Application of Efficient Express Sequence Tags Information for Classification and Functional Study of Simple Sequence Repeats in Cattle Testis Tissue
Abstract
Genomic markers play an important role in tracing the flow of genetic causality of observable signals in animals and plants. In farm animals, the participation of male animals in the gene pool of subsequent generations are much higher than female animals and testes are the most important organs of the male reproductive system. This study was conducted to investigate simple sequence repeats (SSR) within the expressed sequence tags (ESTs) in order to classify the Bos taurus testis tissue’s genes for their relationship and specificity with related reproductive domains. A total of 48,549 publicly available EST sequences from cattle testis tissue downloaded from GenBank database, out of which, 10,237 sequences that their library made from testis tissue were extracted and specialized as the studied sequences using several searching tools and software. Across these selective sequences, 2,039 contigs, 5,097 singletons, and 153 SSRs were detected. EST-SSRs were subsequently evaluated using GenBank and categorized based on their functions in biological systems of dairy cattle. Investigation of these motifs showed that the identified EST-SSRs can be classified into 48 types that GT in dinucleotides and GCC in trinucleotides had the highest frequency. Annotation and gene ontology analysis revealed a relationship among 54 domains with the observed SSRs. Localization and characterization of such markers can help tracing the production of amino acids coded by identified repeats as shown in this study.
References
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Li, Y. C., A. B. Korol, T. Fahima, & E. Nevo. 2004. Microsatellites within genes: structure, function, and evolution. Mol. Biol. Evol. 21: 991-1007. https://doi.org/10.1093/molbev/msh073
Lu, G. & E. N. Moriyama. 2004. Vector NTI, a balanced all-in-one sequence analysis suite. Briefings in Bioinformatics 5: 378-388. https://doi.org/10.1093/bib/5.4.378
Ma, K., G. Qiu, J. Feng, & J. Li. 2012. Transcriptome analysis of the oriental river prawn, Macrobrachium nipponense using 454 pyrosequencing for discovery of genes and markers. PLoS One 7: e39727. https://doi.org/10.1371/journal.pone.0039727
Molla, K. A., A. B. Debnath, S. A. Ganie, & T. K. Mondal. 2015. Identification and analysis of novel salt responsive candidate gene based SSRs (cgSSRs) from rice (Oryza sativa L.). BMC Plant Biol. 15: 122. https://doi.org/10.1186/s12870-015-0498-1
Moore, T., A. McLellan, F. Wynne, & P. Dockery. 2005. Explaining the X-linkage bias of placentally expressed genes. Nat. Genet. 37: 3; author reply 3-4. https://doi.org/10.1038/ng0105-3a
Mostafa, T., L. H. El-Shahid, A. A. El Azeem, O. Shaker, H. Gomaa, & H. M. Abd El Hamid. 2012. Androgen receptor-CAG repeats in infertile Egyptian men. Andrologia 44: 147-51. https://doi.org/10.1111/j.1439-0272.2010.01125.x
Mudunuri, S. B. & H. A. Nagarajaram. 2007. IMEx: Imperfect Microsatellite Extractor. Bioinformatics 23: 1181-7. https://doi.org/10.1093/bioinformatics/btm097
Muller, M. P., S. Rothammer, D. Seichter, I. Russ, D. Hinrichs, J. Tetens, G. Thaller, and I. Medugorac. 2017. Genome-wide mapping of 10 calving and fertility traits in Holstein dairy cattle with special regard to chromosome 18. J. Dairy Sci. 100: 1987-2006. https://doi.org/10.3168/jds.2016-11506
