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Transcriptionally active LTR retroelement-related sequences and their relationship with small RNA in moso bamboo (Phyllostachys edulis)

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Abstract

Many different cultivars or forms with diverse phenotypes of moso bamboo have been produced during its long cultivation history. The diverse phenotypes of moso bamboo are mainly reversible and unpredictable during cultivation, which lead to the hypothesis of their epigenetic origin. Earlier studies have shown that transposable elements might be involved in the different expression patterns of moso bamboo genes. LTR (long terminal repeat) retroelement populations are the main components of moso bamboo genomes. In the present study, a genome-wide analysis addressing their potential impact on host gene expression and the regulatory network was carried out. The results show that LTR retroelements are usually inserted far away from the gene regions. Transcriptional activity appears to be common in some moso bamboo retroelement-related sequences. The expression level and number of retroelement-related sequences tend to decrease with increasing distance from the closest genes, indicating that the interaction between retroelement-related sequences and near genes might play a role in the expression pattern of retroelement-related sequences. Retroelement-related sequences generate more than 30% of the siRNAs in moso bamboo. Both 21-nt siRNA and 24-nt siRNA mainly target within LTR regions of the bamboo LTR retroelements. Given the high copy number of LTR retroelements, the transcriptional activity of LTR retroelements, and the high number of siRNAs derived from the LTR retroelements, moso bamboo LTR retroelements might be involved in the transcriptional regulation of host genes, and this may be responsible for the diverse phenotypes of moso bamboo.

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References

  • An MM, Guo C, Lin PP, Zhou MB (2016) Heterogeneous evolution of Ty3-gypsy retroelements among bamboo species. Genet Mol Res. https://doi.org/10.4238/gmr15038515

  • Bennetzen JF (2000) Transposable element contributions to plant gene and genome evolution. Plant Mol Biol 42:251–269

    Article  CAS  PubMed  Google Scholar 

  • Biemont C, Tsitrone A, Vieira C, Hoogland C (1997) Transposable element distribution in Drosophila. Genetics 147:1997–1999

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bui QT, Grandbastien MA (2012) LTR retroelements as controlling elements of genome response to stress? In: Grandbastien MA, Casacuberta JM (eds) Plant transposable elements. Springer, Berlin Heidelberg, pp 273–296

    Chapter  Google Scholar 

  • Cantu D, Vanzetti LS, Sumner A, Dubcovsky M, Matvienko M, Distelfeld A, Michelmore RW, Dubcovsky J (2010) Small RNAs, DNA methylation and transposable elements in wheat. BMC Genomics 11:408

    Article  PubMed  PubMed Central  Google Scholar 

  • Casacuberta E, González J (2013) The impact of transposable elements in environmental adaptation. Mol Ecol 22:1503–1517

    Article  CAS  PubMed  Google Scholar 

  • Cui X, Cao X (2014) Epigenetic regulation and functional exaptation of transposable elements in higher plants. Curr Opin Plant Biol 21:83–88

    Article  CAS  PubMed  Google Scholar 

  • Echenique V, Stamova B, Wolters P, Lazo G, Carollo L, Dubcovsky J (2002) Frequencies of Ty1- copia and Ty3- gypsy retroelements within the Triticeae EST databases. Theoretical Appl Genet 104:840–844

    Article  CAS  Google Scholar 

  • Eickbush TH, Jamburuthugoda VK (2008) The diversity of retroelements and the properties of their reverse transcriptases. Virus Res 134:221–234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feschotte C (2008) The contribution of transposable elements to the evolution of regulatory networks. Nat Rev Genet 9:397–405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu J (2001) Chinese Moso Bamboo: its importance. Bamboo 22:5–7

    Google Scholar 

  • He C-Y, Cui K, Zhang J-G, Duan A-G, Zeng Y-F (2013) Next-generation sequencing-based mRNA and microRNA expression profiling analysis revealed pathways involved in the rapid growth of developing culms in Moso bamboo. BMC Plant Biol 13(1):119

    Article  PubMed  PubMed Central  Google Scholar 

  • Hirochika H (1993) Activation of tobacco retroelements during tissue culture. EMBO J 12:2521–2528

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hirochika H, Sugimoto K, Otsuki Y, Tsugawa H, Kanda M (1996) Retroelements of rice involved in mutations induced by tissue culture. Proc Natl Acad Sci 93:7783–7788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Article  Google Scholar 

  • Ito H (2013) Small RNAs and regulation of transposons in plants. Genes Genet Syst 88:3–7

    Article  CAS  PubMed  Google Scholar 

  • Ito H, Gaubert H, Bucher E, Mirouze M, Vaillant I, Paszkowski J (2011) An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472:115–119

