Tandem repetitions in transcriptomes of some Solanaceae species

Atul Grover, Prakash C. Sharma

University School of Biotechnology, Guru Gobind Singh Indraprastha University, Dwarka, New Delhi, India.

DOI: 10.4236/ajmb.2012.22016                

Abstract

Characterization of occurrence, density and motif sequence of tandem repeats in the transcribed regions is helpful in understanding the functional significance of these repeats in the modern genomes. We analyzed tandem repeats present in expressed sequences of thirteen species belonging to genera Capsicum, Nicotiana, Petunia and Solanum of family Solanaceae and the genus Coffea of Rubiaceae to investigate the propagation and evolutionary sustenance of these repeats. Tandem repeat containing sequences constituted 1.58% to 7.46% of sequences analyzed. Tandem repetitions of size 2, 15, 18 and 21 bp motifs were more frequent. Repeats with unit sizes 21 and 22 bp were also abundant in genomic sequences of potato and tomato. While mutations occurring in these repeats may alter the repeat number, genomes adjust to these changes by keeping the translated products unaffected. Surprisingly, in majority of the species under study, tandem repeat motif length did not exceed 228 bp. Conserved tandem repeat motifs of sizes 180, 192 and 204 bp were also abundant in the genomic sequences. Our observations lead us to propose that these tandem repeats are actually remnants of ancestral megasatellite repeats, which have split into multiple repeats due to frequent insertions over the course of evolution.

