Advertisement

Tree Genetics & Genomes

, 13:129 | Cite as

A moso bamboo (Phyllostachys edulis) miniature inverted-repeat transposable element (MITE): the possible role of a suppressor

  • Mingbing ZhouEmail author
  • Ang Chen
  • Qianqian Zhou
  • Dingqin Tang
  • Heikki Hänninen
Original Article
  • 207 Downloads
Part of the following topical collections:
  1. Genome Biology

Abstract

Transposable elements (transposons) are fragments of DNA sequences which can move within host genome. Miniature inverted-repeat transposable elements (MITEs) are widespread and high-copy transposable elements in eukaryotic genomes. Tourist-like MITEs are especially abundant in plant kingdom. Earlier genome-wide analysis has shown that MITEs are widely distributed in the moso bamboo genome and preferentially inserted into gene regions. In the present study, in order to examine the potential influence of MITEs on the moso bamboo gene expressions, a highly conserved Tourist-like MITE family, which distributed near genes, was selected as research focus and named PhTst-3 (Phyllostachys edulis Tourist-like element 3). The MITEs’ insertion sites were tested in moso bamboo half-sib seedlings by real-time fluorescence quantitative PCR. Amplification polymorphisms were found in a copy of PhTst-3 (PhTst-3-55) which was located in the intron of PH01002699G0010. This inserted PhTst-3-55 had a significant impact on the gene expression revealed by the real-time fluorescence quantitative PCR. The gene expression levels were four times higher in the absence of PhTst-3-55 than those in the presence of it. This finding suggests that the PhTst-3 located in the intron is involved in the regulation of the gene. In order to examine the impact of PhTst-3-55 on the near genes, the PhTst-3-55 was inserted into a promoter analysis vector, pxk7S2D, between the two promoter sequences. The Agrobacterium-mediated transient expression showed that PhTst-3-55 insertion decreases the expression level of upstream GUS gene and downstream GFP gene. So, PhTst-3-55 can have a silencing role by bidirectionally inhibiting gene expression.

Keywords

Phyllostachys edulis Miniature inverted-repeat transposable elements (MITEs) Tourist-like MITEs Gene regulation 

Notes

Author Contribution Statement

M. B. Zhou designated the experiments, identified PhTst-3, and wrote the paper; A. Chen constructed the vectors and moso bamboo transient expression system; Q. Q. Zhou estimated insertion sites; D. Q. Tang analyzed the experiment data; H. Hänninen revised and edited the paper. All authors read and approved the manuscript.

Data archiving statement

Genomic sequences and gene annotation information of moso bamboo presented in this report are available in the bamboo genome database (BambooGDB, http://www.bamboogdb.org/index.jsp).

Funding

This work was funded by the grants from the National Natural Science Foundation of China (grant no. 31470615 and 31270645) and through Talents Program of Natural Science Foundation of Zhejiang Province (grant no. LR12C16001).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11295_2017_1210_MOESM1_ESM.doc (101 kb)
Supplementary Table S1 (DOC 101 kb)
11295_2017_1210_MOESM2_ESM.doc (32 kb)
Supplementary Table S2 (DOC 32 kb)
11295_2017_1210_MOESM3_ESM.doc (30 kb)
Supplementary table S3 (DOC 30 kb)
11295_2017_1210_MOESM4_ESM.txt (30 kb)
Supplementary file S4 (TXT 30 kb)

