Population Scale Analysis of Centromeric Satellite DNA Reveals Highly Dynamic Evolutionary Patterns and Genomic Organization in Long-Tailed and Rhesus Macaques

Worapong Singchat; Syed Farhan Ahmad; Kitipong Jaisamut; Thitipong Panthum; Nattakan Ariyaraphong; Ekaphan Kraichak; Narongrit Muangmai; Prateep Duengkae; Sunchai Payungporn; Suchinda Malaivijitnond; Kornsorn Srikulnath

doi:10.3390/cells11121953

Population Scale Analysis of Centromeric Satellite DNA Reveals Highly Dynamic Evolutionary Patterns and Genomic Organization in Long-Tailed and Rhesus Macaques

Cells. 2022 Jun 17;11(12):1953. doi: 10.3390/cells11121953.

Authors

Worapong Singchat^{1

2}, Syed Farhan Ahmad^{1

2

3}, Kitipong Jaisamut¹, Thitipong Panthum^{1

2}, Nattakan Ariyaraphong^{1

2}, Ekaphan Kraichak^{1

4}, Narongrit Muangmai^{1

5}, Prateep Duengkae^{1

2}, Sunchai Payungporn⁶, Suchinda Malaivijitnond^{1

7

8}, Kornsorn Srikulnath^{1

2

3

8

9

10}

Affiliations

¹ Animal Genomics and Bioresource Research Unit (AGB Research Unit), Faculty of Science, Kasetsart University, Bangkok 10900, Thailand.
² Special Research Unit for Wildlife Genomics (SRUWG), Department of Forest Biology, Faculty of Forestry, Kasetsart University, 50 Ngamwongwan, Chatuchak, Bangkok 10900, Thailand.
³ The International Undergraduate Program in Bioscience and Technology, Faculty of Science, Kasetsart University, 50 Ngamwongwan, Chatuchak, Bangkok 10900, Thailand.
⁴ Department of Botany, Faculty of Science, Kasetsart University, Bangkok 10900, Thailand.
⁵ Department of Fishery Biology, Faculty of Fisheries, Kasetsart University, Bangkok 10900, Thailand.
⁶ Department of Biochemistry, Faculty of Medicine, Chulalongkorn University, Bangkok 10330, Thailand.
⁷ Department of Biology, Faculty of Science, Chulalongkorn University, Bangkok 10330, Thailand.
⁸ National Primate Research Center of Thailand-Chulalongkorn University, Saraburi 18110, Thailand.
⁹ Laboratory of Animal Cytogenetics and Comparative Genomics (ACCG), Department of Genetics, Faculty of Science, Kasetsart University, Bangkok 10900, Thailand.
¹⁰ Amphibian Research Center, Hiroshima University, 1-3-1 Kagamiyama, Higashihiroshima 739-8526, Japan.

Abstract

Centromeric satellite DNA (cen-satDNA) consists of highly divergent repeat monomers, each approximately 171 base pairs in length. Here, we investigated the genetic diversity in the centromeric region of two primate species: long-tailed (Macaca fascicularis) and rhesus (Macaca mulatta) macaques. Fluorescence in situ hybridization and bioinformatic analysis showed the chromosome-specific organization and dynamic nature of cen-satDNAsequences, and their substantial diversity, with distinct subfamilies across macaque populations, suggesting increased turnovers. Comparative genomics identified high level polymorphisms spanning a 120 bp deletion region and a remarkable interspecific variability in cen-satDNA size and structure. Population structure analysis detected admixture patterns within populations, indicating their high divergence and rapid evolution. However, differences in cen-satDNA profiles appear to not be involved in hybrid incompatibility between the two species. Our study provides a genomic landscape of centromeric repeats in wild macaques and opens new avenues for exploring their impact on the adaptive evolution and speciation of primates.

Keywords: centromere; diversity; macaque; primate; satellite DNA.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
DNA, Satellite* / genetics
Genomics*
In Situ Hybridization, Fluorescence
Macaca fascicularis / genetics
Macaca mulatta / genetics

Substances

DNA, Satellite

Associated data

Dryad/10.5061/dryad.w3r2280sw

Grants and funding

This study was financially supported by grants from the Center for Advanced Studies in Tropical Natural Resources, National Research University-Kasetsart University (CASTNAR, NRU-KU, Thailand) awarded to K.S., the e-ASIA Joint Research Program (no. P1851131) awarded to K.S., the National Science and Technology Development Agency (NSTDA) (NSTDA P-19-52238) awarded to K.S., the Graduate Scholarship Program of the Graduate School, Kasetsart University, Thailand (to T.P. and K.S.), the National Primate Research Center of Thailand-Chulalongkorn University (NPRCT-CU to K.S.), the Thailand Research Fund-Chinese Academy of Science (no. DBG608008 to S.M.), and Thailand Research Fund Senior Scholar (no. RTA6280010 to S.M.).