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Small RNAs from a Big Genome: The piRNA Pathway and Transposable Elements in the Salamander Species Desmognathus fuscus

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An Erratum to this article was published on 02 December 2016

Abstract

Most of the largest vertebrate genomes are found in salamanders, a clade of amphibians that includes 686 species. Salamander genomes range in size from 14 to 120 Gb, reflecting the accumulation of large numbers of transposable element (TE) sequences from all three TE classes. Although DNA loss rates are slow in salamanders relative to other vertebrates, high levels of TE insertion are also likely required to explain such high TE loads. Across the Tree of Life, novel TE insertions are suppressed by several pathways involving small RNA molecules. In most known animals, TE activity in the germline is primarily regulated by the Piwi-interacting RNA (piRNA) pathway. In this study, we test the hypothesis that salamanders’ unusually high TE loads reflect the loss of the ancestral piRNA-mediated TE-silencing machinery. We characterized the small RNA pool in the female and male adult gonads, testing for the presence of small RNA molecules that bear the characteristics of TE-targeting piRNAs. We also analyzed the amino acid sequences of piRNA pathway proteins from salamanders and other vertebrates, testing whether the overall patterns of sequence divergence are consistent with conserved pathway function across the vertebrate clade. Our results do not support the hypothesis of piRNA pathway loss; instead, they suggest that the piRNA pathway is expressed in salamanders. Given these results, we propose hypotheses to explain how the extraordinary TE loads in salamander genomes could have accumulated, despite the expression of TE-silencing machinery.

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Acknowledgments

This research was supported by NSF–DBI 1103746 to MM-V and NSF-DEB 1021489 to RLM. NCL was supported by the Searle Scholars Foundation and the NIH (R00HD057298). J. Krakovil and D. Weisrock (U Kentucky) provided the tissues and access to unpublished Cryptobranchus alleganiensis transcriptome data; funding for collecting trips was provided by Highlands Biological Station and the University of Kentucky Department of Biology to J. Krakovil. D. New at IBEST provided critical technical expertise. Suggestions from anonymous reviewers improved the quality of the manuscript.

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  1. Matthew L. Settles

    Present address: Bioinformatics Core, UC Davis Genome Center, Davis, CA, 95616, USA

Authors and Affiliations

  1. Department of Biology, Colorado State University, Campus Delivery 1878, Fort Collins, CO, 80523-1878, USA

    M. J. Madison-Villar, Cheng Sun & Rachel Lockridge Mueller

  2. Key Laboratory of Pollinating Insect Biology of the Ministry of Agriculture, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, 100093, China

    Cheng Sun

  3. Department of Biology, Brandeis University, Waltham, MA, 02454, USA

    Nelson C. Lau

  4. Institute for Bioinformatics and Evolutionary Studies, University of Idaho, Moscow, ID, 83844, USA

    Matthew L. Settles

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Correspondence to Rachel Lockridge Mueller.

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M. J. Madison-Villar and Cheng Sun have contributed equally.

An erratum to this article is available at http://dx.doi.org/10.1007/s00239-016-9769-1.

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Supplementary material 1 (PDF 483 kb)

Transposable element families targeted by piRNAs and siRNAs in the female and male samples. Results were obtained from mapping each small RNA dataset to its respective reference transcriptome. TE families are ranked by density of mapped small RNA reads

Supplementary material 2 (PDF 1550 kb)

Phylogenies estimated for eleven piRNA pathway protein sequences obtained from salamanders and other vertebrates

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Madison-Villar, M.J., Sun, C., Lau, N.C. et al. Small RNAs from a Big Genome: The piRNA Pathway and Transposable Elements in the Salamander Species Desmognathus fuscus . J Mol Evol 83, 126–136 (2016). https://doi.org/10.1007/s00239-016-9759-3

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