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Characterization and comparison of gene-based simple sequence repeats across Brassica species

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Abstract

Simple sequence repeats (SSRs) are important components of eukaryotic genomes and may play an important role in regulating gene expression. However, the characteristics of genic SSRs and the effect of interspecific hybridization and polyploidization on genic SSRs seem not to have received desired attention in terms of scientific investigations. To determine the features of genic SSRs and elucidate their role in polyploidization process of the Brassica family, we identified SSRs in Plant Genome Database-assembled unique transcripts (PUTs) of Brassica species. A higher density of SSRs and a greater number of compound motif SSRs and mononucleotide motif types with large average number of repeats were detected in allotetraploid Brassica napus than in the diploid parental species (Brassica rapa and Brassica oleracea). In addition, a greater proportion of SSR-PUTs were found to be associated with the stress response and developmental processes in B. napus than in the parents. A negative correlation between the repeat number and the motif type and the total length, and a positive correlation between the repeat number and the total length of SSRs were observed. PUT-SSR might be generated from A/T-rich regions. The successful development of 123 pairs of SSR primers for Brassica PUTs showed that SSR-PUTs could be exploited as gene-based SSR functional markers for application in Brassica breeding. These results indicate that interspecific hybridization and polyploidization could trigger the amplification of SSRs, and long SSRs might become shorter to enable the plant to adapt to environmental and artificial selection.

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Abbreviations

DH:

Doubled haploid

GO:

Gene ontology

PUTs:

Plant genome database assembled unique transcripts

SSR:

Simple sequence repeats

References

  • Allen GC, Flores-Vergara MA, Krasnyanski S, Kumar S, Thompson WF (2006) A modified protocol for rapid DNA isolation from plant tissues using cetyltrimethylammonium bromide. Nat Protoc 1:2320–2325

    Article  PubMed  CAS  Google Scholar 

  • Anmarkrud JA, Kleven O, Bachmann L, Lifjeld JT (2008) Microsatellite evolution: mutations, sequence variation, and homoplasy in the hypervariable avian microsatellite locus HrU10. BMC Evol Biol 8:138–148

    Article  PubMed  Google Scholar 

  • Ashburner M, Lewis S (2002) On ontologies for biologists: the gene ontology—untangling the web. Novart Fdn Symp 247:66–83

    Article  CAS  Google Scholar 

  • Asp T, Frei UK, Didion T, Nielsen KK, Lubberstedt T (2007) Frequency, type, and distribution of EST-SSRs from three genotypes of Lolium perenne, and their conservation across orthologous sequences of Festuca arundinacea, Brachypodium distachyon, and Oryza sativa. BMC Plant Biol 7:35–47

    Article  Google Scholar 

  • da Maia LC, Palmieri DA, de Souza VQ, Kopp MM, de Carvalho FI, Costa de Oliveira A (2008) SSR locator: tool for simple sequence repeat discovery integrated with primer design and pcr simulation. Int J Plant Genomics 2008:412–696

    Google Scholar 

  • da Maia LC, de Souza VQ, Kopp MM, de Carvalho FIF, de Oliveira AC (2009) Tandem repeat distribution of gene transcripts in three plant families. Genet Mol Biol 32:822–833

    Article  PubMed  CAS  Google Scholar 

  • Depeiges A, Farget S, Degroote F, Picard G (2005) A new transgene assay to study microsatellite instability in wild-type and mismatch-repair defective plant progenies. Plant Sci 168:939–947

    Article  CAS  Google Scholar 

  • Dettman JR, Taylor JW (2004) Mutation and evolution of microsatellite loci in neurospora. Genetics 168:1231–1248

    Article  PubMed  CAS  Google Scholar 

  • Fujimori S, Washio T, Higo K, Ohtomo Y, Murakami K, Matsubara K, Kawai J, Carninci P, Hayashizaki Y, Kikuchi S, Tomita M (2003) A novel feature of microsatellites in plants: a distribution gradient along the direction of transcription. Febs Lett 554:17–22

    Article  PubMed  CAS  Google Scholar 

  • Gao H, Cai SL, Yan BL, Chen BY, Yu F (2009) Discrepancy variation of dinucleotide microsatellite repeats in eukaryotic genomes. Biol Res 42:365–375

