Skip to main content

Genome-wide characterization and evolution analysis of miniature inverted-repeat transposable elements (MITEs) in moso bamboo (Phyllostachys heterocycla)

Planta volume 244, pages 775–787 (2016)Cite this article

Abstract

Main conclusion

Moso bamboo MITEs were genome-wide identified first time, and data shows that MITEs contribute to the genomic diversity and differentiation of bamboo.

Miniature inverted-repeat transposable elements (MITEs) are widespread in animals and plants. There are a large number of transposable elements in moso bamboo (Phyllostachys heterocycla var. pubescens) genome, but the genome-wide information of moso bamboo MITEs is not known yet. Here we identified 362 MITE families with a total of 489,592 MITE-related sequences, accounting for 4.74 % of the moso bamboo genome. The 362 MITE families are clustered into six known and one unknown super-families. Our analysis indicated that moso bamboo MITEs preferred to reside in or near the genes that might be involved in regulation of host gene expression. Of the seven super-families, three might undergo major expansion event twice, respectively, during 8–11 million years ago (mya) ago and 22–28 mya ago; two might experience a long expansion period from 6 to 13 mya. Almost 1/3 small RNAs might be derived from the MITE sequences. Some MITE families generate small RNAs mainly from the terminals, while others predominantly from the central region. Given the high copy number of MITEs, many siRNAs and miRNAs derived from MITE sequences and the preferential insertion of MITE into gene regions, MITEs may contribute to the genomic diversity and differentiation of bamboo.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Abbreviations

MITEs:

Miniature inverted-repeat transposable elements

TIRs:

Terminal inverted repeats

TSDs:

Target site duplications

Mya:

Million years ago

References

  • Akagi H, Yokozeki Y, Inagaki A, Mori K, Fujimura T (2001) Micron, a microsatellite-targeting transposable element in the rice genome. Mol Genet Genomics 266:471–480

    CAS  Article  PubMed  Google Scholar 

  • Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    CAS  Article  PubMed  Google Scholar 

  • Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363

    CAS  Article  PubMed  Google Scholar 

  • Bureau TE, Wessler SR (1992) Tourist: a large family of small inverted repeat elements frequently associated with maize genes. Plant Cell 4:1283–1294

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Bureau TE, Wessler SR (1994a) Mobile inverted-repeat elements of the Tourist family are associated with the genes of many cereal grasses. Proc Natl Acad Sci USA 91:1411–1415

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Bureau TE, Wessler SR (1994b) Stowaway: a new family of inverted repeat elements associated with the genes of both monocotyledonous and dicotyledonous plants. Plant Cell 6:907–916

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Cai Y, Zhou Q, Yu C, Wang X, Hu S, Yu J, Yu X (2012) Transposable-element associated small RNAs in Bombyx mori genome. PLoS One 7:e36599

    CAS  Article  PubMed  PubMed Central  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 Genom 11:408

    Article  Google Scholar 

  • Chen J, Hu Q, Zhang Y, Lu C, Kuang H (2013) P-MITE: a database for plant miniature inverted-repeat transposable elements. Nucleic Acids Res 42:1176–1181

    Article  Google Scholar 

  • Depra M, Ludwig A, Valente VL, Loreto EL (2012) Mar, a MITE family of hAT transposons in Drosophila. Mob DNA 3:13

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Dong HT, Zhang L, Zheng KL, Yao HG, Chen J, Yu FC, Yu XX, Mao BZ, Zhao D, Yao J, Li DB (2012) A Gaijin-like miniature inverted repeat transposable element is mobilized in rice during cell differentiation. BMC Genom 13:135

    CAS  Article  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid isolation procedure for small quantities of fresh leaf materials. Phytochem Bull 19:11–15

    Google Scholar 

  • Dufresne M, Hua-Van A, El Wahab HA, Ben M’Barek S, Vasnier C, Teysset L, Kema GH, Daboussi MJ (2007) Transposition of a fungal miniature inverted-repeat transposable element through the action of a Tc1-like transposase. Genetics 175:441–452

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 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 Genet Genomics 267:459–471

    Article  PubMed  Google Scholar 

  • Fattash I, Bhardwaj P, Hui C, Yang G (2013a) A rice Stowaway MITE for gene transfer in yeast. PLoS One 8:e64135

    Article  PubMed  PubMed Central  Google Scholar 

  • Fattash I, Rooke R, Wong A, Hui C, Luu T, Bhardwaj P, Yang G (2013b) Miniature inverted-repeat transposable elements: discovery, distribution, and activity. Genome 56:475–486

