Transposable-Element Associated Small RNAs in Bombyx mori Genome

Small RNAs are a group of regulatory RNA molecules that control gene expression at transcriptional or post-transcriptional levels among eukaryotes. The silkworm, Bombyx mori L., genome harbors abundant repetitive sequences derived from families of retrotransposons and transposons, which together constitute almost half of the genome space and provide ample resource for biogenesis of the three major small RNA families. We systematically discovered transposable-element (TE)-associated small RNAs in B. mori genome based on a deep RNA-sequencing strategy and the effort yielded 182, 788 and 4,990 TE-associated small RNAs in the miRNA, siRNA and piRNA species, respectively. Our analysis suggested that the three small RNA species preferentially associate with different TEs to create sequence and functional diversity, and we also show evidence that a Bombyx non-LTR retrotransposon, bm1645, alone contributes to the generation of TE-associated small RNAs in a very significant way. The fact that bm1645-associated small RNAs partially overlap with each other implies a possibility that this element may be modulated by different mechanisms to generate different products with diverse functions. Taken together, these discoveries expand the small RNA pool in B. mori genome and lead to new knowledge on the diversity and functional significance of TE-associated small RNAs.

[1]  K. Kadota,et al.  The silkworm W chromosome is a source of female-enriched piRNAs. , 2011, RNA.

[2]  S. Kawaoka,et al.  3' end formation of PIWI-interacting RNAs in vitro. , 2011, Molecular cell.

[3]  Hyeshik Chang,et al.  Dicer recognizes the 5′ end of RNA for efficient and accurate processing , 2011, Nature.

[4]  K. Kadota,et al.  Zygotic amplification of secondary piRNAs during silkworm embryogenesis. , 2011, RNA.

[5]  Doron Betel,et al.  Widespread regulatory activity of vertebrate microRNA* species. , 2011, RNA.

[6]  Z. Weng,et al.  Distinct Functions for the Drosophila piRNA Pathway in Genome Maintenance and Telomere Protection , 2010, PLoS genetics.

[7]  P. Zamore,et al.  Somatic piRNA biogenesis , 2010, The EMBO journal.

[8]  N. Lau Small RNAs in the animal gonad: guarding genomes and guiding development. , 2010, The international journal of biochemistry & cell biology.

[9]  Y. Fujii RNA Genes: Retroelements and Virally Retroposable microRNAs in Human Embryonic Stem Cells , 2010, The open virology journal.

[10]  Peng Cui,et al.  Novel microRNAs in silkworm (Bombyx mori) , 2010, Functional & Integrative Genomics.

[11]  N. Lau,et al.  A Broadly Conserved Pathway Generates 3′UTR-Directed Primary piRNAs , 2009, Current Biology.

[12]  K. Asai,et al.  A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila , 2009, Nature.

[13]  N. Lau,et al.  Abundant primary piRNAs, endo-siRNAs, and microRNAs in a Drosophila ovary cell line. , 2009, Genome research.

[14]  S. Sugano,et al.  The Bombyx ovary-derived cell line endogenously expresses PIWI/PIWI-interacting RNA complexes. , 2009, RNA.

[15]  Z. Weng,et al.  Collapse of Germline piRNAs in the Absence of Argonaute3 Reveals Somatic piRNAs in Flies , 2009, Cell.

[16]  Julius Brennecke,et al.  Specialized piRNA Pathways Act in Germline and Somatic Tissues of the Drosophila Ovary , 2009, Cell.

[17]  G. Verbeke,et al.  Evidence for Co-Evolution between Human MicroRNAs and Alu-Repeats , 2009, PloS one.

[18]  K. Jażdżewski,et al.  Polymorphic mature microRNAs from passenger strand of pre-miR-146a contribute to thyroid cancer , 2009, Proceedings of the National Academy of Sciences.

[19]  Kazuei Mita,et al.  The genome of a lepidopteran model insect, the silkworm Bombyx mori. , 2009, Insect biochemistry and molecular biology.

[20]  Y. Kohara,et al.  Bombyx small RNAs: genomic defense system against transposons in the silkworm, Bombyx mori. , 2008, Insect biochemistry and molecular biology.

