Mechanistic framework for cell-intrinsic re-establishment of PIN2 polarity after cell division

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Abstract

Cell polarity, manifested by the localization of proteins to distinct polar plasma membrane domains, is a key prerequisite of multicellular life. In plants, PIN auxin transporters are prominent polarity markers crucial for a plethora of developmental processes. Cell polarity mechanisms in plants are distinct from other eukaryotes and still largely elusive. In particular, how the cell polarities are propagated and maintained following cell division remains unknown. Plant cytokinesis is orchestrated by the cell plate—a transient centrifugally growing endomembrane compartment ultimately forming the cross wall1. Trafficking of polar membrane proteins is typically redirected to the cell plate, and these will consequently have opposite polarity in at least one of the daughter cells2,3,4,5. Here, we provide mechanistic insights into post-cytokinetic re-establishment of cell polarity as manifested by the apical, polar localization of PIN2. We show that the apical domain is defined in a cell-intrinsic manner and that re-establishment of PIN2 localization to this domain requires de novo protein secretion and endocytosis, but not basal-to-apical transcytosis. Furthermore, we identify a PINOID-related kinase WAG1, which phosphorylates PIN2 in vitro6 and is transcriptionally upregulated specifically in dividing cells, as a crucial regulator of post-cytokinetic PIN2 polarity re-establishment.

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Fig. 1: Cell polarity needs to be re-established after cytokinesis.
Fig. 2: Apical–basal polarity of newly divided cells is established in a cell-intrinsic manner.
Fig. 3: PIN2 apical polarity re-establishment requires secretion and endocytosis, but not transcytosis.
Fig. 4: PIN apical polarity re-establishment is mediated by the AGCVIII kinase WAG1.

Data availability

The data that support the findings of this study are available from the corresponding author upon request.

Change history

  • 14 December 2018

    In the version of this Article originally published, Supplementary Video 2 was incorrectly linked to Supplementary Video 1, Supplementary Video 3 was incorrectly linked to Supplementary Video 2, Supplementary Video 4 was incorrectly linked to Supplementary Video 3 and Supplementary Video 5 was incorrectly linked to Supplementary Video 4. Additionally, Supplementary Video 5 was missing from the linked files. The files have now been replaced to rectify this.

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Acknowledgements

We thank N. Geldner, C. Luschnig, G. Jürgens, R. Offringa and Y. Takano for sharing published material. We would also like to acknowledge M. Adamowski, U. Kania and C. Cuesta for providing entry clones, and the Biomaging Facility at IST Austria for providing excellent imaging service and assistance. The research leading to these results has received funding from the European Research Council under the European Union’s Seventh Framework Programme/ERC grant agreement no. 742985. Additionally, funding was received from the Ministry of Education of the Czech Republic/MŠMT project NPUI - LO1417.

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M.G. designed experiments, performed experiments, analysed data and wrote the manuscript. M.F. designed experiments, analysed data and edited the manuscript. J.F. initiated the project, acquired funding, designed experiments and wrote the manuscript.

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Correspondence to Jiří Friml.

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Supplementary information

Supplementary Information

Supplementary Figures 1–6 and Supplementary Table 1.

Reporting Summary

Supplementary Video 1

PIN2::PIN2–Dendra dynamics in dividing cells. The experiment was repeated independently three times with similar results.

Supplementary Video 2

KN::PIN2–GFP dynamics in dividing cells. The experiment was repeated independently more than three times with similar results.

Supplementary Video 3

Effect of AXL2 overexpression on KN::PIN2–GFP dynamics. The experiment was repeated independently three times with similar results.

Supplementary Video 4

KN::PIN2–GFP dynamics in pid wag1 wag2 mutant background. The experiment was repeated independently three times with similar results.

Supplementary Video 5

WAG1::WAG1–GFP dynamics in dividing cells. The experiment was repeated independently three times with similar results.

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Glanc, M., Fendrych, M. & Friml, J. Mechanistic framework for cell-intrinsic re-establishment of PIN2 polarity after cell division. Nature Plants 4, 1082–1088 (2018). https://doi.org/10.1038/s41477-018-0318-3

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