite repeats. Gene, 2009, 448: 198-206,
CrossRef Google scholar
[02]
Martínez-Expósito MJ, Pasantes JJ, Méndez J. NOR activity in larval and juvenile mussels (Mytilus galloprovincialis Lmk.). J Exp Mar Bio Ecol, 1994, 175: 155-165,
CrossRef Google scholar
[37]
Mascagni F, Barghini E, Ceccarelli M, Baldoni L, Trapero C, Díez CM, Natali L, Cavallini A, Giordani T. The singular evolution of Olea genome structure. Front Plant Sci, 2022, 13,
CrossRef Google scholar
[38]
McGurk MP, Barbash DA. Double insertion of transposable elements provides a substrate for the evolution of satellite DNA. Genome Res, 2018, 28: 714-725,
CrossRef Google scholar
[39]
Negm S, Greenberg A, Larracuente AM, Sproul JS. RepeatProfiler: a pipeline for visualization and comparative analysis of repetitive DNA profiles. Mol Ecol Resour, 2021, 21: 969-981,
CrossRef Google scholar
[40]
Novák P, Neumann P. Global analysis of repetitive DNA from unassembled sequence reads using RepeatExplorer2. Nat Protoc, 2020, 15: 3745-3776,
CrossRef Google scholar
[41]
Novák P, Neumann P, Macas J. Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinform, 2010, 11: 378,
CrossRef Google scholar
[42]
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,
CrossRef Google scholar
[43]
Novák P, Robledillo , Koblížková A, Vrbová I, Neumann P, Macas J. TAREAN: a computational tool for identification and characterization of satellite DNA from unassembled short reads. Nucl Acids Res, 2017, 45,
CrossRef Google scholar
[44]
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, 2019, 10: 1014,
CrossRef Google scholar
[45]
Palomeque T, Carrillo JA, Muñoz-López M, Lorite P. Detection of a mariner-like element and a miniature inverted-repeat transposable element (MITE) associated with the heterochromatin from ants of the genus Messor and their possible involvement for satellite DNA evolution. Gene, 2006, 371: 194-205,
CrossRef Google scholar
[46]
Peñaloza C, Gutierrez AP, Eory L, Wang S, Guo X, Archibald AL, Bean TP, Houston RD. A chromosome-level genome assembly for the Pacific oyster (Crassostrea gigas). Gigascience, 2021, 10: 1-9,
CrossRef Google scholar
[47]
Pérez-García C, Morán P, Pasantes JJ. Cytogenetic characterization of the invasive mussel species Xenostrobus securis Lmk. (Bivalvia: Mytilidae). Genome, 2011, 54: 771-778,
CrossRef Google scholar
[48]
Petraccioli A, Odierna G, Capriglione T, Barucca M, Forconi M, Olmo E, Biscotti MA. A novel satellite DNA isolated in Pecten jacobaeus shows high sequence similarity among molluscs. Mol Genet Genomics, 2015, 290: 1717-1725,
CrossRef Google scholar
[49]
Pita S, Panzera F, Mora P, Vela J, Cuadrado Á, Sánchez A, Palomeque T, Lorite P. Comparative repeatome analysis on Triatoma infestans Andean and Non-Andean lineages, main vector of Chagas disease. PLoS ONE, 2017, 12,
CrossRef Google scholar
[50]
Plohl M, Luchetti A, Mestrović N, Mantovani B. Satellite DNAs between selfishness and functionality: structure, genomics and evolution of tandem repeats in centromeric (hetero)chromatin. Gene, 2008, 409: 72-82,
CrossRef Google scholar
[51]
Plohl M, Petrović V, Luchetti A, Ricci A, Šatović E, Passamonti M, Mantovani B. Long-term conservation vs high sequence divergence: the case of an extraordinarily old satellite DNA in bivalve mollusks. Heredity, 2010, 104: 543-551,
CrossRef Google scholar
[52]
Plohl M, Meštrović N, Mravinac B. Garrido-Ramos MA. Satellite DNA evolution. Genome dynamics, 2012 1 Basel Karger 126-152
[53]
Robledo JAF, Yadavalli R, Allam B, Pales-Espinosa E, Gerdol M, Greco S, Stevick RJ, Gómez-Chiarri M, Zhang Y, Heil CA, Tracy AN, Bishop-Bailey D, Metzger MJ. From the raw bar to the bench: bivalves as models for human health. Dev Comp Immunol, 2018, 92: 260-282,
CrossRef Google scholar
[54]
Ruiz-Ruano FJ, López-León MD, Cabrero J, Camacho JPM. High-throughput analysis of the satellitome illuminates satellite DNA evolution. Sci Rep, 2016, 6: 28333,
CrossRef Google scholar
[55]
Šatović E, Plohl M. Tandem repeat-containing MITE elements in the clam Donax trunculus. Genome Biol Evol, 2013, 5: 2549-2559,
CrossRef Google scholar
[56]
Šatović E, Plohl M. Distribution of DTHS3 satellite DNA across 12 bivalve species. J Genet, 2018, 97: 575-580,
CrossRef Google scholar
[57]
