Adaptive selection and coevolution at the proteins of the Polycomb repressive complexes in Drosophila

Abstract

JM Calvo-Martín, P Librado, M Aguadé, M Papaceit and C Segarra Polycomb group (PcG) proteins are important epigenetic regulatory proteins that modulate the chromatin state through posttranslational histone modifications. These interacting proteins form multimeric complexes that repress gene expression. Thus, PcG proteins are expected to evolve coordinately, which might be reflected in their phylogenetic trees by concordant episodes of positive selection and by a correlation in evolutionary rates. In order to detect these signals of coevolution, the molecular evolution of 17 genes encoding the subunits of five Polycomb repressive complexes has been analyzed in the Drosophila genus. The observed distribution of divergence differs substantially among and along proteins. Indeed, CAF1 is uniformly conserved, whereas only the established protein domains are conserved in other proteins, such as PHO, PHOL, PSC, PH-P and ASX. Moreover, regions with a low divergence not yet described as protein domains are present, for instance, in SFMBT and SU(Z)12. Maximum likelihood methods indicate an acceleration in the nonsynonymous substitution rate at the lineage ancestral to the obscura group species in most genes encoding subunits of the Pcl-PRC2 complex and in genes Sfmbt, Psc and Kdm2. These methods also allow inferring the action of positive selection in this lineage at genes E(z) and Sfmbt. Finally, the protein interaction network predicted from the complete proteomes of 12 Drosophila species using a coevolutionary approach shows two tight PcG clusters. These clusters include well-established binary interactions among PcG proteins as well as new putative interactions.

Evidence of neofunctionalization after the duplication of the highly conserved Polycomb group gene Caf1-55 in the obscura group of Drosophila

“…The Caf1-55 and Caf1-55dup sequences retrieved from FlyBase were aligned with those reported in Calvo-Martín et al 14. and in the present study.…”

“…This complex contains three additional proteins: E(Z), ESC and SU(Z)12. In a previous study14, it was shown that the genes coding these proteins suffered a significant increase in the nonsynonymous substitution rate in the lineage ancestral to the obscura group species. Therefore, in this lineage not only took place the duplication of Caf1-55 , but also an acceleration in the fixation rate of nonsynonymous changes in the genes encoding proteins that interact with CAF1-55.…”

“…In a study of the molecular evolution of Caf1-55 and other Polycomb group (PcG) genes in Drosophila 14, the orthologs of Caf1-55 were identified in a set of 15 species, and it was confirmed that CAF1-55 is a highly conserved protein with minimal interspecific amino acid divergence. In the same study, a gene with a high similarity with Caf1-55 was unexpectedly detected in D. pseudoobscura and D. persimilis .…”

Molecular population genetics of the Polycomb genes in Drosophila subobscura

“…These interacting proteins are expected to evolve co-ordinately to maintain the integrity and functionality of the complexes, which can cause a correlation in their evolutionary rates. Evidence of coevolution among the subunits of these complexes has been detected in a previous study of interspecific nucleotide divergence in the Drosophila genus [ 15 ]. Moreover, this study revealed an acceleration in the nonsynonymous substitution rate in the lineage ancestral to the obscura group species, mainly in genes encoding subunits of the Pcl-PRC2 complex.…”

Genomic data reveal high conservation but divergent evolutionary pattern of Polycomb/Trithorax group genes in arthropods

“…PRC1 can recognize the H3K27me3 repressive marks set by PRC2 through the chromodomain of Pc gene. In addition to these two PRC complexes, PcG proteins are also present in the three distinct accessory complexes, as follows: the Polycomb repressive deubiquitinase (PR-DUB), dRING-associated factors (dRAF) and Pho repressive complex (PhoRC) complexes (Calvo-Martin et al, 2016). The PR-DUB complex consists of an ubiquitin carboxy-terminal hydrolase, calypso, and an additional sex comb gene, Asx, which encodes a chromatin protein that regulates the balance of Polycomb and Trithorax function.…”