Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Plant cell polarity as the nexus of tissue mechanics and morphogenesis

Abstract

How reproducible body patterns emerge from the collective activity of individual cells is a key question in developmental biology. Plant cells are encaged in their walls and unable to migrate. Morphogenesis thus relies on directional cell division, by precise positioning of division planes, and anisotropic cellular growth, mediated by regulated mechanical inhomogeneity of the walls. Both processes require the prior establishment of cell polarity, marked by the formation of polar domains at the plasma membrane, in a number of developmental contexts. The establishment of cell polarity involves biochemical cues, but increasing evidence suggests that mechanical forces also play a prominent instructive role. While evidence for mutual regulation between cell polarity and tissue mechanics is emerging, the nature of this bidirectional feedback remains unclear. Here we review the role of cell polarity at the interface of tissue mechanics and morphogenesis. We also aim to integrate biochemistry-centred insights with concepts derived from physics and physical chemistry. Lastly, we propose a set of questions that will help address the fundamental nature of cell polarization and its mechanistic basis.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Mechanical forces in plant cells and tissues.
Fig. 2: Polar domains and PM heterogeneity.
Fig. 3: The link between polar protein domains and morphogenesis.
Fig. 4: Sensitivity of CMTs to tensile stress and their role in growth anisotropy.
Fig. 5: Physical control over PM organization and behaviour.
Fig. 6: The role of polar protein domains in the mechanical regulation of plant morphogenesis.

Similar content being viewed by others

References

  1. Thompson, D. W. On Growth and Form (1942).

  2. Darwin, C. The Origin of Species (PF Collier & Son, 1909).

  3. Turing, A. M. The chemical basis of morphogenesis. Bull. Math. Biol. 52, 153–197 (1990).

    Article  CAS  PubMed  Google Scholar 

  4. Pillitteri, L. J., Guo, X. & Dong, J. Asymmetric cell division in plants: mechanisms of symmetry breaking and cell fate determination. Cell. Mol. Life Sci. 73, 4213–4229 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Yang, Z. & Lavagi, I. Spatial control of plasma membrane domains: ROP GTPase-based symmetry breaking. Curr. Opin. Plant Biol. 15, 601–607 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Dong, J., MacAlister, C. A. & Bergmann, D. C. BASL controls asymmetric cell division in Arabidopsis. Cell 137, 1320–1330 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  7. Muroyama, A. & Bergmann, D. Plant cell polarity: creating diversity from inside the box. Annu. Rev. Cell Dev. Biol. 35, 309–336 (2019).

    Article  CAS  PubMed  Google Scholar 

  8. Goehring, N. W. PAR polarity: from complexity to design principles. Exp. Cell Res. 328, 258–266 (2014).

    Article  CAS  PubMed  Google Scholar 

  9. Hoege, C. & Hyman, A. A. Principles of PAR polarity in Caenorhabditis elegans embryos. Nat. Rev. Mol. Cell Biol. 14, 315–322 (2013).

    Article  CAS  PubMed  Google Scholar 

  10. Yoshida, S. et al. A SOSEKI-based coordinate system interprets global polarity cues in Arabidopsis. Nat. Plants 5, 160–166 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Louveaux, M., Julien, J.-D., Mirabet, V., Boudaoud, A. & Hamant, O. Cell division plane orientation based on tensile stress in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 113, E4294–E4303 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Heisler, M. G. et al. Alignment between PIN1 polarity and microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport. PLoS Biol. 8, e1000516 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Hamant, O. et al. Developmental patterning by mechanical signals in Arabidopsis. Science 322, 1650–1655 (2008).

    Article  CAS  PubMed  Google Scholar 

  14. Sampathkumar, A. et al. Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells. eLife 3, e01967 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  15. Sampathkumar, A., Yan, A., Krupinski, P. & Meyerowitz, E. M. Physical forces regulate plant development and morphogenesis. Curr. Biol. 24, R475–R483 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Uyttewaal, M. et al. Mechanical stress acts via katanin to amplify differences in growth rate between adjacent cells in Arabidopsis. Cell 149, 439–451 (2012).

