Non-allelic gene conversion enables rapid evolutionary change at multiple regulatory sites encoded by transposable elements

  1. Christopher E Ellison
  2. Doris Bachtrog  Is a corresponding author
  1. University of California, Berkeley, United States

Abstract

Transposable elements (TEs) allow rewiring of regulatory networks, and the recent amplification of the ISX-element dispersed 77 functional but suboptimal binding-sites for the dosage-compensation-complex to a newly-formed X-chromosome in Drosophila. Here we identify two linked refining-mutations within ISX that interact epistatically to increase binding affinity to the dosage-compensation-complex. Selection has increased the frequency of this derived haplotype in the population, which is fixed at 30% of ISX-insertions and polymorphic among another 41%. Sharing of this haplotype indicates that high levels of gene-conversion among ISX-elements allow them to 'crowd-source' refining-mutations, and a refining-mutation that occurs at any single ISX-element can spread in two dimensions: horizontally across insertion sites by non-allelic gene-conversion, and vertically through the population by natural selection. These describes a novel route how fully functional regulatory elements can arise rapidly from TEs and implicate non-allelic gene-conversion as having an important role in accelerating the evolutionary fine-tuning of regulatory networks.

Article and author information

Author details

  1. Christopher E Ellison

    Department of Integrative Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Doris Bachtrog

    Department of Integrative Biology, University of California, Berkeley, Berkeley, United States
    For correspondence
    dbachtrog@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.

Copyright

© 2015, Ellison & Bachtrog

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 2,311
    views
  • 372
    downloads
  • 31
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Christopher E Ellison
  2. Doris Bachtrog
(2015)
Non-allelic gene conversion enables rapid evolutionary change at multiple regulatory sites encoded by transposable elements
eLife 4:e05899.
https://doi.org/10.7554/eLife.05899

Share this article

https://doi.org/10.7554/eLife.05899

Further reading

    1. Biochemistry and Chemical Biology
    2. Genetics and Genomics
    Jiale Zhou, Ding Zhao ... Zhanjun Li
    Research Article

    5-Methylcytosine (m5C) is one of the posttranscriptional modifications in mRNA and is involved in the pathogenesis of various diseases. However, the capacity of existing assays for accurately and comprehensively transcriptome-wide m5C mapping still needs improvement. Here, we develop a detection method named DRAM (deaminase and reader protein assisted RNA methylation analysis), in which deaminases (APOBEC1 and TadA-8e) are fused with m5C reader proteins (ALYREF and YBX1) to identify the m5C sites through deamination events neighboring the methylation sites. This antibody-free and bisulfite-free approach provides transcriptome-wide editing regions which are highly overlapped with the publicly available bisulfite-sequencing (BS-seq) datasets and allows for a more stable and comprehensive identification of the m5C loci. In addition, DRAM system even supports ultralow input RNA (10 ng). We anticipate that the DRAM system could pave the way for uncovering further biological functions of m5C modifications.

    1. Genetics and Genomics
    2. Microbiology and Infectious Disease
    Iti Mehta, Jacob B Hogins ... Larry Reitzer
    Research Article

    Polyamines are biologically ubiquitous cations that bind to nucleic acids, ribosomes, and phospholipids and, thereby, modulate numerous processes, including surface motility in Escherichia coli. We characterized the metabolic pathways that contribute to polyamine-dependent control of surface motility in the commonly used strain W3110 and the transcriptome of a mutant lacking a putrescine synthetic pathway that was required for surface motility. Genetic analysis showed that surface motility required type 1 pili, the simultaneous presence of two independent putrescine anabolic pathways, and modulation by putrescine transport and catabolism. An immunological assay for FimA—the major pili subunit, reverse transcription quantitative PCR of fimA, and transmission electron microscopy confirmed that pili synthesis required putrescine. Comparative RNAseq analysis of a wild type and ΔspeB mutant which exhibits impaired pili synthesis showed that the latter had fewer transcripts for pili structural genes and for fimB which codes for the phase variation recombinase that orients the fim operon promoter in the ON phase, although loss of speB did not affect the promoter orientation. Results from the RNAseq analysis also suggested (a) changes in transcripts for several transcription factor genes that affect fim operon expression, (b) compensatory mechanisms for low putrescine which implies a putrescine homeostatic network, and (c) decreased transcripts of genes for oxidative energy metabolism and iron transport which a previous genetic analysis suggests may be sufficient to account for the pili defect in putrescine synthesis mutants. We conclude that pili synthesis requires putrescine and putrescine concentration is controlled by a complex homeostatic network that includes the genes of oxidative energy metabolism.