Protamine-like Proteins in 12 Sequenced Species of Drosophila

Alvi, Zain A; Chu, Tin-Chun; Schawaroch, Valerie; Klaus, Angela V.

doi:10.2174/0929866511307010017

Cited by 4 publications

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“…Other proteins involved in spermatid chromatin compaction show variable levels of conservation across Drosophila . For example, the protamines that contribute to DNA packaging in mature sperm [ 57 ] are found across all sequenced Drosophila species [ 61 ], and orthologs are also reported in FlyBase from other Dipteran and non-Dipteran insects [ 90 ]. However, transition protein Tpl94D is reported to be restricted to species ranging from D .…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2021

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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 showed 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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Section: Discussionmentioning

confidence: 99%

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

et al. 2021

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“…Alternatively, the protamines coded by the divergent parental genomes may not properly bind to DNA or link to neighbouring protamines through the appropriate amino acid residues involved in these interactions (reviewed in [23]). This explanation is unlikely, as protamines are highly conserved across many species within the Drosophila genus [74]. Lastly, the transition pathway of histone-base to protamine-base nuclear organization may be compromised within interspecific sterile hybrid males.…”

Section: Discussionmentioning

confidence: 99%

A common suite of cellular abnormalities and spermatogenetic errors in sterile hybrid males inDrosophila

2020

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When two species interbreed, the resulting hybrid offspring are often sterile, with the heterogametic (e.g. XY) hybrid usually being more severely affected. The prevailing theory for this pattern of sterility evokes divergent changes in separate lineages having maladaptive interactions when placed together in a hybrid individual, with recessive factors on the sex chromosome interacting with dominant factors on the autosomes. The effect of these interactions on gametogenesis should not be uniform across species pairs unless genetic divergence follows the same paths in different lineages or if a specific stage of gametogenesis is more susceptible to detrimental genetic interactions. Here, we perform a detailed cellular characterization of hybrid male sterility across three recently diverged species pairs of Drosophila . Across all three pairs, sterile hybrid sperm are alive but exhibit rapid nuclear de-condensation with age, with active, but non-differentiated, mitochondria. Surprisingly, all three sets of interspecies hybrids produce half of the number of sperm per round of spermatogenesis, with each sperm cell containing two tails. We identify non-disjunction failures during meiosis I as the likely cause. Thus, errors during meiosis I may be a general phenomenon underlying Drosophila male sterility, indicating either a heightened sensitivity of this spermatogenic stage to failure, or a basis to sterility other than the prevailing model.

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“…It allows for a striking degree of nuclear compaction to maintain the paternal genome integrity and promote sperm motility (Miller et al 2010;Rathke et al 2014). Drosophila male-specific transcripts of protamine A (ProtA) and ProtB encode protamine-like proteins that exhibit homology with mammalian protamines and constitute the major protein component of sperm chromatin (Raja and Renkawitz-Pohl 2005;Alvi et al 2013;Kanippayoor et al 2013). After egg fertilization, sperm chromatin undergoes remodeling (Loppin et al 2015), whereupon protamines are expelled from DNA by the combined action of a family of protamine chaperones (Emelyanov et al 2014) and replaced by core histones in a process dependent on the histone chaperone HIRA (Loppin et al 2005) and the ATP-driven motor protein CHD1 (Konev et al 2007).…”

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confidence: 99%

Thioredoxin-dependent disulfide bond reduction is required for protamine eviction from sperm chromatin

Emelyanov

Fyodorov

2016

Genes Dev.

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Cysteine oxidation in protamines leads to their oligomerization and contributes to sperm chromatin compaction. Here we identify the Drosophila thioredoxin Deadhead (DHD) as the factor responsible for the reduction of intermolecular disulfide bonds in protamines and their eviction from sperm during fertilization. Protamine chaperone TAP/p32 dissociates DNA-protamine complexes in vitro only when protamine oligomers are first converted to monomers by DHD. dhd-null embryos cannot decondense sperm chromatin and terminate development after the first pronuclear division. Therefore, the thioredoxin DHD plays a critical role in early development to facilitate the switch from protamine-based sperm chromatin structures to the somatic nucleosomal chromatin.

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Protamine-like Proteins in 12 Sequenced Species of Drosophila

Cited by 4 publications

References 0 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

A common suite of cellular abnormalities and spermatogenetic errors in sterile hybrid males inDrosophila

Thioredoxin-dependent disulfide bond reduction is required for protamine eviction from sperm chromatin

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