Abstract
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Transposable elements are abundant in the promoter regions of moso bamboo genome and influence the expression of downstream genes.
Abstract
As important components of animal and plant genomes, transposable elements (TEs) can shape host genomes and regulate gene expression. In the present study, TEs distributed in the promoter regions of moso bamboo genome were systematically investigated with stringy parameters using RepeatMasker. Approximately 85.7% of the promoter regions were anchored into the TE sequences. Among TE families, three types of TEs are preferentially inserted into the promoter regions: hAT-like transposons, miniature inverted-repeat elements (MITEs), and short interspersed elements (SINEs). The TE insertion sites in promoter regions were amplified by PCR. One site (TE-20) exhibited insertion polymorphism. The expression of downstream gene PH01003704G0280 was three to five times higher with the absence of TE-20 than with the presence of it. On the basis of previous studies it was hypothesized that TEs distributed in the promoter regions of four homologs of floral pathway integrators (FPIs) might be responsible for the observed low expression level. To test the hypothesis, four promoter sequences with TE insertions and TE deletions were inserted upstream of the open reading frame of the β-glucuronidase (GUS) gene and green fluorescent protein (GFP) reporter genes. The expression level of downstream genes was higher with TE deletions than with TE insertions. These results show that the TEs are abundant in the promoter regions and influence the expression of downstream genes in moso bamboo genome.
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References
Barkan A, Martienssen RA (1991) Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1. PNAS 88(8):3502–3506
Bourque G (2009) Transposable elements in gene regulation and in the evolution of vertebrate genomes. Curr Opin Cell Biol 19:607–612
Bureau TE, Wessler SR (1992) Tourist: a large family of small inverted repeat elements frequently associated with maize genes. Plant Cell 4:1283–1294
Butelli E, Licciardello C, Zhang Y, Liu J, Mackay S, Bailey P, Reforgiato-Recupero G, Martin C (2012) Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell 24:1242–1255
Dhadi SR, Deshpande A, Ramakrishna W (2012) A novel non-wounding transient expression assay for cereals mediated by Agrobacterium tumefaciens. Plant Mol Biol Rep 30:36–45
Dhadi SR, Xu Z, Shaik R, Driscoll K, Ramakrishna W (2015) Differential regulation of genes by retrotransposons in rice promoters. Plant Mol Biol 87(6):603–613
Fan CJ, Ma JM, Guo QR, Li XT, Wang H, Lu MZ (2013) Selection of reference genes for quantitative real-time PCR in bamboo (Phyllostachys edulis). PLoS One 8:e56573
Feschotte C, Mouches C (2000) Evidence that a family of miniature inverted-repeat transposable elements (MITEs) from the Arabidopsis thaliana genome has arisen from a pogo-like DNA transposon. Mol Biol Evol 17(5):730–737
Feschotte C, Pritham EJ (2007) DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 41:331–368
Gray YH (2000) It takes two transposons to tango: transposable-element-mediated chromosomal rearrangements. Trends Genet 16(10):461–468
Hanson MR, Köhler RH (2001) GFP imaging: methodology and application to investigate cellular compartmentation in plants. J Exp Bot 52(356):529–539
Hirsch CD, Springer NM (2017) Transposable element influences on gene expression in plants. Biochim Biophys Acta 1860(1):157–165
Hu T, He S, Yang G, Zeng H, Wang G, Chen Z, Huang X (2011) Isolation and characterization of a rice glutathione S-transferase gene promoter regulated by herbicides and hormones. Plant Cell Rep 30:539–549
Hu H, Zhou MB, Yang P, Tang DQ (2015) Cloning and analysis of miniature inverted repeat transposable elements PhTourist1 from Phyllostachys edulis. Scientia Silvae Sinicae 51:127–134
Jordan IK, Rogozin IB, Glazko GV (2003a) Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet 19(2):68–72
Jordan IK, Rogozin IB, Glazko GV, Koonin EV (2003b) Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet 19:68–72
Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33(1):479–532
Lin X, Ruan X, Lou Y (2009) Genetic similarity among cultivars of Phyllostachys pubescens. Plant Syst Evol 277:67–73
