The Role of Maternal HP1a in Early Drosophila Embryogenesis via Regulation of Maternal Transcript Production

Abstract

Heterochromatin protein 1a (HP1a) is a highly conserved and versatile epigenetic factor that can both silence and activate transcription. However, the function of HP1a in development has been underinvestigated. Here, we report the role of maternal HP1a in producing maternal transcripts that drive early Drosophila embryogenesis. Maternal HP1a upregulates genes involved in translation, mRNA splicing, and cell division, but downregulates genes involved in neurogenesis, organogenesis, and germline development, which all occur later in development. Our study reveals the earliest contribution of HP1a during oogenesis in regulating the production of maternal transcripts that drive early Drosophila embryogenesis.

Maternally inherited piRNAs direct transient heterochromatin formation at active transposons during early Drosophila embryogenesis

“…Though embryonically repressed transposons bore hallmarks of piRNA-guided heterochromatin formation, the reliance of the pathway on maternally deposited Piwi-piRNA complexes prevented a demonstration that silencing depended on the pathway through conventional genetics. Ovaries that lack key piRNA pathway silencing factors show substantial expression changes and produce morphologically altered eggs that largely fail to develop normally (Cox et al, 1998;Czech et al, 2013;Handler et al, 2013;Khurana et al, 2010;Klattenhoff et al, 2007;Klenov et al, 2011;Li et al, 2009a;Malone et al, 2009;Mani et al, 2014;Muerdter et al, 2013;Pane et al, 2007;Park et al, 2019). To investigate the effect of Piwi depletion on Drosophila embryogenesis without affecting oogenesis, we used the auxin-inducible degron (AID) system (Nishimura et al, 2009).…”

“…However, probing piRNA pathway function during early embryogenesis has been hampered by a lack of suitable experimental approaches. Disrupting Piwi or other piRNA pathway factors in the female parent either via mutation or RNAi leads to oogenesis defects and often results in sterility or patterning defects that would confound the outcome of analyses ( Cox et al, 1998 ; Czech et al, 2013 ; Handler et al, 2013 ; Khurana et al, 2010 ; Klattenhoff et al, 2007 ; Klenov et al, 2011 ; Li et al, 2009a ; Malone et al, 2009 ; Mani et al, 2014 ; Muerdter et al, 2013 ; Pane et al, 2007 ; Park et al, 2019 ). RNAi-mediated depletion in embryos or generation of homozygous mutant embryos carrying piRNA pathway defects enables analysis of later developmental stages ( Akkouche et al, 2017 ; Gu and Elgin, 2013 ; Marie et al, 2017 ), but not time windows where maternally deposited proteins predominate and generally drive development.…”

When Down Is Up: Heterochromatin, Nuclear Organization and X Upregulation

“…Reduced levels of HP1a disorganize banding of the male polytene X chromosome, producing a short, bloated chromosome [ 107 ]. HP1a is also modestly enriched along the male X [ 124 , 125 , 126 ]. The morphology of the polytene male X chromosome is similarly affected by reduction of Su(var)3-9 and by reduction or overexpression of Su(var)3-7, a heterochromatin protein that interacts with HP1a and Su(var)3-9 [ 107 , 108 , 127 ].…”

Affinity hierarchies and amphiphilic proteins underlie the co-assembly of nucleolar and heterochromatin condensates

“…All crosses were maintained at 25° C. To visualize the dynamics of HP1a and nucleolar assembly, To knockdown HP1a in Drosophila embryos, we crossed matα-GAL4 (BDSC #7063) females to HP1a RNAi males (BDSC #33400) to generate an F1 generation with HP1a depleted in the female germlines. F1 siblings were crossed to collect embryos depleted for HP1a, most of which exhibit severe developmental defects (Park et al 2019). We selected embryos that reached nuclear cycle 14 for analyses of nucleolar morphology.…”