    Article  PubMed  CAS  Google Scholar 

  • Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hong CP, Piao ZY, Kang TW, Batley J, Yang TJ, Hur YK, Bhak J, Park BS, Edwards D, Lim YP (2007) Genomic distribution of simple sequence repeats in Brassica rapa. Mol Cells 23:349–356

    PubMed  CAS  Google Scholar 

  • Iniguez-Luy FL, Voort AV, Osborn TC (2008) Development of a set of public SSR markers derived from genomic sequence of a rapid cycling Brassica oleracea L. genotype. Theor Appl Genet 117:977–985

    Article  PubMed  CAS  Google Scholar 

  • Institute S (1996) SAS Users Guide: Statistic. SAS Institute Cary, NC

  • Jiang D, Zhong GY, Hong QB (2006) Analysis of microsatellites in citrus unigenes. Yi Chuan Xue Bao 33:345–353

    PubMed  CAS  Google Scholar 

  • Kashi Y, King DG (2006) Simple sequence repeats as advantageous mutators in evolution. Trends Genet 22:253–259

    Article  PubMed  CAS  Google Scholar 

  • Kawase D, Ueno S, Tsumura Y, Tomaru N, Seo A, Yumoto T (2009) Development and characterization of EST-SSR markers for Sciadopitys verticillata (Sciadopityaceae). Conserv Genet 10:1997–1999

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Lai Y, Sun F (2003) The relationship between microsatellite slippage mutation rate and the number of repeat units. Mol Biol Evol 20:2123–2131

    Article  PubMed  CAS  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  Google Scholar 

  • Levinson G, Gutman GA (1987) Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol 4:203–221

    PubMed  CAS  Google Scholar 

  • Li YC, Korol AB, Fahima T, Beiles A, Nevo E (2002) Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol Ecol 11:2453–2465

    Article  PubMed  CAS  Google Scholar 

  • Li YC, Fahima T, Roder MS, Kirzhner VM, Beiles A, Korol AB, Nevo E (2003) Genetic effects on microsatellite diversity in wild emmer wheat (Triticum dicoccoides) at the Yehudiyya microsite, Israel. Heredity 90:150–156

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Liu JX, Ely B (2009) Complex evolution of a highly conserved microsatellite locus in several fish species. J Fish Biol 75:442–447

    Article  PubMed  Google Scholar 

  • Martin P, Makepeace K, Hill SA, Hood DW, Moxon ER (2005) Microsatellite instability regulates transcription factor binding and gene expression. Proc Natl Acad Sci USA 102:3800–3804

    Article  PubMed  CAS  Google Scholar 

  • McConnell R, Middlemist S, Scala C, Strassmann JE, Queller DC (2007) An unusually low microsatellite mutation rate in Dictyostelium discoideum, an organism with unusually abundant microsatellites. Genetics 177:1499–1507

    Article  PubMed  CAS  Google Scholar 

  • Moe KT, Chung JW, Cho YI, Moon JK, Ku JH, Jung JK, Lee J, Park YJ (2011) Sequence information on simple sequence repeats and single nucleotide polymorphisms through transcriptome analysis of mungbean. J Integr Plant Biol 53:63–73

    Article  PubMed  CAS  Google Scholar 

  • Muir G, Schlotterer C (2005) Evidence for shared ancestral polymorphism rather than recurrent gene flow at microsatellite loci differentiating two hybridizing oaks (Quercus spp.). Mol Ecol 14:549–561

    Article  PubMed  CAS  Google Scholar 

  • Nagaharu U (1935) Genome analysis in Brassica with special reference to the experimental formation of B.napus and peculiar mode of fertilization. Japan J Bot 7:389–452

    Google Scholar 

  • Nevo E, Beharav A, Meyer RC, Hackett CA, Forster BP, Russell JR, Powell W (2005) Genomic microsatellite adaptive divergence of wild barley by microclimatic stress in ‘Evolution Canyon’, Israel. Bio J Linn Soc 84:205–224

    Article  Google Scholar 

  • Parida SK, Yadava DK, Mohapatra T (2010) Microsatellites in Brassica unigenes: relative abundance, marker design, and use in comparative physical mapping and genome analysis. Genome 53:55–67