[21]  K. Mita,et al.  Genome-wide screening and characterization of transposable elements and their distribution analysis in the silkworm, Bombyx mori. , 2008, Insect biochemistry and molecular biology.

[22]  C. Brun,et al.  piRNA-mediated nuclear accumulation of retrotransposon transcripts in the Drosophila female germline , 2008, Proceedings of the National Academy of Sciences.

[23]  Songnian Hu,et al.  The Silkworm (Bombyx mori) microRNAs and Their Expressions in Multiple Developmental Stages , 2008, PloS one.

[24]  D. Bartel,et al.  The Drosophila hairpin RNA pathway generates endogenous short interfering RNAs , 2008, Nature.

[25]  N. Perrimon,et al.  An endogenous small interfering RNA pathway in Drosophila , 2008, Nature.

[26]  Taishin Kin,et al.  Drosophila endogenous small RNAs bind to Argonaute 2 in somatic cells , 2008, Nature.

[27]  E. Lai,et al.  Endogenous RNA Interference Provides a Somatic Defense against Drosophila Transposons , 2008, Current Biology.

[28]  T. Nilsen Endo-siRNAs: yet another layer of complexity in RNA silencing , 2008, Nature Structural &Molecular Biology.

[29]  Z. Weng,et al.  Endogenous siRNAs Derived from Transposons and mRNAs in Drosophila Somatic Cells , 2008, Science.

[30]  Y. Sakaki,et al.  Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes , 2008, Nature.

[31]  Oliver H. Tam,et al.  Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes , 2008, Nature.

[32]  Peer Bork,et al.  The Genome of the Model Beetle and Pest Tribolium Castaneum Vertebrate-specific Orthologues Insect-specific Orthologues Homology Undetectable Similarity , 2022 .

[33]  Ruiqiang Li,et al.  SOAP: short oligonucleotide alignment program , 2008, Bioinform..

[34]  Melanie A. Huntley,et al.  Evolution of genes and genomes on the Drosophila phylogeny , 2007, Nature.

[35]  G. Hannon,et al.  The Piwi-piRNA Pathway Provides an Adaptive Defense in the Transposon Arms Race , 2007, Science.

[36]  Kuniaki Saito,et al.  Gene silencing mechanisms mediated by Aubergine piRNA complexes in Drosophila male gonad. , 2007, RNA.

[37]  Evgeny M. Zdobnov,et al.  Genome Sequence of Aedes aegypti, a Major Arbovirus Vector , 2007, Science.

[38]  I. K. Jordan,et al.  Origin and Evolution of Human microRNAs From Transposable Elements , 2007, Genetics.

[39]  Manolis Kellis,et al.  Discrete Small RNA-Generating Loci as Master Regulators of Transposon Activity in Drosophila , 2007, Cell.

[40]  I. King Jordan,et al.  A Family of Human MicroRNA Genes from Miniature Inverted-Repeat Transposable Elements , 2007, PloS one.

[41]  Ying Wang,et al.  Insights into social insects from the genome of the honeybee Apis mellifera , 2006, Nature.

[42]  N. Lau,et al.  Characterization of the piRNA Complex from Rat Testes , 2006, Science.

[43]  The Honeybee Genome Sequencing Consortium,et al.  Erratum: Insights into social insects from the genome of the honeybee Apis mellifera , 2006, Nature.

[44]  M. Batzer,et al.  From the margins of the genome: mobile elements shape primate evolution , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[45]  Vetle I. Torvik,et al.  Mammalian microRNAs derived from genomic repeats. , 2005, Trends in genetics : TIG.

[46]  A. Reynolds,et al.  The contributions of dsRNA structure to Dicer specificity and efficiency. , 2005, RNA.

[47]  Anton J. Enright,et al.  MicroRNA targets in Drosophila , 2003, Genome Biology.

[48]  J. V. Moran,et al.  Mobile elements and mammalian genome evolution. , 2003, Current opinion in genetics & development.

[49]  Michael Zuker,et al.  Mfold web server for nucleic acid folding and hybridization prediction , 2003, Nucleic Acids Res..

[50]  Jian Wang,et al.  The Genome Sequence of the Malaria Mosquito Anopheles gambiae , 2002, Science.

[51]  S. B. Atienza-Samols,et al.  With Contributions by , 1978 .