References

  1. Bejerano G, Lowe CB, Ahituv N, King B, Siepel A, Salama SR, Rubin EM, Kent WJ, Haussler D (2006) A distal enhancer and an ultraconserved exon are derived from a novel retroposon. Nature 441(7089):87–90.  https://doi.org/10.1038/nature04696 CrossRefPubMedGoogle Scholar
  2. Bustos-Sanmamed P, Hudik E, Laffont C, Reynes C, Sallet E, Wen J, Mysore KS, Camproux AC, Hartmann C, Gouzy J, Frugier F, Crespi M, Lelandais-Brière C (2014) A Medicago truncatula rdr6 allele impairs transgene silencing and endogenous phased siRNA production but not development. Plant Biotechnol J 12(9):1308–1318.  https://doi.org/10.1111/pbi.12230 CrossRefPubMedGoogle Scholar
  3. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14(6):1188–1190.  https://doi.org/10.1101/gr.849004 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 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.  https://doi.org/10.1007/s11103-015-0300-7 CrossRefPubMedGoogle Scholar
  5. El Amrani A, Marie L, Ainouche A, Nicolas J, Couee I (2002) Genome-wide distribution and potential regulatory functions of AtATE, a novel family of miniature inverted-repeat transposable elements in Arabidopsis thaliana. Mol Gen Genomics 267(4):459–471.  https://doi.org/10.1007/s00438-002-0675-4 CrossRefGoogle Scholar
  6. Fan CJ, Ma JM, Guo QR, Li XT, Wang H, MZ L (2013) Selection of reference genes for quantitative real-time PCR in bamboo (Phyllostachys edulis). PLoS One 8(2):e56573.  https://doi.org/10.1371/journal.pone.0056573 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Feschotte C (2008) Transposable elements and the evolution of regulatory networks. Nat Rev Genet 9(5):397–405.  https://doi.org/10.1038/nrg2337 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Feschotte C, Jiang N, Wessler SR (2002) Plant transposable elements: where genetics meets genomics. Nat Rev Genet 3(5):329–341.  https://doi.org/10.1038/nrg793 CrossRefPubMedGoogle Scholar
  9. Han MJ (2013) Identification, evolution and function of silkworm MITEs as well as evolutionary dynamics of silkworm TEs. Ph. D. Thesis, Chongqin, Chinese Southwest University, 2013: 22Google Scholar
  10. Han MJ, Shen YH, Gao YH, Chen LY, Xiang ZH, Zhang Z (2010) Burst expansion, distribution and diversification of MITEs in the silkworm genome. BMC Genomics 11(1):520.  https://doi.org/10.1186/1471-2164-11-520 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Hu H, Zhou M, Yang P, Tang D (2015) Cloning and analysis of miniature inverted repeat transposable elements PhTourist1 from Phyllostachys edulis. Scientia Silvae Sinicae 51(5):127–134Google Scholar
  12. Le Hir H, Nott A, Moore MJ (2003) How introns influence and enhance eukaryotic gene expression. Trends Biochem Sci 28(4):215–220.  https://doi.org/10.1016/S0968-0004(03)00052-5 CrossRefPubMedGoogle Scholar
  13. Lowe CB, Bejerano G, Haussler D (2007) Thousands of human mobile element fragments under go strong purifying selection near developmental genes. Proc Natl Acad Sci U S A 104(19):8005–8010.  https://doi.org/10.1073/pnas.0611223104 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Marino-Ramirez L, Ik J (2006) Transposable element derived DNasel-hypersensitive sites in the human genome. Biol Direct 1(1):20.  https://doi.org/10.1186/1745-6150-1-20 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Markham NR, Zuker M (2008) UNAFold: software for nucleic acid folding and hybridization. Methods Mol Biol 453:3–31.  https://doi.org/10.1007/978-1-60327-429-6_1 CrossRefPubMedGoogle Scholar
  16. Mcclintock B (1951) Chromosome organization and gene expression. Cold Spring Harbor Symp 16:131CrossRefGoogle Scholar
  17. 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(47):17620–17625.  https://doi.org/10.1073/pnas.0605421103 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 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.  https://doi.org/10.1038/nature08479 CrossRefPubMedGoogle Scholar
  19. Oki N, Yano K, Okumoto Y, Tsukiyama T, Teraishi M, Tanisaka T (2008) A genome-wide view of miniature inverted-repeat transposable elements (MITEs) in rice, Oryza sativa ssp. Japonica. Genes Genet Syst 83(4):321–329.  https://doi.org/10.1266/ggs.83.321 CrossRefPubMedGoogle Scholar
  20. Sampath P, Lee SC, Lee J, Izzah NK, Choi BS, Jin M, Park BS, Yang TJ (2013) Characterization of a new high copy Stowaway family MITE, BRAMI-1 in Brassica genome. BMC Plant Biol 13(1):56.  https://doi.org/10.1186/1471-2229-13-56 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Santiago N, Herráiz C, Goñi JR, Messeguer X, Casacuberta JM (2002) Genome-wide analysis of the emigrant family of MITEs of Arabidopsis thaliana. Mol Biol Evol 19(12):2285–2293Google Scholar
  22. Surendar RD, Aparna D, Wusirika R (2012) A novel non-wounding transient expression assay for cereals mediated by Agrobacterium tumefaciens. Plant Mol Biol Rep 2012(30):36–45Google Scholar
  23. Yang G, Lee YH, Jiang Y, Shi X, Kertbundit S, Hall TC (2005) A two-edged role for the transposable element Kiddo in the rice ubiquitin2 promoter. Plant Cell 17(5):1559–1568.  https://doi.org/10.1105/tpc.104.030528 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Yang G, Nagel DH, Feschotte C, Hancock CN, Wessler SR (2009) Tuned for transposition: molecular determinants underlying the hyperactivity of stowaway MITE. Science 325(11):1391–1394.  https://doi.org/10.1126/science.1175688 CrossRefPubMedGoogle Scholar
  25. 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 Breeding 32(3):505–516.  https://doi.org/10.1007/s11032-013-9885-1 CrossRefGoogle Scholar
  26. Zeijal T, Joets J, Alix K, Grandbastien MA, Tenaillon MI (2009) Contrasting evolutionary patterns and target specificities among three Tourist-like MITE families in the maize genome. Plant Mol Biol 71(1–2):99–114Google Scholar
  27. Zhang X, Feschotte C, Zhang Q, Jiang N, Eggleston WB, Wessler SR (2001) P instability factor: an active maize transposon system associated with the amplification of Tourist-like MITEs and a new superfamily of transposases. Proc Natl Acad Sci U S A 98(22):12572–12577.  https://doi.org/10.1073/pnas.211442198 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Zhou M, Tao G, P P, Zhu Y, Bai Y, Meng X (2016a) Genome-wide characterization and evolution analysis of miniature inverted-repeat transposable elements (MITEs) in moso bamboo (Phyllostachys heterocycla). Planta 244(4):775–787.  https://doi.org/10.1007/s00425-016-2544-0 CrossRefPubMedGoogle Scholar
  29. Zhou MB, Zheng Y, Liu ZG, Xia XW, Ding-Qin Tang DQ, Fu Y, Chen M (2016b) Endo-1,4-b-glucanase gene involved into the rapid elongation of Phyllostachys heterocycla var. pubescens. Trees 30(4):1259–1274.  https://doi.org/10.1007/s00468-016-1363-z CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Mingbing Zhou
    • 1
    • 2
    Email author
  • Ang Chen
    • 1
  • Qianqian Zhou
    • 1
  • Dingqin Tang
    • 1
  • Heikki Hänninen
    • 1
  1. 1.The State Key Laboratory of Subtropical SilvicultureZhejiang A & F UniversityHangzhouPeople’s Republic of China
  2. 2.Zhejiang Provincial Collaborative Innovation Center for Bamboo Resources and High-efficiency UtilizationZhejiang A & F UniversityHangzhouPeople’s Republic of China

Personalised recommendations