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Extensive tRNA Gene Changes in Synthetic Brassica napus

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Abstract

Allopolyploidization, where two species come together to form a new species, plays a major role in speciation and genome evolution. Transfer RNAs (abbreviated tRNA) are typically 73–94 nucleotides in length, and are indispensable in protein synthesis, transferring amino acids to the cell protein synthesis machinery (ribosome). To date, the regularity and function of tRNA gene sequence variation during the process of allopolyploidization have not been well understood. In this study, the inter-tRNA gene corresponding to tRNA amplification polymorphism method was used to detect changes in tRNA gene sequences in the progeny of interspecific hybrids between Brassica rapa and B. oleracea, mimicking the original B. napus (canola) species formation event. Cluster analysis showed that tRNA gene variation during allopolyploidization did not appear to have a genotypic basis. Significant variation occurred in the early generations of synthetic B. napus (F1 and F2 generations), but fewer alterations were observed in the later generation (F3). The variation-prone tRNA genes tended to be located in AT-rich regions. BlastN analysis of novel tRNA gene variants against a Brassica genome sequence database showed that the variation of these tRNA-gene-associated sequences in allopolyploidization might result in variation of gene structure and function, e.g., metabolic process and transport.

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References

  • Albertin W, Balliau T, Brabant P, Chevre AM, Eber F, Malosse C, Thiellement H (2006) Numerous and rapid nonstochastic modifications of gene products in newly synthesized Brassica napus allotetraploids. Genetics 173:1101–1113

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Albertin W, Alix K, Balliau T, Brabant P, Davanture M, Malosse C, Valot B, Thiellement H (2007) Differential regulation of gene products in newly synthesized Brassica napus allotetraploids is not related to protein function nor subcellular localization. BMC Genomics 8:56

    Article  PubMed Central  PubMed  Google Scholar 

  • An Z, Tang Z, Ma B, Mason AS, Guo Y, Yin J, Gao C, Wei L, Li J, Fu D (2013) Transposon variation by order during allopolyploidisation between Brassica oleracea and Brassica rapa. Plant Biol. doi:10.1111/plb.12121

  • Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol 58:377–406

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cheng F, Liu S, Wu J, Fang L, Sun S, Liu B, Li P, Hua W, Wang X (2011) BRAD, the genetics and genomics database for Brassica plants. BMC Plant Biol 11:136

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cheng F, Mandakova T, Wu J, Xie Q, Lysak MA, Wang X (2013) Deciphering the diploid ancestral genome of the Mesohexaploid Brassica rapa. Plant Cell 25:1541–1554

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Conesa A, Gotz S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008:619832

    Article  PubMed Central  PubMed  Google Scholar 

  • Dong ZY, Wang HY, Dong YZ, Wang YM, Liu W, Miao GJ, Lin XY, Wang DQ, Liu B (2013) Extensive microsatellite variation in rice induced by introgression from wild rice (Zizania latifolia Griseb.). PLoS ONE 8:e62317

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Edmands S, Feaman HV, Harrison JS, Timmerman CC (2005) Genetic consequences of many generations of hybridization between divergent copepod populations. J Hered 96:114–123

    Article  CAS  PubMed  Google Scholar 

  • Erickson DL, Fenster CB (2006) Intraspecific hybridization and the recovery of fitness in the native legume Chamaecrista fasciculata. Evolution 60:225–233

    Article  PubMed  Google Scholar 

  • Feldman M, Levy AA (2005) Allopolyploidy—a shaping force in the evolution of wheat genomes. Cytogenet Genome Res 109:250–258

    Article  CAS  PubMed  Google Scholar 

  • Feldman M, Levy AA (2009) Genome evolution in allopolyploid wheat—a revolutionary reprogramming followed by gradual changes. J Genet Genomics 36:511–518

    Article  CAS  PubMed  Google Scholar 

  • Gaeta RT, Pires JC, Iniguez-Luy F, Leon E, Osborn TC (2007) Genomic changes in resynthesized Brassica napus and their effect on gene expression and phenotype. Plant Cell 19:3403–3417

