Characterization of Satellite DNAs in Squirrel Monkeys genus Saimiri (Cebidae, Platyrrhini).
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
08 05 2020
08 05 2020
Historique:
received:
03
12
2019
accepted:
15
04
2020
entrez:
10
5
2020
pubmed:
10
5
2020
medline:
10
5
2020
Statut:
epublish
Résumé
The genus Saimiri is a decades-long taxonomic and phylogenetic puzzle to which cytogenetics has contributed crucial data. All Saimiri species apparently have a diploid number of 2n = 44 but vary in the number of chromosome arms. Repetitive sequences such as satellite DNAs are potentially informative cytogenetic markers because they display high evolutionary rates. Our goal is to increase the pertinent karyological data by more fully characterizing satellite DNA sequences in the Saimiri genus. We were able to identify two abundant satellite DNAs, alpha (~340 bp) and CapA (~1,500 bp), from short-read clustering of sequencing datasets from S. boliviensis. The alpha sequences comprise about 1% and the CapA 2.2% of the S. boliviensis genome. We also mapped both satellite DNAs in S. boliviensis, S. sciureus, S. vanzolinii, and S. ustus. The alpha has high interspecific repeat homogeneity and was mapped to the centromeres of all analyzed species. CapA is associated with non-pericentromeric heterochromatin and its distribution varies among Saimiri species. We conclude that CapA genomic distribution and its pervasiveness across Platyrrhini makes it an attractive cytogenetic marker for Saimiri and other New World monkeys.
Identifiants
pubmed: 32385398
doi: 10.1038/s41598-020-64620-1
pii: 10.1038/s41598-020-64620-1
pmc: PMC7210261
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
7783Commentaires et corrections
Type : ErratumIn
Références
Lavergne, A. et al. Phylogeny and phylogeography of squirrel monkeys (genus Saimiri) based on cytochrome b genetic analysis. Am. J. Primatol. 72, 242–253 (2010).
pubmed: 19937739
Chiou, K. L., Pozzi, L., Lynch Alfaro, J. W. & Di Fiore, A. Pleistocene diversification of living squirrel monkeys (Saimiri spp.) inferred from complete mitochondrial genome sequences. Mol. Phylogenet. Evol. 59, 736–745 (2011).
pubmed: 21443955
Lynch Alfaro, J. W. et al. Biogeography of squirrel monkeys (genus Saimiri): South-central Amazon origin and rapid pan-Amazonian diversification of a lowland primate. Mol. Phylogenet. Evol. 82, 436–454 (2015).
pubmed: 25305518
Hershkovitz, P. Taxonomy of squirrel monkeys genus Saimiri (Cebidae, Platyrrhini): A preliminary report with description of a hitherto unnamed form. Am. J. Primatol. 7, 155–210 (1984).
Hershkovitz, P. Uacaries, New World monkeys of the genus Cacajao (Cebidae, Platyrrhini): A preliminary taxonomic review with the description of a new subspecies. Am. J. Primatol. 12, 1–53 (1987).
pubmed: 31973512
Thorington, R. W. The taxonomy and distribution of squirrel monkeys (Saimiri) in Handbook of squirrel monkey research (ed. Rosenblum, L. A. & Coe, C. L.) 1–33 (Springer, 1985).
Costello, R. K., Dickinson, C., Rosenberger, A. L., Boinski, S. & Szalay, F. S. Squirrel monkey (genus Saimiri) taxonomy in Species, species concepts and primate evolution (ed. Kimbel, W. H.& Martin, L. B.) 177–210 (Springer, 1993).
Cropp, S. & Boinski, S. The Central American squirrel monkey (Saimiri oerstedii): Introduced hybrid or endemic species? Mol. Phylogenet. Evol. 16, 350–365 (2000).
pubmed: 10991789
Boinski, S. & Cropp, S. J. Disparate data sets resolve squirrel monkey (Saimiri) taxonomy: Implications for behavioral ecology and biomedical usage. Int. J. Primatol. 20, 237–256 (1999).
Groves C., Wilson D.E. & Reeder D.A.M. Order Primates in Mammal species of the world: a taxonomic and geographic reference (ed. Wilson, D. & Reeder, D.) 111–184 (The Johns Hopkins University Press, 2005).
Rylands, A. B., Mittermeier, R.A., Bezerra, B. M., Paim, F. P. & Queiroz, H. L. Family Cebidae (squirrel monkeys and capuchins) in Handbook of the mammals of the world,volume 3. Primates (ed. Mittermeier, R. A., Rylands, A. B. & Wilson, D. E.) 348–413 (Lynx Edicions, 2013).
