Evolution of Chromatin-Remodeling Complexes: Comparative Genomics Reveals the Ancient Origin of "Novel" Compensasome Genes

Abstract

Abstract. Dosage compensation in Drosophila is mediated by a complex, called compensasome, composed of at least five proteins and two noncoding RNAs. Genes encoding compensasome proteins have been collectively named male-specific lethals or msls. Recent work showed that three of the Drosophila msls (msl-3, mof, and mle) have an ancient origin. In this study, I describe likely orthologues of the two remaining msls, msl-1 and msl-2, in several invertebrates and vertebrates. The MSL-2 protein is the only one found in Drosophila and vertebrate genomes that contains both a RING finger and a peculiar type of CXC domain, related to the one present in Enhancer of Zeste proteins. MSL-1 also contains two evolutionarily conserved domains: a leucine zipper and a second characteristic region, described here for the first time, which I have called the PEHE domain. These two domains are present in the likely orthologues of MSL-1 as well as in other genes in several invertebrate and vertebrate species. Although it cannot be excluded that the compensasome complex is a recent evolutionary novelty, these results shows that all msls are found in mammals, suggesting that protein complexes related to the compensasome may be present in mammalian species. Metazoans that lack several of the msls, such as Caenorhabditis elegans, cannot contain compensasomes. The evolutionary relationships of the compensasome and the NuA4 complex, another chromatin-remodeling complex that contains related subunits, are discussed.

The nuclear protein Waharan is required for endosomal-lysosomal trafficking inDrosophila

“…S1B), typical of proteins that mediate DNA metabolism (Arents and Moudrianakis, 1995). This prediction was consistent with the previous identification of Wah and KIAA1267 as uncharacterized components of the dosage compensation complex (DCC) implicated in the regulation of chromatin conformation (Marin, 2003;Mendjan et al, 2006). Accordingly, haemagglutinin (HA)-tagged Wah (HAWah) was predominantly detected in nuclei of larval motorneurons and muscles (but also in small puncta in the cytoplasm; Fig.…”

Structural basis of X chromosome DNA recognition by the MSL2 CXC domain during Drosophila dosage compensation

“…Such a binding mode is consistent with and would be facilitated by the dimeric organization of the MSL1/MSL2 complex (Hallacli et al 2012). The tesmin/ TSO1 family of proteins often contain two clustered homologous CXC domains (Cvitanich et al 2000;Marin 2003;Schmit et al 2009), which are distantly related to the CXC of MSL2 and probably recognize DNA by forming an intramolecular dimer.…”

Incorporation of the Noncoding roX RNAs Alters the Chromatin-Binding Specificity of the Drosophila MSL1/MSL2 Complex

“…Previous comparisons of Drosophila melanogaster MSL2 amino acid sequence with orthologous sequences from invertebrates and vertebrates identified two well-conserved motifs, a RING finger domain at the amino end and a cysteine-rich "CXC" domain toward the carboxyl end (29). The function of the CXC domain is unknown.…”