    CAS  Article  PubMed  Google Scholar 

  • 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 17:730–737

    CAS  Article  PubMed  Google Scholar 

  • Feschotte C, Swamy L, Wessler SR (2003) Genome-wide analysis of mariner-like transposable elements reveals complex relationships with Stowaway MITEs. Genetics 143:747–758

    Google Scholar 

  • Gao J, Zhang Y, Zhang C, Qi F, Li X, Mu S, Peng Z (2014) Characterization of the floral transcriptome of Moso bamboo (Phyllostachys edulis) at different flowering developmental stages by transcriptome sequencing and RNA-seq analysis. PLoS One 9:e98910

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 Genom 11:520

    Article  Google Scholar 

  • He CY, Cui K, Zhang JG, Duan AG, Zeng YF (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 13:119

    Article  PubMed  PubMed Central  Google Scholar 

  • Hollister JD, Gaut BS (2009) Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res 19:1419–1428

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Hollister JD, Smith LM, Guo YL, Ott F, Weigel D, Gaut BS (2011) Transposable elements and small RNAs contribute to gene expression divergence between Arabidopsis thaliana and Arabidopsis lyrata. Proc Natl Acad Sci USA 108:2322–2327

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Jiang N, Bao Z, Zhang X, Hirochika H, Eddy SR, McCouch SR, Wessler SR (2003) An active DNA transposon family in rice. Nature 421:163–167

    CAS  Article  PubMed  Google Scholar 

  • Jiang N, Feschotte C, Zhang X, Wessler SR (2004) Using rice to understand the origin and amplification of miniature inverted repeat transposable elements (MITEs). Curr Opin Plant Biol 7:115–119

    CAS  Article  PubMed  Google Scholar 

  • Jobling MA, Hurles ME, Tyler-Smith C (2004) Human evolutionary genetics. Garland, Abingdon and New York

    Google Scholar 

  • Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462–467

    CAS  Article  PubMed  Google Scholar 

  • Kawaoka S, Hayashi N, Katsuma S, Kishino H, Kohara Y, Mita K, Shimada T (2008) Bombyx small RNAs: genomic defense system against transposons in the silkworm, Bombyx mori. Insect Biochem Mol Biol 38:1058–1065

    CAS  Article  PubMed  Google Scholar 

  • Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2011) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36. doi:10.1186/gb-2013-14-4-r36

    Article  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    CAS  Article  PubMed  Google Scholar 

  • Kuang H, Padmanabhan C, Li F, Kamei A, Bhaskar PB, Ouyang S, Jiang J, Buell CR, Baker B (2009) Identification of miniature inverted- repeat transposable elements (MITEs) and biogenesis of their siRNAs in the Solanaceae: new functional implications for MITEs. Genome Res 19:42–56

    CAS  Article  PubMed  PubMed Central  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 10:25

    Article  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettiga PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    CAS  Article  PubMed  Google Scholar 

  • Liu J, He Y, Amasino R, Chen X (2004) siRNAs targeting an intronic transposon in the regulation of natural flowering behavior in Arabidopsis. Genes Dev 18:2873–2878

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Lu C, Chen J, Zhang Y, Hu Q, Su W, Kuang H (2012) Miniature inverted-repeat transposable elements (MITEs) have been accumulated through amplification bursts and play important roles in gene expression and species diversity in Oryza sativa. Mol Biol Evol 29:1005–1017

    CAS  Article  PubMed  Google Scholar 

  • Ma J, Jackson SA (2006) Retrotransposon accumulation and satellite amplification mediated by segmental duplication facilitate centromere expansion in rice. Genome Res 16:251–259

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  • Miskey C, Papp B, Mates L, Sinzelle L, Keller H, Izsvak Z, Ivics Z (2007) The ancient mariner sails again: transposition of the human Hsmar1 element by a reconstructed transposase and activities of the SETMAR protein on transposon ends. Mol Cell Biol 27:4589–4600

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Momose M, Abe Y, Ozeki Y (2010) Miniature inverted-repeat transposable elements of Stowaway are active in potato. Genetics 186:59–66

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Moreno-Vazquez S, Ning J, Meyers BC (2005) hATpin, a family of MITE-like hAT mobile elements conserved in diverse plant species that forms highly stable secondary structures. Plant Mol Biol 58:869–886

