Retrotransposon mapping in spider monkey genomes of the family Atelidae (Platyrrhini, Primates) shows a high level of LINE-1 amplification
Abstract
To investigate the distribution of LINE-1 repeat sequences, a LINE-1 probe was Fluorescence In Situ Hybridized (FISH) on the chromosomes of Ateles geoffroyi and Ateles fusciceps (Atelidae); a LINE-1 probe was also mapped on Cebuella pygmaea (Cebidae) and used as an outgroup for phylogenetic comparison. Ateles spider monkeys have a highly rearranged genome and are an ideal model for testing whether LINE-1 is involved in genome evolution. The LINE-1 probe has been mapped in the two Atelidae species for the first time, revealing a high accumulation of LINE-1 sequences along chromosomal arms, including telomeres, and a scarcity of LINE-1 signals at centromere positions. LINE-1 mapping in C. pygmaea (Cebidae) revealed signals at centromere positions and along chromosome arms, which was consistent with previous published data from other Cebidae species. In a broader sense, the results were analyzed in light of published data on whole-chromosomal human probes mapped in these genomes. This analysis allows us to speculate about the presence of LINE-1 sequences at the junction of human chromosomal syntenies, as well as a possible link between these sequences and chromosomal rearrangements.
References
- Ahmad SF, Singchat W, Jehangir M, et al. Dark matter of primate genomes: Satellite DNA repeats and their evolutionary dynamics. Cells 2020:9:2714.
- Mazzoleni S, Rovatsos M, Schillaci O, Dumas F. Evolutionary insight on localization of 18S, 28S rDNA genes on homologous chromosomes in primates genomes. Comp Cytogenet 2018;12:27–40.
- Mazzoleni S, Schillaci O, Sineo L, Dumas F. Distribution of interstitial telomeric sequences in primates and the pygmy tree shrew (Scandentia). Cytogenet Genome Res 2017;151:141–50.
- Ceraulo S, Perelman PL, Mazzoleni S, et al. Repetitive sequence distribution on Saguinus, Leontocebus and Leontopithecus Tamarins (Platyrrhine, Primates) by mapping telomeric (TTAGGG) motifs and rDNA loci. Biology 2021;10:844.
- Böhne A, Brunet F, Galiana-Arnoux D, et al. Transposable elements as drivers of genomic and biological diversity in vertebrates. Chromosome Res 2008;16:203–15.
- Paço A, Adega F, Chaves R. Line-1 retrotransposons: From “parasite” sequences to functional elements. J Appl Genet 2015;56:133–45.
- 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 2016;10:1014.
- Gray YH. It takes two transposons to tango: transposable element-mediated chromosomal rearrangements. Trends Genet 2000;16:461–68.
- Bulazel KV, Ferreri GC, Eldridge MD, O'Neill RJ. Species specific shifts in centromere sequence composition are coincident with breakpoint reuse in karyotypically divergent lineages. Genome Biol 2007;8:1.
- Belyayev A. Bursts of transposable elements as an evolutionary driving force. J Evol Biol 2014;27:2573–84.
- Boissinot S, Furano AV. Adaptive evolution in LINE-1 retrotransposons. Mol Biol Evol 2001;18:2186–94.
- Klein SJ, O’Neill RJ. Transposable elements: genome innovation, chromosome diversity, and centromere conflict. Chromosome Res 2018;26:5-23.
- Richardson SR, Doucet AJ, Kopera HC, et al. The influence of LINE-1 and SINE retrotransposons on mammalian genomes. Microbiol Spectr 2015;3:1165–208.
- Ovchinnikov I, Rubin A, Swergold GD. Tracing the LINEs of human evolution. Proc Natl Acad Sci USA 2002;6;99:10522-7.
- Tang W, Mun S, Joshi A, et al. Mobile elements contribute to the uniqueness of human genome with 15,000 human-specific insertions and 14 Mbp sequence increase. DNA Res 2018;25:521-33.
- Mathews LM, Chi SY, Greenberg N, et al. Large differences between LINE-1 amplification rates in the human and chimpanzee lineages. Am J Hum Genet 2003;72:739-48.
- Kim YJ, Han K. Endogenous retrovirus-mediated genomic variations in chimpanzees. Mob Genet Elements 2015;4:1–4.
