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Universal signatures of transposable element compartmentalization across eukaryotic genomes.

ABSTRACT: The evolutionary mechanisms that drive the emergence of genome architecture remain poorly understood but can now be assessed with unprecedented power due to the massive accumulation of genome assemblies spanning phylogenetic diversity^1,2. Transposable elements (TEs) are a rich source of large-effect mutations since they directly and indirectly drive genomic structural variation and changes in gene expression³. Here, we demonstrate universal patterns of TE compartmentalization across eukaryotic genomes spanning ~1.7 billion years of evolution, in which TEs colocalize with gene families under strong predicted selective pressure for dynamic evolution and involved in specific functions. For non-pathogenic species these genes represent families involved in defense, sensory perception and environmental interaction, whereas for pathogenic species, TE-compartmentalized genes are highly enriched for pathogenic functions. Many TE-compartmentalized gene families display signatures of positive selection at the molecular level. Furthermore, TE-compartmentalized genes exhibit an excess of high-frequency alleles for polymorphic TE insertions in fruit fly populations. We postulate that these patterns reflect selection for adaptive TE insertions as well as TE-associated structural variants. This process may drive the emergence of a shared TE-compartmentalized genome architecture across diverse eukaryotic lineages.

SUBMITTER: Gozashti L

PROVIDER: S-EPMC10996525 | biostudies-literature | 2024 Mar

REPOSITORIES: biostudies-literature

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Universal signatures of transposable element compartmentalization across eukaryotic genomes.

Gozashti Landen L Hartl Daniel L DL Corbett-Detig Russell R

bioRxiv : the preprint server for biology 20240327

The evolutionary mechanisms that drive the emergence of genome architecture remain poorly understood but can now be assessed with unprecedented power due to the massive accumulation of genome assemblies spanning phylogenetic diversity<sup>1,2</sup>. Transposable elements (TEs) are a rich source of large-effect mutations since they directly and indirectly drive genomic structural variation and changes in gene expression<sup>3</sup>. Here, we demonstrate universal patterns of TE compartmentalizati ...[more]

PMID: 38585780

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Project description:Purpose: The goals of this study are to identify Mutator insertion sites and determine the affect of these insertions on nearby genes Methods: Wiseq-based Mu element profiling was performed as described previously using B73/Mo17 F1 hybrid progeny seedlings. The B73 parent was carried Mutator activity that had been introgressed into the B73 genetic background. The Mo17 parent lacked active Mu elements. Thus, all new insertions were into the B73 genome. Genomic DNA was extracted from 6-day-old seedlings of B73/Mo17 hybrid plants. Amplicon-based enrichment of Mu flanking DNA was then performed. The purified PCR products were subject to Miseq-based Wideseq pipeline at Purdue Genomics Core Facility (https://www.purdue.edu/hla/sites/genomics/wideseq-2/). Wideseq reads were mapped to the B73 reference genome as described previously. By identifying the Mu target site duplications (TSDs), a set of genes targeted by Mu insertions that segregated in hybrid progeny was obtained and those containing B73/Mo17 SNPs in their mRNA sequences were used for allele-specific expression analysis. Because new insertions were into the B73 genome, the effect of these insertions would be expected to be specific in all cases to the B73 allele. To quantify the allele frequency, we performed RT-PCR followed by Wideseq from the identical shoot tissues of the hybrid seedlings mentioned above. Total RNA was extracted using the RNA Extraction Kit (Zymo) and cDNAs were synthesized using Promega M-MLV Reverse Transcriptase. For for a subset of 16 genes that carried SNPs, RNA fragments containing B73/Mo17 SNPs were amplified by RT-PCR. Libraries were prepared using an mRNA preparation kit (Illumina) following a standard protocol (https://www.purdue.edu/hla/sites/genomics/wi-deseq-2/). The RT-PCR products were then sequenced by the “WideSeq” pipeline. Results: A knockdown index was deduced by normalizing the observed ratio to that observed in genes that lacked Mu insertions in both genetic backgrounds for each insertion. We found that none of the four promoter insertions changed the expression of nearby genes. A quarter of 5’ UTR insertions (5 out of 20) caused knockout or strong knockdown effects and one of seven intronic insertions resulted in a knockout effect. Collectively, of a total of 33 Mu insertions, all of which were within 200 bp of genes, only 11 significantly reduced gene expression, and only two knocked it out completely. Conclusions: These results indicate that that Mu element insertions near TSSs of host genes are often associated with quantitative and in many cases neglectable functional consequences on nearby gene expression.

Dataset Information

Universal signatures of transposable element compartmentalization across eukaryotic genomes.

Publications

Universal signatures of transposable element compartmentalization across eukaryotic genomes.

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