Chiatante, G. et al. Centromere repositioning explains fundamental number variability in the New World monkey genus Saimiri. Chromosoma 126, 519–529 (2017).
pubmed: 27834006
Jones, T. C., Thorington, R. W., Hu, M. M., Adams, E. & Cooper, R. W. Karyotypes of squirrel monkeys (Saimiri sciureus) from different geographic regions. Am. J. Phys. Anthropol. 38, 269–277 (1973).
pubmed: 4632076
Ma, N. S. & Jones, T. C. Added heterochromatin segments in chromosomes of squirrel monkeys (Saimiri sciureus). Folia Primatol. (Basel) 24, 282–292 (1975).
Lau, Y. F. & Arrighi, F. E. Studies of the squirrel monkey, Saimiri sciureus, genome. Cytological characterizations of chromosomal heterozygosity. Cytogenet. Genome Res. 17, 51–60 (1976).
Cambefort, Y. & Moro, F. Cytogenetics and taxonomy of some South Bolivian monkeys. Folia Primatol. (Basel) 29, 307–314 (1978).
Fanning, T. G., Seuánez, H. N. & Forman, L. Satellite DNA sequences in the New World primate Cebus apella (Platyrrhini, Primates). Chromosoma 102, 306–311 (1993).
pubmed: 8325162
Alkan, C. et al. Organization and evolution of primate centromeric DNA from whole-genome shotgun sequence data. PLoS Comput. Biol. 3, 1807–1818 (2007).
pubmed: 17907796
Prakhongcheep, O. et al. Two types of alpha satellite DNA in distinct chromosomal locations in Azara’s owl monkey. DNA Res. 20, 235–240 (2013).
pubmed: 23477842
pmcid: 3686428
Plohl, M., Meštrović, N. & Mravinac, B. Satellite DNA evolution in Repetitive DNA (ed. Schmid, M.) 126–152 (Karger, 2012).
Dover, G. Molecular drive: A cohesive mode of species evolution. Nature 299, 111–117 (1982).
pubmed: 7110332
Kuhn, G. C. S., Sene, F. M., Moreira-Filho, O., Schwarzacher, T. & Heslop-Harrison, J. S. Sequence analysis, chromosomal distribution and long-range organization show that rapid turnover of new and old pBuM satellite DNA repeats leads to different patterns of variation in seven species of the Drosophila buzzatii cluster. Chromosom. Res. 16, 307–324 (2008).
Bachmann, L., Schibel, J. M., Raab, M. & Sperlich, D. Satellite DNA as a taxonomic marker. Biochem. Syst. Ecol. 21, 3–11 (1993).
Baicharoen, S. et al. Locational diversity of alpha satellite DNA and intergeneric hybridization aspects in the Nomascus and Hylobates genera of small apes. PLoS One 9, e109151, https://doi.org/10.1371/journal.pone.0109151 (2014).
doi: 10.1371/journal.pone.0109151
pubmed: 25290445
pmcid: 4188616
Picariello, O., Feliciello, I., Bellinello, R. & Chinali, G. S1 satellite DNA as a taxonomic marker in brown frogs: Molecular evidence that Rana graeca graeca and Rana graeca italica are different species. Genome 45, 63–70 (2002).
pubmed: 11908670
Garrido-Ramos, M. A. et al. Evolution of centromeric satellite DNA and its use in phylogenetic studies of the Sparidae family (Pisces, Perciformes). Mol. Phylogenet. Evol. 12, 200–204 (1999).
pubmed: 10381322
Kirov, I. V., Kiseleva, A. V., Van Laere, K., Van Roy, N. & Khrustaleva, L. I. Tandem repeats of Allium fistulosum associated with major chromosomal landmarks. Mol. Genet. Genomics 292, 453–464 (2017).
pubmed: 28150039
Alves, G., Seuánez, H. N. & Fanning, T. Alpha satellite DNA in neotropical primates (Platyrrhini). Chromosoma 103, 262–267 (1994).
pubmed: 7988287
Cellamare, A. et al. New insights into centromere organization and evolution from the white-cheeked gibbon and marmoset. Mol. Biol. Evol. 26, 1889–1900 (2009).
pubmed: 19429672
pmcid: 2734153
Malfoy, B. et al. Nucleotide sequence of an heterochromatic segment recognized by the antibodies to Z-DNA in fixed metaphase chromosomes. Nucleic Acids Res. 14, 3197–3214 (1986).
