Molecular characterization of the piggyBac-like element, a candidate marker for phylogenetic research of Chilo suppressalis (Walker) in China

BMC Molecular Biology

Ji-Chao Fang³  Lu Qian²  Bao-Sheng Liu³  Zhi-Chun Zhang³  Min Wu¹  Qiong Yang³  Hui-Fang Guo³  Zhao-Jun Han¹  Xiao-Huan Li³  Guang-Hua Luo³ 

[1] Education Ministry Key Laboratory of Integrated Management of Crop Diseases and Pests, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China;Jiangsu Entry-Exit Inspection and Quarantine Bureau, Nanjing 210001, China;Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, China

关键词: Chilo suppressalis;    Evolution;    Molecular characterization;    piggyBac;    Transposon;   

Others  :  1090148
DOI  :  10.1186/s12867-014-0028-y

 received in 2014-11-19, accepted in 2014-12-08,  发布年份 2014

【 摘 要 】

Background

Transposable elements (TEs, transposons) are mobile genetic DNA sequences. TEs can insert copies of themselves into new genomic locations and they have the capacity to multiply. Therefore, TEs have been crucial in the shaping of hosts’ current genomes. TEs can be utilized as genetic markers to study population genetic diversity. The rice stem borer Chilo suppressalis Walker is one of the most important insect pests of many subtropical and tropical paddy fields. This insect occurs in all the rice-growing areas in China. This research was carried out in order to find diversity between C. suppressalis field populations and detect the original settlement of C. suppressalis populations based on the piggyBac-like element (PLE). We also aim to provide insights into the evolution of PLEs in C. suppressalis and the phylogeography of C. suppressalis.

Results

Here we identify a new piggyBac-like element (PLE) in the rice stem borer Chilo suppressalis Walker, which is called CsuPLE1.1 (GenBank accession no. JX294476). CsuPLE1.1 is transcriptionally active. Additionally, the CsuPLE1.1 sequence varied slightly between field populations, with polymorphic indels (insertion/deletion) and hyper-variable regions including the identification of the 3′ region outside the open reading frame (ORF). CsuPLE1.1 insertion frequency varied between field populations. Sequences variation was found between CsuPLE1 copies and varied within and among field populations. Twenty-one different insertion sites for CsuPLE1 copies were identified with at least two insertion loci found in all populations.

Conclusions

Our results indicate that the initial invasion of CsuPLE1 into C. suppressalis occurred before C. suppressalis populations spread throughout China, and suggest that C. suppressalis populations have a common ancestor in China. Additionally, the lower reaches of the Yangtze River are probably the original settlement of C. suppressalis in China. Finally, the CsuPLE1 insertion site appears to be a candidate marker for phylogenetic research of C. suppressalis.

