Clustered nuclei maintain autonomy and nucleocytoplasmic ratio control in a syncytium

Mol Biol Cell. 2016 Jul 1;27(13):2000-7. doi: 10.1091/mbc.E16-02-0129. Epub 2016 May 18.

Abstract

Nuclei in syncytia found in fungi, muscles, and tumors can behave independently despite cytoplasmic translation and the homogenizing potential of diffusion. We use a dynactin mutant strain of the multinucleate fungus Ashbya gossypii with highly clustered nuclei to assess the relative contributions of nucleus and cytoplasm to nuclear autonomy. Remarkably, clustered nuclei maintain cell cycle and transcriptional autonomy; therefore some sources of nuclear independence function even with minimal cytosol insulating nuclei. In both nuclear clusters and among evenly spaced nuclei, a nucleus' transcriptional activity dictates local cytoplasmic contents, as assessed by the localization of several cyclin mRNAs. Thus nuclear activity is a central determinant of the local cytoplasm in syncytia. Of note, we found that the number of nuclei per unit cytoplasm was identical in the mutant to that in wild-type cells, despite clustered nuclei. This work demonstrates that nuclei maintain autonomy at a submicrometer scale and simultaneously maintain a normal nucleocytoplasmic ratio across a syncytium up to the centimeter scale.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, N.I.H., Intramural
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Cycle / physiology
  • Cell Nucleus / metabolism*
  • Cell Nucleus / physiology
  • Cell Nucleus Division / physiology
  • Cyclins / metabolism
  • Cytoplasm / metabolism
  • Cytoplasm / pathology
  • Fungal Proteins / metabolism
  • Fungi / metabolism
  • Giant Cells / metabolism*
  • Giant Cells / physiology
  • Mitosis
  • Saccharomycetales / metabolism
  • Transcriptional Activation

Substances

  • Cyclins
  • Fungal Proteins