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Genetic analysis of loop sequences in the let-7 gene family reveal a relationship between loop evolution and multiple isomiRs.

Liang T, Yang C, Li P, Liu C, Guo L - PLoS ONE (2014)

Bottom Line: Examination of these loop sequence length distributions, in addition to phylogenetic tree construction, implicated loop sequences as the main evolutionary drivers in miRNA genes.Moreover, loops from relevant clustered miRNA gene families showed varying length distributions and higher levels of nucleotide divergence, even between homologous pre-miRNA loops.Overall, this study provides further insight into miRNA processing and maturation and further enriches our understanding of miRNA biogenesis.

View Article: PubMed Central - PubMed

Affiliation: Jiangsu Key Laboratory for Molecular and Medical Biotechnology, College of Life Science, Nanjing Normal University, Nanjing, 210023, China.

ABSTRACT
While mature miRNAs have been widely studied, the terminal loop sequences are rarely examined despite regulating both primary and mature miRNA functions. Herein, we attempted to understand the evolutionary pattern of loop sequences by analyzing loops in the let-7 gene family. Compared to the stable miRNA length distributions seen in most metazoans, higher metazoan species exhibit a longer length distribution. Examination of these loop sequence length distributions, in addition to phylogenetic tree construction, implicated loop sequences as the main evolutionary drivers in miRNA genes. Moreover, loops from relevant clustered miRNA gene families showed varying length distributions and higher levels of nucleotide divergence, even between homologous pre-miRNA loops. Furthermore, we found that specific nucleotides were dominantly distributed in the 5' and 3' terminal loop ends, which may contribute to the relatively precise cleavage that leads to a stable isomiR expression profile. Overall, this study provides further insight into miRNA processing and maturation and further enriches our understanding of miRNA biogenesis.

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Related in: MedlinePlus

Sequence diversity and length distribution of the loop sequences among different animal species.(aae, Aedes aegypti; aca, Anolis carolinensis; aga, Anopheles gambiae; age, Ateles geoffroyi; aja, Artibeus jamaicensis; ame, Apis mellifera; api, Acyrthosiphon pisum; asu, Ascaris suum; bbe, Branchiostoma belcheri; bfl, Branchiostoma floridae; bma, Brugia malayi; bmo, Bombyx mori; bta, Bos taurus; cbn, Caenorhabditis brenneri; cbr, Caenorhabditis briggsae; ccr, Cyprinus carpio; cel, Caenorhabditis elegans; cfa, Canis familiaris; cgr, Cricetulus griseus; cin, Ciona intestinalis; cqu, Culex quinquefasciatus; crm, Caenorhabditis remanei; csa, Ciona savignyi; cte, Capitella teleta; dan, Drosophila ananassae; der, Drosophila erecta; dgr, Drosophila grimshawi; dme, Drosophila melanogaster; dmo, Drosophila mojavensis; dpe, Drosophila persimilis; dps, Drosophila pseudoobscura; dre, Danio rerio; dse, Drosophila sechellia; dsi, Drosophila simulans; dvi, Drosophila virilis; dwi, Drosophila willistoni; dya, Drosophila yakuba; eca, Equus caballus; egr, Echinococcus granulosus; emu, Echinococcus multilocularis; fru, Fugu rubripes; gga, Gallus gallus; ggo, Gorilla gorilla; hhi, Hippoglossus hippoglossus; hme, Heliconius melpomene; hsa, Homo sapiens; ipu, Ictalurus punctatus; isc, Ixodes scapularis; lgi, Lottia gigantean; mdo, Monodelphis domestica; mml, Macaca mulatta; mmu, Mus musculus; mse, Manduca sexta; ngi, Nasonia giraulti; nvi, Nasonia vitripennis; oan, Ornithorhynchus anatinus; oar, Ovis aries; ola, Oryzias latipes; pma, Petromyzon marinus; pol, Paralichthys olivaceus; ppa, Pan paniscus; ppc, Pristionchus pacificus; ppy, Pongo pygmaeus; ptr, Pan troglodytes; rno, Rattus norvegicus; sha, Sarcophilus harrisii; sja, Schistosoma japonicum; sko, Saccoglossus kowalevskii; sma, Schistosoma mansoni; spu, Strongylocentrotus purpuratus; ssc, Sus scrofa; tca, Tribolium castaneum; tgu, Taeniopygia guttata; tni, Tetraodon nigroviridis; xtr, Xenopus tropicalis).
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pone-0113042-g002: Sequence diversity and length distribution of the loop sequences among different animal species.(aae, Aedes aegypti; aca, Anolis carolinensis; aga, Anopheles gambiae; age, Ateles geoffroyi; aja, Artibeus jamaicensis; ame, Apis mellifera; api, Acyrthosiphon pisum; asu, Ascaris suum; bbe, Branchiostoma belcheri; bfl, Branchiostoma floridae; bma, Brugia malayi; bmo, Bombyx mori; bta, Bos taurus; cbn, Caenorhabditis brenneri; cbr, Caenorhabditis briggsae; ccr, Cyprinus carpio; cel, Caenorhabditis elegans; cfa, Canis familiaris; cgr, Cricetulus griseus; cin, Ciona intestinalis; cqu, Culex quinquefasciatus; crm, Caenorhabditis remanei; csa, Ciona savignyi; cte, Capitella teleta; dan, Drosophila ananassae; der, Drosophila erecta; dgr, Drosophila grimshawi; dme, Drosophila melanogaster; dmo, Drosophila mojavensis; dpe, Drosophila persimilis; dps, Drosophila pseudoobscura; dre, Danio rerio; dse, Drosophila sechellia; dsi, Drosophila simulans; dvi, Drosophila virilis; dwi, Drosophila willistoni; dya, Drosophila yakuba; eca, Equus caballus; egr, Echinococcus granulosus; emu, Echinococcus multilocularis; fru, Fugu rubripes; gga, Gallus gallus; ggo, Gorilla gorilla; hhi, Hippoglossus hippoglossus; hme, Heliconius melpomene; hsa, Homo sapiens; ipu, Ictalurus punctatus; isc, Ixodes scapularis; lgi, Lottia gigantean; mdo, Monodelphis domestica; mml, Macaca mulatta; mmu, Mus musculus; mse, Manduca sexta; ngi, Nasonia giraulti; nvi, Nasonia vitripennis; oan, Ornithorhynchus anatinus; oar, Ovis aries; ola, Oryzias latipes; pma, Petromyzon marinus; pol, Paralichthys olivaceus; ppa, Pan paniscus; ppc, Pristionchus pacificus; ppy, Pongo pygmaeus; ptr, Pan troglodytes; rno, Rattus norvegicus; sha, Sarcophilus harrisii; sja, Schistosoma japonicum; sko, Saccoglossus kowalevskii; sma, Schistosoma mansoni; spu, Strongylocentrotus purpuratus; ssc, Sus scrofa; tca, Tribolium castaneum; tgu, Taeniopygia guttata; tni, Tetraodon nigroviridis; xtr, Xenopus tropicalis).

