A Role for Maternal Factors in Suppressing Cytoplasmic Incompatibility

Momtaz, Ajm Zehadee; Sabagh, Abraham D. Ahumada; Amortegui, Julian G Gonzalez; Salazar, Samuel A.; Finessi, Andrea; Hernandez, Jethel; Christensen, Søren T.; Serbus, Laura R.

doi:10.3389/fmicb.2020.576844

Cited by 5 publications

(6 citation statements)

References 149 publications

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“…Our data reinforce that DNA integrity, damage, and repair are key aspects of Cif-mediated CI and rescue. Indeed, treating aposymbiotic females with DNA repair chemicals suppressed CI ( 45 ). These results suggest that there is a CI cascade of damage, spanning prefertilization chromatin integrity changes to postfertilized embryos.…”

Section: Embryos Succumb To Dna Damagementioning

confidence: 99%

Prophage proteins alter long noncoding RNA and DNA of developing sperm to induce a paternal-effect lethality

Kaur,

McGarry,

Shropshire

et al. 2024

Science

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The extent to which prophage proteins interact with eukaryotic macromolecules is largely unknown. In this work, we show that cytoplasmic incompatibility factor A (CifA) and B (CifB) proteins, encoded by prophage WO of the endosymbiont Wolbachia, alter long noncoding RNA (lncRNA) and DNA during Drosophila sperm development to establish a paternal-effect embryonic lethality known as cytoplasmic incompatibility (CI). CifA is a ribonuclease (RNase) that depletes a spermatocyte lncRNA important for the histone-to-protamine transition of spermiogenesis. Both CifA and CifB are deoxyribonucleases (DNases) that elevate DNA damage in late spermiogenesis. lncRNA knockdown enhances CI, and mutagenesis links lncRNA depletion and subsequent sperm chromatin integrity changes to embryonic DNA damage and CI. Hence, prophage proteins interact with eukaryotic macromolecules during gametogenesis to create a symbiosis that is fundamental to insect evolution and vector control.

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Section: Embryos Succumb To Dna Damagementioning

confidence: 99%

Prophage proteins alter long noncoding RNA and DNA of developing sperm to induce a paternal-effect lethality

Kaur,

McGarry,

Shropshire

et al. 2024

Science

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“…We speculate that cifA in host females alters ubiquitination, which may have prevented the binding of cifA to cifB. In Drosophila simulans, chemically induced degradation of DNA in WU females significantly increased CI egg hatchability, which raises the possibility that Wolbachia rescues CI by degrading the DNA of the host (Momtaz et al, 2020). Deubiquitylating enzyme (Beckmann et al, 2017) and nuclease (Chen et al, 2019) were shown to be major causes of CI.…”

Section: Discussionmentioning

confidence: 95%

“…In Drosophila simulans , chemically induced degradation of DNA in WU females significantly increased CI egg hatchability, which raises the possibility that Wolbachia rescues CI by degrading the DNA of the host (Momtaz et al. , 2020). Deubiquitylating enzyme (Beckmann et al.…”

Section: Discussionmentioning

confidence: 99%

NDUFA8 potentially rescues Wolbachia‐induced cytoplasmic incompatibility in Laodelphax striatellus

et al. 2023

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The endosymbiont Wolbachia manipulates host reproduction by several strategies, one of the most important of which is cytoplasmic incompatibility (CI). CI can be rescued when Wolbachia‐infected males mate with females infected with the same Wolbachia strain. However, the potential rescue mechanism of CI in the small brown planthopper Laodelphax striatellus is unclear. In this study, comparative transcriptome analysis was applied to explore the effect of Wolbachia on L. striatellus eggs. A total of 1387 differentially expressed genes were identified. RNA interference of 7 Wolbachia‐upregulated key planthopper genes reduced egg reproduction, suggesting that Wolbachia might improve fecundity in L. striatellus by affecting these 7 genes. Suppressing the expression of another upregulated gene, NDUFA8 (encoding NADH dehydrogenase [ubiquinone] 1 α subcomplex subunit 8‐like) by RNA interference significantly increased the mortality of early embryos without affecting the number of deposited eggs. Wolbachia infection upregulated the mRNA level of NDUFA8, and dsNDUFA8 treatment of Wolbachia‐infected females recreated CI‐like symptoms, suggesting that NDUFA8 is associated with the rescue phenotype. Because all L. striatellus populations worldwide are infected with Wolbachia, NDUFA8 is a potential pest control target.

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“…For example, studies of hybrid incompatibilities between D. simulans and D. melanogaster show that heterochromatin establishment may be particularly sensitive, and its disruption can result in defects strikingly similar to the late CI defects (Ferree & Barbash, 2009). Other important processes, such as those involved in DNA integrity, protein turnover, and cell cycle timing, may be also involved (Momtaz et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

Wolbachia action in the sperm produces developmentally deferred chromosome segregation defects during the Drosophila mid-blastula transition

Warecki

Titen

Alam

et al. 2022

Preprint

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Wolbachia, a vertically transmitted endosymbiont infecting many insects, spreads rapidly through uninfected populations by a mechanism known as Cytoplasmic Incompatibility (CI). In CI, embryos from crosses between Wolbachia-infected males and uninfected females fail to develop due to the immediate action of Wolbachia-produced factors in the first zygotic division. In contrast, viable progeny are produced when the female parent is infected. Here, we find ~1/3 of embryos from CI crosses in Drosophila simulans develop normally beyond the first and subsequent pre-blastoderm divisions. Developing CI-derived embryos then exhibit chromosome segregation errors during the mid-blastula transition and gastrulation. Single embryo PCR and whole genome sequencing reveal a large percentage of the developed CI-derived embryos bypass the first division defect. Using fluorescence in situ hybridization, we find increased chromosome segregation errors in gastrulating CI-derived embryos that had avoided the first division defect. Thus, Wolbachia in the sperm induces independent immediate and developmentally deferred defects. Like the initial immediate defect, the delayed defect is rescued through crosses to infected females.

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A Role for Maternal Factors in Suppressing Cytoplasmic Incompatibility

Cited by 5 publications

References 149 publications

Prophage proteins alter long noncoding RNA and DNA of developing sperm to induce a paternal-effect lethality

Prophage proteins alter long noncoding RNA and DNA of developing sperm to induce a paternal-effect lethality

NDUFA8 potentially rescues Wolbachia‐induced cytoplasmic incompatibility in Laodelphax striatellus

Wolbachia action in the sperm produces developmentally deferred chromosome segregation defects during the Drosophila mid-blastula transition

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