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

• Published in: eLife Vol. 11
• Main Authors: Warecki, Brandt, Titen, Simon William Abraham, Alam, Mohammad Shahriyar, Vega, Giovanni, Lemseffer, Nassim, Hug, Karen, Minden, Jonathan S, Sullivan, William
• Format: Journal Article
• Language: English
• Published: England eLife Sciences Publications Ltd 23.09.2022; eLife Sciences Publications, Ltd
• Subjects: Animals; Blastoderm; Blastula; Cell Biology; Cell cycle; Chromatin; Chromosome Segregation; Chromosomes; Chromosomes and Gene Expression; Cytoplasm; Cytoplasmic incompatibility; Drosophila - genetics; Drosophila simulans; Eggs; Embryogenesis; Embryos; Female; Females; Fluorescence in situ hybridization; Gastrulation; Genomes; In Situ Hybridization, Fluorescence; Insects; Lethality; Male; Males; mid-blastula transition; Mitosis; Molecular modelling; nuclear fallout; Semen; Sperm; Spermatozoa; Whole genome sequencing; Wolbachia; Wolbachia - genetics; Drosophila simulans; cell biology; chromosome segregation; Wolbachia; chromosomes; mid-blastula transition; nuclear fallout; cytoplasmic incompatibility; gene expression
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.81292

, a vertically transmitted endosymbiont infecting many insects, spreads rapidly through uninfected populations by a mechanism known as cytoplasmic incompatibility (CI). In CI, a paternally delivered modification of the sperm leads to chromatin defects and lethality during and after the first mitosis of embryonic development in multiple species. However, whether CI-induced defects in later stage embryos are a consequence of the first division errors or caused by independent defects remains unresolved. To address this question, we focused on ~1/3 of embryos from CI crosses in that develop apparently normally through the first and subsequent pre-blastoderm divisions before exhibiting mitotic errors during the mid-blastula transition and gastrulation. We performed single embryo PCR and whole genome sequencing to find a large percentage of these 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, action in the sperm induces developmentally deferred defects that are not a consequence of the first division errors. Like the immediate defect, the delayed defect is rescued through crosses to infected females. These studies inform current models on the molecular and cellular basis of CI.