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Goodenbour JM, Pan T (2006) Diversity of tRNA genes in eukaryotes. Nucleic Acids Res 34:6137–6146

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ha M, Lu J, Tian L, Ramachandran V, Kasschau KD, Chapman EJ, Carrington JC, Chen XM, Wang XJ, Chen ZJ (2009) Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. Proc Natl Acad Sci USA 106:17835–17840

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Hegarty MJ, Barker GL, Wilson ID, Abbott RJ, Edwards KJ, Hiscock SJ (2006) Transcriptome shock after interspecific hybridization in senecio is ameliorated by genome duplication. Curr Biol 16:1652–1659

    Article  CAS  PubMed  Google Scholar 

  • Hwang AS, Northrup SL, Alexander JK, Vo KT, Edmands S (2011) Long-term experimental hybrid swarms between moderately incompatible Tigriopus californicus populations: hybrid inferiority in early generations yields to hybrid superiority in later generations. Conserv Genet 12:895–909

    Article  Google Scholar 

  • Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS, Soltis DE, Clifton SW, Schlarbaum SE, Schuster SC, Ma H, Leebens-Mack J, dePamphilis CW (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473:97–100

    Article  CAS  PubMed  Google Scholar 

  • Kenan-Eichler M, Leshkowitz D, Tal L, Noor E, Melamed-Bessudo C, Feldman M, Levy AA (2011) Wheat hybridization and polyploidization results in deregulation of small RNAs. Genetics 188:263–272

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Leitch AR, Leitch IJ (2008) Genomic plasticity and the diversity of polyploid plants. Science 320:481–483

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Heneen WK (1999) Production and cytogenetics of intergeneric hybrids between the three cultivated Brassica diploids and Orychophragmus violaceus. Theor Appl Genet 99:694–704

    Article  CAS  PubMed  Google Scholar 

  • Lim KY, Soltis DE, Soltis PS, Tate J, Matyasek R, Srubarova H, Kovarik A, Pires JC, Xiong Z, Leitch AR (2008) Rapid chromosome evolution in recently formed polyploids in Tragopogon (Asteraceae). PLoS ONE 3:e3353

    Article  PubMed Central  PubMed  Google Scholar 

  • Lukens LN, Pires JC, Leon E, Vogelzang R, Oslach L, Osborn T (2006) Patterns of sequence loss and cytosine methylation within a population of newly resynthesized Brassica napus allopolyploids. Plant Physiol 140:336–348

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Madlung A, Wendel JF (2013) Genetic and epigenetic aspects of polyploid evolution in plants. Cytogenet Genome Res 140:270–285

    Article  CAS  PubMed  Google Scholar 

  • Mallet J (2007) Hybrid speciation. Nature 446:279–283

    Article  CAS  PubMed  Google Scholar 

  • Marin MA, Lopez A, Uribe SI (2012) Interspecific variation in mitochondrial serine transfer RNA (UCN) in Euptychiina butterflies (Lepidoptera: Satyrinae): structure and alignment. Mitochondrial DNA 23:208–215

    Article  CAS  PubMed  Google Scholar 

  • Marmagne A, Brabant P, Thiellement H, Alix K (2010) Analysis of gene expression in resynthesized Brassica napus allotetraploids: transcriptional changes do not explain differential protein regulation. N Phytol 186:216–227

    Article  CAS  Google Scholar 

  • McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801

    Article  CAS  PubMed  Google Scholar 

  • Michaud M, Cognat V, Duchene AM, Marechal-Drouard L (2011) A global picture of tRNA genes in plant genomes. Plant J 66:80–93

    Article  CAS  PubMed  Google Scholar 

  • Negron-Ortiz V (2007) Chromosome numbers, nuclear DNA content, and polyploidy in Consolea (Cactaceae), an endemic cactus of the Caribbean Islands. Am J Bot 94:1360–1370

