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

Nature Plants volume 4, pages 1082–1088 (2018)Cite this article

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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.

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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.

References

  1. Smertenko, A. et al. Plant cytokinesis: terminology for structures and processes. Trends Cell Biol. 27, 885–894 (2017).

    Article  CAS  Google Scholar 

  2. Geldner, N. et al. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413, 425–428 (2001).

    Article  CAS  Google Scholar 

  3. Mravec, J. et al. Cell plate restricted association of DRP1A and PIN proteins is required for cell polarity establishment in Arabidopsis. Curr. Biol. 21, 1055–1060 (2011).

    Article  CAS  Google Scholar 

  4. Men, S. et al. Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nat. Cell Biol. 10, 237–244 (2008).

    Article  CAS  Google Scholar 

  5. Yoshinari, A. et al. DRP1-dependent endocytosis is essential for polar localization and boron-induced degradation of the borate transporter BOR1 in Arabidopsis thaliana. Plant Cell Physiol. 57, 1985–2000 (2016).

    Article  CAS  Google Scholar 

  6. Dhonukshe, P. et al. Plasma membrane-bound AGC3 kinases phosphorylate PIN auxin carriers at TPRXS(N/S) motifs to direct apical PIN recycling. Development 137, 3245–3255 (2010).

    Article  CAS  Google Scholar 

  7. Kania, U. et al. Polar delivery in plants; commonalities and differences to animal epithelial cells. Open Biol. 4, 140017 (2014).

    Article  Google Scholar 

  8. Abas, L. et al. Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat. Cell Biol. 8, 249–256 (2006).

    Article  CAS  Google Scholar 

  9. Baster, P. et al. SCF(TIR1/AFB)-auxin signalling regulates PIN vacuolar trafficking and auxin fluxes during root gravitropism. EMBO J. 32, 260–274 (2013).

    Article  CAS  Google Scholar 

  10. Dhonukshe, P. et al. Endocytosis of cell surface material mediates cell plate formation during plant cytokinesis. Dev. Cell 10, 137–150 (2006).

    Article  CAS  Google Scholar 

  11. Gurskaya, N. G. et al. Engineering of a monomeric green-to-red photoactivatable fluorescent protein induced by blue light. Nat. Biotechnol. 24, 461–465 (2006).

    Article  CAS  Google Scholar 

  12. Richter, S. et al. Delivery of endocytosed proteins to the cell-division plane requires change of pathway from recycling to secretion. eLife 3, e02131 (2014).

    Article  Google Scholar 

  13. Lauber, M. H. et al. The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J. Cell Biol. 139, 1485–1493 (1997).

    Article  CAS  Google Scholar 

  14. Sparks, E. et al. Spatiotemporal signalling in plant development. Nat. Rev. Genet. 14, 631–644 (2013).

    Article  CAS  Google Scholar 

  15. Mazur, E. et al. Vascular cambium regeneration and vessel formation in wounded inflorescence stems of Arabidopsis. Sci. Rep. 6, 33754 (2016).

    Article  CAS  Google Scholar 

  16. Prát, T. et al. WRKY23 is a component of the transcriptional network mediating auxin feedback on PIN polarity. PLoS Genet. 14, e1007177 (2018).

    Article  Google Scholar 

  17. Simon, S. et al. Defining the selectivity of processes along the auxin response chain: a study using auxin analogues. New Phytol. 200, 1034–1048 (2013).

    Article  CAS  Google Scholar 

  18. Sena, G. et al. Organ regeneration does not require a functional stem cell niche in plants. Nature 457, 1150–1153 (2009).

    Article  CAS  Google Scholar 

  19. Kleine-Vehn, J. et al. Cellular and molecular requirements for polar PIN targeting and transcytosis in plants. Mol. Plant 1, 1056–1066 (2008).

    Article  CAS  Google Scholar 

  20. Kleine-Vehn, J. et al. Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Mol. Syst. Biol. 7, 540 (2011).

    Article  Google Scholar 

  21. Feraru, E. et al. PIN polarity maintenance by the cell wall in Arabidopsis. Curr. Biol. 21, 338–343 (2011).

    Article  CAS  Google Scholar 

  22. Martinière, A. et al. Cell wall constrains lateral diffusion of plant plasma-membrane proteins. Proc. Natl Acad. Sci. USA 109, 12805–12810 (2012).

    Article  Google Scholar 

  23. Kitakura, S. et al. Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell 23, 1920–1931 (2011).

    Article  CAS  Google Scholar 

  24. Adamowski, M. et al. A functional study of AUXILIN-LIKE1 and 2, two putative clathrin uncoating factors in Arabidopsis. Plant Cell 30, 700–716 (2018).

    Article  CAS  Google Scholar 

  25. Friml, J. et al. A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306, 862–865 (2004).

    Article  CAS  Google Scholar 

  26. Michniewicz, M. et al. Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130, 1044–1056 (2007).

    Article  CAS  Google Scholar 

  27. Kleine-Vehn, J. et al. PIN auxin efflux carrier polarity is regulated by PINOID kinase-mediated recruitment into GNOM-independent trafficking in Arabidopsis. Plant Cell 21, 3839–3849 (2009).

    Article  CAS  Google Scholar 

  28. Zhang, J. et al. PIN phosphorylation is sufficient to mediate PIN polarity and direct auxin transport. Proc. Natl Acad. Sci. USA 107, 918–922 (2010).

    Article  CAS  Google Scholar 

  29. Huang, F. et al. Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport. Plant Cell 22, 1129–1142 (2010).

    Article  CAS  Google Scholar 

  30. Weller, B. et al. Dynamic PIN-FORMED auxin efflux carrier phosphorylation at the plasma membrane controls auxin efflux-dependent growth. Proc. Natl Acad. Sci. USA 114, E887–E896 (2017).

    Article  CAS  Google Scholar 

  31. Furutani, M. et al. Polar-localized NPH3-like proteins regulate polarity and endocytosis of PIN-FORMED auxin efflux carriers. Development 138, 2069–2078 (2011).

    Article  CAS  Google Scholar 

  32. Salanenka, Y. et al. Gibberellin DELLA signaling targets the retromer complex to redirect protein trafficking to the plasma membrane. Proc. Natl Acad. Sci. USA 115, 3716–3721 (2018).

    Article  CAS  Google Scholar 

  33. Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998).

    Article  CAS  Google Scholar 

  34. Luschnig, C. et al. EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 12, 2175–2187 (1998).

    Article  CAS  Google Scholar 

  35. von Wangenheim, D. et al. Live tracking of moving samples in confocal microscopy for vertically grown roots. eLife 6, e26792 (2017).

    Article  Google Scholar 

  36. Jásik, J. et al. PIN2 turnover in Arabidopsis root epidermal cells explored by the photoconvertible protein Dendra2. PLoS ONE 8, e61403 (2013).

    Article  Google Scholar 

  37. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).

    Article  CAS  Google Scholar 

  38. Grabov, A. et al. Morphometric analysis of root shape. New Phytol. 165, 641–651 (2005).

    Article  CAS  Google Scholar 

Download references

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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Authors and Affiliations

  1. IST Austria, Klosterneuburg, Austria

    Matouš Glanc, Matyáš Fendrych & Jiří Friml

  2. Department of Experimental Plant Biology, Faculty of Science, Charles University, Prague, Czech Republic

    Matouš Glanc & Matyáš Fendrych

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  1. Matouš Glanc
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Contributions

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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The authors declare no competing interests.

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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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