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Open Access Highly Accessed Research article

Song exposure regulates known and novel microRNAs in the zebra finch auditory forebrain

Preethi H Gunaratne123, Ya-Chi Lin4, Ashley L Benham1, Jenny Drnevich5, Cristian Coarfa11, Jayantha B Tennakoon1, Chad J Creighton6, Jong H Kim1, Aleksandar Milosavljevic11, Michael Watson7, Sam Griffiths-Jones8 and David F Clayton1049*

Author Affiliations

1 Department of Biology and Biochemistry, University of Houston, Houston, Texas 77204, USA

2 Departments of Pathology, Baylor College of Medicine, Houston, Texas 77030, USA

3 Human Genome Sequencing Center, Baylor College of Medicine, Houston, Texas 77030, USA

4 Department of Cell and Developmental Biology, University of Illinois, Urbana-Champaign, IL 61801, USA

5 W.M. Keck Center for Comparative and Functional Genomics, Roy J. Carver Biotechnology Center, University of Illinois, Urbana-Champaign, IL 61801, USA

6 Dan Duncan Cancer Center, Baylor College of Medicine, Houston, TX 77030, USA

7 ARK-Genomics, The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, EH25 9RG, UK

8 Faculty of Life Sciences, University of Manchester, Manchester, M13 9PT, UK

9 Institute for Genomic Biology, University of Illinois, Urbana-Champaign, IL 61801, USA

10 Beckman Institute, University of Illinois, Urbana-Champaign, IL 61801, USA

11 Bioinformatics Research Laboratory (BRL), Department of Molecular & Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA

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BMC Genomics 2011, 12:277  doi:10.1186/1471-2164-12-277

Published: 31 May 2011

Abstract

Background

In an important model for neuroscience, songbirds learn to discriminate songs they hear during tape-recorded playbacks, as demonstrated by song-specific habituation of both behavioral and neurogenomic responses in the auditory forebrain. We hypothesized that microRNAs (miRNAs or miRs) may participate in the changing pattern of gene expression induced by song exposure. To test this, we used massively parallel Illumina sequencing to analyse small RNAs from auditory forebrain of adult zebra finches exposed to tape-recorded birdsong or silence.

Results

In the auditory forebrain, we identified 121 known miRNAs conserved in other vertebrates. We also identified 34 novel miRNAs that do not align to human or chicken genomes. Five conserved miRNAs showed significant and consistent changes in copy number after song exposure across three biological replications of the song-silence comparison, with two increasing (tgu-miR-25, tgu-miR-192) and three decreasing (tgu-miR-92, tgu-miR-124, tgu-miR-129-5p). We also detected a locus on the Z sex chromosome that produces three different novel miRNAs, with supporting evidence from Northern blot and TaqMan qPCR assays for differential expression in males and females and in response to song playbacks. One of these, tgu-miR-2954-3p, is predicted (by TargetScan) to regulate eight song-responsive mRNAs that all have functions in cellular proliferation and neuronal differentiation.

Conclusions

The experience of hearing another bird singing alters the profile of miRNAs in the auditory forebrain of zebra finches. The response involves both known conserved miRNAs and novel miRNAs described so far only in the zebra finch, including a novel sex-linked, song-responsive miRNA. These results indicate that miRNAs are likely to contribute to the unique behavioural biology of learned song communication in songbirds.