Prickle isoform participation in distinct polarization events in the Drosophila eye.

Bomsoo Cho,Jeffrey D Axelrod,Song Song,Joy Y Wan,Carlos Oliva

doi:10.1371/journal.pone.0262328

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.

Highlights

Planar cell polarity (PCP) signaling controls the polarization of cells within the plane of an epithelium, orienting asymmetric cellular structures, cell divisions and cell migration
These observations are consistent with the R3/R4 fate decision depending on participation of Pksple for the PCP-dependent biasing of the N signaling event
Our results show that ommatidial rotation can occur in the absence of intact PCP signaling, but that timely initiation, rotation in the correct direction, and conclusion at 90 ̊ all depend on PCP signaling

Summary

Introduction

PCP signaling controls the polarization of cells within the plane of an epithelium, orienting asymmetric cellular structures, cell divisions and cell migration. PCP signaling controls the orientation of hairs on the adult cuticle, chirality and orientation of ommatidia in the eye, orientation of cell divisions, and related processes in other tissues. While much mechanistic understanding of PCP signaling derives from work using Drosophila as a model system, medically important developmental defects and physiological processes in vertebrates are under control of PCP signaling, motivating considerable interest in studying PCP both in Drosophila and in vertebrate model systems. Prickle isoform participation in distinct polarization events in the Drosophila eye (https://www.nigms.nih.gov). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

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Conclusion