    Article  PubMed  Google Scholar 

  • Nicolas SD, Le Mignon G, Eber F, Coriton O, Monod H, Clouet V, Huteau V, Lostanlen A, Delourme R, Chalhoub B, Ryder CD, Chevre AM, Jenczewski E (2007) Homeologous recombination plays a major role in chromosome rearrangements that occur during meiosis of Brassica napus haploids. Genetics 175:487–503

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Osborn TC, Pires JC, Birchler JA, Auger DL, Chen ZJ, Lee HS, Comai L, Madlung A, Doerge RW, Colot V, Martienssen RA (2003) Understanding mechanisms of novel gene expression in polyploids. Trends Genet 19:141–147

    Article  CAS  PubMed  Google Scholar 

  • Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34:401–437

    Article  CAS  PubMed  Google Scholar 

  • Pires JC, Zhao JW, Schranz ME, Leon EJ, Quijada PA, Lukens LN, Osborn TC (2004) Flowering time divergence and genomic rearrangements in resynthesized Brassica polyploids (Brassicaceae). Biol J Linn Soc 82:675–688

    Article  Google Scholar 

  • Pontes O, Neves N, Silva M, Lewis MS, Madlung A, Comai L, Viegas W, Pikaard CS (2004) Chromosomal locus rearrangements are a rapid response to formation of the allotetraploid Arabidopsis suecica genome. Proc Natl Acad Sci USA 101:18240–18245

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Randau L, Soll D (2008) Transfer RNA genes in pieces. EMBO Rep 9:623–628

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Röbbelen G (1960) Contributions to the analysis of the Brassica-genome. Chromosoma 11:205–228

    Article  Google Scholar 

  • Rogers SO, Bendich AJ (1985) Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. Plant Mol Biol 5:69–76

    Article  CAS  PubMed  Google Scholar 

  • Rohlf FJ (1998) NTSYSpc: numerical taxonomy and multivariate analysis system, version 2.01. Department of Ecology and Evolution, State University of New York

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    CAS  PubMed  Google Scholar 

  • Saks ME, Sampson JR (1995) Evolution of tRNA recognition systems and tRNA gene sequences. J Mol Evol 40:509–518

    Article  CAS  PubMed  Google Scholar 

  • Sarilar V, Palacios PM, Rousselet A, Ridel C, Falque M, Eber F, Chevre AM, Joets J, Brabant P, Alix K (2013) Allopolyploidy has a moderate impact on restructuring at three contrasting transposable element insertion sites in resynthesized Brassica napus allotetraploids. N Phytol 198:593–604

    Article  CAS  Google Scholar 

  • Schattner P, Brooks AN, Lowe TM (2005) The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33:W686–W689

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schranz ME, Osborn TC (2004) De novo variation in life-history traits and responses to growth conditions of resynthesized polyploid Brassica napus (Brassicaceae). Am J Bot 91:174–183

    Article  PubMed  Google Scholar 

  • Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27:431–432

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Song K, Lu P, Tang K, Osborn TC (1995) Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. Proc Natl Acad Sci USA 92:7719–7723

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sun FJ, Caetano-Anolles G (2008a) Evolutionary patterns in the sequence and structure of transfer RNA: a window into early translation and the genetic code. PLoS ONE 3:e2799

    Article  PubMed Central  PubMed  Google Scholar 

  • Sun FJ, Caetano-Anolles G (2008b) The origin and evolution of tRNA inferred from phylogenetic analysis of structure. J Mol Evol 66:21–35

    Article  CAS  PubMed  Google Scholar 

  • Sun FJ, Caetano-Anolles G (2008c) Transfer RNA and the origins of diversified life. Sci Prog 91:265–284

    Article  CAS  PubMed  Google Scholar 

  • Szadkowski E, Eber F, Huteau V, Lode M, Huneau C, Belcram H, Coriton O, Manzanares-Dauleux MJ, Delourme R, King GJ, Chalhoub B, Jenczewski E, Chevre AM (2010) The first meiosis of resynthesized Brassica napus, a genome blender. N Phytol 186:102–112

