Evolution of SUMO Function and Chain Formation in Insects

Abstract

SUMOylation, the covalent binding of Small Ubiquitin-like Modifier (SUMO) to target proteins, is a posttranslational modification that regulates critical cellular processes in eukaryotes. In insects, SUMOylation has been studied in holometabolous species, particularly in the dipteran Drosophila melanogaster, which contains a single SUMO gene (smt3). This has led to the assumption that insects contain a single SUMO gene. However, the analysis of insect genomes shows that basal insects contain two SUMO genes, orthologous to vertebrate SUMO1 and SUMO2/3. Our phylogenetical analysis reveals that the SUMO gene has been duplicated giving rise to SUMO1 and SUMO2/3 families early in Metazoan evolution, and that later in insect evolution the SUMO1 gene has been lost after the Hymenoptera divergence. To explore the consequences of this loss, we have examined the characteristics and different biological functions of the two SUMO genes (SUMO1 and SUMO3) in the hemimetabolous cockroach Blattella germanica and compared them with those of Drosophila Smt3. Here, we show that the metamorphic role of the SUMO genes is evolutionary conserved in insects, although there has been a regulatory switch from SUMO1 in basal insects to SUMO3 in more derived ones. We also show that, unlike vertebrates, insect SUMO3 proteins cannot form polySUMO chains due to the loss of critical lysine residues within the N-terminal part of the protein. Furthermore, the formation of polySUMO chains by expression of ectopic human SUMO3 has a deleterious effect in Drosophila. These findings contribute to the understanding of the functional consequences of the evolution of SUMO genes.

Sex‐specific changes in the aphid DNA methylation landscape

“…The average methylation level in Buchnera for Cs in any sequence context was 0.45% ± 0.68 (mean ± SD). This confirms that without a functioning DNA methylation pathway (van Ham et al, 2003), B. aphidicola cannot methylate its genes. It also indicates that bisulphite treatment of the aphid DNA was 99.55% efficient (i.e., a 0.45% false positive rate), and that it was consistent across samples.…”

“…Protein SUMOylation is enriched among genes with male‐biased methylation. This is interesting because protein SUMOylation is essential for dosage compensation of the Caenorhabditis elegans sex chromosome (Pferdehirt & Meyer, ) and plays a key role in insect development and metamorphosis (Ureña et al, ). Changes in methylation appear to be associated with core processes in aphid polyphenism and sex determination.…”

“…Myzus persicae individuals harbour an obligate endosymbiont, B. aphidicola. The Buchnera genus underwent an extensive genome reduction (Chong, Park, & Moran, 2019;Chong et al, 2019;van Ham et al, 2003), and lacks a functional DNA methylation system (van Ham et al, 2003). We made use of Buchnera derived reads in each sample to establish rates of false positive methylation calls caused by incomplete cytosine conversions by mapping each sample to the M. persicae Buchnera genome (Mathers et al, 2017) and quantifying methylation levels (Table S4).…”

“…GO terms are arranged in the semantic space according to their similarity in physiological and metabolically processes, as well as their functional categories, which reflects their biological meaning. A full list of enriched GO terms for each DM class and functional category is given in Meyer, 2013) and plays a key role in insect development and metamorphosis (Ureña et al, 2015). Changes in methylation appear to be associated with core processes in aphid polyphenism and sex determination.…”

Ongoing resolution of duplicate gene functions shapes the diversification of a metabolic network

“…In several cases, paralogs encoding enzymes have been recruited to perform regulatory functions, such as S. cerevisiae HXK2 , GAL3 , and ARG82 (Gancedo and Flores, 2008; Conant et al, 2014; Gancedo et al, 2014). Previously differentiated developmental roles can even be transferred from one paralog to another during evolution (Ureña et al, 2016). Perhaps more significantly, long-preserved paralogs can be lost in lineage-specific manners, a common phenomenon observed across the tree of life, including in bacteria (Gómez-Valero et al, 2007), yeasts (Scannell et al, 2007), Paramecium (Aury et al, 2006; McGrath et al, 2014), plants (De Smet et al, 2013), fishes (Amores et al, 2004), and mammals (Amores et al 1998; Blomme et al, 2006).…”