    CAS  Article  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 USA 103:17620–17625

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Naito K, Zhang F, Tsukiyama T, Saito H, Hancock CN, Richardson AO, Okumoto Y, Tanisaka T, Wessler SR (2009) Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461:1130–1134

    CAS  Article  PubMed  Google Scholar 

  • Nakazaki T, Okumoto Y, Horibata A, Yamahira S, Teraishi M, Nishida H, Inoue H, Tanisaka T (2003) Mobilization of a transposon in the rice genome. Nature 421:170–172

    CAS  Article  PubMed  Google Scholar 

  • 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 83:321–329

    CAS  Article  PubMed  Google Scholar 

  • 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 45:456–461

    CAS  Article  PubMed  Google Scholar 

  • Piriyapongsa J, Jordan IK (2007) A family of human microRNA genes from miniature inverted-repeat transposable elements. PLoS One 2:e203

    Article  PubMed  PubMed Central  Google Scholar 

  • Saito K, Nishida KM, Mori T, Kawamura Y, Miyoshi K, Nagami T, Siomi H, Siomi MC (2006) Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes Dev 20:2214–2222

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 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 13:56. doi:10.1186/1471-2229-13-56

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 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 19:2285–2293

    CAS  Article  PubMed  Google Scholar 

  • Wessler SR, Bureau TE, White SE (1995) LTR-retrotransposons and MITEs: important players in the evolution of plant genomes. Curr Opin Genetics 5:814–821

    CAS  Article  Google Scholar 

  • 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 8:973–982

    CAS  Article  PubMed  Google Scholar 

  • Xia X, Xie Z (2001) DAMBE: software package for data analysis in molecular biology and evolution. J Hered 92:371–373

    CAS  Article  PubMed  Google Scholar 

  • Xu P, Mohorianu I, Yang L, Zhao H, Gao Z, Dalmay T (2014) Small RNA profile in moso bamboo root and leaf obtained by high definition adapters. PLoS One 9:e103590

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang G (2013) MITE Digger, an efficient and accurate algorithm for genome wide discovery of miniature inverted repeat transposable elements. BMC Bioinform 14:186

    Article  Google Scholar 

  • Yang G, Hall TC (2003) MDM-1 and MDM-2: two mutator-derived MITE families in rice. J Mol Evol 56:255–264

    CAS  Article  PubMed  Google Scholar 

  • 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 17:1559–1568

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Zerjal 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 71:99–114

    CAS  Article  PubMed  Google Scholar 

  • Zhang X, Jiang N, Feschotte C, Wessler SR (2004) PIF- and Pong-like transposable elements: distribution, evolution and relationship with Tourist-like miniature inverted-repeat transposable elements. Genetics 166:971–986

    CAS  Article  PubMed  PubMed Central  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 (Oxford) 2014: bau006

  • Zhao H, Wang L, Dong L, Sun H, Ga Z (2014b) Discovery and comparative profiling of microRNAs in representative monopodial bamboo (Phyllostachys edulis) and sympodial bamboo (Dendrocalamus latiflorus). PLoS One 9:e102375

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Affiliations

  1. The Nurturing Station for the State Key Laboratory of Subtropical Silviculture, Zhejiang A & F University, LinAn, 311300, Zhejiang Province, People’s Republic of China

    Mingbing Zhou, Guiyun Tao, Peiyao Pi, Yihang Zhu, Youhuang Bai & Xianwen Meng

Authors
  1. Mingbing Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guiyun Tao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peiyao Pi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yihang Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Youhuang Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xianwen Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mingbing Zhou.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Funding

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Table S1 The sequences of primers for test PhTo25 insertion sites (DOCX 15 kb)

425_2016_2544_MOESM2_ESM.xls

Supplementary Table S2 The structural characteristics, sequences and copy number of the representative sequences of 362 MITE families (XLS 242 kb)

Supplementary Table S3 The AT content of 362 MITE family sequences (XLS 66 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zhou, M., Tao, G., Pi, P. et al. Genome-wide characterization and evolution analysis of miniature inverted-repeat transposable elements (MITEs) in moso bamboo (Phyllostachys heterocycla). Planta 244, 775–787 (2016). https://doi.org/10.1007/s00425-016-2544-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-016-2544-0

Keywords

  • Amplification
  • Bamboo
  • Gene expression
  • Insertion date
  • Miniature inverted-repeat transposable elements (MITEs)
  • Small RNA