Mentions: Although loop sequences were believed to not be well-conserved relative to the miR-#-5p and miR-#-3psequences, loop sequences in Drosophila were found to be highly conserved (Figure 2A). Loop sequences among different species or from homologous miRNAs or multicopy pre-miRNAs showed higher levels of sequence divergence. Nucleotide insertions/deletions were common in the loop sequences, even between homologous miRNAs in the same species or between multicopy pre-miRNAs. Interestingly, varying length distributions between loop sequences from different animal species were noted (Figure 2B, Padj<0.05, except between Urochordata and Lophotrochozoa, Table S1 in File S1).


Genetic analysis of loop sequences in the let-7 gene family reveal a relationship between loop evolution and multiple isomiRs.

Liang T, Yang C, Li P, Liu C, Guo L - PLoS ONE (2014)

Sequence diversity and length distribution of the loop sequences among different animal species.(aae, Aedes aegypti; aca, Anolis carolinensis; aga, Anopheles gambiae; age, Ateles geoffroyi; aja, Artibeus jamaicensis; ame, Apis mellifera; api, Acyrthosiphon pisum; asu, Ascaris suum; bbe, Branchiostoma belcheri; bfl, Branchiostoma floridae; bma, Brugia malayi; bmo, Bombyx mori; bta, Bos taurus; cbn, Caenorhabditis brenneri; cbr, Caenorhabditis briggsae; ccr, Cyprinus carpio; cel, Caenorhabditis elegans; cfa, Canis familiaris; cgr, Cricetulus griseus; cin, Ciona intestinalis; cqu, Culex quinquefasciatus; crm, Caenorhabditis remanei; csa, Ciona savignyi; cte, Capitella teleta; dan, Drosophila ananassae; der, Drosophila erecta; dgr, Drosophila grimshawi; dme, Drosophila melanogaster; dmo, Drosophila mojavensis; dpe, Drosophila persimilis; dps, Drosophila pseudoobscura; dre, Danio rerio; dse, Drosophila sechellia; dsi, Drosophila simulans; dvi, Drosophila virilis; dwi, Drosophila willistoni; dya, Drosophila yakuba; eca, Equus caballus; egr, Echinococcus granulosus; emu, Echinococcus multilocularis; fru, Fugu rubripes; gga, Gallus gallus; ggo, Gorilla gorilla; hhi, Hippoglossus hippoglossus; hme, Heliconius melpomene; hsa, Homo sapiens; ipu, Ictalurus punctatus; isc, Ixodes scapularis; lgi, Lottia gigantean; mdo, Monodelphis domestica; mml, Macaca mulatta; mmu, Mus musculus; mse, Manduca sexta; ngi, Nasonia giraulti; nvi, Nasonia vitripennis; oan, Ornithorhynchus anatinus; oar, Ovis aries; ola, Oryzias latipes; pma, Petromyzon marinus; pol, Paralichthys olivaceus; ppa, Pan paniscus; ppc, Pristionchus pacificus; ppy, Pongo pygmaeus; ptr, Pan troglodytes; rno, Rattus norvegicus; sha, Sarcophilus harrisii; sja, Schistosoma japonicum; sko, Saccoglossus kowalevskii; sma, Schistosoma mansoni; spu, Strongylocentrotus purpuratus; ssc, Sus scrofa; tca, Tribolium castaneum; tgu, Taeniopygia guttata; tni, Tetraodon nigroviridis; xtr, Xenopus tropicalis).
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4232593&req=5

