Skip to main content

Genome-wide mining and comparative analysis of microsatellites in three macaque species

Molecular Genetics and Genomics volume 292, pages 537–550 (2017)Cite this article

Abstract

Microsatellites are found in taxonomically different organisms, and such repeats are related with genomic structure, function and certain diseases. To characterize microsatellites for macaques, we searched and compared SSRs with 1–6 bp nucleotide motifs in rhesus, cynomolgus and pigtailed macaque. A total of 1395671, 1284929 and 1266348 perfect SSRs were mined, respectively. The most frequent perfect SSRs were mononucleotide SSRs. The most GC-content was in dinucleotide SSRs and the least was in the mononucleotide SSRs. Chromosome size was positively correlated with SSR number and negatively correlated with the relative frequency and density of SSRs. The GC content of chromosome SSRs were negatively correlated with relative frequency of SSRs and GC content of chromosome sequences. The features of microsatellite distribution in assembled genomes of the three species were greatly similar, which revealed that the distributional pattern of microsatellites is probably conservative in genus Macaca. The degenerated number of repeat motifs was found to be different in pentanucleotide and hexanucleotide repeats. Species-specific motifs for each macaque were significantly underrepresented. Overall, SSR frequencies of each chromosome in rhesus macaque were higher than in cynomolgus macaque. The maximum repeat times of mono- to pentanucleotide repeats in cynomolgus macaque was more than other two macaques. These results emphasize the genetic diversity and phylogenetic relationship of genus Macaca species. Our data will be beneficial for comparative genome mapping, understanding the distribution of SSRs and genome structure between these animal models, and provide a foundation for further development and identification of more macaque-specific SSRs.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Abdelkrim J, Robertson BC, Stanton JAL, Gemmell NJ (2009) Fast, cost-effective development of species-specific microsatellite markers by genomic sequencing. Biotechniques 46:185

    CAS  Article  PubMed  Google Scholar 

  • Bachtrog D (2006) A dynamic view of sex chromosome evolution. Curr Opin Genet Dev 16(6):578–585

    CAS  Article  PubMed  Google Scholar 

  • Batten CJ, Rose RD, Wilson KM, Agy MB, Chea S, Stratov I et al (2006) Comparative evaluation of simian, simian-human, and human immunodeficiency virus infections in the pigtail macaque (Macaca nemestrina) model. AIDS Res Hum Retrov 22:580–588

    CAS  Article  Google Scholar 

  • Campregher C, Scharl T, Nemeth M, Honeder C, Jascur T, Boland CR et al (2010) The nucleotide composition of microsatellites impacts both replication fidelity and mismatch repair in human colorectal cells. Hum Mol Genet. doi:10.1093/hmg/ddq175

    PubMed  PubMed Central  Google Scholar 

  • Castagnone-Sereno P, Danchin EG, Deleury E, Guillemaud T, Malausa T, Abad P (2010) Genome-wide survey and analysis of microsatellites in nematodes, with a focus on the plant-parasitic species Meloidogyne incognita. BMC Genom 11:598

    Article  Google Scholar 

  • Chistiakov DA, Hellemans B, Volckaert FA (2006) Microsatellites and their genomic distribution, evolution, function and applications: a review with special reference to fish genetics. Aquaculture 255:1–29

    CAS  Article  Google Scholar 

  • Choudhary OP, Trivedi S (2010) Microsatellite or simple sequence repeat (SSR) instability depends on repeat characteristics during replication and repair. J Cell Mol Biol 8:21–34

    CAS  Google Scholar 

  • Du L, Li Y, Zhang X, Yue B (2013) MSDB: a user-friendly program for reporting distribution and building databases of microsatellites from genome sequences. J Hered 104:154–157

    Article  PubMed  Google Scholar 

  • Duret L, Mouchiroud D, Gautier C (1995) Statistical analysis of vertebrate sequences reveals that long genes are scarce in GC-rich isochores. J Mol Evol 40:308–317

    CAS  Article  PubMed  Google Scholar 

  • Ellegren H (2000) Heterogeneous mutation processes in human microsatellite DNA sequences. Nat Genet 24:400–402

    CAS  Article  PubMed  Google Scholar 

  • Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5:435–445

    CAS  Article  PubMed  Google Scholar 

  • Ely JJ, Aivaliotis MJ, Kalmin B, Manis GS, VandeBerg JL, Stone WH (1999) Comparison of biochemical polymorphisms and short tandem repeat (STR) DNA markers for paternity testing in rhesus monkeys (Macaca mulatta). Biochem Genet 37:323–334