- Seuánez HN, Forman L, Matayoshi T, Fanning TG. The Callimico goeldii (Primates, Platyrrhini) genome: karyology and middle repetitive (LINE- 1) DNA sequences. Chromosoma 1989;98:389–95.
- Boissinot S, Roos C, Furano AV. Different rates of LINE-1 (L1) retrotransposon amplification and evolution in New World monkeys. J Mol Evol 2004;58:122-30.
- Sookdeo A, Ruiz-García M, Schneider H, Boissinot S. Contrasting rates of LINE-1 amplification among New World Primates of the Atelidae family. Cytogenetic Genome Res 2018;154:217-28.
- Tang W, Liang P. Comparative genomics analysis reveals high levels of differential retrotransposition among primates from the hominidae and the cercopithecidae families. Genome Biol Evol 2019;11:3309–25.
- Lee S, Tang W, Liang P, Han K. A comprehensive analysis of chimpanzee (Pan troglodytes)-specific LINE-1 retrotransposons. Gene 2019;693:46-51.
- Jeon S, Kim S, Oh MH, et al. A comprehensive analysis of gorilla-specific LINE-1 retrotransposons. Genes & Genomics 2021;43:1133-41.
- Waters PD, Dobigny G, Pardini AT, Robinson TJ. LINE-1 distribution in Afrotheria and Xenarthra: implications for understanding the evolution of LINE-1 in eutherian genomes. Chromosoma 2004;113:137–44.
- Ovchinnikov I, Troxel AB, Swergold GD. Genomic characterization of recent human LINE-1 insertions: evidence supporting random insertion. Genome Res 2001;11:2050–58.
- Parish D, Vise P, Wichman H, et al. Distribution of LINEs and other repetitive elements in the karyotype of the bat Carollia: implications for X-chromosome inactivation. Cytogenet Genome Res 2002;96:191–97.
- Kapitonov VV, Holmquist GP, Jurka J. L1 repeat is a basic unit of heterochromatin satellites in cetaceans. Mol Biol Evol 1998;15:611–12.
- Acosta MJ, Marchal JA, Fernández-Espartero CH. Retroelements (LINEs and SINEs) in vole genomes: differential distribution in the constitutive heterochromatin. Chromosome Res 2008;16:949–59.
- Bulazel K, Metcalfe C, Ferreri GC, et al. Cytogenetic and molecular evaluation of centromere-associated DNA sequences from a marsupial (Macropodidae: Macropus rufogriseus) X chromosome. Genetics 2006;172:1129–37.
- Carbone L, Harris RA, Mootnick AR, et al. Centromere remodelling in Hoolock leuconedys (Hylobatidae) by a new transposable element unique to the gibbons. Genome Biol Evol 2012;4:760–70.
- De Sotero-Caio CG, Cabral-de-Mello DC, da Silva Calixto M, et al. Centromeric enrichment of LINE-1 retrotransposons and its significance for the chromosome evolution of Phyllostomid bats. Chromosome Res 2017;25:313-25.
- Rebuzzini P, Castiglia R, Nergadze SG, et al. Quantitative variation of LINE-1 sequences in five species and three subspecies of the subgenus Mus and in five Robertsonian races of Mus musculus domesticus. Chromosome Res 2009;17:65–76.
- Perelman P, Johnson WE, Roos C, et al. A molecular phylogeny of living primates. PLoS Genetics 2011;73:e1001342.
- Dumas F, Sineo L. The evolution of human synteny 4 by mapping sub-chromosomal specific probes in Primates. Caryologia 2014;67:281–91.
- Dumas F, Sineo L, Ishida T. Taxonomic identification of Aotus (Platyrrhinae) through cytogenetics. [Identificazione tassonomica di Aotus (Platyrrhinae) mediante la citogenetica.] J Biol Res 2015;88:65-6.
- Serfaty DMB, Carvalho NDM, Gross MC, et al.Differential chromosomal organisation between Saguinus midas and Saguinus bicolor with accumulation of differences in the repetitive sequence DNA. Genetica 2017;145:359-69.
- Ceraulo S, Perelman PL, Dumas F. Massive LINE-1 retrotransposon enrichment in tamarins of the Cebidae family (Platyrrhini, Primates) and its significance for genome evolution. J Zoolog System Evolut Res 2021;59:2553–61.
- Milioto V, Perelman PL, La Paglia L, et al. Mapping retrotransposonLINE-1 sequences into two cebidae species and Homo sapiens genomes and a short review on primates. Genes 2022;13:1742.
