Abstract
In eukaryotes, small noncoding RNA molecules of 16–29 nucleotides in length play crucial roles in the regulation of gene expression. Some 377 sequences representing rice pseudo-microRNAs (miRNAs) are available in release 13.0 of the miRBase sequence database (http://microrna.sanger.ac.uk/sequences/index.shtml) and are grouped into 143 families. Most newly deposited miRNA sequences are likely to be species-specific. To understand the relationship between miRNAs and transposable elements (TEs) in rice, the RepeatMasker application (http://www.repeatmasker.org/cgi-bin/WEBRepeatMasker) was used to screen single-stranded precursor miRNA (pre-miRNA) sequences. This analysis revealed that 33.1% of miRNAs and 36.4% of miRNA families are associated with interspersed repeats, and most of them are species-specific. Furthermore, multiple miRNA families can be encoded by the same TE class. Alignment analysis revealed that miR439 originated from an MuDR4-OS TE, which amplified and diversified in the genome as an inverted repeat of the core sequence followed by multiple repeats. Multiple copies of miR445 and its complexity originate from and are driven by the DNA/Tourist TE class. These results provide an important contribution to the elucidation of TE-driven mechanisms that regulate the species specificity and complexity of rice miRNAs.
Similar content being viewed by others
References
Allen E, Xie Z, Gustafson AM, Sung GH, Spatafora JW, Carrington JC (2004) Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat Genet 36:1282–1290
Arteaga-Vázquez M, Caballero-Pérez J, Vielle-Calzada JP (2006) A family of microRNAs present in plants and animals. Plant Cell 18:3355–3369
Barakat A, Wall K, Leebens-Mack J, Wang YJ, Carlson JE, Depamphilis CW (2007) Large-scale identification of microRNAs from a basal eudicot (Eschscholzia californica) and conservation in flowering plants. Plant J 51:991–1003
Bartel B, Bartel DP (2003) MicroRNAs: at the root of plant development. Plant Physiol 132:709–717
Bartel DP, Chen CZ (2004) Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs. Nat Rev Genet 5:396–400
Bennetzen JL (2000) Transposable element contributions to plant gene and genome evolution. Plant Mol Biol 42:251–269
Bennetzen JL, Coleman C, Liu R, Ma J, Ramakrishna W (2004) Consistent over-estimation of gene number in complex plant genomes. Curr Opin Plant Biol 7:732–736
Bompfünewerer AF, Flamm C, Fried C, Fritzsch G, Hofacker IL, Lehmann J, Missal K, Mosig A, Müller B, Prohaska SJ, MR SB, Stadler PF, Tanzer A, Washietl S, Witwer C (2005) Evolutionary patterns of non-coding RNAs. Theor Biosci 123:301–369
Bonnet E, Wuyts J, Rouze P, Peer Y (2004) Detection of 91 potential conserved plant microRNAs in Arabidopsis thaliana and Oryza sativa identifies important target genes. Proc Natl Acad Sci U S A 101:11511–11516
de Felippes FF, Schneeberger K, Dezulian T, Huson DH, Weigel D (2008) Evolution of Arabidopsis thaliana microRNAs from random sequences. RNA 14:2455–2459
Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Law TF, Grant SR, Dangl JL, Carrington JC (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS ONE 2:e219
Feschotte C, Jiang N, Wessler SR (2002) Plant transposable elements: where genetics meets genomics. Nat Rev Genet 3:329–341
Guyot R, Keller B (2004) Ancestral genome duplication in rice. Genome 47:610–614
Hutvagner G, Zamo PD (2002) A microRNA in a multiple-turnover RNAi enzyme complex. Science 297:2056–2060
International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800
Jiang N, Bao Z, Zhang X, Eddy SR, Wessler SR (2004) Pack-MULE transposable elements mediate gene evolution in plants. Nature 431:569–573
Jiang DH, Yin CS, Yu AP, Zhou XF, Liang WQ, Yuan Z, Xu Y, Yu QB, Wen TQ, Zhang DB (2006) Duplication and expression analysis of multicopy miRNA gene family members in Arabidopsis and rice. Cell Res 16:507–518
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
Lagos-Quintana M, Rauhut R, Meyer J, Borkhardt A, Tuschl T (2003) New microRNAs from mouse and human. RNA 9:175–179
Lai EC (2002) Micro RNAs are complementary to 3′ UTR sequence motifs that mediate negative post-transcriptional regulation. Nat Genet 30:363–364
Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854
Lee YS, Nakahara K, Pham JW, Kim K, He Z, Sontheimer EJ, Carthew RW (2004) Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117:69–81
Lewis BP, Shih I, Jones-Rhoades M, Bartel D, Burge C (2003) Prediction of mammalian microRNA targets. Cell 115:787–798
Li A, Mao L (2007) Evolution of plant microRNA gene families. Cell Res 17:212–218