Mundlos, S., F. Otto, C. Mundlos, J. B. Mulliken, A. S. Aylsworth, S. Albright, D. Lindhout, W. G. Cole, W. Henn, J. H. Knoll, M. J. Owen, R. Mertelsmann, B. U. Zabel, & B. R. Olsen. 1997. Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia. Cell 89: 773-9. https://doi.org/10.1016/S0092-8674(00)80260-3
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Qian, F., J. Guo, Z. Jiang, & B. Shen. 2018. Translational bioinformatics for cholangiocarcinoma: opportunities and challenges. International Journal of Biological Sciences 14: 920. https://doi.org/10.7150/ijbs.24622
Riar, D. S., S. Rustgi, I. C. Burke, K. S. Gill, & J. P. Yenish. 2011. EST-SSR Development from 5 Lactuca Species and Their Use in Studying Genetic Diversity Among L. serriola Biotypes. Journal of Heredity 102: 17-28. https://doi.org/10.1093/jhered/esq103
Sharma, P. C., A. Grover, & G. Kahl. 2007. Mining microsatellites in eukaryotic genomes. Trends Biotechnol. 25: 490-8. https://doi.org/10.1016/j.tibtech.2007.07.013
Stamatoyannopoulos, J. A. 2004. The genomics of gene expression. Genomics 84: 449-57. https://doi.org/10.1016/j.ygeno.2004.05.002
Tae, H., D. Ryu, S. Sureshchandra, & J. H. Choi. 2012. ESTclean: a cleaning tool for next-gen transcriptome shotgun sequencing. BMC Bioinformatics 13: 247. https://doi.org/10.1186/1471-2105-13-247
Taheri, S., T. L. Abdullah, M. Y. Rafii, J. A. Harikrishna, S. P. O. Werbrouck, C. H. Teo, Ma. Sahebi, & P. Azizi. 2019. De novo assembly of transcriptomes, mining, and development of novel EST-SSR markers in Curcuma alismatifolia (Zingiberaceae family) through Illumina sequencing. Scientific Reports 9: 3047. https://doi.org/10.1038/s41598-019-53129-x
Tanaka, H., N. Iguchi, Y. Toyama, K. Kitamura, T. Takahashi, K. Kaseda, M. Maekawa, & Y. Nishimune. 2004. Mice deficient in the axonemal protein Tektin-t exhibit male infertility and immotile-cilium syndrome due to impaired inner arm dynein function. Mol. Cell Biol. 24: 7958-64. https://doi.org/10.1128/MCB.24.18.7958-7964.2004
Temnykh, S., G. DeClerck, A. Lukashova, L. Lipovich, S. Cartinhour, & S. McCouch. 2001. Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. Genome Res. 11: 1441-52. https://doi.org/10.1101/gr.184001
Thiel, T., W. Michalek, R. K. Varshney, & A. Graner. 2003. Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor. Appl. Genet. 106: 411-22. https://doi.org/10.1007/s00122-002-1031-0
Toth, G., Z. Gaspari, & J. Jurka. 2000. Microsatellites in different eukaryotic genomes: survey and analysis. Genome Res. 10: 967-81. https://doi.org/10.1101/gr.10.7.967
Varshney, R. K., T. Thiel, N. Stein, P. Langridge, & A. Graner. 2002. In silico analysis on frequency and distribution of microsatellites in ESTs of some cereal species. Cell. Mol. Biol. Lett. 7: 537-46.
Voorrips, R. E. 2002. MapChart: Software for the graphical presentation of linkage Maps and QTLs. Journal of Heredity 93: 77-78. https://doi.org/10.1093/jhered/93.1.77
Wang, Z., G. Yu, B. Shi, X. Wang, H. Qiang, & H. Gao. 2014. Development and characterization of simple sequence repeat (SSR) markers based on RNA-sequencing of Medicago sativa and in silico mapping onto the M. truncatula genome. PLoS One 9: e92029. https://doi.org/10.1371/journal.pone.0092029
Weber, J. L. 1990. Informativeness of human (dC-dA)n.(dG-dT)n polymorphisms. Genomics 7: 524-30. https://doi.org/10.1016/0888-7543(90)90195-Z
Yan, Q., Y. Zhang, H. Li, C. Wei, L. Niu, S. Guan, S. Li, & L. Du. 2008. Identification of microsatellites in cattle unigenes. J. Genet. Genomics. 35: 261-6. https://doi.org/10.1016/S1673-8527(08)60037-5