- Ceraulo S, Milioto V, Dumas F. Centromeric enrichment of LINE-1 retrotransposon in two species of South American monkeys Alouatta belzebul and Ateles nancymaae (Platyrrhini, Primates). Caryologia 2021;74:111-19.
- Neusser M, Stanyon R, Bigoni F, et al. Molecular cytotaxonomy of New World monkeys (Platyrrhini) – comparative analysis of five species by multi-color chromosome painting gives evidence for a classification of Callimico goeldii within the family of Callitrichidae. Cytogenet Cell Genet 2001;94:206–15.
- Morescalchi MA, Schempp W, Wienberg J, Stanyon R. Chromosome painting in the New World monkey, Ateles geoffroyi, the black-handed spider monkey. Chromosome Res 1997;5:527–36.
- Garcia F, Ruiz-Herrera A, Egozcue J, et al. Chromosomal homologies between Cebus and Ateles (Primates) based on ZOO-FISH and G-banding comparisons. Am J Primatol 2002;57:177-88.
- De Oliveira EHC, Neusser DM, Pieczarka JC, et al. Phylogenetic inferences of Atelinae (Platyrrhini) based on multi-directional chromosome painting in Brachyteles arachnoides, Ateles paniscus paniscus and Ateles b. marginatus. Cytog Genome Res 2005;108:183-90.
- Nagamachi CY, Pieczarka JC, de Souza Barros RM. Karyotypic comparison among Cebuella pygmaea, Callithrix jacchus and C. emiliae (Callitrichidae, Primates) and its taxonomic implications. Genetica 1992;85:249-57.
- Fernàndez R, Barragàn M, Bullejos M, et al. New C-band protocol by heat denaturation in the presence of formamide. Hereditas 2002;137:145-8.
- Nieves M, Ascunce MS, Rahn MI, Mudry MD. Phylogenetic relationships among some Ateles species: the use of chromosomal and molecular characters. Primates 2005;46:155-64.
- Fantini L, Jeffery NW, Pierossi P, et al. Qualitative and quantitative analysis of the genomes and chromosomes of spider monkeys (Primates: Atelidae). Biol J Linnean Soc 2016;118:752-62.
- Medeiros MA, Barros RMS, Pieczarka JC, et al. Radiation and speciation of spider monkeys, genus Ateles, from the cytogenetic viewpoint. Am J Primatol 1997;42:167-78.
- Scardino R, Milioto V, Proskuryakova AA, et al. Evolution of the human chromosome 13 synteny: Evolutionary rearrangements, plasticity, human disease genes and cancer breakpoints. Genes 2020;11:383.
- Scardino R, Mazzoleni S, Rovatsos M, et al. Molecular cytogenetic characterization of the sicilian endemic pond turtle Emys trinacris and the yellow-bellied slider Trachemys scripta scripta (Testudines, Emydidae). Genes 2020;11:702.
- Milioto V, Vlah S, Mazzoleni S, et al. Chromosomal localization of 18S-28S rDNA and (TTAGGG)n Sequences in two south african dormice of the genus Graphiurus (Rodentia: Gliridae). Cytogenet Genome Res 2019;158:145-51.
- Lemskaya NA, Kulemzina AI, Beklemisheva VR, et al. A combined banding method that allows the reliable identification of chromosomes as well as differentiation of AT-and GC-rich heterochromatin. Chromosome Res 2018;26:307-15.
- Dumas F, Mazzoleni S. Neotropical primate evolution and phylogenetic reconstruction using chromosomal data. Eur Zool J 2017;84:1-18.
- Cellamare A, Catacchio CR, Alkan C, et al. New insights into centromere organization and evolution from the white-cheeked gibbon and marmoset. Molec Biol Evol 2009;26:1889-900.
- Logsdon GA, Vollger MR, Hsieh P, et al. The structure, function and evolution of a complete human chromosome 8. Nature 2021;593:101-7.
- Nurk S, Koren S, Rhie A, et al.The complete sequence of a human genome. Science 2022;376:44-53.
Metrics
Citations and online attention from Dimensions, Altmetric and PlumX.
License
Copyright (c) 2022 the Authors

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
PAGEPress has chosen to apply the Creative Commons Attribution NonCommercial 4.0 International License (CC BY-NC 4.0) to all manuscripts to be published.