Transposable Elements Employ Distinct Integration Strategies with Respect to Transcriptional Landscapes in Eukaryotic Genomes

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2020 May 23

PMID 32442316

Citations 17

Authors

Xinyan Zhang

Meixia Zhao

Donald R McCarty

Damon Lisch

Affiliations

Soon will be listed here.

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.

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References

Miyao A, Tanaka K, Murata K, Sawaki H, Takeda S, Abe K . Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retrotransposon-rich regions of the genome. Plant Cell. 2003; 15(8):1771-80. PMC: 167168. DOI: 10.1105/tpc.012559. View

Baller J, Gao J, Stamenova R, Curcio M, Voytas D . A nucleosomal surface defines an integration hotspot for the Saccharomyces cerevisiae Ty1 retrotransposon. Genome Res. 2012; 22(4):704-13. PMC: 3317152. DOI: 10.1101/gr.129585.111. View

Brookfield J . The ecology of the genome - mobile DNA elements and their hosts. Nat Rev Genet. 2005; 6(2):128-36. DOI: 10.1038/nrg1524. View

Sultana T, Zamborlini A, Cristofari G, Lesage P . Integration site selection by retroviruses and transposable elements in eukaryotes. Nat Rev Genet. 2017; 18(5):292-308. DOI: 10.1038/nrg.2017.7. View

McCarty D, Suzuki M, Hunter C, Collins J, Avigne W, Koch K . Genetic and molecular analyses of UniformMu transposon insertion lines. Methods Mol Biol. 2013; 1057:157-66. DOI: 10.1007/978-1-62703-568-2_11. View

Huang C, Burns K, Boeke J . Active transposition in genomes. Annu Rev Genet. 2012; 46:651-75. PMC: 3612533. DOI: 10.1146/annurev-genet-110711-155616. View

Chuong E, Elde N, Feschotte C . Regulatory activities of transposable elements: from conflicts to benefits. Nat Rev Genet. 2016; 18(2):71-86. PMC: 5498291. DOI: 10.1038/nrg.2016.139. View

Liu S, Yeh C, Ji T, Ying K, Wu H, Tang H . Mu transposon insertion sites and meiotic recombination events co-localize with epigenetic marks for open chromatin across the maize genome. PLoS Genet. 2009; 5(11):e1000733. PMC: 2774946. DOI: 10.1371/journal.pgen.1000733. View

Arkhipova I . Using bioinformatic and phylogenetic approaches to classify transposable elements and understand their complex evolutionary histories. Mob DNA. 2017; 8:19. PMC: 5718144. DOI: 10.1186/s13100-017-0103-2. View

10.

Tucker S, Reece J, Ream T, Pikaard C . Evolutionary history of plant multisubunit RNA polymerases IV and V: subunit origins via genome-wide and segmental gene duplications, retrotransposition, and lineage-specific subfunctionalization. Cold Spring Harb Symp Quant Biol. 2011; 75:285-97. DOI: 10.1101/sqb.2010.75.037. View

11.

Rodgers-Melnick E, Vera D, Bass H, Buckler E . Open chromatin reveals the functional maize genome. Proc Natl Acad Sci U S A. 2016; 113(22):E3177-84. PMC: 4896728. DOI: 10.1073/pnas.1525244113. View

12.

Blumenstiel J, Chen X, He M, Bergman C . An age-of-allele test of neutrality for transposable element insertions. Genetics. 2013; 196(2):523-38. PMC: 3914624. DOI: 10.1534/genetics.113.158147. View

13.

Mularoni L, Zhou Y, Bowen T, Gangadharan S, Wheelan S, Boeke J . Retrotransposon Ty1 integration targets specifically positioned asymmetric nucleosomal DNA segments in tRNA hotspots. Genome Res. 2012; 22(4):693-703. PMC: 3317151. DOI: 10.1101/gr.129460.111. View

14.

Zhang X, Zhao M, Lisch D . Cost-Effective Profiling of Mutator Transposon Insertions in Maize by Next-Generation Sequencing. Methods Mol Biol. 2019; 2072:39-50. DOI: 10.1007/978-1-4939-9865-4_5. View

15.

Zamudio N, Bourchis D . Transposable elements in the mammalian germline: a comfortable niche or a deadly trap?. Heredity (Edinb). 2010; 105(1):92-104. DOI: 10.1038/hdy.2010.53. View

16.

Spradling A, Stern D, Beaton A, Rhem E, Laverty T, Mozden N . The Berkeley Drosophila Genome Project gene disruption project: Single P-element insertions mutating 25% of vital Drosophila genes. Genetics. 1999; 153(1):135-77. PMC: 1460730. DOI: 10.1093/genetics/153.1.135. View

17.

Anxolabehere D, Kidwell M, Periquet G . Molecular characteristics of diverse populations are consistent with the hypothesis of a recent invasion of Drosophila melanogaster by mobile P elements. Mol Biol Evol. 1988; 5(3):252-69. DOI: 10.1093/oxfordjournals.molbev.a040491. View

18.

Jiang N, Ferguson A, Slotkin R, Lisch D . Pack-Mutator-like transposable elements (Pack-MULEs) induce directional modification of genes through biased insertion and DNA acquisition. Proc Natl Acad Sci U S A. 2011; 108(4):1537-42. PMC: 3029777. DOI: 10.1073/pnas.1010814108. View

19.

Zhang J, Yu C, Krishnaswamy L, Peterson T . Transposable elements as catalysts for chromosome rearrangements. Methods Mol Biol. 2010; 701:315-26. DOI: 10.1007/978-1-61737-957-4_18. View

20.

Spradling A, Bellen H, Hoskins R . Drosophila P elements preferentially transpose to replication origins. Proc Natl Acad Sci U S A. 2011; 108(38):15948-53. PMC: 3179094. DOI: 10.1073/pnas.1112960108. View