pone-0113042-g002: Sequence diversity and length distribution of the loop sequences among different animal species.(aae, Aedes aegypti; aca, Anolis carolinensis; aga, Anopheles gambiae; age, Ateles geoffroyi; aja, Artibeus jamaicensis; ame, Apis mellifera; api, Acyrthosiphon pisum; asu, Ascaris suum; bbe, Branchiostoma belcheri; bfl, Branchiostoma floridae; bma, Brugia malayi; bmo, Bombyx mori; bta, Bos taurus; cbn, Caenorhabditis brenneri; cbr, Caenorhabditis briggsae; ccr, Cyprinus carpio; cel, Caenorhabditis elegans; cfa, Canis familiaris; cgr, Cricetulus griseus; cin, Ciona intestinalis; cqu, Culex quinquefasciatus; crm, Caenorhabditis remanei; csa, Ciona savignyi; cte, Capitella teleta; dan, Drosophila ananassae; der, Drosophila erecta; dgr, Drosophila grimshawi; dme, Drosophila melanogaster; dmo, Drosophila mojavensis; dpe, Drosophila persimilis; dps, Drosophila pseudoobscura; dre, Danio rerio; dse, Drosophila sechellia; dsi, Drosophila simulans; dvi, Drosophila virilis; dwi, Drosophila willistoni; dya, Drosophila yakuba; eca, Equus caballus; egr, Echinococcus granulosus; emu, Echinococcus multilocularis; fru, Fugu rubripes; gga, Gallus gallus; ggo, Gorilla gorilla; hhi, Hippoglossus hippoglossus; hme, Heliconius melpomene; hsa, Homo sapiens; ipu, Ictalurus punctatus; isc, Ixodes scapularis; lgi, Lottia gigantean; mdo, Monodelphis domestica; mml, Macaca mulatta; mmu, Mus musculus; mse, Manduca sexta; ngi, Nasonia giraulti; nvi, Nasonia vitripennis; oan, Ornithorhynchus anatinus; oar, Ovis aries; ola, Oryzias latipes; pma, Petromyzon marinus; pol, Paralichthys olivaceus; ppa, Pan paniscus; ppc, Pristionchus pacificus; ppy, Pongo pygmaeus; ptr, Pan troglodytes; rno, Rattus norvegicus; sha, Sarcophilus harrisii; sja, Schistosoma japonicum; sko, Saccoglossus kowalevskii; sma, Schistosoma mansoni; spu, Strongylocentrotus purpuratus; ssc, Sus scrofa; tca, Tribolium castaneum; tgu, Taeniopygia guttata; tni, Tetraodon nigroviridis; xtr, Xenopus tropicalis).
Mentions: Although loop sequences were believed to not be well-conserved relative to the miR-#-5p and miR-#-3psequences, loop sequences in Drosophila were found to be highly conserved (Figure 2A). Loop sequences among different species or from homologous miRNAs or multicopy pre-miRNAs showed higher levels of sequence divergence. Nucleotide insertions/deletions were common in the loop sequences, even between homologous miRNAs in the same species or between multicopy pre-miRNAs. Interestingly, varying length distributions between loop sequences from different animal species were noted (Figure 2B, Padj<0.05, except between Urochordata and Lophotrochozoa, Table S1 in File S1).

Bottom Line: Examination of these loop sequence length distributions, in addition to phylogenetic tree construction, implicated loop sequences as the main evolutionary drivers in miRNA genes.Moreover, loops from relevant clustered miRNA gene families showed varying length distributions and higher levels of nucleotide divergence, even between homologous pre-miRNA loops.Overall, this study provides further insight into miRNA processing and maturation and further enriches our understanding of miRNA biogenesis.

View Article: PubMed Central - PubMed

Affiliation: Jiangsu Key Laboratory for Molecular and Medical Biotechnology, College of Life Science, Nanjing Normal University, Nanjing, 210023, China.

ABSTRACT
While mature miRNAs have been widely studied, the terminal loop sequences are rarely examined despite regulating both primary and mature miRNA functions. Herein, we attempted to understand the evolutionary pattern of loop sequences by analyzing loops in the let-7 gene family. Compared to the stable miRNA length distributions seen in most metazoans, higher metazoan species exhibit a longer length distribution. Examination of these loop sequence length distributions, in addition to phylogenetic tree construction, implicated loop sequences as the main evolutionary drivers in miRNA genes. Moreover, loops from relevant clustered miRNA gene families showed varying length distributions and higher levels of nucleotide divergence, even between homologous pre-miRNA loops. Furthermore, we found that specific nucleotides were dominantly distributed in the 5' and 3' terminal loop ends, which may contribute to the relatively precise cleavage that leads to a stable isomiR expression profile. Overall, this study provides further insight into miRNA processing and maturation and further enriches our understanding of miRNA biogenesis.

Show MeSH
Related in: MedlinePlus