Open Access Research article

Billions of basepairs of recently expanded, repetitive sequences are eliminated from the somatic genome during copepod development

Cheng Sun1, Grace Wyngaard2, D Brian Walton3, Holly A Wichman4 and Rachel Lockridge Mueller1*

Author Affiliations

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

2 Department of Biology, James Madison University, Harrisonburg, VA 22807, USA

3 Department of Mathematics and Statistics, James Madison University, Harrisonburg, VA 22807, USA

4 Department of Biological Sciences, The Institute for Bioinformatics and Evolutionary Studies, University of Idaho, Moscow, ID 83844–3051, USA

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BMC Genomics 2014, 15:186  doi:10.1186/1471-2164-15-186

Published: 11 March 2014

Abstract

Background

Chromatin diminution is the programmed deletion of DNA from presomatic cell or nuclear lineages during development, producing single organisms that contain two different nuclear genomes. Phylogenetically diverse taxa undergo chromatin diminution — some ciliates, nematodes, copepods, and vertebrates. In cyclopoid copepods, chromatin diminution occurs in taxa with massively expanded germline genomes; depending on species, germline genome sizes range from 15 – 75 Gb, 12–74 Gb of which are lost from pre-somatic cell lineages at germline – soma differentiation. This is more than an order of magnitude more sequence than is lost from other taxa. To date, the sequences excised from copepods have not been analyzed using large-scale genomic datasets, and the processes underlying germline genomic gigantism in this clade, as well as the functional significance of chromatin diminution, have remained unknown.

Results

Here, we used high-throughput genomic sequencing and qPCR to characterize the germline and somatic genomes of Mesocyclops edax, a freshwater cyclopoid copepod with a germline genome of ~15 Gb and a somatic genome of ~3 Gb. We show that most of the excised DNA consists of repetitive sequences that are either 1) verifiable transposable elements (TEs), or 2) non-simple repeats of likely TE origin. Repeat elements in both genomes are skewed towards younger (i.e. less divergent) elements. Excised DNA is a non-random sample of the germline repeat element landscape; younger elements, and high frequency DNA transposons and LINEs, are disproportionately eliminated from the somatic genome.

Conclusions

Our results suggest that germline genome expansion in M. edax reflects explosive repeat element proliferation, and that billions of base pairs of such repeats are deleted from the somatic genome every generation. Thus, we hypothesize that chromatin diminution is a mechanism that controls repeat element load, and that this load can evolve to be divergent between tissue types within single organisms.

Keywords:
Chromatin diminution; Genome size; Transposable elements; Germline-soma differentiation; Copepod