    Article  CAS  PubMed  Google Scholar 

  • Jiang KY, Zhou MB (2016) Cloning and functional characterization of PjPORB, a member of the POR gene family in Pseudosasa japonica cv Akebonosuji. Plant Growth Regul 79(1):95–106

    Article  CAS  Google Scholar 

  • Jiang KY, Zhou MB, Yang HY, Fang W (2016) Cloning and functional characterization of PjCAO gene involved in chlorophyll b biosynthesis in Pseudosasa japonica cv Akebonosuji. Trees 30:1303–1314

    Article  CAS  Google Scholar 

  • Kaeppler SM, Kaeppler HF, Rhee Y (2000) Epigenetic aspects of somaclonal variation in plants. Plant Mol Biol 43:179–188

    Article  CAS  PubMed  Google Scholar 

  • Kashkush K, Khasdan V (2007) Large-scale survey of cytosine methylation of retroelements and the impact of readout transcription from long terminal repeats on expression of adjacent rice genes. Genetics 177:1975–1985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kashkush K, Feldman M, Levy AA (2003) Transcriptional activation of retroelements alters the expression of adjacent genes in wheat. Nat Genet 33:102–106

    Article  CAS  PubMed  Google Scholar 

  • Langley CH, Montgomery E, Hudson R, Kaplan N, Charlesworth B (1988) On the role of unequal exchange in the containment of transposable element copy number. Genet Res 52:223–235

    Article  CAS  PubMed  Google Scholar 

  • Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10(3):R25

    Article  PubMed  PubMed Central  Google Scholar 

  • Lisch D (2012) Regulation of transposable elements in maize. Curr Opin Plant Biol 13:1–6

    Google Scholar 

  • Lisch D (2013) How important are transposons for plant evolution? Nat Rev Genet 14:49–61

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Llorens C, Mñoz-Pomer A, Bernad L, Botella H, Moya A (2009) Network dynamics of eukaryotic LTR retroelements beyond phylogenetic trees. Biol Direct 4:41

    Article  PubMed  PubMed Central  Google Scholar 

  • Llorens C, Futami R, Covelli L, Domínguez-Escribá L, Viu JM, Tamarit D, Aguilar-Rodríguez J, Vicente-Ripolles M, Fuster G, Bernet GP, Maumus F, Munoz-Pomer A, Sempere JM, Latorre A, Moya A (2011) The gypsy Database (GyDB) of mobile genetic elements: release 20. Nucleic Acids Res 39:70–74

    Article  Google Scholar 

  • Makarevitch I, Waters AJ, West PT, Stitzer M, Hirsch CN, Ross-Ibarra J, Springer NM (2015) Transposable elements contribute to activation of maize genes in response to abiotic stress. PLoS Genet 11:e1004915

    Article  PubMed  PubMed Central  Google Scholar 

  • McCue AD, Slotkin RK (2012) Transposable element small RNAs as regulators of gene expression. Trends Genet 28(12):616–623

    Article  CAS  PubMed  Google Scholar 

  • McCue AD, Nuthikattu S, Reeder SH, Slotkin RK (2012) Gene expression and stress response mediated by the epigenetic regulation of a transposable element small RNA. PLoS Genet 8(2):e1002474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyao A, Nakagome M, Ohnuma T, Yamagata H, Kanamori H, Katayose Y, Takahashi A, Matsumoto T, Hirochika H (2012) Molecular spectrum of somaclonal variation in regenerated rice revealed by whole-genome sequencing. Plant Cell Physiol 53:256–264

    Article  CAS  PubMed  Google Scholar 

  • Naito K, Cho E, Yang G, Campbell MA, Yano K, Okumoto Y, Tanisaka T, Wessler SR (2006) Dramatic amplification of a rice transposable element during recent domestication. Proc Natl Acad Sci U S A 103:17620–17625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nobuta K, Lu C, Shrivastava R, Pillay M, De Paoli E, Accerbi M, Arteaga-Vazquez M, Sidorenko L, Jeong DH, Yen Y, Green PJ, Chandler VL, Meyers BC (2008) Distinct size distribution of endogenous siRNAs in maize: Evidence from deep sequencing in the mop1-1 mutant. Proc Natl Acad Sci U S A 105:14958–14963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nosaka M, Itoh J, Nagato Y, Ono A, Ishiwata A, Sato Y (2012) Role of transposon-derived small RNAs in the interplay between genomes and parasitic DNA in rice. PLoS Genet 8:e1002953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nuzhdin SV, Pasyukova EG, Mackay TF (1996) Positive association between copia transposition rate and copy number in Drosophila melanogaster. Proc R Soc Lond B Biol Sci 263:823–831

