Dataset Information

Unexpected invasion of miniature inverted-repeat transposable elements in viral genomes.

ABSTRACT: Background:Transposable elements (TEs) are common and often present with high copy numbers in cellular genomes. Unlike in cellular organisms, TEs were previously thought to be either rare or absent in viruses. Almost all reported TEs display only one or two copies per viral genome. In addition, the discovery of pandoraviruses with genomes up to 2.5-Mb emphasizes the need for biologists to rethink the fundamental nature of the relationship between viruses and cellular life. Results:Herein, we performed the first comprehensive analysis of miniature inverted-repeat transposable elements (MITEs) in the 5170 viral genomes for which sequences are currently available. Four hundred and fifty one copies of ten miniature inverted-repeat transposable elements (MITEs) were found and each MITE had reached relatively large copy numbers (some up to 90) in viruses. Eight MITEs belonging to two DNA superfamilies (hobo/Activator/Tam3 and Chapaev-Mirage-CACTA) were for the first time identified in viruses, further expanding the organismal range of these two superfamilies. TEs may play important roles in shaping the evolution of pandoravirus genomes, which were here found to be very rich in MITEs. We also show that putative autonomous partners of seven MITEs are present in the genomes of viral hosts, suggesting that viruses may borrow the transpositional machinery of their cellular hosts' autonomous elements to spread MITEs and colonize their own genomes. The presence of seven similar MITEs in viral hosts, suggesting horizontal transfers (HTs) as the major mechanism for MITEs propagation. Conclusions:Our discovery highlights that TEs contribute to shape genome evolution of pandoraviruses. We concluded that as for cellular organisms, TEs are part of the pandoraviruses' diverse mobilome.

SUBMITTER: Zhang HH

PROVIDER: S-EPMC6004678 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Unexpected invasion of miniature inverted-repeat transposable elements in viral genomes.

Zhang Hua-Hao HH Zhou Qiu-Zhong QZ Wang Ping-Lan PL Xiong Xiao-Min XM Luchetti Andrea A Raoult Didier D Levasseur Anthony A Santini Sebastien S Abergel Chantal C Legendre Matthieu M Drezen Jean-Michel JM Béliveau Catherine C Cusson Michel M Jiang Shen-Hua SH Bao Hai-Ou HO Sun Cheng C Bureau Thomas E TE Cheng Peng-Fei PF Han Min-Jin MJ Zhang Ze Z Zhang Xiao-Gu XG Dai Fang-Yin FY

Mobile DNA 20180618

<h4>Background</h4>Transposable elements (TEs) are common and often present with high copy numbers in cellular genomes. Unlike in cellular organisms, TEs were previously thought to be either rare or absent in viruses. Almost all reported TEs display only one or two copies per viral genome. In addition, the discovery of pandoraviruses with genomes up to 2.5-Mb emphasizes the need for biologists to rethink the fundamental nature of the relationship between viruses and cellular life.<h4>Results</h4 ...[more]

PMID: 29946369

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Project description:BackgroundMiniature inverted-repeat transposable elements (MITEs) are non-autonomous DNA transposable elements that play important roles in genome organization and evolution. Genome-wide identification and characterization of MITEs provide essential information for understanding genome structure and evolution.ResultsWe performed genome-wide identification and characterization of MITEs in the pineapple genome. The top two MITE families, accounting for 29.39% of the total MITEs and 3.86% of the pineapple genome, have insertion preference in (TA) n dinucleotide microsatellite regions. We therefore named these MITEs A. comosus microsatellite-associated MITEs (Ac-mMITEs). The two Ac-mMITE families, Ac-mMITE-1 and Ac-mMITE-2, shared sequence similarity in the terminal inverted repeat (TIR) regions, suggesting that these two Ac-mMITE families might be derived from a common or closely related autonomous elements. The Ac-mMITEs are frequently clustered via adjacent insertions. Among the 21,994 full-length Ac-mMITEs, 46.1% of them were present in clusters. By analyzing the Ac-mMITEs without (TA) n microsatellite flanking sequences, we found that Ac-mMITEs were likely derived from Mutator-like DNA transposon. Ac-MITEs showed highly polymorphic insertion sites between cultivated pineapples and their wild relatives. To better understand the evolutionary history of Ac-mMITEs, we filtered and performed comparative analysis on the two distinct groups of Ac-mMITEs, microsatellite-targeting MITEs (mt-MITEs) that are flanked by dinucleotide microsatellites on both sides and mutator-like MITEs (ml-MITEs) that contain 9/10 bp TSDs. Epigenetic analysis revealed a lower level of host-induced silencing on the mt-MITEs in comparison to the ml-MITEs, which partially explained the significantly higher abundance of mt-MITEs in pineapple genome. The mt-MITEs and ml-MITEs exhibited differential insertion preference to gene-related regions and RNA-seq analysis revealed their differential influences on expression regulation of nearby genes.ConclusionsAc-mMITEs are the most abundant MITEs in the pineapple genome and they were likely derived from Mutator-like DNA transposon. Preferential insertion in (TA) n microsatellite regions of Ac-mMITEs occurred recently and is likely the result of damage-limiting strategy adapted by Ac-mMITEs during co-evolution with their host. Insertion in (TA) n microsatellite regions might also have promoted the amplification of mt-MITEs. In addition, mt-MITEs showed no or negligible impact on nearby gene expression, which may help them escape genome control and lead to their amplification.

Dataset Information

Unexpected invasion of miniature inverted-repeat transposable elements in viral genomes.

Publications

Unexpected invasion of miniature inverted-repeat transposable elements in viral genomes.

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