Award details

The role of transposable elements in generating functional diversity

Reference	BB/R017174/1
Principal Investigator / Supervisor	Dr Martin Taylor
Co-Investigators / Co-Supervisors	Professor Tracey Chapman, Dr Levi Yant
Institution	University of East Anglia
Department	Biological Sciences
Funding type	Research
Value (£)	450,024
Status	Completed
Type	Research Grant
Start date	01/10/2018
End date	31/03/2022
Duration	42 months

Abstract

Transposable Elements (TEs) are ubiquitous repetitive DNA sequences that can move and multiply within genomes. They make up significant proportions of most eukaryotic genomes, for example, 85% of the maize genome and 45% of the human genome (Human Genome Consortium 2001) are TEs. Transposable Elements have historically been viewed as deleterious, however, this idea is now changing with a number of apparently beneficial impacts on host gene function and structure identified. More broadly, TEs may have macro-evolutionary impacts, with the 'epi-transposon' and 'TE-Thrust' hypotheses suggesting TE proliferation may increase speciation rates. However, a robust statistical relationship between TE abundance and speciation rate has yet to be identified. The Corydoradinae are sexual neotropical armoured catfishes comprising more than 200 extant species. A well-resolved mtDNA phylogeny which identified 9 major lineages has been previously generated by Taylor's group (Alexandrou MA, et al. (2011) Nature 469:84-88) which provides a phylogenetic framework for macro-evolutionary investigation. Further work in the Taylor group has identified considerable variation in genome size, with the smallest genome sizes with C-values of ~0.5pg and the largest ~4.5pg per haploid cell (Marburger et al. under revision Proc Roy Soc B). Transposable Element abundance increases dramatically in the species with largest genome sizes, with the TC1-superfamily increasing from <1% of the genome to ~70% of the genome across the Corydoras lineages (Marburger et al. under review Proc Roy Soc B). In this proposal, we will test the hypothesis that TE insertion and excision increases the mutation rate of gene promoter regions as a result of imperfect DNA repair by the cell and that these TE generated mutations underpins increases in lineage diversification rate - with lineages with more TEs and higher mutation rates evolving more rapidly than lineages with fewer TEs in their genomes.

Summary

The DNA housed inside the cells of all organisms contains the genes required for building and maintaining living bodies. However, in most organisms, there are other components of the genome that are not specifically required for life and these elements may multiply within the genome in a manner similar to computer viruses multiplying on a computer hard-drive. These genetic elements are known as transposable elements and come in two forms: those which use a copy and paste mechanism (type I) and those that use a cut and paste mechanism (type II). Scientists have typically viewed the presence of these elements in genomes as parasitic and their effects on the host as either neutral or negative. However, it is increasingly recognised that these mobile elements can have a positive effect on the evolutionary potential of a species. For example, the resistance of the fruit fly Drosophila melanogaster to an organophosphate pesticide has increased as a result of the production of a novel truncated protein generated by the insertion of a transposable element in an existing longer gene. Other researchers have suggested that transposable elements may have more profound impacts on biodiversity as a whole and have suggested that the insertion of transposable elements may lead to increased evolutionary potential and may explain why some groups of organisms are particularly species rich. However, to date there has been little research that goes beyond identifying a circumstantial relationship between the abundance of transposable elements and the speciation rates of a group of organisms. In this study, we will focus on a species rich group of Neotropical catfishes that (i) have considerable differences in the transposable element content of their genomes and (ii) have lineages with different rates of speciation and (iii) show a sudden increase in speciation rate ~25 million year before present which is broadly contemporaneous with the TE expansion. We will firstly quantify the abundance of different transposable elements across the genomes of Corydoras catfishes. This will provide an accurate estimate of the TE density in different species, and by mapping these onto a phylogenetic framework, the timing of TE expansions in different species will be quantified. Subsequently, we will investigate whether TEs increase the mutation rates of promoter regions as a result of the intrinsic DNA repair mechanisms that heal TE insertion / excision sites. Next we will investigate whether catfish lineages with high speciation rates have more TEs inserted in genes and promoter regions than species with low diversification rates. Finally, we will investigate whether certain groups of genes (e.g. colour pattern genes) have been more greatly affected by TEs than other genes (e.g. housekeeping genes). The results generated in this proposal will allow a thorough investigation of the role of transposable elements in increasing the diversity of genes and their promoter regions and provide important evidence as to whether TEs underpin rapid speciation in some taxonomic groups.

Impact Summary

The proposed work is expected to generate significant impacts - we describe below who will benefit and the mechanisms in place to show how that impact will be achieved. 1. DISSEMINATION OF FUNDAMENTAL SCIENCE ACROSS ACADEMIC AND PUBLIC DOMAINS: This proposal will generate a wealth of data of great interest to molecular biologists, evolutionary biologists, developmental biologists, ichthyologists, aquarists and hobbyists interested in catfishes and the general public (including schools). The data generated in the project will act as a catalyst for future investigation by both the Pi, Co-Is and PDRA as well as the groups of researchers described above. These impacts will be delivered by full research team through published papers, submission of sequences to repositories such as Genbank, press releases, science blogs and conference presentations. Public dissemination will be achieved through the whole team via the diverse outreach and engagement activities specified in the pathways to impact plan. Collectively we have a strong record in such activities We have identified a number of possibilities where the proposed research may generate broad interest. i) TE insertions and mutation rates. The role of non-coding DNA in genomes is a topic generating much debate. While this proposal does not address the role per se, it does address the IMPACT of non-coding DNA on the genome in the form of whether or not they increase mutation rates, and how this then influences macro-evolutionary patterns. Thus, linking the activity of autonomous genetic elements to organismal diversification rates would be of great interest to many molecular and evolutionary biologists and also the general public in terms of why some groups are species rich and others species poor. ii) Comparative genomics. We will generate whole genomes for 2 species of Corydoras catfish and improve the assemblies of two others. This will be of great benefit for comparative evolutionary genomics as the species sequenced are part of an adaptive radiation, some species of which have undergone whole genome duplications. Thus workers in the fields of comparative genomics, transposable elements and whole genome duplication will benefit from the genomic resources generated. This research will also interest researchers in the field of salmonid aquaculture which have also undergone a whole genome duplication iii) Developmental biologists - transposable elements (sleeping beauty) are being used to 'barcode' cells (Sun et al Nature. 2014. 514:322-327). By inducing TE activity, every cell has a unique pattern of TE insertions allowing cell lineages to be tracked during development. Thus, additional knowledge of the potential impacts of these 'barcoding' systems on the genome will be beneficial. iv) Mimicry researchers (will benefit from the genomic resources generated in this project. The Corydoras are one of the few vertebrate species that have evolved Müllerian mimicry. Thus there is ample scope to investigate the role of TEs in increasing mutation rates of colour pattern genes in this group. 2. TRAINING OF SKILLED PEOPLE FOR NON-ACADEMIC PROFESSIONS The named PDRA will benefit from manifold aspects of the project including developing computational and bioinformatics skills (python/perl/R languages) which will increase employability in both academic and non-academic environments, participation in impact and outreach activities which will develop communication and presentation skills, digital media skills (websites and animations), conference attendance will lead to better networks, increasing employability.

Committee	Research Committee C (Genes, development and STEM approaches to biology)
Research Topics	X – not assigned to a current Research Topic
Research Priority	X – Research Priority information not available
Research Initiative	X - not in an Initiative
Funding Scheme	X – not Funded via a specific Funding Scheme

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