    Article  CAS  Google Scholar 

  • Paszkowski J (2015) Controlled activation of retrotransposition for plant breeding. Curr Opin Biotechnol 32:2000–2006

    Article  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob-ur-Rahman WD, Westhoff P, Mayer KF, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556

    Article  CAS  PubMed  Google Scholar 

  • Pereira V (2004) Insertion bias and purifying selection of retrotransposons in the Arabidopsis thaliana genome. Genome Biol 5(10):R79

    Article  PubMed  PubMed Central  Google Scholar 

  • Pouteau S, Huttner E, Grandbastien MA, Caboche M (1991) Specific expression of the tobacco Tnt1 retroelement in protoplasts. EMBO J 10:1911–1918

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115

    Article  CAS  PubMed  Google Scholar 

  • Smulders M, de Klerk G (2011) Epigenetics in plant tissue culture. Plant Growth Regul 63:137–146

    Article  CAS  Google Scholar 

  • Söderbom F, Avrova AO, Whisson SC, Dixelius C (2012) Evidence for small RNAs homologous to effector-encoding genes and transposable elements in the oomycete Phytophthora infestans. PLoS One 7:e51399

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun F, Guo W, Du J, Ni Z, Sun Q, Yao Y (2013) Widespread, abundant, and diverse TE-associated siRNAs in developing wheat grain. Gene 522(1):1–7

    Article  CAS  PubMed  Google Scholar 

  • Suoniemi A, Narvanto A, Schulman AH (1996) The BARE-1 retroelement is transcribed in barley from an LTR promoter active in transient assays. Plant Mol Biol 31:295–306

    Article  CAS  PubMed  Google Scholar 

  • Todorovska E (2007) Retroelements and their role in plant-genome evolution. Biotechnol Biotechnol Equip 21:294–305

    Article  CAS  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7(3):562–578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vetukuri RR, Åsman AK, Tellgren-Roth C, Jahan SN, Reimegård J, Fogelqvist J, Savenkov E, Vicient CM (2010) Transcriptional activity of transposable elements in maize. BMC Genomics 11:601

    Article  Google Scholar 

  • 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 Physiology Biochem 97:156–164

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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. Database (Oxford): bau006

  • Zhou MB, Zhang Y, Tang DQ (2011) Characterization and Primary Functional Analysis of BvCIGR, a Member of the GRAS Gene Family in Bambusa ventricosa. Bot Rev 77(3):233–242

    Article  Google Scholar 

  • Zhou M, Hu B, Zhu Y (2017) Genome-wide characterization and evolution analysis of long terminal repeat retroelements in moso bamboo (Phyllostachys edulis). Tree Genetics Genomes. https://doi.org/10.1007/s11295-017-1114-3

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Acknowledgements

This work was supported by Talents Program of Natural Science Foundation of Zhejiang Province (grant No. LR12C16001), and the grant from the National Natural Science Foundation of China (grant No 31470615 and 31270645).

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Authors and Affiliations

  1. The State Key Laboratory of Subtropical Silviculture, Zhejiang A & F University, Lin’an, Hangzhou, 311300, Zhejiang Province, People’s Republic of China

    Mingbing Zhou, Yihang Zhu, Youhuang Bai, Heikki Hänninen & Xianwen Meng

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  1. Mingbing Zhou
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  2. Yihang Zhu
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  3. Youhuang Bai
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  4. Heikki Hänninen
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Contributions

M. B. Zhou was responsible for designing the experiments and writing the paper; B. J. Hu for estimation of the LTR retroelement insertion sites; Y. H. Zhu and Y. H. Bai for analysis of the LTR retroelement-related sequence expression; X. W. Meng for identification of small RNA and LTR retroelement derived small RNA; and H. Hänninen for revising and editing the manuscript. All authors read and approved the manuscript.

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Correspondence to Mingbing Zhou.

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Supplementary fig. S3

The relative expression level measured by RT-qPCR (bars and vertical axis on the left) and the FPKM value counted by Cufflink (line and vertical axis on the right) of selected nine LTR retroelement-related sequences in seven moso bamboo tissues. a, PhUn30-locus1; b, PhTo59-locus1; c, PhTa192-locus1; d, PhSi85-locus1; e, PhRet44-locus1; f, PhCr84-locus1; g, PhOr53-locus1; h, PhDe87-locus1; i, PhRe42-locus1. (GIF 78 kb)

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Zhou, M., Zhu, Y., Bai, Y. et al. Transcriptionally active LTR retroelement-related sequences and their relationship with small RNA in moso bamboo (Phyllostachys edulis). Mol Breeding 37, 132 (2017). https://doi.org/10.1007/s11032-017-0733-6

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