    CAS  Article  PubMed  Google Scholar 

  • Fa JE (1989) The genus Macaca: a review of taxonomy and evolution. Mamm Rev 19:45–81

    Article  Google Scholar 

  • Fernandez CS, Reece JC, Saepuloh U, De Rose R, Ishkandriati D, O’Connor DH et al (2011) Screening and confirmatory testing of MHC class I alleles in pig-tailed macaques. Immunogenetics 63:511–521

    Article  PubMed  Google Scholar 

  • Fooden JACK (1976) Provisional classification and key to living species of macaques (Primates: Macaca). Folia Primatol 25:225–236

    CAS  Article  PubMed  Google Scholar 

  • Fullerton SM, Carvalho AB, Clark AG (2001) Local rates of recombination are positively correlated with GC content in the human genome. Mol Biol Evol 18:1139–1142

    CAS  Article  PubMed  Google Scholar 

  • Galtier N, Piganeau G, Mouchiroud D, Duret L (2001) GC-content evolution in mammalian genomes: the biased gene conversion hypothesis. Genetics 159:907–911

    CAS  PubMed  PubMed Central  Google Scholar 

  • Griffiths A, Link MA, Furness CL, Coen DM (2006) Low-level expression and reversion both contribute to reactivation of herpes simplex virus drug-resistant mutants with mutations on homopolymeric sequences in thymidine kinase. J Virol 80:6568–6574

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Guichoux E, Lagache L, Wagner S, Chaumeil P, Léger P, Lepais O et al (2011) Current trends in microsatellite genotyping. Mol Ecol Resour 11:591–611

    CAS  Article  PubMed  Google Scholar 

  • Huang J, Du LM, Li YZ, Li WJ, Zhang XY, Yue BS (2012) Distribution regularities of microsatellites in the Gallus gallus genome. Sichuan J Zool 31:358–363

    CAS  Google Scholar 

  • Huang J, Li YZ, Du LM, Yang B, Shen FJ, Zhang HM et al (2015) Genome-wide survey and analysis of microsatellites in giant panda (Ailuropoda melanoleuca), with a focus on the applications of a novel microsatellite marker system. BMC Genom 16:61

    Article  Google Scholar 

  • Jabbari K, Bernardi G (1998) CpG doublets, CpG islands and Alu repeats in long human DNA sequences from different isochore families. Gene 224:123–128

    CAS  Article  PubMed  Google Scholar 

  • Jensen-Seaman MI, Furey TS, Payseur BA, Lu Y, Roskin KM, Chen CF, Jacob HJ (2004) Comparative recombination rates in the rat, mouse, and human genomes. Genome Res 14(4):528–538

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Jones PA, Takai D (2001) The role of DNA methylation in mammalian epigenetics. Science 293:1068–1070

    CAS  Article  PubMed  Google Scholar 

  • Kanthaswamy S, Satkoski J, George D, Kou A, Erickson BJA, Smith DG (2008) Hybridization and stratification of nuclear genetic variation in Macaca mulatta and M. fascicularis. Int J Primatol 29:1295–1311

    Article  PubMed  PubMed Central  Google Scholar 

  • Karaoglu H, Lee CMY, Meyer W (2005) Survey of simple sequence repeats in completed fungal genomes. Mol Biol Evol 22:639–649

    CAS  Article  PubMed  Google Scholar 

  • Katti MV, Ranjekar PK, Gupta VS (2001) Differential distribution of simple sequence repeats in eukaryotic genome sequences. Mol Biol Evol 18:1161–1167

    CAS  Article  PubMed  Google Scholar 

  • Kim TS, Booth JG, Gauch HG, Sun Q, Park J, Lee YH et al (2008) Simple sequence repeats in Neurospora crassa: distribution, polymorphism and evolutionary inference. BMC Genom 9:31

    Article  Google Scholar 

  • Kofler R, Schlötterer C, Lelley T (2007) SciRoKo: a new tool for whole genome microsatellite search and investigation. Bioinformatics 23(13):1683–1685

    CAS  Article  PubMed  Google Scholar 

  • Kumpatla SP, Mukhopadhyay S (2005) Mining and survey of simple sequence repeats in expressed sequence tags of dicotyledonous species. Genome 48:985–998