Yan, Z., F. Wu, K. Luo, Y. Zhao, Q. Yan, Y. Zhang, Y. Wang, & J. Zhang. 2017. Cross-species transferability of EST-SSR markers developed from the transcriptome of Melilotus and their application to population genetics research. Scientific Reports 7: 17959. https://doi.org/10.1038/s41598-017-18049-8
Zhang, W., Z. Wang, Z. Zhao, X. Zeng, H. Wu, & P. Yu. 2010. Using bioinpormcotics methods to develop EST-SSR makers from sheep’s ESTs. J. Anim. Vet. Adv. 9:2759-2762. https://doi.org/10.3923/javaa.2010.2759.2762
Bakhtiarizadeh, M. R., B. Arefnejad, E. Ebrahimie, & M. Ebrahimi. 2012a. Application of functional genomic information to develop efficient EST-SSRs for the chicken (Gallus gallus). Genet. Mol. Res. 11: 1558-74. https://doi.org/10.4238/2012.May.21.12
Bakhtiarizadeh, M.R., B. Arefnejad, E. Ebrahimie, & M. Ebrahimi. 2012b. Application of functional genomic information to develop efficient EST-SSRs for the chicken (Gallus gallus). Genet. Mol. Res. 11: 1558-1574. https://doi.org/10.4238/2012.May.21.12
Bhattacharjee, R., C. O. Nwadili, C. A. Saski, A. Paterne, B. E. Scheffler, J. Augusto, A. Lopez-Montes, J. T. Onyeka, P. L. Kumar, & R. Bandyopadhyay. 2018. An EST-SSR based genetic linkage map and identification of QTLs for anthracnose disease resistance in water yam (Dioscorea alata L.). PloS One 13: e0197717. https://doi.org/10.1371/journal.pone.0197717
Blair, M. W., F. Pedraza, H. F. Buendia, E. Gaitan-Solis, S. E. Beebe, P. Gepts, & J. Tohme. 2003. Development of a genome-wide anchored microsatellite map for common bean (Phaseolus vulgaris L.). Theor. Appl. Genet. 107: 1362-74. https://doi.org/10.1007/s00122-003-1398-6
Djureinovic, D., L. Fagerberg, B. Hallström, A. Danielsson, C. Lindskog, M. Uhlén, & F. Pontén. 2014. The human testis-specific proteome defined by transcriptomics and antibody-based profiling. MHR: Basic science of reproductive medicine 20: 476-488. https://doi.org/10.1093/molehr/gau018
Duan, Y., P. Liu, J. Li, J. Li, & P. Chen. 2013. Immune gene discovery by expressed sequence tag (EST) analysis of hemocytes in the ridgetail white prawn Exopalaemon carinicauda. Fish Shellfish Immunol. 34: 173-82. https://doi.org/10.1016/j.fsi.2012.10.026
Ehsani, A., L. Janss, D. Pomp, & P. Sorensen. 2016. Decomposing genomic variance using information from GWA, GWE and eQTL analysis. Anim. Genet. 47: 165-73. https://doi.org/10.1111/age.12396
Ellis, J. R. & J. M. Burke. 2007. EST-SSRs as a resource for population genetic analyses. Heredity (Edinb) 99: 125-32. https://doi.org/10.1038/sj.hdy.6801001
Garcia-Ruiz, A., J. B. Cole, P. M. VanRaden, G. R. Wiggans, F. J. Ruiz-Lopez, & C. P. Van Tassell. 2016. Changes in genetic selection differentials and generation intervals in US Holstein dairy cattle as a result of genomic selection. Proc. Natl. Acad. Sci. U S A 113: E3995-4004. https://doi.org/10.1073/pnas.1519061113
Gerashchenko, M. V., D. Su, & V. N. Gladyshev. 2010. CUG start codon generates thioredoxin/glutathione reductase isoforms in mouse testes. J. Biol. Chem. 285: 4595-602. https://doi.org/10.1074/jbc.M109.070532
Gupta, P.K. & R.K. Varshney. 2000. The development and use of microsatellite markers for genetic analysis and plant breeding with emphasis on bread wheat. Euphytica 113: 163-185. https://doi.org/10.1023/A:1003910819967
Huson, K.M., W. Haresign, M.J. Hegarty, T.M. Blackmore, C. Morgan, & N.R. McEwan. 2015. Assessment of genetic relationship between six populations of Welsh Mountain sheep using microsatellite markers. Notes 216: 223. https://doi.org/10.17221/8171-CJAS
Janatova, M. & P. Pohlreich. 2004. Microsatellite markers in breast cancer studies. Prague Med Rep 105: 111-8.
