Abstract
Most actin-related proteins (Arps) are highly conserved and carry out well-defined cellular functions in eukaryotes. However, many lineages like Drosophila and mammals encode divergent non-canonical Arps whose roles remain unknown. To elucidate the function of non-canonical Arps, we focus on Arp53D, which is highly expressed in testes and retained throughout Drosophila evolution. We show that Arp53D localizes to fusomes and actin cones, two germline-specific actin structures critical for sperm maturation, via a unique N-terminal tail. Surprisingly, we find that male fertility is not impaired upon Arp53D loss, yet population cage experiments reveal that Arp53D is required for optimal fitness in Drosophila melanogaster. To reconcile these findings, we focus on Arp53D function in ovaries and embryos where it is only weakly expressed. We find that under heat stress Arp53D-knockout (KO) females lay embryos with reduced nuclear integrity and lower viability; these defects are further exacerbated in Arp53D-KO embryos. Thus, despite its relatively recent evolution and primarily testis-specific expression, non-canonical Arp53D is required for optimal embryonic development in Drosophila.
Highlights
Actin is an ancient, highly conserved protein that performs many cytoplasmic and nuclear functions vital for eukaryotes, including division, motility, cargo transport, DNA repair, and gene expression (Dominguez and Holmes, 2011; Schrank et al, 2018; Wei et al, 2020)
Arp53D was not found in any other noninsect genomes in a broad survey of eukaryotes, raising the possibility that it only exists in a few Drosophila species
We found that KO females expressing the Arp53D rescue transgene in one or two copies had robustly increased fertility compared to KO females without the transgene (Figure 7C, Figure 7—figure supplement 1D) despite low expression of the rescue transgene (Figure 5—figure supplement 2I)
Summary
Highly conserved protein that performs many cytoplasmic and nuclear functions vital for eukaryotes, including division, motility, cargo transport, DNA repair, and gene expression (Dominguez and Holmes, 2011; Schrank et al, 2018; Wei et al, 2020). Most eukaryotes encode an expanded repertoire of actin-related proteins (Arps) because of ancient gene duplications (Goodson and Hawse, 2002; Muller et al, 2005) These Arps have specialized for a wide range of functions, including regulation of actin (Arps 2/3) (Mullins et al, 1998), chromatin remodeling (Arps 4–8) (Harata et al, 2000; Blessing et al, 2004; Klages-Mundt et al, 2018), and microtubule-based transport (Arps 1 and 10) (Muhua et al, 1994; Lee et al, 2001). All Arps maintain a conserved actin fold, they have specialized for their novel roles via distinct structural insertions (Liu et al, 2013; Chen and Shen, 2007) These ‘canonical’ Arps significantly diverged from each other early in eukaryote evolution, but evolve under stringent evolutionary constraints, like actin
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