pubmed: 3010230
pmcid: 339742
Valeri, M. P., Dias, G. B., Pereira, V. D. S., Kuhn, G. C. S. & Svartman, M. An eutherian intronic sequence gave rise to a major satellite DNA in Platyrrhini. Biol. Lett. 14, 20170686, https://doi.org/10.1098/rsbl.2017.0686 (2018).
doi: 10.1098/rsbl.2017.0686
pubmed: 29386361
pmcid: 5803596
Stanyon, R. et al. Fluorescence in situ hybridization (FISH) maps chromosomal homologies between the dusky titi and squirrel monkey. Am. J. Primatol. 50, 95–107 (2000).
pubmed: 10676707
Kugou, K., Hirai, H., Masumoto, H. & Koga, A. Formation of functional CENP-B boxes at diverse locations in repeat units of centromeric DNA in New World monkeys. Sci. Rep. 6, 27833, https://doi.org/10.1038/srep27833 (2016).
doi: 10.1038/srep27833
pubmed: 27292628
pmcid: 4904201
Silva, B. T. F. et al. Protein electrophoretic variability in Saimiri and the question of its species status. Am. J. Primatol. 29, 183–193 (1993).
pubmed: 31941191
Carneiro, J., Rodrigues-Filho, L. F. S., Schneider, H. & Sampaio, I. Molecular data highlight hybridization in squirrel monkeys (Saimiri, Cebidae). Genet. Mol. Biol. 39, 539–546 (2016).
pubmed: 27801483
pmcid: 5127161
Smalec, B. M., Heider, T. N., Flynn, B. L. & O’Neill, R. J. A centromere satellite concomitant with extensive karyotypic diversity across the Peromyscus genus defies predictions of molecular drive. Chromosome Res. 27, 237–252 (2019).
pubmed: 30771198
pmcid: 6733818
Willard, H. F. Chromosome-specific organization of human alpha satellite DNA. Am. J. Hum. Genet. 37, 524–532 (1985).
Stanyon, R. et al. Primate chromosome evolution: Ancestral karyotypes, marker order and neocentromeres. Chromosome Res. 16, 17–39 (2008).
pubmed: 18293103
Moore, C. M., Harris, C. P. & Abee, C. R. Distribution of chromosomal polymorphisms in three subspecies of squirrel monkeys (genus Saimiri). Cytogenet. Cell Genet. 53, 118–122 (1990).
pubmed: 2369837
García, F. et al. Chromosomal homologies between humans and Cebus apella chromosomes revealed by ZOO-FISH. Mamm. Genome 11, 399–401 (2000).
pubmed: 10790541
IUCN 2019. The IUCN Red List of Threatened Species. Version 2019-2. Downloaded on 18 July 2019. http://www.iucnredlist.org .
Stanyon, R. & Galleni, L. A rapid fibroblast culture technique for high resolution karyotypes. Bolletino di Zool. 58, 81–83 (1991).
Seabright, M. A rapid banding technique for human chromosomes. The Lancet 298, 971–972 (1971).
Sumner, A. T. A simple technique for demonstrating centromeric heterochromatin. Exp. Cell Res. 75, 304–306 (1972).
pubmed: 4117921
Capozzi, O., Archidiacono, N., Lorusso, N., Stanyon, R. & Rocchi, M. The 14/15 association as a paradigmatic example of tracing karyotype evolution in New World monkeys. Chromosoma 125, 747–756 (2016).
pubmed: 26667930
Yonenaga Yassuda, Y. & Chu, T. H. Chromosome banding patterns of Saimiri vanzolinii ayres, 1965 (Primates, Cebidae). Pap. Avulsos Zool. 36, 165–168 (1985).
Novák, P., Neumann, P. & Macas, J. Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinformatics 11, 378, https://doi.org/10.1186/1471-2105-11-378 (2010).
doi: 10.1186/1471-2105-11-378
pubmed: 20633259
pmcid: 20633259
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 29, 792–793 (2013).
pubmed: 23376349
pmcid: 23376349
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
pubmed: 2231712
Edgar, R. C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).
pubmed: 15034147
pmcid: 390337
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).
pubmed: 5967553
pmcid: 5967553
Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 47, W256–W259, https://doi.org/10.1093/nar/gkz239 (2019).
doi: 10.1093/nar/gkz239
pubmed: 30931475
pmcid: 6602468
Dixon, P. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14, 927–930 (2003).
RStudio Team. RStudio: Integrated Development for R [Computer software]. RStudio, Inc.; http://www.rstudio.com/ (2015).