    Article  PubMed  CAS  Google Scholar 

  • Riley DE, Krieger JN (2009) UTR dinucleotide simple sequence repeat evolution exhibits recurring patterns including regulatory sequence motif replacements. Gene 429:80–86

    Article  PubMed  CAS  Google Scholar 

  • Rocha EP, Matic I, Taddei F (2002) Over-representation of repeats in stress response genes: a strategy to increase versatility under stressful conditions? Nucleic Acids Res 30:1886–1894

    Article  PubMed  CAS  Google Scholar 

  • Sharma RK, Bhardwaj P, Negi R, Mohapatra T, Ahuja PS (2009) Identification characterization and utilization of unigene derived microsatellite markers in tea (Camellia sinensis L.). BMC Plant Biol 9:53–76

    Article  PubMed  Google Scholar 

  • Subramanian S, Madgula VM, George R, Kumar S, Pandit MW, Singh L (2003) SSRD: simple sequence repeats database of the human genome. Comp Funct Genome 4:342–345

    Article  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Tang Z, Fu S, Ren Z, Zou Y (2009) Rapid evolution of simple sequence repeat induced by allopolyploidization. J Mol Evol 69:217–228

    Article  PubMed  CAS  Google Scholar 

  • Thuillet AC, Bataillon T, Sourdille P, David JL (2004) Factors affecting polymorphism at microsatellite loci in bread wheat [Triticum aestivum (L.) Thell]: effects of mutation processes and physical distance from the centromere. Theor Appl Genet 108:368–377

    Article  PubMed  CAS  Google Scholar 

  • Ueno S, Taguchi Y, Tsumura Y (2008) Microsatellite markers derived from Quercus mongolica var. crispula (Fagaceae) inner bark expressed sequence tags. Genes Genet Syst 83:179–187

    Article  PubMed  CAS  Google Scholar 

  • Vigouroux Y, Jaqueth JS, Matsuoka Y, Smith OS, Beavis WD, Smith JS, Doebley J (2002) Rate and pattern of mutation at microsatellite loci in maize. Mol Biol Evol 19:1251–1260

    PubMed  CAS  Google Scholar 

  • Vigouroux Y, Matsuoka Y, Doebley J (2003) Directional evolution for microsatellite size in maize. Mol Biol Evol 20:1480–1483

    Article  PubMed  CAS  Google Scholar 

  • Zhang LD, Yuan DJ, Yu SW, Li ZG, Cao YF, Miao ZQ, Qian HM, Tang KX (2004) Preference of simple sequence repeats in coding and non-coding regions of Arabidopsis thaliana. Bioinformatics 20:1081–1086

    Article  PubMed  CAS  Google Scholar 

  • Zhang LD, Zuo KJ, Zhang F, Cao YF, Wang J, Zhang YD, Sun XF, Tang KX (2006) Conservation of noncoding microsatellites in plants: implication for gene regulation. BMC Genomics 7:323–336

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported financially by grants from the Fundamental Research Funds for the Central Universities, National Natural Science Foundation of China (code: 31071450) and National Science and Technology Ministry (code: 2009BADA8B01). We thank Doctor Qiu Xiao in Saskatchewan University, Saskatoon Canada and Doctor Joe Dise in Southwest University, Chongqing China for editing the manuscript.

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Authors and Affiliations

  1. Chongqing Engineering Research Center for Rapeseed, College of Agronomy and Biotechnology, Southwest University, Chongqing, 400716, China

    Caihua Gao, Zhanglin Tang, Jiaming Yin, Zeshan An, Donghui Fu & Jiana Li

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  1. Caihua Gao
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  2. Zhanglin Tang
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  3. Jiaming Yin
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  4. Zeshan An
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  5. Donghui Fu
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Correspondence to Donghui Fu or Jiana Li.

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Communicated by Y. Van de Peer.

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Gao, C., Tang, Z., Yin, J. et al. Characterization and comparison of gene-based simple sequence repeats across Brassica species. Mol Genet Genomics 286, 161–170 (2011). https://doi.org/10.1007/s00438-011-0636-x

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  • DOI: https://doi.org/10.1007/s00438-011-0636-x

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