Recurrent Losses and Rapid Evolution of the Condensin II Complex in Insects

Abstract

Condensins play a crucial role in the organization of genetic material by compacting and disentangling chromosomes. Based on studies in a few model organisms, the condensins I and II complexes are considered to have distinct functions, with the condensin II complex playing a role in meiosis and somatic pairing of homologous chromosomes in Drosophila. Intriguingly, the Cap-G2 subunit of condensin II is absent in Drosophila melanogaster, and this loss may be related to the high levels of chromosome pairing seen in flies. Here, we find that all three non-SMC subunits of condensin II (Cap-G2, Cap-D3, and Cap-H2) have been repeatedly and independently lost in taxa representing multiple insect orders, with some taxa lacking all three. We also find that all non-Dipteran insects display near-uniform low-pairing levels regardless of their condensin II complex composition, suggesting that some key aspects of genome organization are robust to condensin II subunit losses. Finally, we observe consistent signatures of positive selection in condensin subunits across flies and mammals. These findings suggest that these ancient complexes are far more evolutionarily labile than previously suspected, and are at the crossroads of several forms of genomic conflicts. Our results raise fundamental questions about the specific functions of the two condensin complexes in taxa that have experienced subunit losses, and open the door to further investigations to elucidate the diversity of molecular mechanisms that underlie genome organization across various life forms.

Live imaging and biophysical modeling support a button-based mechanism of somatic homolog pairing inDrosophila

“…For example, in Drosophila , an additional layer of nuclear organization exists in somatic cells wherein homologous chromosomes are closely juxtaposed from end to end, a phenomenon known as somatic homolog pairing (Joyce, Erceg, and Wu 2016;Stevens 1908) . While similar interchromosomal interactions occur transiently in somatic cells of other species and during early meiotic phases of most sexually-reproducing eukaryotes, the widespread and stable pairing of homologous chromosomes observed in somatic cells of Drosophila appears to be unique to Dipteran flies (King et al 2019;Joyce, Erceg, and Wu 2016;McKee 2004) . Notably, the close juxtaposition of paired homologs can have a dramatic impact on gene expression through a process known as transvection, where regulatory elements on one chromosome influence chromatin and gene expression on a paired chromosome (Fukaya and Levine 2017;Duncan 2002) .…”

Live imaging and biophysical modeling support a button-based mechanism of somatic homolog pairing in Drosophila

“…For example, in somatic cells in Drosophila, an additional layer of nuclear organization exists: homologous chromosomes are closely juxtaposed from end to end, a phenomenon known as somatic homolog pairing (Joyce, Erceg, and Wu 2016;Stevens 1908). While similar interchromosomal interactions occur transiently in somatic cells of other species and during early meiotic phases of most sexually reproducing eukaryotes, the widespread and stable pairing of homologous chromosomes in somatic cells of Drosophila appears to be unique to Dipteran flies (King et al 2019;Joyce, Erceg, and Wu 2016;McKee 2004). Notably, the close juxtaposition of paired homologs can have a dramatic impact on gene expression through a process known as transvection, whereby regulatory elements on one chromosome influence chromatin and gene expression on a paired chromosome (Fukaya and Levine 2017;Duncan 2002).…”

Condensin I is required for faithful meiosis in Drosophila males

“…This lack of complementation may be caused by putatively post-meiotic functions of condensin II, which are unrelated to shaping meiotic chromatin (Hartl et al 2008b). It is important to note that Drosophila condensin II, like the condensin IIcomplexes in a number of other insect clades, lacks the subunit Cap-G2 (Herzog et al 2013;King et al 2019). Since Cap-G knockdown does not result in more severe phenotypes than knockdown of Barren, it is unlikely that Cap-G takes over the function of Cap-G2 and is part of both condensin complexes, consistent with our previous report (Herzog et al 2013).…”

“…Despite thorough genetic and biochemical analyses, no Cap-G2 subunit could be found in the fly (Herzog et al 2013). In fact, a recent query of insect genomes has revealed that species in many taxa lack one or more condensin II-specific genes (King et al 2019). Obviously, in the taxa without a complete condensin II set of proteins, this complex may have evolved to perform different tasks besides organization of mitotic chromosomes.…”