Recurrent Amplification of the Heterochromatin Protein 1 (HP1) Gene Family across Diptera

Abstract

The heterochromatic genome compartment mediates strictly conserved cellular processes such as chromosome segregation, telomere integrity, and genome stability. Paradoxically, heterochromatic DNA sequence is wildly unconserved. Recent reports that many hybrid incompatibility genes encode heterochromatin proteins, together with the observation that interspecies hybrids suffer aberrant heterochromatin-dependent processes, suggest that heterochromatic DNA packaging requires species-specific innovations. Testing this model of coevolution between fast-evolving heterochromatic DNA and its packaging proteins begins with defining the latter. Here we describe many such candidates encoded by the Heterochromatin Protein 1 (HP1) gene family across Diptera, an insect Order that encompasses dramatic episodes of heterochromatic sequence turnover. Using BLAST, synteny analysis, and phylogenetic tree building across 64 Diptera genomes, we discovered a staggering 121 HP1 duplication events. In contrast, we observed virtually no gene duplication in gene families that share a common “chromodomain” with HP1s, including Polycomb and Su(var)3-9. The remarkably high number of Dipteran HP1 paralogs arises from distant clades undergoing convergent HP1 family amplifications. These independently derived, young HP1s span diverse ages, domain structures, and rates of molecular evolution, including episodes of positive selection. Moreover, independently derived HP1s exhibit convergent expression evolution. While ancient HP1 parent genes are transcribed ubiquitously, young HP1 paralogs are transcribed primarily in male germline tissue, a pattern typical of young genes. Pervasive gene youth, rapid evolution, and germline specialization implicate heterochromatin-encoded selfish elements driving recurrent HP1 gene family expansions. The 121 young genes offer valuable experimental traction for elucidating the germline processes shaped by Diptera’s many dramatic episodes of heterochromatin turnover.

Impacts of sex ratio meiotic drive on genome structure and defense in a stalk-eyed fly

“…In Drosophila simulans, a young duplicate of heterochromatin protein 1 (HP1D) causes sex ratio meiotic drive (Montchamp-Moreau et al 2006;Helleu et al 2016), and HP1D (also known as rhino) is a key player in piRNA genome defense in D. melanogaster and presumably other species (Klattenhoff et al 2009). Furthermore, recurrent amplification of HP1 copies occurs in lineages where sex ratio drive is common (Helleu and Levine 2018). We identified multiple HP1 family members in the T. dalmanni genome, and one (the HP1E ortholog) was Xlinked, but it did not show signs of SR-associated divergence, differential expression or coverage.…”

“…In addition to the canonical piRNA genes, piwi, maelstrom, aubergine, and Argonaute3, we identified an additional 168 piRNArelated genes from three recent studies in D. melanogaster(Handler et al 2013;Palmer et al 2018;Ozata et al 2019) for further analysis. In addition, the Heterochromatin protein 1 family is expanding within diptera in association with meiotic drive(Helleu and Levine 2018) and is associated with de novo heterochromatic silencing near novel TE insertions(Lee and Karpen 2017). In Drosophila the HP1E family includes rhino (HP1E) which is a key piRNA gene in…”

Establishment and evolution of heterochromatin

“…149 Similarly, disruption of the euchromatin mark H4K16ac-associated gene Sas2 or overexpression of the gene Sir3, which participates in the deacetylation in budding yeast, 150,151 leads to heterochromatin spreading. It has been demonstrated that the copy numbers and expression patterns of cHet-associated genes dramatically vary between species, 152,153 probably in response to the rapid evolution of repetitive DNA sequences (see below). This may result in the shift in boundaries between euchromatin and heterochromatin, reshaping the chromatin architecture of the entire genome.…”

“…157 The rapid evolution of heterochromatin must be contained to avoid impairing its important structural and regulatory functions. This is manifested as an "arms race" of sorts between heterochromatin and its regulatory proteins and RNAs, including those involved in heterochromatin packaging, 152,153 telomere protection, 158 and small RNA pathways. 159,160 These proteins either show an excess of amino acid change, that is, have the signature of positive selection, 161,162 or undergo rampant gene birth and death processes accompanied by newly evolved expression patterns that are usually restricted in the germline.…”

“…159,160 These proteins either show an excess of amino acid change, that is, have the signature of positive selection, 161,162 or undergo rampant gene birth and death processes accompanied by newly evolved expression patterns that are usually restricted in the germline. 152,153 To date, a recent characterization of 64 Diptera genomes found a total of 121 HP1 duplications, but almost no duplications in SU(VAR)3-9 and PcG proteins. Interestingly, the loss of a male-specific HP1 family protein HP1E correlates with the transformation of the ancestral Y chromosome to an autosome in D. pseudoobscura, suggesting a relaxed selective constraint on HP1E due to the loss of Y-linked heterochromatin.…”