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Transposable elements employ distinct integration strategies with respect to transcriptional landscapes in eukaryotic genomes.

ABSTRACT: Transposable elements (TEs) are ubiquitous DNA segments capable of moving from one site to another within host genomes. The extant distributions of TEs in eukaryotic genomes have been shaped by both bona fide TE integration preferences in eukaryotic genomes and by selection following integration. Here, we compare TE target site distribution in host genomes using multiple de novo transposon insertion datasets in both plants and animals and compare them in the context of genome-wide transcriptional landscapes. We showcase two distinct types of transcription-associated TE targeting strategies that suggest a process of convergent evolution among eukaryotic TE families. The integration of two precision-targeting elements are specifically associated with initiation of RNA Polymerase II transcription of highly expressed genes, suggesting the existence of novel mechanisms of precision TE targeting in addition to passive targeting of open chromatin. We also highlight two features that can facilitate TE survival and rapid proliferation: tissue-specific transposition and minimization of negative impacts on nearby gene function due to precision targeting.

SUBMITTER: Zhang X

PROVIDER: S-EPMC7337890 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Transposable elements employ distinct integration strategies with respect to transcriptional landscapes in eukaryotic genomes.

Zhang Xinyan X Zhao Meixia M McCarty Donald R DR Lisch Damon D

Nucleic acids research 20200701 12

Transposable elements (TEs) are ubiquitous DNA segments capable of moving from one site to another within host genomes. The extant distributions of TEs in eukaryotic genomes have been shaped by both bona fide TE integration preferences in eukaryotic genomes and by selection following integration. Here, we compare TE target site distribution in host genomes using multiple de novo transposon insertion datasets in both plants and animals and compare them in the context of genome-wide transcriptiona ...[more]

PMID: 32442316

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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.

Project description:BackgroundMutator-like elements (MULEs) are a significant superfamily of DNA transposons on account of their: (i) great transpositional activity and propensity for insertion in or near gene sequences, (ii) their consequent high mutagenic capacity, and, (iii) their tendency to acquire host gene fragments. Consequently, MULEs are important genetic tools and represent a key study system for research into host-transposon interactions. Yet, while several studies have focused on the impacts of MULEs on crop and fungus genomes, their evolution remains poorly explored.ResultsWe perform comprehensive bioinformatic and phylogenetic analyses to address currently available MULE diversity and reconstruct evolution for the group. For this, we mine MULEs from online databases, and combine search results with available transposase sequences retrieved from previously published studies. Our analyses uncover two entirely new MULE clades that contain elements almost entirely restricted to arthropod hosts, considerably expanding the set of MULEs known from this group, suggesting that many additional MULEs may await discovery from further arthropod genomes. In several cases, close relationships occur between MULEs recovered from distantly related host organisms, suggesting that horizontal transfer events may have played an important role in the evolution of the group. However, it is apparent that MULEs from plants remain separate from MULEs identified from other host groups. MULE structure varies considerably across phylogeny, and TIR length is shown to vary greatly both within and between MULE groups. Our phylogeny suggests that MULE diversity is clustered in well-supported groups, typically according to host taxonomy. With reference to this, we make suggestions on how MULE diversity can be partitioned to provide a robust taxonomic framework.ConclusionsOur study represents a considerable advance in the understanding of MULE diversity, host range and evolution, and provides a taxonomic framework for the classification of further MULE elements that await discovery. Our findings also raise a number of questions relating to MULE biology, suggesting that this group will provide a rich avenue for future study.

Project description:BackgroundClass 2 transposable elements (TEs) are the predominant elements in and around plant genes where they generate significant allelic diversity. Using the complete sequences of four grasses, we have performed a novel comparative analysis of class 2 TEs. To ensure consistent comparative analyses, we re-annotated class 2 TEs in Brachypodium distachyon, Oryza sativa (rice), Sorghum bicolor and Zea mays and assigned them to one of the five cut-and-paste superfamilies found in plant genomes (Tc1/mariner, PIF/Harbinger, hAT, Mutator, CACTA). We have focused on noncoding elements because of their abundance, and compared superfamily copy number, size and genomic distribution as well as correlation with the level of nearby gene expression.ResultsOur comparison revealed both unique and conserved features. First, the average length or size distribution of elements in each superfamily is largely conserved, with the shortest always being Tc1/mariner elements, followed by PIF/Harbinger, hAT, Mutator and CACTA. This order also holds for the ratio of the copy numbers of noncoding to coding elements. Second, with the exception of CACTAs, noncoding TEs are enriched within and flanking genes, where they display conserved distribution patterns, having the highest peak in the promoter region. Finally, our analysis of microarray data revealed that genes associated with Tc1/mariner and PIF/Harbinger noncoding elements have significantly higher expression levels than genes without class 2 TEs. In contrast, genes with CACTA elements have significantly lower expression than genes without class 2 TEs.ConclusionsWe have achieved the most comprehensive annotation of class 2 TEs to date in these four grass genomes. Comparative analysis of this robust dataset led to the identification of several previously unknown features of each superfamily related to copy number, element size, genomic distribution and correlation with the expression levels of nearby genes. These results highlight the importance of distinguishing TE superfamilies when assessing their impact on gene and genome evolution.

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Transposable elements employ distinct integration strategies with respect to transcriptional landscapes in eukaryotic genomes.

Publications

Transposable elements employ distinct integration strategies with respect to transcriptional landscapes in eukaryotic genomes.

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