Keywords

ESTs; Solanaceae; Tandem Repeats; Transcriptome; TRF

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Haubold, B. and Wiehe, T. (2006) How repetitive are genomes? BMC Bioinformatics, 7, 541. doi:10.1186/1471-2105-7-541
[2]	Shaprio, J.A. and Von Stanberg, R. (2005) Why repetitive DNA is essential to genome function? Biological Reviews of the Cambridge Philosophical Society, 80, 227-250. doi:10.1017/S1464793104006657
[3]	Kashi, Y. and King, D.G. (2006) Simple sequence repeats as advantageous mutators in evolution. Trends in Genetics, 22, 253-259. doi:10.1016/j.tig.2006.03.005
[4]	Piegu, B., Guyot, R., Picault, N., et al. (2006) Doubling genome size without polyploidization: Dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Research, 16, 1262-1269. doi:10.1101/gr.5290206
[5]	Navajas-Perez, R. and Patterson, A. (2009) Patterns of tandem repetition in plant whole genome assemblies. Mol Genet Genomics, 281, 579-590. doi:10.1007/s00438-009-0433-y
[6]	Sharma, P.C., Grover, A. and Kahl, G. (2007) Mining microsatellite repeats in eukaryotic genomes. Trends in Biotechnology, 25, 490-498. doi:10.1016/j.tibtech.2007.07.013
[7]	Grover, A., Aishwarya, V. and Sharma, P.C. (2007) Biased distribution of microsatellite motifs in the rice genome. Molecular Genetics and Genomics, 277, 469-480. doi:10.1007/s00438-006-0204-y
[8]	Mueller, L.A., Solow, T.H., Taylor, N., et al. (2005) The SOL Genomics Network: A comparative resource for Solanaceae biology and beyond. Plant Physiology, 138, 1310-1317. doi:10.1104/pp.105.060707
[9]	Bombarely, A., Menda, N., Tecle, I.Y., et al. (2011) The sol genomics network (solgenomics.net): Growing tomatoes using Perl. Nucleic Acids Research, 39, D1149-D1155. doi:10.1093/nar/gkq866
[10]	Huang, X. and Madan, A. (1999) CAP3: A DNA sequence assembly program. Genome Research, 9, 868-877. doi:10.1101/gr.9.9.868
[11]	Benson, G. (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Research, 27, 573-580. doi:10.1093/nar/27.2.573
[12]	Jurka, J. and Pethiyagoda, C. (1995) Simple repetitive DNA sequences from primates: compilation and analysis. Journal of Molecular Evolution, 40, 120-126. doi:10.1007/BF00167107
[13]	O’Dushlaine, C.T. and Shields, D.C. (2006) Tools for the identification of the variable and potentially variable tandem repeats. BMC Genomics, 7, 290. doi:10.1186/1471-2164-7-290
[14]	Brudno, M., Malde, S., Poliakov, A., et al. (2003) Glocal alignment: Finding rearrangements during alignment. Bioinformatics, 1, i54-i62. doi:10.1093/bioinformatics/btg1005
[15]	Frazer, K.A., Pachter, L., Poliakov, A., et al. (2004) VISTA: Computational tools for comparative genomics. Nucleic Acids Research, 32, W273-W279. doi:10.1093/nar/gkh458
[16]	Li, Y.C., Korol, A.B., Fahima, T. and Nevo, E. (2004) Microsatellites within genes: Structure, function and evolution. Molecular Biology and Evolution, 21, 991-1007. doi:10.1093/molbev/msh073
[17]	Zhang, L., Yuan, D., Yu, S., et al. (2004) Preference of simple sequence repeats in coding and non-coding regions of Arabidopsis thaliana. Bioinformatics, 20, 1081-1086. doi:10.1093/bioinformatics/bth043
[18]	Roorkiwal, M., Grover, A. and Sharma, P.C. (2009) Genome-wide analysis of conservation and divergence of microsatellites in rice. Molecular Genetics and Genomics, 282, 205-215. doi:10.1007/s00438-009-0457-3
[19]	Brock, G.J.R., Anderson, N.H. and Monckton, D.G. (1999) Cis-acting modifiers of expanded CAG/CTG triplet repeat expandability: Associations with flanking GC content and proximity to CpG islands. Human Molecular Genetics, 8, 1061-1067. doi:10.1093/hmg/8.6.1061
[20]	Ng, T.K., Lam, C.Y., Lam, D.S.C., et al. (2009) AC and AG dinucleotide repeats in the PAX6 P1 promoter are associated with high myopia. Molecular Vision, 15, 2239-2248.
[21]	Hohn, T., Corsten, S., Ricke, S. and Rothnie, H. (1996) Methylation of coding region alone inhibits gene expression in plant protoplasts. Proceedings of the National Academy of Sciences of the United States of America, 93, 8334-8339. doi:10.1073/pnas.93.16.8334
[22]	Colot, V. and Rossignol, J.L. (1999) Eukaryotic DNA methylation as an evolutionary device. BioEssays, 21, 402-411. doi:10.1002/(SICI)1521-1878(199905)21:5<402::AID-BIES7>3.0.CO;2-B
[23]	Jeong, Y.H., Kim, M.C., Ahn, E.-K., et al. (2007) Rare exonic microsatellite alleles in MUC2 influence susceptibility to gastric carcinoma. PloS One, 11, e1163. doi:10.1371/journal.pone.0001163
[24]	De Grassi, A. and Ciccarelli, F.D. (2009) Tandem repeats modify the structure of human genes hosted in segmental duplications. Genome Biology, 10, R137. doi:10.1186/gb-2009-10-12-r137
[25]	Leem, S.H., Londo?o-Vallejo, J.A., Kim, J.H., et al. (2002) The human telomerase gene: Complete genomic sequence and analysis of tandem repeat polymorphisms in intronic regions. Oncogene, 21, 769-777. doi:10.1038/sj.onc.1205122