Li Y, Li W, Jin YX (2005) Computational identification of novel family members of microRNA genes in Arabidopsis thaliana and Oryza sativa. Acat Biochim Biophys Sin (Shanghai) 37:75–87
Lu C, Jeong DH, Kulkarni K, Pillay M, Nobuta K, German R, Thatcher SR, Maher C, Zhang LF, Ware D, Liu B, Cao XF, Meyers BC, Green PJ (2008) Genome-wide analysis for discovery of rice microRNAs reveals natural antisense microRNAs (nat-miRNAs). Proc Natl Acad Sci U S A 105:4951–4956
Ma J, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci U S A 101:12404–12410
Maher C, Stein L, Ware D (2006) Evolution of Arabidopsis microRNA families through duplication events. Genome Res 16:510–519
Mallory AC, Vaucheret H (2006) Function of microRNAs and related small RNAs in plants. Nat Genet 38 Suppl:S31–S36
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
Parsons TJ, Bradshaw HD Jr, Gordon MP (1989) Systemic accumulation of specific mRNAs in response to wounding in poplar trees. Proc Natl Acad Sci USA 86:7895–7899
Piriyapongsa J, Jordan IK (2008) Dual coding of siRNAs and miRNAs by plant transposable elements. RNA 14:814–821
Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16:1616–1626
Ruvkun G (2001) Glimpses of a tiny rNA world molecular biology. Science 294:797–799
Schween G, Gorr G, Hohe A, Reski R (2003) Unique tissue-specific cell cycle in Physcomitrella. Plant Biol 5:50–58
Slotkin RK, Freeling M, Lisch D (2005) Heritable transposon silencing initiated by a naturally occurring transposon inverted duplication. Nat Genet 37:641–644
Sunkar R, Jagadeeswaran G (2008) In silico identification of conserved microRNAs in large number of diverse plant species. BMC Plant Biol 8:37
Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2005
Sunkar R, Girke T, Jain PK, Zhu JK (2005) Cloning and characterization of microRNAs from rice. Plant Cell 17:1397–1411
Sunkar R, Zhou X, Zheng Y, Zhang W, Zhu JK (2008) Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol 8:25
Takuno S, Innan H (2008) Evolution of complexity in miRNA-mediated gene regulation systems. Trend Genet 24:56–59
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Wang S, Zhu QH, Guo XY, Gui YJ, Bao JD, Helliwell C, Fan LJ (2007) Molecular evolution and selection of a gene encoding two tandem microRNAs in rice. FEBS Lett 581:4789–4793
Wightman B, Ha I, Ruvkun G (1993) Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75:855–862
Xue LJ, Zhang JJ, Xue HW (2009) Characterization and expression profiles of miRNAs in rice seeds. Nucl Acids Res 37:916–930
Zhang BH, Pan XP, Wang QL, Cobb GP, Anderson TA (2005) Identification and characterization of new plant microRNAs using EST analysis. Cell Res 15:336–360
Zhang B, Pan X, Cannon CH, Cobb GP, Anderson TA (2006) Conservation and divergence of plant microRNA genes. Plant J 46:243–259
Zhang B, Stellwag EJ, Pan X (2009) Large-scale genome analysis reveals unique features of microRNAs. Gene 443:100–109
Zhu QH, Spriggs A, Matthew L, Fan L, Kennedy G, Gubler F, Helliwell C (2008) A diverse set of microRNAs and microRNA-like small RNAs in developing rice grains. Genome Res 18:1456–1465
Acknowledgements
We thank Dr. Lida Zhang (Plant Biotechnology Research Center, Shanghai Jiaotong University, Shanghai, China) for giving some valuable advice. This research is supported by National Natural Science Foundation of China (30830071) and Shanghai Rising-Star Program (07QA14045).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplement Table 1
List of microRNA families and its members in rice (XLS 72 kb)
Supplement Table 2
Rice microRNA genes derived from interspersed repeats (XLS 41 kb)
Supplement Table 3
Arabidopsis microRNA genes derived from interspersed repeats (XLS 19 kb)
Supplement Table 4
Pre-miR439, pre-miR439*, and their homologs in rice genome (XLS 20 kb)
Supplement Table 5
Pre-miR445 and their homologs in rice genome (XLS 39 kb)
Supplement Fig. 1
Potential secondary structures of precursor miR439i and its homologs in rice genome. The genome loci of miR439i1-5 were shown in Supplement Table 4. The bars indicate the responding miR439i sequence (GIF 206 kb)
Supplement Fig. 2
Alignment of miR439 gene region in rice genome. The box and broken box indicated the mature sequence domain and the complementary sequences, respectively. The underline and broken lines indicated the matrue sequence of miR439j and its complementary sequence (GIF 1025 kb)
Rights and permissions
About this article
Cite this article
Yu, S., Li, J. & Luo, L. Complexity and Specificity of Precursor microRNAs Driven by Transposable Elements in Rice. Plant Mol Biol Rep 28, 502–511 (2010). https://doi.org/10.1007/s11105-009-0175-3
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-009-0175-3