    Article  CAS  Google Scholar 

  • Szadkowski E, Eber F, Huteau V, Lode M, Coriton O, Jenczewski E, Chevre AM (2011) Polyploid formation pathways have an impact on genetic rearrangements in resynthesized Brassica napus. N Phytol 191:884–894

    Article  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Udall JA, Quijada PA, Osborn TC (2005) Detection of chromosomal rearrangements derived from homeologous recombination in four mapping populations of Brassica napus L. Genetics 169:967–979

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Widmann J, Di Giulio M, Yarus M, Knight R (2005) tRNA creation by hairpin duplication. J Mol Evol 61:524–530

    Article  CAS  PubMed  Google Scholar 

  • Xiong Z, Gaeta RT, Pires JC (2011) Homeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus. Proc Natl Acad Sci USA 108:7908–7913

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xu Y, Zhong L, Wu X, Fang X, Wang J (2009) Rapid alterations of gene expression and cytosine methylation in newly synthesized Brassica napus allopolyploids. Planta 229:471–483

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Ge X, Shao Y, Sun G, Li Z (2013) Genomic change, retrotransposon mobilization and extensive cytosine methylation alteration in Brassica napus introgressions from two intertribal hybridizations. PLoS ONE 8:e56346

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zou J, Fu D, Gong H, Qian W, Xia W, Pires JC, Li R, Long Y, Mason AS, Yang TJ, Lim YP, Park BS, Meng J (2011) De novo genetic variation associated with retrotransposon activation, genomic rearrangements and trait variation in a recombinant inbred line population of Brassica napus derived from interspecific hybridization with Brassica rapa. Plant J 68:212–224

    Article  CAS  PubMed  Google Scholar 

  • Zuo Z, Peng D, Yin X, Zhou X, Cheng H, Zhou R (2013) Genome-wide analysis reveals origin of transfer RNA genes from tRNA halves. Mol Biol Evol. doi:10.1093/molbev/mst107

    PubMed  Google Scholar 

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Acknowledgments

This work was supported financially by National Natural Science Foundation of China (code 31260335), and Jiangxi Science and Technology Support Program (code 20132BBF60013). Annaliese S. Mason is supported by an Australian Research Council Discovery Early Career Researcher Award (DE120100668).

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Authors and Affiliations

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

    Lijuan Wei, Meili Xiao, Jiaming Yin & Jiana Li

  2. Key Laboratory of Crop Physiology, Ecology and Genetic Breeding, Ministry of Education, Agronomy College, Jiangxi Agricultural University, Nanchang, 330045, China

    Lijuan Wei & Donghui Fu

  3. Crops Research Institute, Gansu Academy of Agricultural Sciences, Lanzhou, 730070, Gansu, China

    Zeshan An

  4. Centre for Integrative Legume Research, School of Agriculture and Food Sciences, The University of Queensland, Brisbane, 4072, Australia

    Annaliese S. Mason

  5. Wheat Research Institute, Gansu Academy of Agricultural Sciences, Lanzhou, 730070, Gansu, China

    Ying Guo

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  1. Lijuan Wei
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  2. Zeshan An
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  3. Annaliese S. Mason
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  4. Meili Xiao
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  8. Donghui Fu
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Correspondence to Donghui Fu.

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Lijuan Wei and Zeshan An have contributed equally to this study.

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Supplementary Table 1

tRNA-gene-associated sequence information (PDF 215 kb)

Supplementary Table 2

Homologous sequence and 100 bp flanking sequences of tRNA genes (PDF 230 kb)

Supplementary Table 3

Alignments between tRNA-gene-associated sequences and genes in Brassica rapa and Brassica oleracea (PDF 161 kb)

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Wei, L., An, Z., Mason, A.S. et al. Extensive tRNA Gene Changes in Synthetic Brassica napus . J Mol Evol 78, 38–49 (2014). https://doi.org/10.1007/s00239-013-9598-4

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