Transcriptional Rewiring of the Sex Determining dmrt1 Gene Duplicate by Transposable Elements

Abstract

Control and coordination of eukaryotic gene expression rely on transcriptional and posttranscriptional regulatory networks. Evolutionary innovations and adaptations often require rapid changes of such networks. It has long been hypothesized that transposable elements (TE) might contribute to the rewiring of regulatory interactions. More recently it emerged that TEs might bring in ready-to-use transcription factor binding sites to create alterations to the promoters by which they were captured. A process where the gene regulatory architecture is of remarkable plasticity is sex determination. While the more downstream components of the sex determination cascades are evolutionary conserved, the master regulators can switch between groups of organisms even on the interspecies level or between populations. In the medaka fish (Oryzias latipes) a duplicated copy of dmrt1, designated dmrt1bY or DMY, on the Y chromosome was shown to be the master regulator of male development, similar to Sry in mammals. We found that the dmrt1bY gene has acquired a new feedback downregulation of its expression. Additionally, the autosomal dmrt1a gene is also able to regulate transcription of its duplicated paralog by binding to a unique target Dmrt1 site nested within the dmrt1bY proximal promoter region. We could trace back this novel regulatory element to a highly conserved sequence within a new type of TE that inserted into the upstream region of dmrt1bY shortly after the duplication event. Our data provide functional evidence for a role of TEs in transcriptional network rewiring for sub- and/or neo-functionalization of duplicated genes. In the particular case of dmrt1bY, this contributed to create new hierarchies of sex-determining genes.

Analysis of a novel gene, Sdgc, reveals sex chromosome-dependent differences of medaka germ cells prior to gonad formation

“…This evolutionary process was associated with the insertion of a transposable element called Izanagi that confers a novel expression pattern upon DMY/ dmrt1bY (Herpin et al, 2010). Unexpectedly, in our study, sexually different characters of germ cells were not impaired by knockdown and overexpression of DMY/dmrt1bY.…”

“…Many studies indicate that the medaka (Oryzias latipes) sex chromosome arose relatively recently (Herpin et al, 2010;Kondo et al, 2004;Myosho et al, 2012;Takehana et al, 2007) and is not as differentiated as in mammals, in which sexual plasticity is much reduced in germ cells (e.g. Lavery et al, 2011;Koopman et al, 1991).…”

A Brief History of the Status of Transposable Elements: From Junk DNA to Major Players in Evolution

“…On the basis of many recent findings, we now consider that TEs have considerably shaped the structure, function, and evolution of the genomes and that the regulatory sequences that they possess can interfere with the networks of regulation of many genes, even of genes located at some distance from them (Feschotte 2008;Herpin et al 2010). TEs must therefore be considered to be integrated components of the genomes, which have played a major role in evolution.…”

Construction and Characterization of a Repetitive DNA Library in Parodontidae (Actinopterygii: Characiformes): A Genomic and Evolutionary Approach to the Degeneration of the W Sex Chromosome

“…3 Repetitive elements are important for the genome structure and function. [4][5][6] For example, satellite DNAs play a role in chromosome segregation during the cell cycle and comprise the centromeres of chromosomes, which bind microtubules. 7 Furthermore, both types of repeats can control gene expression on transcriptional and post-transcriptional regulatory networks.…”

“…7 Furthermore, both types of repeats can control gene expression on transcriptional and post-transcriptional regulatory networks. [4][5][6] Studies demonstrated that satellite DNA plays a role in position-effect variegation and that TEs had been coopted to serve gene regulatory functions for the host, a process that fits under the term ''molecular exaptation. '' 8 Several methods are used to isolate repetitive DNA sequences.…”