    CAS  Article  PubMed  Google Scholar 

  • Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921

    CAS  Article  PubMed  Google Scholar 

  • Lawson MJ, Zhang L (2006) Distinct patterns of SSR distribution in the Arabidopsis thaliana and rice genomes. Genome Biol 7:R14

    Article  PubMed  PubMed Central  Google Scholar 

  • Leopoldino AM, Pena SD (2003) The mutational spectrum of human autosomal tetranucleotide microsatellites. Hum Mutat 21:71–79

    CAS  Article  PubMed  Google Scholar 

  • Li YC, Korol AB, Fahima T, Nevo E (2004) Microsatellites within genes: structure, function, and evolution. Mol Biol Evol 21:991–1007

    CAS  Article  PubMed  Google Scholar 

  • Li A, Sun Z, Zeng L, Li R, Kong D, Zhao Y, Shi Y (2012) Microsatellite variation in two subspecies of cynomolgus monkeys (Macaca fascicularis). Am J Primatol 74:561–568

    CAS  Article  PubMed  Google Scholar 

  • Li WJ, Li YZ, Du LM, Huang J, Shen YM, Zhang XY, Yue BS (2014) Comparative analysis of microsatellite sequences distribution in the genome of giant panda and polar bear. Sichuan J Zool 33:874–878

    Google Scholar 

  • Liu L, Dybvig K, Panangala VS, van Santen VL, French CT (2000) GAA trinucleotide repeat region regulates M9/pMGA gene expression in Mycoplasma gallisepticum. Infect Immun 68:871–876

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Ma Z (2015) Genome-wide characterization of perfect microsatellites in yak (Bos grunniens). Genetica 143:515–520

    CAS  Article  PubMed  Google Scholar 

  • Meissier E, Li SH, Stewart CB (1996) The birth of microsatellite. Nature 381:483

    Article  Google Scholar 

  • Meunier J, Duret L (2004) Recombination drives the evolution of GC-content in the human genome. Mol Biol Evol 21(6):984–990

    CAS  Article  PubMed  Google Scholar 

  • Miret JJ, Pessoa-Brandão L, Lahue RS (1998) Orientation-dependent and sequence-specific expansions of CTG/CAG trinucleotide repeats in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 95:12438–12443

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Mouchiroud D, D’Onofrio G, Aissani B, Macaya G, Gautier C, Bernardi G (1991) The distribution of genes in the human genome. Gene 100:181–187

    CAS  Article  PubMed  Google Scholar 

  • Oliveira EJ, Pádua JG, Zucchi MI, Vencovsky R, Vieira MLC (2006) Origin, evolution and genome distribution of microsatellites. Genet Mol Biol 29:294–307

    CAS  Article  Google Scholar 

  • Ouyang Q, Zhao X, Feng H, Tian Y, Li D, Li M et al (2012) High GC content of simple sequence repeats in Herpes simplex virus type 1 genome. Gene 499:37–40

    CAS  Article  PubMed  Google Scholar 

  • Pajuelo MJ, Eguiluz M, Dahlstrom E, Requena D, Guzmán F, Ramirez M et al (2015) Identification and characterization of microsatellite markers derived from the whole genome analysis of Taenia solium. PLoS Negl Trop Dis 9:e0004316

    Article  PubMed  PubMed Central  Google Scholar 

  • Perwitasari-Farajallah D, Kyes RC, Iskandar E (2010) Microsatellite DNA polymorphisms for colony management of long-tailed macaques (Macaca fascicularis) population on the Tinjil Island. Biodiversitas 11:55–58

    Article  Google Scholar 

  • Qi WH, Jiang XM, Du LM, Xiao GS, Hu TZ, Yue BS et al (2015) Genome-wide survey and analysis of microsatellite sequences in bovid species. PLoS One 10:e0133667

    Article  PubMed  PubMed Central  Google Scholar 

  • Rasmussen DA, Noor MA (2009) What can you do with 0.1 × genome coverage? A case study based on a genome survey of the scuttle fly Megaselia scalaris (Phoridae). BMC Genom 10:382

    Article  Google Scholar 

  • Ren L, Gao G, Zhao D, Ding M, Luo J, Deng H (2007) Developmental stage related patterns of codon usage and genomic GC content: searching for evolutionary fingerprints with models of stem cell differentiation. Genome Biol 8:R35

