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Fusome topology and inheritance during insect gametogenesis.

Publication ,  Journal Article
Diegmiller, R; Imran Alsous, J; Li, D; Yamashita, YM; Shvartsman, SY
Published in: PLoS computational biology
February 2023

From insects to mammals, oocytes and sperm develop within germline cysts comprising cells connected by intercellular bridges (ICBs). In numerous insects, formation of the cyst is accompanied by growth of the fusome-a membranous organelle that permeates the cyst. Fusome composition and function are best understood in Drosophila melanogaster: during oogenesis, the fusome dictates cyst topology and size and facilitates oocyte selection, while during spermatogenesis, the fusome synchronizes the cyst's response to DNA damage. Despite its distinct and sex-specific roles during insect gametogenesis, elucidating fusome growth and inheritance in females and its structure and connectivity in males has remained challenging. Here, we take advantage of advances in three-dimensional (3D) confocal microscopy and computational image processing tools to reconstruct the topology, growth, and distribution of the fusome in both sexes. In females, our experimental findings inform a theoretical model for fusome assembly and inheritance and suggest that oocyte selection proceeds through an 'equivalency with a bias' mechanism. In males, we find that cell divisions can deviate from the maximally branched pattern observed in females, leading to greater topological variability. Our work consolidates existing disjointed experimental observations and contributes a readily generalizable computational approach for quantitative studies of gametogenesis within and across species.

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Published In

PLoS computational biology

DOI

EISSN

1553-7358

ISSN

1553-734X

Publication Date

February 2023

Volume

19

Issue

2

Start / End Page

e1010875

Related Subject Headings

  • Semen
  • Oogenesis
  • Oocytes
  • Mammals
  • Male
  • Female
  • Drosophila melanogaster
  • Cell Division
  • Bioinformatics
  • Animals
 

Citation

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Diegmiller, R., Imran Alsous, J., Li, D., Yamashita, Y. M., & Shvartsman, S. Y. (2023). Fusome topology and inheritance during insect gametogenesis. PLoS Computational Biology, 19(2), e1010875. https://doi.org/10.1371/journal.pcbi.1010875
Diegmiller, Rocky, Jasmin Imran Alsous, Duojia Li, Yukiko M. Yamashita, and Stanislav Y. Shvartsman. “Fusome topology and inheritance during insect gametogenesis.PLoS Computational Biology 19, no. 2 (February 2023): e1010875. https://doi.org/10.1371/journal.pcbi.1010875.
Diegmiller R, Imran Alsous J, Li D, Yamashita YM, Shvartsman SY. Fusome topology and inheritance during insect gametogenesis. PLoS computational biology. 2023 Feb;19(2):e1010875.
Diegmiller, Rocky, et al. “Fusome topology and inheritance during insect gametogenesis.PLoS Computational Biology, vol. 19, no. 2, Feb. 2023, p. e1010875. Epmc, doi:10.1371/journal.pcbi.1010875.
Diegmiller R, Imran Alsous J, Li D, Yamashita YM, Shvartsman SY. Fusome topology and inheritance during insect gametogenesis. PLoS computational biology. 2023 Feb;19(2):e1010875.

Published In

PLoS computational biology

DOI

EISSN

1553-7358

ISSN

1553-734X

Publication Date

February 2023

Volume

19

Issue

2

Start / End Page

e1010875

Related Subject Headings

  • Semen
  • Oogenesis
  • Oocytes
  • Mammals
  • Male
  • Female
  • Drosophila melanogaster
  • Cell Division
  • Bioinformatics
  • Animals