Altered chromatin localization of hybrid lethality proteins inDrosophila

Abstract

Understanding hybrid incompatibilities is a fundamental pursuit in evolutionary genetics. In crosses between Drosophila melanogaster females and Drosophila simulans males, the interaction of at least three genes is necessary for hybrid male lethality: Hmr mel , Lhr sim , and gfzf sim . All three hybrid incompatibility genes are chromatin associated factors. While HMR and LHR physically bind each other and function together in a single complex, the connection between either of these proteins and gfzf remains mysterious. Here, we investigate the allele specific chromatin binding patterns of gfzf. First, our cytological analyses show that there is little difference in protein localization of GFZF between the two species except at telomeric sequences. In particular, GFZF binds the telomeric retrotransposon repeat arrays, and the differential binding of GFZF at telomeres reflects the rapid changes in sequence composition at telomeres between D. melanogaster and D. simulans. Second, we investigate the patterns of GFZF and HMR co-localization and find that the two proteins do not normally co-localize in D. melanogaster. However, in inter-species hybrids, HMR shows extensive mis-localization to GFZF sites, and this altered localization requires the presence of gfzf sim . Third, we find by ChIP-Seq that over-expression of HMR and LHR within species is sufficient to cause HMR to mis-localize to GFZF binding sites, indicating that HMR has a natural low affinity for GFZF sites. Together, these studies provide the first insights into the different properties of gfzf between D. melanogaster and D. simulans as well as a molecular interaction between gfzf and Hmr in the form of altered protein localization.

A triple-hybrid cross reveals a new hybrid incompatibility locus betweenD. melanogaster and D. sechellia

“…This adds a much more direct connection between Lhr and gfzf than has previously been identified. Combined with our recent work to show that Hmr and gfzf co-localize on DNA in hybrids (Cooper et al 2018), a new picture of these three hybrid incompatibility genes is beginning to emerge. Rather than acting as additive entities, it appears that all three of these genes have the ability to influence the actions of each other.…”

“…gfzf is a general transcriptional co-activator for TATA-less genes along with M1BP (Baumann et al 2018). Recent work also demonstrates that Hmr mislocalizes to gfzf bound chromatin in F1 hybrids, indicating that they have the capability to interact with many other loci (Cooper et al 2018). Though the identity of these three genes has been established, there is still no comprehensive explanation of their role in hybrid incompatibility, and an incomplete picture of other genes they interact with to cause hybrid incompatibility.…”

Intricate structure of the interphase chromocenter revealed by the analysis of a factor involved in species formation

“…To simulate the hybrid situation where increased levels of the complex containing HMR and LHR are found (13), we compared a HMR ChIP-seq analysis upon overexpression of HMR and LHR (39) with the condensin and cohesin profiles. Upon overexpression we detected 1314 additional HMR peaks, many of them colocalizing with binding sites of CAP-H2 (Fig.…”

Molecular evolution across developmental time reveals rapid divergence in early embryogenesis

“…In Drosophila , rapidly evolving proteins involved in chromatin regulation and genomic conflict are known to play important roles in creating postzygotic reproductive barriers between species during early development (Presgraves ; Maheshwari and Barbash ; Cooper et al. ). Evolutionary conflict over allelic expression in early embryos also can drive rapid sequence evolution (Haig ), as can less effective selection on genes expressed by one sex (Cruickshank and Wade ; Dapper and Wade ).…”