Structural and functional characterization of a putative<i>de novo</i>gene in<i>Drosophila</i>

Lange, Andreas; Patel, Prajal H.; Heames, Brennen; Damry, Adam M.; Saenger, Thorsten; Jackson, C.J.; Findlay, Geoffrey D.; Bornberg‐Bauer, Erich

doi:10.1101/2021.01.18.427054

Cited by 5 publications

(16 citation statements)

References 92 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…We showed previously that the putative de novo gene saturn is required for maximal sperm production, as well as for the ability of transferred sperm to migrate successfully to sperm storage organs in females (Gubala et al 2017). Another putative de novo gene, goddard, is required for sperm production and encodes a cytoplasmic protein that appears to localize to elongating axonemes (Gubala et al 2017;Lange et al 2021). Loss of goddard impairs the individualization of spermatid bundles (Lange et al 2021), thus exerting an effect that appears to be upstream of those observed for saturn and atlas.…”

Section: Discussionmentioning

confidence: 99%

“…Another putative de novo gene, goddard, is required for sperm production and encodes a cytoplasmic protein that appears to localize to elongating axonemes (Gubala et al 2017;Lange et al 2021). Loss of goddard impairs the individualization of spermatid bundles (Lange et al 2021), thus exerting an effect that appears to be upstream of those observed for saturn and atlas. Here, we report another novel function for a putative de novo gene: encoding an essential transition protein that is necessary for proper nuclear condensation in spermiogenesis.…”

Section: Discussionmentioning

confidence: 99%

“…Likewise, for the IC-nuclear bundle association and IC progression analysis (Fig. 3C-D), we selected sample sizes of N = ~15 per genotype based on pilot experiments showing that aberrant actin phenotypes were highly consistent in null testes and previous experience with such quantification (Lange et al 2021).…”

Section: Imaging Spermatogenesis and Spermatid Nuclear Condensationmentioning

confidence: 99%

“…Multiple models explain how protein-coding de novo genes may acquire both an open reading frame (ORF) and regulatory sequences permitting transcription (Carvunis et al 2012;Schlötterer 2015;Wilson et al 2017;Schmitz et al 2018). Interrogation of the biochemical and biophysical properties of the proteins encoded by de novo genes has offered initial insight into the mechanisms of emergence and functional potential of these genes (Schmitz et al 2018;Vakirlis et al 2018;Heames et al 2020;Lange et al 2021).…”

Section: Introductionmentioning

confidence: 99%

“…Saturn knockdown males produced fewer sperm, which were inefficient at migrating to female sperm storage organs. Subsequent characterization of Goddard using null deletion alleles and a biochemically tagged rescue construct showed that the protein localizes to elongating sperm axonemes and that, in its absence, individualization complexes associate less efficiently with spermatid nuclei and do not successfully progress along sperm tails (Lange et al 2021). These data suggested that putative de novo genes can evolve essential roles in a rapidly evolving reproductive process, spermatogenesis.…”

Section: Introductionmentioning

confidence: 99%

See 4 more Smart Citations

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

Rivard

Ludwig

Patel

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

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.

show abstract

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Imaging Spermatogenesis and Spermatid Nuclear Condensationmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

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

Rivard

Ludwig

Patel

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

Molecular Evolution across Mouse Spermatogenesis

Larson

Callahan

Keeble

et al. 2021

Preprint

View full text Add to dashboard Cite

Genes involved in spermatogenesis tend to evolve rapidly, but we still lack a clear understanding of how different components of molecular evolution vary across this complex developmental process. We used fluorescence activated cell sorting (FACS) to generate expression data for both early (meiotic) and late (postmeiotic) cell types across thirteen inbred strains of mice (Mus) spanning ~7 million years of evolution. We used these comparative developmental data to investigate the evolution of lineage-specific expression, protein-coding sequences, and expression levels. We found increased lineage specificity and more rapid protein-coding and expression divergence during late spermatogenesis, suggesting that signatures of rapid testis molecular evolution are punctuated across sperm development. Despite strong overall developmental parallels in these components of molecular evolution, protein and expression divergences were only weakly correlated across genes. We detected more rapid protein evolution on the X chromosome relative to the autosomes, while X-linked gene expression tended to be relatively more conserved likely reflecting chromosome-wide regulatory constraints. Using allele-specific FACS expression data from crosses between four strains, we found that the relative contributions of different regulatory mechanisms also differed between cell-types. Genes showing cis-regulatory changes were more common late in spermatogenesis, and tended to be associated with larger differences in expression levels and greater expression divergence between species. In contrast, genes with trans-acting changes were more common early and tended to be more conserved across species. Our findings advance understanding of gene evolution across spermatogenesis and underscore the fundamental importance of developmental context in molecular evolutionary studies.

show abstract

New genomic signals underlying the emergence of human proto-genes

Grandchamp

Berk

Dohmen

et al. 2022

Preprint

Self Cite

View full text Add to dashboard Cite

De novo genes are novel genes which emerge from non-coding DNA. Until now, little is known about de novo genes properties, correlated to their age and mechanisms of emergence. In this study, we investigate four properties: introns, upstream regulatory motifs, 5 prime UTRs and protein domains, in 23135 human proto-genes. We found that proto-genes contain introns, whose number and position correlates with the genomic position of proto-gene emergence. The origin of these introns is debated, as our result suggest that 41% proto-genes might have captured existing introns, as well as the fact that 13.7% of them do not splice the ORF. We show that proto-genes which emerged via overprinting tend to be more enriched in core promotor motifs, while intergenic and intronic ones are more enriched in enhancers, even if the motif TATA is most expressed upstream these genes. Intergenic and intronic 5 prime UTRs of proto-genes have a lower potential to stabilise mRNA structures than exonic proto-genes and established human genes. Finally, we confirm that proto-genes gain new putative domains with age. Overall, we find that regulatory motifs inducing transcription and translation of previously non-coding sequences may facilitate proto-gene emergence. Our paper demonstrates that introns, 5 prime UTRs, and domains have specific properties in proto-genes. We also show the importance of studying proto-genes in relation to their genomic position, as it strongly impacts these properties.

show abstract

Structural and functional characterization of a putativede novogene inDrosophila

Cited by 5 publications

References 92 publications

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

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

Molecular Evolution across Mouse Spermatogenesis

New genomic signals underlying the emergence of human proto-genes

Contact Info

Product

Resources

About