Kalyana Babu, B., P. K. Agrawal, D. Pandey, J. P. Jaiswal, & A. Kumar. 2014. Association mapping of agro-morphological characters among the global collection of finger millet genotypes using genomic SSR markers. Mol. Biol. Rep. 41: 5287-97. https://doi.org/10.1007/s11033-014-3400-6
Kaur, S., P. S. Panesar, M. B. Bera, & V. Kaur. 2015. Simple sequence repeat markers in genetic divergence and marker-assisted selection of rice cultivars: a review. Crit. Rev. Food Sci. Nutr. 55: 41-9. https://doi.org/10.1080/10408398.2011.646363
Kirungu, J., Y. Deng, X. Cai, R. Magwanga, Z. Zhou, X. Wang, Y. Wang, Z. Zhang, K. Wang, & F. Liu. 2018. Simple sequence repeat (SSR) genetic linkage map of D genome diploid cotton derived from an interspecific cross between Gossypium davidsonii and Gossypium klotzschianum. International Journal of Molecular Sciences 19: 204. https://doi.org/10.3390/ijms19010204
Li, L., B. P. Brunk, J. C. Kissinger, D. Pape, K. Tang, R. H. Cole, J. Martin, T. Wylie, M. Dante, S. J. Fogarty, D. K. Howe, P. Liberator, C. Diaz, J. Anderson, M. White, M. E. Jerome, E. A. Johnson, J. A. Radke, C. J. Stoeckert, Jr., R. H. Waterston, S. W. Clifton, D. S. Roos, & L. D. Sibley. 2003. Gene discovery in the apicomplexa as revealed by EST sequencing and assembly of a comparative gene database. Genome Res. 13: 443-54. https://doi.org/10.1101/gr.693203
Li, Y. C., A. B. Korol, T. Fahima, & E. Nevo. 2004. Microsatellites within genes: structure, function, and evolution. Mol. Biol. Evol. 21: 991-1007. https://doi.org/10.1093/molbev/msh073
Lu, G. & E. N. Moriyama. 2004. Vector NTI, a balanced all-in-one sequence analysis suite. Briefings in Bioinformatics 5: 378-388. https://doi.org/10.1093/bib/5.4.378
Ma, K., G. Qiu, J. Feng, & J. Li. 2012. Transcriptome analysis of the oriental river prawn, Macrobrachium nipponense using 454 pyrosequencing for discovery of genes and markers. PLoS One 7: e39727. https://doi.org/10.1371/journal.pone.0039727
Molla, K. A., A. B. Debnath, S. A. Ganie, & T. K. Mondal. 2015. Identification and analysis of novel salt responsive candidate gene based SSRs (cgSSRs) from rice (Oryza sativa L.). BMC Plant Biol. 15: 122. https://doi.org/10.1186/s12870-015-0498-1
Moore, T., A. McLellan, F. Wynne, & P. Dockery. 2005. Explaining the X-linkage bias of placentally expressed genes. Nat. Genet. 37: 3; author reply 3-4. https://doi.org/10.1038/ng0105-3a
Mostafa, T., L. H. El-Shahid, A. A. El Azeem, O. Shaker, H. Gomaa, & H. M. Abd El Hamid. 2012. Androgen receptor-CAG repeats in infertile Egyptian men. Andrologia 44: 147-51. https://doi.org/10.1111/j.1439-0272.2010.01125.x
Mudunuri, S. B. & H. A. Nagarajaram. 2007. IMEx: Imperfect Microsatellite Extractor. Bioinformatics 23: 1181-7. https://doi.org/10.1093/bioinformatics/btm097
Muller, M. P., S. Rothammer, D. Seichter, I. Russ, D. Hinrichs, J. Tetens, G. Thaller, and I. Medugorac. 2017. Genome-wide mapping of 10 calving and fertility traits in Holstein dairy cattle with special regard to chromosome 18. J. Dairy Sci. 100: 1987-2006. https://doi.org/10.3168/jds.2016-11506
Mundlos, S., F. Otto, C. Mundlos, J. B. Mulliken, A. S. Aylsworth, S. Albright, D. Lindhout, W. G. Cole, W. Henn, J. H. Knoll, M. J. Owen, R. Mertelsmann, B. U. Zabel, & B. R. Olsen. 1997. Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia. Cell 89: 773-9. https://doi.org/10.1016/S0092-8674(00)80260-3
Pu, Y., W. Wang, Y. Yang, & R. R. Alfano. 2013. Native fluorescence spectra of human cancerous and normal breast tissues analyzed with non-negative constraint methods. Appl. Opt. 52: 1293-301. https://doi.org/10.1364/AO.52.001293
Qian, F., J. Guo, Z. Jiang, & B. Shen. 2018. Translational bioinformatics for cholangiocarcinoma: opportunities and challenges. International Journal of Biological Sciences 14: 920. https://doi.org/10.7150/ijbs.24622