Lin XC, Chow TY, Chen HH, Liu CC, Chou SJ, Huang BL, Kuo CI, Wen CK, Huang LC, Fang W (2010) Understanding bamboo flowering based on large-scale analysis of expressed sequence tags. Genet Mol Res 9(2):1085–1093
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25:402–408
Lonnig WE, Saedler H (2002) Chromosome rearrangements and transposable elements. Annu Rev Genet 36:389–410
Mathelier A, Fornes O, Arenillas DJ, Chen CY, Denay G, Lee J, Shi W, Shyr C, Tan G, Worsley-Hunt R, Zhang AW, Parcy F, Lenhard B, Sandelin A, Wasserman WW (2016) JASPAR 2016: a major expansion and update of the open-access database of transcription factor binding profiles. Nucleic Acids Res 44(D1):D110–D115
Naito K, Zhang F, Tsukiyama T (2009) Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461(7267):1130–1134
Okumoto Y, Naito K, Tanisaka T (2007) Potential roles of a transposon MITE in gene regulation. Tanpakushitsu Kakusan Koso 52(3):214–220
Palin K, Taipale J, Ukkonen E (2006) Locating potential enhancer elements by comparative genomics using the EEL software. Nat Protoc 1(1):368–374
Peng Z, Lu Y, Li L, Zhao Q, Feng Q, Gao Z, Lu H, Hu T, Yao N, Liu K, Li Y, Fan D, Guo Y, Li W, Lu Y, Weng Q, Zhou C, Zhang L, Huang T, Zhao Y, Zhu C, Liu X, Yang X, Wang T, Miao K, Zhuang C, Cao X, Tang W, Liu G, Liu Y, Chen J, Liu Z, Yuan L, Liu Z, Huang X, Lu T, Fei B, Ning Z, Han B, Jiang Z (2013) The draft genome of the fast-growing non-timber forest species moso bamboo (Phyllostachys heterocycla). Nat Genet 45(4):456–461
Pereira V, Enard D, Eyer WA (2009) The effect of transposable element insertions on gene expression evolution in rodents. PLoS One 4(2):4321
Rastogi A, Gupato D (2014) GFF-Ex: a genome feature extraction package. BMC Res Notes 7:315
Seberg O, Petersen G (2009) A unified classification system for eukaryotic transposable elements should reflect their phylogeny. Nat Rev Genet 10(4):276
Settles AM, Baron A, Barkan A, Martienssen RA (2001) Duplication and suppression of chloroplast protein translocation genes in maize. Genetics 157:349–360
Surendar RD, Zijun X, Rafi S (2015) Differential regulation of genes by retrotransposons in rice promoters. Plant Mol Biol 87(6):603–613
Tang D, Li J, Zhang S (2010) Development characterization and utilization of GenBank microsatellite markers in Phyllostachys pubescens and related species. Mol Breed 25(2):299–311
Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8(12):973–982
Xia XW, Gui RY, Yang HY, Fu Y, Fang W, Zhou MB (2015) Identification of genes involved in color variation of bamboo culms by suppression subtractive hybridization. Plant Physiol Biochem 97:156–164
Xu Z, Rafi S, Ramakrishna W (2011) Polymorphisms and evolutionary history of retrotransposon insertions in rice promoters. Genome 54(8):629–638
Yang HY, Xia XW, Fang W, Fu Y, An MM, Zhou MB (2015) Identification of genes involved in spontaneous leaf color variation in Pseudosasa japonica. Genet Mol Res 14(4):11827–11840
Yasuda K, Ito M, Sugita T (2013) Utilization of transposable element mPing as a novel genetic tool for modification of the stress response in rice. Mol Breed 32(3):505–516
Zhao H, Peng Z, Fei B, Li L, Hu T, Gao Z, Jiang Z (2014) BambooGDB: a bamboo genome database with functional annotation and an analysis platform. Database (Oxford) 2014:bau006
Zhou MB, Zheng Y, Liu ZG, Xia XW, Ding-Qin Tang DQ, Fu Y, Chen M (2016) Endo-1,4-b-glucanase gene involved into the rapid elongation of Phyllostachys heterocycla var. pubescens. Trees 30:1259–1274
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The National Natural Science Foundation of China (Grant nos. 31470615 and 31270645) and the Talents Program of Zhejiang Province Natural Science Foundation of China (Grant no. LR12C16001) supported this study.
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Communicated by F. Canovas.
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Zhou, M., Zhou, Q. & Hänninen, H. The distribution of transposable elements (TEs) in the promoter regions of moso bamboo genes and its influence on downstream genes. Trees 32, 525–537 (2018). https://doi.org/10.1007/s00468-017-1650-3
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DOI: https://doi.org/10.1007/s00468-017-1650-3