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

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 Pric...

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Main Authors: Bomsoo Cho, Song Song, Joy Y Wan, Jeffrey D Axelrod
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2022-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0262328
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author Bomsoo Cho
Song Song
Joy Y Wan
Jeffrey D Axelrod
author_facet Bomsoo Cho
Song Song
Joy Y Wan
Jeffrey D Axelrod
author_sort Bomsoo Cho
collection DOAJ
description 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.
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spelling doaj.art-59e15363ef23415cbe9a0af01371cb492022-12-22T02:59:52ZengPublic Library of Science (PLoS)PLoS ONE1932-62032022-01-01172e026232810.1371/journal.pone.0262328Prickle isoform participation in distinct polarization events in the Drosophila eye.Bomsoo ChoSong SongJoy Y WanJeffrey D AxelrodPlanar 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.https://doi.org/10.1371/journal.pone.0262328
spellingShingle Bomsoo Cho
Song Song
Joy Y Wan
Jeffrey D Axelrod
Prickle isoform participation in distinct polarization events in the Drosophila eye.
PLoS ONE
title Prickle isoform participation in distinct polarization events in the Drosophila eye.
title_full Prickle isoform participation in distinct polarization events in the Drosophila eye.
title_fullStr Prickle isoform participation in distinct polarization events in the Drosophila eye.
title_full_unstemmed Prickle isoform participation in distinct polarization events in the Drosophila eye.
title_short Prickle isoform participation in distinct polarization events in the Drosophila eye.
title_sort prickle isoform participation in distinct polarization events in the drosophila eye
url https://doi.org/10.1371/journal.pone.0262328
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AT jeffreydaxelrod prickleisoformparticipationindistinctpolarizationeventsinthedrosophilaeye