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Auxin-induced nanoclustering of membrane signaling complexes underlies cell polarity establishment in Arabidopsis

Xue Pan, Linjing Fang, Jianfeng Liu, Betul Senay-Aras, Wenwei Lin, Shuan Zheng, Tong Zhang, View ORCID ProfileUri Manor, Weitao Chen, Zhenbiao Yang
doi: https://doi.org/10.1101/734665
Xue Pan
1FAFU-UCR Joint Center for Horticultural Biology and Metabolomics Center, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, China
2Center for Plant Cell Biology, Institute of Integrative Genome Biology, and Department of Botany and Plant Sciences, University of California, Riverside, 11 CA92521, USA
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Linjing Fang
3Waitt Advanced Biophotonics Center, The Salk Institute for Biological Studies, 10010 N Torrey Pines Rd., La Jolla, CA 92037, USA
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Jianfeng Liu
2Center for Plant Cell Biology, Institute of Integrative Genome Biology, and Department of Botany and Plant Sciences, University of California, Riverside, 11 CA92521, USA
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Betul Senay-Aras
4Department of Mathematics, University of California, Riverside, 11 CA92521, USA
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Wenwei Lin
1FAFU-UCR Joint Center for Horticultural Biology and Metabolomics Center, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, China
2Center for Plant Cell Biology, Institute of Integrative Genome Biology, and Department of Botany and Plant Sciences, University of California, Riverside, 11 CA92521, USA
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Shuan Zheng
1FAFU-UCR Joint Center for Horticultural Biology and Metabolomics Center, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, China
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Tong Zhang
3Waitt Advanced Biophotonics Center, The Salk Institute for Biological Studies, 10010 N Torrey Pines Rd., La Jolla, CA 92037, USA
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Uri Manor
3Waitt Advanced Biophotonics Center, The Salk Institute for Biological Studies, 10010 N Torrey Pines Rd., La Jolla, CA 92037, USA
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  • ORCID record for Uri Manor
Weitao Chen
4Department of Mathematics, University of California, Riverside, 11 CA92521, USA
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  • For correspondence: weitaoc@ucr.edu yang@ucr.edu
Zhenbiao Yang
1FAFU-UCR Joint Center for Horticultural Biology and Metabolomics Center, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, China
2Center for Plant Cell Biology, Institute of Integrative Genome Biology, and Department of Botany and Plant Sciences, University of California, Riverside, 11 CA92521, USA
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  • For correspondence: weitaoc@ucr.edu yang@ucr.edu
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Abstract

Cell polarity is fundamental to the development of both eukaryotic and prokaryotic organisms, yet the mechanism of its establishment remains poorly understood. Here we show that signal-activated nanoclustering of membrane proteins and a cytoskeleton-based feedback loop provide an important mechanism for the establishment of cell polarity. The phytohormone auxin promoted sterol-dependent nanoclustering of cell surface transmembrane receptor-like kinase 1 (TMK1) to initiate cell polarity during the morphogenesis of Arabidopsis puzzle piece-shaped leaf pavement cells (PC). Auxin-triggered nanoclustering of TMK1 stabilized flotillin-associated ordered nanodomains, which were essential for auxin-mediated formation of ROP6 GTPase nanoclusters that act downstream TMK1 to promote cortical microtubule ordering. Mathematical modeling further demonstrated the essential role of this auxin-mediated stabilization of TMK1 and ROP6 nanoclusters, and predicted the additional requirement of ROP6-dependent cortical microtubules for further stabilization of TMK1-sterol nanodomains and the polarization of PC. This prediction was experimentally validated by genetic and biochemical data. Our studies reveal a new paradigm for polarity establishment: A diffusive signal triggers cell polarization by activating cell surface receptor-mediated lateral segregation of signaling components and a cytoskeleton-mediated positive feedback loop of nanodomain stabilization.

Highlights

  • Sterols are required for cell polarity in Arabidopsis leaf epidermal cells

  • Auxin promotes lipid ordering and polar distribution of ordered lipid nanodomains at the plasma membrane (PM)

  • Auxin stabilizes sterol-dependent nanoclustering of transmembrane kinase (TMK1), a PM auxin signal transducer

  • Auxin-induced TMK1 nanoclustering is required but insufficient for cell polarization

  • Microtubule-based feedback stabilization of the auxin-induced TMK1 nanodomains can generate cell polarity

Footnotes

  • Figure 7 has been revised in this version

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted August 14, 2019.
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Auxin-induced nanoclustering of membrane signaling complexes underlies cell polarity establishment in Arabidopsis
Xue Pan, Linjing Fang, Jianfeng Liu, Betul Senay-Aras, Wenwei Lin, Shuan Zheng, Tong Zhang, Uri Manor, Weitao Chen, Zhenbiao Yang
bioRxiv 734665; doi: https://doi.org/10.1101/734665
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Auxin-induced nanoclustering of membrane signaling complexes underlies cell polarity establishment in Arabidopsis
Xue Pan, Linjing Fang, Jianfeng Liu, Betul Senay-Aras, Wenwei Lin, Shuan Zheng, Tong Zhang, Uri Manor, Weitao Chen, Zhenbiao Yang
bioRxiv 734665; doi: https://doi.org/10.1101/734665

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