Dynamic sex chromosome expression in Drosophila male germ cells

Mahadevaraju, Sharvani; Fear, Justin M.; Akeju, Miriam; Galletta, Brian J.; Pinheiro, Mara; Avelino, Camila C.; Cabral-de-Mello, Diogo Cavalcanti; Conlon, Katie; Dell'Orso, Stafania; Demere, Zelalem; Mansuria, Kush; Mendonca, Carolina A.; Palacios-Gimenez, Octavio M.; Ross, Eli; Savery, Max; Yu, Kevin Shengyang; Smith, Harold E.; Sartorelli, Vittorio; Yang, Haiwang; Rusan, Nasser M.; Vibranovski, Maria D.; Matunis, Erika; Oliver, Brian

doi:10.1038/s41467-021-20897-y

Cited by 66 publications

(118 citation statements)

References 97 publications

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“…We took advantage of transcriptomic profiling of various adult tissues in D. melanogaster and nine other Drosophila species to investigate tissue-specific expression of Arp53D . Confirming previous analyses, we found that all Drosophila species show significantly male-biased expression of Arp53D and almost undetectable expression in adult females ( Figure 1—figure supplement 1F , Table 2 ; Benner et al, 2019 ; Luo et al, 2020 ; Ma et al, 2018 ; Mahadevaraju et al, 2021 ; Nozawa et al, 2016 ; Rogers et al, 2014 ; Yang et al, 2018 ). In all these cases, Arp53D RNA expression is much higher in the testis than the remaining male carcass ( Figure 1—figure supplement 1F , Table 2 ).…”

Section: Resultssupporting

confidence: 90%

An actin-related protein that is most highly expressed in Drosophila testes is critical for embryonic development

Schroeder

Tomlin

Natividad

et al. 2021

eLife

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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.

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Section: Resultssupporting

confidence: 90%

An actin-related protein that is most highly expressed in Drosophila testes is critical for embryonic development

Schroeder

Tomlin

Natividad

et al. 2021

eLife

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“…roX1 , one of the strongest markers of MCsp1, plays a central role in dosage compensation (Mukherjee and Beermann 1965; Meller et al 1997; Hallacli et al 2012). We investigated patterns of broadly expressed genes using the methods of Mahadevaraju et al . (2021), but found no evidence of correlations between roX1 abundance and X-to-autosome expression, or variation in X-to- autosome expression among subclusters or cell types.…”

Section: Resultsmentioning

confidence: 99%

Single-nucleus transcriptomes reveal functional and evolutionary properties of cell types in the Drosophila accessory gland

2021

Preprint

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Many traits responsible for male reproduction evolve quickly, including gene expression phenotypes in germline and somatic male reproductive tissues. Rapid male evolution in polyandrous species is thought to be driven by competition among males for fertilizations and conflicts between male and female fitness interests that manifest in post-copulatory phenotypes. In Drosophila, seminal fluid proteins secreted by three major cell types of the male accessory gland and ejaculatory duct are required for female sperm storage and use, and influence female post-copulatory traits. Recent work has shown that these cell types have overlapping but distinct effects on female post-copulatory biology, yet relatively little is known about their evolutionary properties. Here we use single-nucleus RNA-Seq of the accessory gland and ejaculatory duct from Drosophila melanogaster and two closely related species to comprehensively describe the cell diversity of these tissues and their transcriptome evolution for the first time. We find that seminal fluid transcripts are strongly partitioned across the major cell types, and expression of many other genes additionally define each cell type. We also report previously undocumented diversity in main cells. Transcriptome divergence was found to be heterogeneous across cell types and lineages, revealing a complex evolutionary process. Furthermore, protein adaptation varied across cell types, with potential consequences for our understanding of selection on male post-copulatory traits.

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“…The copyright holder for this preprint this version posted June 11, 2021. ; https://doi.org/10.1101/2021.06.10.447990 doi: bioRxiv preprint Rivard,Ludwig,Patel et al 20 2016; Mahadevaraju et al 2021), but continued research in this area might inform further interrogation of the forces driving atlas off of the X chromosome.…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, Drosophila exhibit suppression of X-linked testis-expressed genes, and transfer of such genes from the X chromosome to autosomal loci results in higher expression levels (Kemkemer et al 2014;Argyridou et al 2017;Argyridou and Parsch 2018). One of several proposed mechanisms for both the paucity of X-linked testis-expressed genes and the suppression of their expression is meiotic sex chromosome inactivation (MSCI), in which the X chromosome becomes transcriptionally silenced earlier than autosomes (Vibranovski, Lopes, et al 2009;Zhang, Vibranovski, Krinsky, et al 2010;Zhang, Vibranovski, Landback, et al 2010;Vibranovski et al 2012;Gao et al 2014;Mahadevaraju et al 2021). Thus, genes that affect meiotic or postmeiotic processes, as atlas does, could exert beneficial effects more strongly and/or for a longer period of time if they become encoded autosomally.…”

Section: Discussionmentioning

confidence: 99%

“…While the atlas protein-coding sequence appears to show male-specific expression regardless of its chromosomal location, it is possible that the movement of atlas to chromosome 2 allowed it to evolve a broader or different expression pattern that expanded or modified its role in spermiogenesis. The complex molecular bases of both X suppression and "escape" from the X chromosome in Drosophila continue to be actively investigated and debated (Meiklejohn et al 2011;Mikhaylova and Nurminsky 2011;Vibranovski et al 2012;Gao et al 2014;Vibranovski 2014;Landeen et al 2016;Mahadevaraju et al 2021), but continued research in this area might inform further interrogation of the forces driving atlas off of the X chromosome.…”

Section: Discussionmentioning

confidence: 99%

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A putative de novo evolved gene required for spermatid chromatin condensation in Drosophila melanogaster

Rivard

Ludwig

Patel

et al. 2021

Preprint

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Comparative genomics has enabled the identification of genes that potentially evolved de novo from non-coding sequences. Many such genes are expressed in male reproductive tissues, but their functions remain poorly understood. To address this, we conducted a functional genetic screen of over 40 putative de novo genes with testis-enriched expression in Drosophila melanogaster and identified one gene, atlas, required for male fertility. Detailed genetic and cytological analyses show that atlas is required for proper chromatin condensation during the final stages of spermatogenesis. Atlas protein is expressed in spermatid nuclei and facilitates the transition from histone- to protamine-based chromatin packaging. Complementary evolutionary analyses revealed the complex evolutionary history of atlas. The protein-coding portion of the gene likely arose at the base of the Drosophila genus on the X chromosome but was unlikely to be essential, as it was then lost in several independent lineages. Within the last ~15 million years, however, the gene moved to an autosome, where it fused with a conserved non-coding RNA and evolved a non-redundant role in male fertility. Altogether, this study provides insight into the integration of novel genes into biological processes, the links between genomic innovation and functional evolution, and the genetic control of a fundamental developmental process, gametogenesis.

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Dynamic sex chromosome expression in Drosophila male germ cells

Cited by 66 publications

References 97 publications

An actin-related protein that is most highly expressed in Drosophila testes is critical for embryonic development

An actin-related protein that is most highly expressed in Drosophila testes is critical for embryonic development

Single-nucleus transcriptomes reveal functional and evolutionary properties of cell types in the Drosophila accessory gland

A putative de novo evolved gene required for spermatid chromatin condensation in Drosophila melanogaster

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