Riar, D. S., S. Rustgi, I. C. Burke, K. S. Gill, & J. P. Yenish. 2011. EST-SSR Development from 5 Lactuca Species and Their Use in Studying Genetic Diversity Among L. serriola Biotypes. Journal of Heredity 102: 17-28. https://doi.org/10.1093/jhered/esq103
Sharma, P. C., A. Grover, & G. Kahl. 2007. Mining microsatellites in eukaryotic genomes. Trends Biotechnol. 25: 490-8. https://doi.org/10.1016/j.tibtech.2007.07.013
Stamatoyannopoulos, J. A. 2004. The genomics of gene expression. Genomics 84: 449-57. https://doi.org/10.1016/j.ygeno.2004.05.002
Tae, H., D. Ryu, S. Sureshchandra, & J. H. Choi. 2012. ESTclean: a cleaning tool for next-gen transcriptome shotgun sequencing. BMC Bioinformatics 13: 247. https://doi.org/10.1186/1471-2105-13-247
Taheri, S., T. L. Abdullah, M. Y. Rafii, J. A. Harikrishna, S. P. O. Werbrouck, C. H. Teo, Ma. Sahebi, & P. Azizi. 2019. De novo assembly of transcriptomes, mining, and development of novel EST-SSR markers in Curcuma alismatifolia (Zingiberaceae family) through Illumina sequencing. Scientific Reports 9: 3047. https://doi.org/10.1038/s41598-019-53129-x
Tanaka, H., N. Iguchi, Y. Toyama, K. Kitamura, T. Takahashi, K. Kaseda, M. Maekawa, & Y. Nishimune. 2004. Mice deficient in the axonemal protein Tektin-t exhibit male infertility and immotile-cilium syndrome due to impaired inner arm dynein function. Mol. Cell Biol. 24: 7958-64. https://doi.org/10.1128/MCB.24.18.7958-7964.2004
Temnykh, S., G. DeClerck, A. Lukashova, L. Lipovich, S. Cartinhour, & S. McCouch. 2001. Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. Genome Res. 11: 1441-52. https://doi.org/10.1101/gr.184001
Thiel, T., W. Michalek, R. K. Varshney, & A. Graner. 2003. Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor. Appl. Genet. 106: 411-22. https://doi.org/10.1007/s00122-002-1031-0
Toth, G., Z. Gaspari, & J. Jurka. 2000. Microsatellites in different eukaryotic genomes: survey and analysis. Genome Res. 10: 967-81. https://doi.org/10.1101/gr.10.7.967
Varshney, R. K., T. Thiel, N. Stein, P. Langridge, & A. Graner. 2002. In silico analysis on frequency and distribution of microsatellites in ESTs of some cereal species. Cell. Mol. Biol. Lett. 7: 537-46.
Voorrips, R. E. 2002. MapChart: Software for the graphical presentation of linkage Maps and QTLs. Journal of Heredity 93: 77-78. https://doi.org/10.1093/jhered/93.1.77
Wang, Z., G. Yu, B. Shi, X. Wang, H. Qiang, & H. Gao. 2014. Development and characterization of simple sequence repeat (SSR) markers based on RNA-sequencing of Medicago sativa and in silico mapping onto the M. truncatula genome. PLoS One 9: e92029. https://doi.org/10.1371/journal.pone.0092029
Weber, J. L. 1990. Informativeness of human (dC-dA)n.(dG-dT)n polymorphisms. Genomics 7: 524-30. https://doi.org/10.1016/0888-7543(90)90195-Z
Yan, Q., Y. Zhang, H. Li, C. Wei, L. Niu, S. Guan, S. Li, & L. Du. 2008. Identification of microsatellites in cattle unigenes. J. Genet. Genomics. 35: 261-6. https://doi.org/10.1016/S1673-8527(08)60037-5
Yan, Z., F. Wu, K. Luo, Y. Zhao, Q. Yan, Y. Zhang, Y. Wang, & J. Zhang. 2017. Cross-species transferability of EST-SSR markers developed from the transcriptome of Melilotus and their application to population genetics research. Scientific Reports 7: 17959. https://doi.org/10.1038/s41598-017-18049-8
Zhang, W., Z. Wang, Z. Zhao, X. Zeng, H. Wu, & P. Yu. 2010. Using bioinpormcotics methods to develop EST-SSR makers from sheep’s ESTs. J. Anim. Vet. Adv. 9:2759-2762. https://doi.org/10.3923/javaa.2010.2759.2762
Authors
ManavipourM., EhsaniA., & MasoudiA. A. (2020). Application of Efficient Express Sequence Tags Information for Classification and Functional Study of Simple Sequence Repeats in Cattle Testis Tissue. Tropical Animal Science Journal, 43(1), 25-34. https://doi.org/10.5398/tasj.2020.43.1.25
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