[26]	Catania, F. and Lynch, M. (2008) Where do introns come from? PLoS Biology, 6, e283. doi:10.1371/journal.pbio.0060283
[27]	Varshney, R.K., Graner, A. and Sorrells, M.E. (2005) Genic microsatellite markers in plants: Features and applications. Trends in Biotechnology, 23, 48-54. doi:10.1016/j.tibtech.2004.11.005
[28]	Brandstorm, M., Bagshaw, A.T., Gemmell, N.J. and Ellegren, H. (2008) The relationship between microsatellite polymorphism and recombination hot spots in the human genome. Molecular Biology and Evolution, 25, 2579-2587. doi:10.1093/molbev/msn201
[29]	Sharma, S. and Raina, S.N. (2005) Organization and evolution of highly repeated satellite DNA sequences in plant chromosomes. Cytogenetic and Genome Research, 109, 15-26. doi:10.1159/000082377
[30]	Ugarkovic, D. and Plohl, M. (2002) Variation in satellite DNA profiles—Causes and effects. EMBO Journal, 21, 5955-5959.
[31]	Richard, G.-F. and Dujon, B. (2006) Molecular evolution of minisatellites in hemiascomycetous yeasts. Molecular Biology and Evolution, 23, 189-202. doi:10.1093/molbev/msj022
[32]	O’Dushlaine, C.T., Edwards, R.J., Park, S.D. and Shields, D.C. (2005) Tandem repeat copy number variation in protein-coding regions of human genes. Genome Biology, 6, R69. doi:10.1186/gb-2005-6-8-r69
[33]	Yu, F., Sabeti, P.C., Hardenbol, P., et al. (2005) Positive selection of a pre-expansion CAG repeat of the human SCA2 gene. PLoS Genetics, 1, e41. doi:10.1371/journal.pgen.0010041
[34]	Jordon, P., Snyder, L.A. and Saunders, N.J. (2003) Diversity in coding tandem repeats in related Neisseria spp. BMC Microbiology, 3, 23. doi:10.1186/1471-2180-3-23
[35]	Verstrepen, K.J., Jansen, A., Lewitter, F. and Fink, G.R. (2005) Intragenic tandem repeats generate functional variability. Nature Genetics, 37, 986-990. doi:10.1038/ng1618
[36]	Levdansky, E., Romano, J., Shadkchan, Y., et al. (2007) Coding tandem repeats generate diversity in Aspergillus fumigatus genes. Eukaryotic Cell, 6, 1380-1391. doi:10.1128/EC.00229-06
[37]	Calabrese, P.P., Durrett, R.T. and Aquadro, C.A. (2001) Dynamics of microsatellite divergence under stepwise mutation and proportional slippage/ point mutation model. Genetics, 159, 839-852.
[38]	Ohta, T. and Kimura, M. (1973) A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population. Genetics Research, 22, 201-204. doi:10.1017/S0016672300012994
[39]	Naamati, G., Fromer, M. and Linial, M. (2009) Expansion of tandem repeats in sea anemone Nematostella vectensis proteome: A source for gene novelty? BMC Genomics, 10, 593. doi:10.1186/1471-2164-10-593
[40]	Trifonov, E.N. (2003) Tuning function of tandemly repeating sequences: A molecular device for fast adaptation. In: Wasser, S.P., Ed., Evolutionary Theory and Processes: Modern Horizons, Papers in Honour of Eviatar Nevo. Kluwer Academic Publishers, Amsterdam, 1-24.
[41]	Fujimori, S., Washio, T., Higo, K., et al. (2003) A novel feature of microsatellites in plants: A distribution gradient along the direction of transcription. FEBS Letters, 554, 17-22. doi:10.1016/S0014-5793(03)01041-X
[42]	Kashi, Y., King, D. and Soller, M. (1997) Simple sequence repeats as a source of quantitative genetic variation. Trends in Genetics, 13, 74-78. doi:10.1016/S0168-9525(97)01008-1
[43]	Richard, G.F., Kerrest, A. and Dujon, B. (2008) Comparative genomics and molecular dynamics of DNA repeats in eukaryotes. Microbiology and Molecular Biology Reviews, 72, 686-727. doi:10.1128/MMBR.00011-08
[44]	Kloss, E., Courtemanche, N. and Barrick, D. (2008) Repeat-protein folding: New insights into origins of cooperativity, stability, and topology. Archives of Biochemistry and Biophysics, 469, 83-99. doi:10.1016/j.abb.2007.08.034
[45]	Hancock, J.M. and Simon, M. (2005) Simple sequence repeats in proteins and their significance for network evolution. Gene, 345, 113-118. doi:10.1016/j.gene.2004.11.023
[46]	Marcotte, E.M., Pellegrini, M., Yeates, T.O. and Eisenberg, D. (1999) A census of protein repeats. Journal of Molecular Biology, 293, 151-160. doi:10.1006/jmbi.1999.3136
[47]	Gangloff, S., Zou, H. and Rothstein, R. (1996) Gene conversion plays the major role in controlling the stability of large tandem repeats in yeast. EMBO Journal, 15, 1715-1725.
[48]	Vergnaud, G. and Denoeud, F. (2000) Minisatellites: Mutability and genome architecture. Genome Research, 10, 899-907. doi:10.1101/gr.10.7.899
[49]	Armour, J.A., Povey, S., Jeremiah, S. and Jeffreys, A.J. (1990) Systematic cloning of human minisatellites from ordered array charomid libraries. Genomics, 8, 501-512. doi:10.1016/0888-7543(90)90037-U
[50]	Denoeud, F., Vergnaud, G. and Benson, G. (2003) Predicting human minisatellite polymorphism. Genome Research, 13, 856-867. doi:10.1101/gr.574403