【 授权许可】

   
2014 Luo et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Sarkar A, Sim C, Hong YS, Hogan JR, Fraser MJ, Robertson HM, Collins FH: Molecular evolutionary analysis of the widespread piggyBac transposon family and related “domesticated” sequences. Mol Genet Genomics 2003, 270(2):173-180.
• [2]Feschotte C, Pritham EJ: DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 2007, 41:331-368.
• [3]Langley CH, Montgomery E, Hudson R, Kaplan N, Charlesworth B: On the role of unequal exchange in the containment of transposable element copy number. Genet Res 1988, 52(3):223-235.
• [4]Kazazian HH Jr: Mobile elements: drivers of genome evolution. Science 2004, 303(5664):1626-1632.
• [5]Oliver KR, Greene WK: Transposable elements: powerful facilitators of evolution. Bioessays 2009, 31(7):703-714.
• [6]Feschotte C: Transposable elements and the evolution of regulatory networks. Nat Rev Genet 2008, 9(5):397-405.
• [7]Finnegan DJ: Transposable elements. Curr Opin Genet Dev 1992, 2(6):861-867.
• [8]Fraser MJ, Smith GE, Summers MD: Acquisition of host cell DNA sequences by baculoviruses: relationship between host DNA Insertions and FP mutants of autographa californica and galleria mellonella nuclear polyhedrosis viruses. J Virol 1983, 47(2):287-300.
• [9]Cary LC, Goebel M, Corsaro BG, Wang HG, Rosen E, Fraser MJ: Transposon mutagenesis of baculoviruses: analysis of Trichoplusia ni transposon IFP2 insertions within the FP-locus of nuclear polyhedrosis viruses. Virology 1989, 172(1):156-169.
• [10]Fraser MJ, Ciszczon T, Elick T, Bauser C: Precise excision of TTAA-specific lepidopteran transposons piggyBac (IFP2) and tagalong (TFP3) from the baculovirus genome in cell lines from two species of Lepidoptera. Insect Mol Biol 1996, 5(2):141-151.
• [11]Zimowska GJ, Handler AM: Highly conserved piggyBac elements in noctuid species of Lepidoptera. Insect Biochem Mol Biol 2006, 36(5):421-428.
• [12]Xu HF, Xia QY, Liu C, Cheng TC, Zhao P, Duan J, Zha XF, Liu SP: Identification and characterization of piggyBac-like elements in the genome of domesticated silkworm, Bombyx mori. Mol Genet Genomics 2006, 276(1):31-40.
• [13]Wang J, Miller ED, Simmons GS, Miller TA, Tabashnik BE, Park Y: piggyBac-like elements in the pink bollworm, Pectinophora gossypiella. Insect Mol Biol 2010, 19(2):177-184.
• [14]Wu M, Sun Z, Luo G, Hu C, Zhang W, Han Z: Cloning and characterization of piggyBac-like elements in lepidopteran insects. Genetica 2011, 139(1):149-154.
• [15]Luo GH, Wu M, Wang XF, Zhang W, Han ZJ: A new active piggyBac-like element in Aphis gossypii. Insect Sci 2011, 18(6):652-662.
• [16]Sheng C, Wang H, Sheng S, Gao L, Xuan W: Pest status and loss assessment of crop damage caused by the rice borers, Chilo suppressalis and Tryporyza incertulas in China. Entomol Knowl 2003, 40(4):289-294.
• [17]Ding S, Wu X, Li G, Han M, Zhuang Y, Xu T: Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell 2005, 122(3):473-483.
• [18]Hikosaka A, Kobayashi T, Saito Y, Kawahara A: Evolution of the Xenopus piggyBac transposon family TxpB: domesticated and untamed strategies of transposon subfamilies. Mol Biol Evol 2007, 24(12):2648-2656.
• [19]Wu M, Sun ZC, Hu CL, Zhang GF, Han ZJ: An active piggyBac-like element in Macdunnoughia crassisigna. Insect Sci 2008, 15(6):521-528.
• [20]Deceliere G, Charles S, Biemont C: The dynamics of transposable elements in structured populations. Genetics 2005, 169(1):467-474.
• [21]Wang J, Ren X, Miller TA, Park Y: piggyBac-like elements in the tobacco budworm, Heliothis virescens (Fabricius). Insect Mol Biol 2006, 15(4):435-443.
• [22]Garcia Guerreiro MP, Fontdevila A: The evolutionary history of Drosophila buzzatii. XXXVI. Molecular structural analysis of Osvaldo retrotransposon insertions in colonizing populations unveils drift effects in founder events. Genetics 2007, 175(1):301-310.
• [23]Bui QT, Delauriere L, Casse N, Nicolas V, Laulier M, Chenais B: Molecular characterization and phylogenetic position of a new mariner-like element in the coastal crab, Pachygrapsus marmoratus. Gene 2007, 396(2):248-256.
• [24]Lippman Z, May B, Yordan C, Singer T, Martienssen R: Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification. PLoS Biol 2003, 1(3):E67.
• [25]Tran RK, Zilberman D, de Bustos C, Ditt RF, Henikoff JG, Lindroth AM, Delrow J, Boyle T, Kwong S, Bryson TD, Jacobsen SE, Henikoff S: Chromatin and siRNA pathways cooperate to maintain DNA methylation of small transposable elements in Arabidopsis. Genome Biol 2005, 6(11):R90. BioMed Central Full Text
• [26]Castro JP, Carareto CM: Drosophila melanogaster P transposable elements: mechanisms of transposition and regulation. Genetica 2004, 121(2):107-118.
• [27]Wang J, Du Y, Wang S, Brown SJ, Park Y: Large diversity of the piggyBac-like elements in the genome of Tribolium castaneum. Insect Biochem Mol Biol 2008, 38(4):490-498.
• [28]Osanai-Futahashi M, Suetsugu Y, Mita K, Fujiwara H: Genome-wide screening and characterization of transposable elements and their distribution analysis in the silkworm, Bombyx mori. Insect Biochem Mol Biol 2008, 38(12):1046-1057.
• [29]Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du F, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, et al.: The B73 maize genome: complexity, diversity, and dynamics. Science 2009, 326(5956):1112-1115.
• [30]Rogozin I, Kondrashov F, Glazko G: Use of mutation spectra analysis software. Hum Mutat 2001, 17(2):83-102.
• [31]Rogozin IB, Pavlov YI: Theoretical analysis of mutation hotspots and their DNA sequence context specificity. Mutat Res 2003, 544(1):65-85.
• [32]Meng XF, Shi M, Chen XX: Population genetic structure of Chilo suppressalis (Walker) (Lepidoptera: Crambidae): strong subdivision in China inferred from microsatellite markers and mtDNA gene sequences. Mol Ecol 2008, 17(12):2880-2897.
• [33]Li XH, Luo GH, Zhang ZC, Liu BS, Fang JC: Coling and characterization of Ty3/gypsy retrotransposon in Chilo suppressalis (Lepidoptera: Pyralidae). Chin J Rice Sci 2014, 28(3):314-321.
• [34]Wang W-M, Ding J-L, Shu J-W, Chen W: Exploration of early rice farming in China. Quat Int 2010, 227(1):22-28.
• [35]Molina J, Sikora M, Garud N, Flowers JM, Rubinstein S, Reynolds A, Huang P, Jackson S, Schaal BA, Bustamante CD, Boyko AR, Purugganan MD: Molecular evidence for a single evolutionary origin of domesticated rice. Proc Natl Acad Sci U S A 2011, 108(20):8351-8356.
• [36]Crawford G: Early rice exploitation in the lower Yangzi valley: what are we missing? The Holocene 2012, 22(6):613-621.
• [37]Luo GH, Zhang ZC, Han GJ, Han ZJ, Fang JC: Characteristics of overwintering populations of rice stem borers and mutation frequencies of resistance to triazophos. Chin J Rice Sci 2012, 26(4):481-486.
• [38]Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG: The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997, 25(24):4876-4882.
• [39]Tamura K, Dudley J, Nei M, Kumar S: MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24(8):1596-1599.
• [40]Ko WY, David RM, Akashi H: Molecular phylogeny of the Drosophila melanogaster species subgroup. J Mol Evol 2003, 57(5):562-573.
• [41]Dice LR: Measures of the amount of ecologic association between species. Ecology 1945, 26(3):297-302.
• [42]Nei M, Li WH: Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci U S A 1979, 76(10):5269-5273.
• [43]Felsenstein J: PHYLIP-phylogeny inference package (version 3.2). Cladistics 1989, 5:164-166.