Šatović E, Vojvoda Zeljko T, Luchetti A, Mantovani B, Plohl M. Adjacent sequences disclose potential for intra-genomic dispersal of satellite DNA repeats and suggest a complex network with transposable elements. BMC Genom, 2016, 17: 997,
CrossRef Google scholar
[58]
Šatović E, Vojvoda Zeljko T, Plohl M. Characteristics and evolution of satellite DNA sequences in bivalve mollusks. Eur Zool J, 2018, 85: 95-104,
CrossRef Google scholar
[59]
Šatović E, Tunjić Cvitanić M, Plohl M. Tools and databases for solving problems in detection and identification of repetitive DNA sequences. Period Biol, 2020, 121–122: 7-14,
CrossRef Google scholar
[60]
Šatović Vukšić E, Plohl M. Ugarković Đ. Exploring satellite DNAs: specificities of bivalve mollusks genomes. Satellite DNAs in physiology and evolution, 2021 1 Cham Springer 57-83,
CrossRef Google scholar
[61]
Šatović-Vukšić E, Plohl M. Classification problems of repetitive DNA sequences. DNA, 2021, 1: 84-90,
CrossRef Google scholar
[62]
Šatović-Vukšić E, Plohl M. Satellite DNAs—from localized to highly dispersed genome components. Genes, 2023, 14: 742,
CrossRef Google scholar
[63]
Scalvenzi T, Pollet N. Insights on genome size evolution from a miniature inverted repeat transposon driving a satellite DNA. Mol Phylogenet Evol, 2014, 81: 1-9,
CrossRef Google scholar
[64]
Schmidt T, Heslop-Harrison JS. Genomes, genes and junk: the large-scale organization of plant chromosomes. Trends Plant Sci, 1998, 3: 195-199,
CrossRef Google scholar
[65]
Sedlazeck FJ, Lee H, Darby CA, Schatz MC. Piercing the dark matter: bioinformatics of long-range sequencing and mapping. Nat Rev Genet, 2018, 19: 329-346,
CrossRef Google scholar
[66]
Sharma A, Wolfgruber TK, Presting GG. Tandem repeats derived from centromeric retrotransposons. BMC Genom, 2013, 14: 142,
CrossRef Google scholar
[67]
Suárez-Ulloa V, Fernández-Tajes J, Manfrin C, Gerdol M, Venier P, Eirín-López JM. Bivalve omics: state of the art and potential applications for the biomonitoring of harmful marine compounds. Mar Drugs, 2013, 11: 4370-4389,
CrossRef Google scholar
[68]
Tek AL, Song J, Macas J, Jiang J. Sobo, a recently amplified satellite repeat of potato, and its implications for the origin of tandemly repeated sequences. Genetics, 2005, 170: 1231-1238,
CrossRef Google scholar
[69]
Thakur J, Packiaraj J, Henikoff S. Sequence, chromatin and evolution of satellite DNA. Int J Mol Sci, 2021, 22: 4309,
CrossRef Google scholar
[70]
Thomas J, Pritham EJ. Helitrons, the eukaryotic rolling-circle transposable elements. Microbiol Spectr, 2015, 3: 891-924,
CrossRef Google scholar
[71]
Tunjić Cvitanić M, Vojvoda Zeljko T, Pasantes JJ, García-Souto D, Gržan T, Despot-Slade E, Plohl M, Šatović E. Sequence composition underlying centromeric and heterochromatic genome compartments of the Pacific oyster Crassostrea gigas. Genes, 2020, 11: 695,
CrossRef Google scholar
[72]
Tunjić-Cvitanić M, Pasantes JJ, García-Souto D, Cvitanić T, Plohl M, Šatović-Vukšić E. Satellitome analysis of the Pacific oyster Crassostrea gigas reveals new pattern of satellite DNA organization, highly scattered across the genome. Int J Mol Sci, 2021, 22: 6798,
CrossRef Google scholar
[73]
Vojvoda Zeljko T, Pavlek M, Meštrović N, Plohl M. Satellite DNA - like repeats are dispersed throughout the genome of the Pacific oyster Crassostrea gigas carried by Helentron non-autonomous mobile elements. Sci Rep, 2020, 10: 15107,
CrossRef Google scholar
[74]
Vondrak T, Robledillo ÁL, Novák P, Koblížková A, Neumann P, Macas J. Characterization of repeat arrays in ultra-long nanopore reads reveals frequent origin of satellite DNA from retrotransposon-derived tandem repeats. Plant J, 2020, 101: 484-500,
CrossRef Google scholar
[75]
Xiong W, Dooner HK, Du C. Rolling-circle amplification of centromeric Helitrons in plant genomes. Plant J, 2016, 88: 1038-1045,
CrossRef Google scholar
[76]
Zattera ML, Bruschi DP. Transposable elements as a source of novel repetitive DNA in the eukaryote genome. Cells, 2022, 11: 1-17,
CrossRef Google scholar
[77]
Zhang G, Fang X, Guo X, Li L, Luo R, Xu F, Yang P, Zhang L, Wang X, Qi H, Xiong Z, Que H, Xie Y, Holland PWH, Paps J, Zhu Y, Wu F, Chen Y, Wang J, Peng C, et al.. The oyster genome reveals stress adaptation and complexity of shell formation. Nature, 2012, 490: 49-54,
CrossRef Google scholar

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