A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis

Rachel T. Cox, Allan C. Spradling

Research output: Contribution to journalArticle

Abstract

Maternally inherited mitochondria and other cytoplasmic organelles play essential roles supporting the development of early embryos and their germ cells. Using methods that resolve individual organelles, we studied the origin of oocyte and germ plasm-associated mitochondria during Drosophila oogenesis. Mitochondria partition equally on the spindle during germline stem cell and cystocyte divisions. Subsequently, a fraction of cyst mitochondria and Golgi vesicles associates with the fusome, moves through the ring canals, and enters the oocyte in a large mass that resembles the Balbiani bodies of Xenopus, humans and diverse other species. Some mRNAs, including oskar RNA, specifically associate with the oocyte fusome and a region of the Balbiani body prior to becoming localized. Balbiani body development requires an intact fusome and microtubule cytoskeleton as it is blocked by mutations in hu-li tai shao, while egalitarian mutant follicles accumulate a large mitochondrial aggregate in all 16 cyst cells. Initially, the Balbiani body supplies virtually all the mitochondria of the oocyte, including those used to form germ plasm, because the oocyte ring canals specifically block inward mitochondrial transport until the time of nurse cell dumping. Our findings reveal new similarities between oogenesis in Drosophila and vertebrates, and support our hypothesis that developing oocytes contain specific mechanisms to ensure that germ plasm is endowed with highly functional organelles.

Original languageEnglish (US)
Pages (from-to)1579-1590
Number of pages12
JournalDevelopment
Volume130
Issue number8
DOIs
StatePublished - Apr 2003
Externally publishedYes

Fingerprint

Oogenesis
Mitochondrial Genes
Drosophila
Oocytes
Mitochondria
Organelles
Cysts
Body Regions
Xenopus
Cytoskeleton
Human Body
Germ Cells
Microtubules
Cell Division
Embryonic Development
Vertebrates
Stem Cells
Nurses
RNA
Messenger RNA

Keywords

  • Balbiani body
  • Fusome
  • Germ plasm
  • Mitochondria
  • Oogenesis
  • Patterning

ASJC Scopus subject areas

  • Anatomy
  • Cell Biology

Cite this

A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. / Cox, Rachel T.; Spradling, Allan C.

In: Development, Vol. 130, No. 8, 04.2003, p. 1579-1590.

Research output: Contribution to journalArticle

Cox, Rachel T. ; Spradling, Allan C. / A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. In: Development. 2003 ; Vol. 130, No. 8. pp. 1579-1590.
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