Sex and the TEs: Transposable Elements in Sexual Development and Function in Animals

Overview

Journal Mob DNA

Publisher Biomed Central

Specialty Genetics

Date 2019 Nov 9

PMID 31700550

Citations 38

Authors

Corentin Dechaud

Jean-Nicolas Volff

Manfred Schartl

Magali Naville

Affiliations

Soon will be listed here.

Abstract

Transposable elements are endogenous DNA sequences able to integrate into and multiply within genomes. They constitute a major source of genetic innovations, as they can not only rearrange genomes but also spread ready-to-use regulatory sequences able to modify host gene expression, and even can give birth to new host genes. As their evolutionary success depends on their vertical transmission, transposable elements are intrinsically linked to reproduction. In organisms with sexual reproduction, this implies that transposable elements have to manifest their transpositional activity in germ cells or their progenitors. The control of sexual development and function can be very versatile, and several studies have demonstrated the implication of transposable elements in the evolution of sex. In this review, we report the functional and evolutionary relationships between transposable elements and sexual reproduction in animals. In particular, we highlight how transposable elements can influence expression of sexual development genes, and how, reciprocally, they are tightly controlled in gonads. We also review how transposable elements contribute to the organization, expression and evolution of sexual development genes and sex chromosomes. This underscores the intricate co-evolution between host functions and transposable elements, which regularly shift from a parasitic to a domesticated status useful to the host.

Citing Articles

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References

Koene J . Sex determination and gender expression: Reproductive investment in snails. Mol Reprod Dev. 2016; 84(2):132-143. PMC: 6220956. DOI: 10.1002/mrd.22662. View

Graveley B, Brooks A, Carlson J, Duff M, Landolin J, Yang L . The developmental transcriptome of Drosophila melanogaster. Nature. 2010; 471(7339):473-9. PMC: 3075879. DOI: 10.1038/nature09715. View

Tomaszkiewicz M, Chalopin D, Schartl M, Galiana D, Volff J . A multicopy Y-chromosomal SGNH hydrolase gene expressed in the testis of the platyfish has been captured and mobilized by a Helitron transposon. BMC Genet. 2014; 15:44. PMC: 4021074. DOI: 10.1186/1471-2156-15-44. View

Wang M, Branco A, Lemos B . The Y Chromosome Modulates Splicing and Sex-Biased Intron Retention Rates in . Genetics. 2017; 208(3):1057-1067. PMC: 5844322. DOI: 10.1534/genetics.117.300637. View

Jazin E, Cahill L . Sex differences in molecular neuroscience: from fruit flies to humans. Nat Rev Neurosci. 2009; 11(1):9-17. DOI: 10.1038/nrn2754. View

Wright S, Finnegan D . Genome evolution: sex and the transposable element. Curr Biol. 2001; 11(8):R296-9. DOI: 10.1016/s0960-9822(01)00168-3. View

Hadziselimovic F, Hadziselimovic N, Demougin P, Krey G, Oakeley E . Piwi-pathway alteration induces LINE-1 transposon derepression and infertility development in cryptorchidism. Sex Dev. 2015; 9(2):98-104. DOI: 10.1159/000375351. View

Kapitonov V, Jurka J . RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol. 2005; 3(6):e181. PMC: 1131882. DOI: 10.1371/journal.pbio.0030181. View

Biemont C, Vieira C . Genetics: junk DNA as an evolutionary force. Nature. 2006; 443(7111):521-4. DOI: 10.1038/443521a. View

10.

Rishishwar L, Tellez Villa C, Jordan I . Transposable element polymorphisms recapitulate human evolution. Mob DNA. 2015; 6:21. PMC: 4647816. DOI: 10.1186/s13100-015-0052-6. View

11.

Zempleni J, Chew Y, Bao B, Pestinger V, Wijeratne S . Repression of transposable elements by histone biotinylation. J Nutr. 2009; 139(12):2389-92. PMC: 2777482. DOI: 10.3945/jn.109.111856. View

12.

Schartl M, Schories S, Wakamatsu Y, Nagao Y, Hashimoto H, Bertin C . Sox5 is involved in germ-cell regulation and sex determination in medaka following co-option of nested transposable elements. BMC Biol. 2018; 16(1):16. PMC: 5789577. DOI: 10.1186/s12915-018-0485-8. View

13.

Schartl M, Schmid M, Nanda I . Dynamics of vertebrate sex chromosome evolution: from equal size to giants and dwarfs. Chromosoma. 2015; 125(3):553-71. DOI: 10.1007/s00412-015-0569-y. View

14.

Dolgin E, Charlesworth B . The fate of transposable elements in asexual populations. Genetics. 2006; 174(2):817-27. PMC: 1602064. DOI: 10.1534/genetics.106.060434. View

15.

Kim V, Han J, Siomi M . Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol. 2009; 10(2):126-39. DOI: 10.1038/nrm2632. View

16.

Zeyl C, Bell G, Green D . Sex and the spread of retrotransposon Ty3 in experimental populations of Saccharomyces cerevisiae. Genetics. 1996; 143(4):1567-77. PMC: 1207421. DOI: 10.1093/genetics/143.4.1567. View

17.

Chen S, Zhang G, Shao C, Huang Q, Liu G, Zhang P . Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle. Nat Genet. 2014; 46(3):253-60. DOI: 10.1038/ng.2890. View

18.

Lyon M . The Lyon and the LINE hypothesis. Semin Cell Dev Biol. 2004; 14(6):313-8. DOI: 10.1016/j.semcdb.2003.09.015. View

19.

Meisel R, Gonzales C, Luu H . The house fly Y Chromosome is young and minimally differentiated from its ancient X Chromosome partner. Genome Res. 2017; 27(8):1417-1426. PMC: 5538557. DOI: 10.1101/gr.215509.116. View

20.

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