    Article  PubMed  PubMed Central  Google Scholar 

  • Schlötterer C (1998) Genome evolution: are microsatellites really simple sequences? Curr Biol 8:R132–R134

    Article  PubMed  Google Scholar 

  • Schlötterer C (2000) Evolutionary dynamics of microsatellite DNA. Chromosoma 109:365–371

    Article  PubMed  Google Scholar 

  • Sharma PC, Grover A, Kahl G (2007) Mining microsatellites in eukaryotic genomes. Trends Biotechnol 25:490–498

    CAS  Article  PubMed  Google Scholar 

  • Sherman SL (2000) Premature ovarian failure in the fragile X syndrome. Am J Med Genet 97:189–194

    CAS  Article  PubMed  Google Scholar 

  • Subramanian S, Mishra RK, Singh L (2003) Genome-wide analysis of microsatellite repeats in humans: their abundance and density in specific genomic regions. Genome Biol 4:R13

    Article  PubMed  PubMed Central  Google Scholar 

  • Sunnucks P (2000) Efficient genetic markers for population biology. Trends Ecol Evol 15:199–203

    CAS  Article  PubMed  Google Scholar 

  • Tortereau F, Servin B, Frantz L, Megens HJ, Milan D, Rohrer G, Groenen MA (2012) A high density recombination map of the pig reveals a correlation between sex-specific recombination and GC content. BMC Genom 13:586

    CAS  Article  Google Scholar 

  • Tóth G, Gáspári Z, Jurka J (2000) Microsatellites in different eukaryotic genomes: survey and analysis. Genome Res 10:967–981

    Article  PubMed  PubMed Central  Google Scholar 

  • Vinogradov AE (2003) DNA helix: the importance of being GC-rich. Nucl Acids Res 31:1838–1844

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Chen M, Wang H, Wang JF, Bao D (2014) Microsatellites in the genome of the edible mushroom, Volvariella volvacea. BioMed Res Int. doi:10.1155/2014/281912

    Google Scholar 

  • Wierdl M, Dominska M, Petes TD (1997) Microsatellite instability in yeast: dependence on the length of the microsatellite. Genetics 146:769–779

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Hu Z, Wang C, Zhang X, Li J, Yue B (2016) Characterization of perfect microsatellite based on genome-wide and chromosome level in Rhesus monkey (Macaca mulatta). Gene 592:269–275

    CAS  Article  PubMed  Google Scholar 

  • Yan G, Zhang G, Fang X, Zhang Y, Li C, Ling F et al (2011) Genome sequencing and comparison of two nonhuman primate animal models, the cynomolgus and Chinese rhesus macaques. Nat Biotechnol 29:1019–1023

    CAS  Article  PubMed  Google Scholar 

  • Zimin AV, Cornish AS, Maudhoo MD, Gibbs RM, Zhang X, Pandey S, Tharp GK (2014) A new rhesus macaque assembly and annotation for next-generation sequencing analyses. Biol Direct 9:20

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Chen Wang and Changjun Peng for assistance with statistical work. This research was supported by the National Natural Science Foundation of China (Grants No. 31270431 and No. 31501871), the State Key Program of National Natural Science Foundation of China (Grants No. 31530068) and the Sichuan Application Foundation Project (2015JY0268).

Author information

Affiliations

  1. Key Laboratory of Bio-resources and Eco-environment (Ministry of Education), College of Life Sciences, Sichuan University, Chengdu, 610064, People’s Republic of China

    Sanxu Liu, Wei Hou, Tianlin Sun, Yongtao Xu, Peng Li, Bisong Yue, Zhenxin Fan & Jing Li

  2. Sichuan Key Laboratory of Conservation Biology on Endangered Wildlife, College of Life Sciences, Sichuan University, Chengdu, 610064, People’s Republic of China

    Bisong Yue & Jing Li

Authors
  1. Sanxu Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wei Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tianlin Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yongtao Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Peng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bisong Yue
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhenxin Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jing Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jing Li.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

S. Liu and W. Hou have contributed equally to the work.

Communicated by S. Hohmann.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 23 KB)

Supplementary material 2 (XLSX 26 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Liu, S., Hou, W., Sun, T. et al. Genome-wide mining and comparative analysis of microsatellites in three macaque species. Mol Genet Genomics 292, 537–550 (2017). https://doi.org/10.1007/s00438-017-1289-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-017-1289-1

Keywords

  • Genus Macaca
  • Genome-wide
  • Chromosome
  • Microsatellite
  • Comparative analysis