Prickle isoform participation in distinct polarization events in the Drosophila eye

PLoS One. 2022 Feb 11;17(2):e0262328. doi: 10.1371/journal.pone.0262328. eCollection 2022.

Abstract

Planar cell polarity (PCP) signaling regulates several polarization events during development of ommatidia in the Drosophila eye, including directing chirality by polarizing a cell fate choice and determining the direction and extent of ommatidial rotation. The pksple isoform of the PCP protein Prickle is known to participate in the R3/R4 cell fate decision, but the control of other polarization events and the potential contributions of the three Pk isoforms have not been clarified. Here, by characterizing expression and subcellular localization of individual isoforms together with re-analyzing isoform specific phenotypes, we show that the R3/R4 fate decision, its coordination with rotation direction, and completion of rotation to a final ±90° rotation angle are separable polarization decisions with distinct Pk isoform requirements and contributions. Both pksple and pkpk can enforce robust R3/R4 fate decisions, but only pksple can correctly orient them along the dorsal-ventral axis. In contrast, pksple and pkpk can fully and interchangeably sustain coordination of rotation direction and rotation to completion. We propose that expression dynamics and competitive interactions determine isoform participation in these processes. We propose that the selective requirement for pksple to orient the R3/R4 decision and their interchangeability for coordination and completion of rotation reflects their previously described differential interaction with the Fat/Dachsous system which is known to be required for orientation of R3/R4 decisions but not for coordination or completion of rotation.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Brain / metabolism
  • CRISPR-Cas Systems / genetics
  • DNA-Binding Proteins / antagonists & inhibitors
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Drosophila / metabolism*
  • Drosophila Proteins / antagonists & inhibitors
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Eye / metabolism*
  • Gene Editing
  • Genotype
  • LIM Domain Proteins / antagonists & inhibitors
  • LIM Domain Proteins / genetics
  • LIM Domain Proteins / metabolism*
  • Membrane Proteins / metabolism
  • Phenotype
  • Protein Isoforms / antagonists & inhibitors
  • Protein Isoforms / genetics
  • Protein Isoforms / metabolism
  • RNA Interference
  • RNA, Small Interfering / metabolism
  • Signal Transduction / genetics

Substances

  • DNA-Binding Proteins
  • Drosophila Proteins
  • LIM Domain Proteins
  • Membrane Proteins
  • Protein Isoforms
  • RNA, Small Interfering
  • Vang protein, Drosophila
  • pk protein, Drosophila