    Article  CAS  PubMed  Google Scholar 

  17. Nakayama, N. et al. Mechanical regulation of auxin-mediated growth. Curr. Biol. 22, 1468–1476 (2012).

    Article  CAS  PubMed  Google Scholar 

  18. Hervieux, N. et al. A mechanical feedback restricts sepal growth and shape in Arabidopsis. Curr. Biol. 26, 1019–1028 (2016).

    Article  CAS  Google Scholar 

  19. Landrein, B. et al. Mechanical stress contributes to the expression of the STM homeobox gene in Arabidopsis shoot meristems. eLife 4, e07811 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  20. Bringmann, M. & Bergmann, D. C. Tissue-wide mechanical forces influence the polarity of stomatal stem cells in Arabidopsis. Curr. Biol. 27, 877–883 (2017).

    Article  CAS  PubMed  Google Scholar 

  21. Hong, L. et al. Variable cell growth yields reproducible organ development through spatiotemporal averaging. Dev. Cell 38, 15–32 (2016).

    Article  CAS  PubMed  Google Scholar 

  22. Dalous, J. et al. Reversal of cell polarity and actin–myosin cytoskeleton reorganization under mechanical and chemical stimulation. Biophys. J. 94, 1063–1074 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Aigouy, B. et al. Cell flow reorients the axis of planar polarity in the wing epithelium of Drosophila. Cell 142, 773–786 (2010).

    Article  CAS  PubMed  Google Scholar 

  24. Paredez, A. R., Somerville, C. R. & Ehrhardt, D. W. Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312, 1491–1495 (2006).

    Article  CAS  PubMed  Google Scholar 

  25. Ambrose, C., Allard, J. F., Cytrynbaum, E. N. & Wasteneys, G. O. A CLASP-modulated cell edge barrier mechanism drives cell-wide cortical microtubule organization in Arabidopsis. Nat. Commun. 2, 430 (2011).

    Article  PubMed  Google Scholar 

  26. Kirchhelle, C., Garcia-Gonzalez, D., Irani, N. G., Jérusalem, A. & Moore, I. Two mechanisms regulate directional cell growth in Arabidopsis lateral roots. eLife 8, e47988 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Ambrose, C. & Wasteneys, G. O. Cell edges accumulate gamma tubulin complex components and nucleate microtubules following cytokinesis in Arabidopsis thaliana. PLoS ONE 6, e27423 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Fu, Y., Xu, T., Zhu, L., Wen, M. & Yang, Z. A ROP GTPase signaling pathway controls cortical microtubule ordering and cell expansion in Arabidopsis. Curr. Biol. 19, 1827–1832 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Hamant, O. & Traas, J. The mechanics behind plant development. N. Phytol. 185, 369–385 (2010).

    Article  Google Scholar 

  30. Fuller, B. Tensegrity. Portf. Art News Annu. 4, 112–127 (1961).

    Google Scholar 

  31. Stamenović, D. & Ingber, D. E. Tensegrity-guided self assembly: from molecules to living cells. Soft Matter 5, 1137–1145 (2009).

    Article  Google Scholar 

  32. Ingber, D. E. Tensegrity-based mechanosensing from macro to micro. Prog. Biophys. Mol. Biol. 97, 163–179 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  33. Hernández-Hernández, V., Rueda, D., Caballero, L., Alvarez-Buylla, E. R. & Benítez, M. Mechanical forces as information: an integrated approach to plant and animal development. Front. Plant Sci. 5, 265 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  34. Kutschera, U., Bergfeld, R. & Schopfer, P. Cooperation of epidermis and inner tissues in auxin-mediated growth of maize coleoptiles. Planta 170, 168–180 (1987).

    Article  CAS  PubMed  Google Scholar 

  35. Hernández-Hernández, V., Benítez, M. & Boudaoud, A. Interplay between turgor pressure and plasmodesmata during plant development. J. Exp. Bot. 71, 768–777 (2020).

    PubMed  Google Scholar 

  36. Kutschera, U. Tissue stresses in growing plant organs. Physiol. Plant. 77, 157–163 (1989).

    Article  Google Scholar 

  37. Williamson, R. E. Alignment of cortical microtubules by anisotropic wall stresses. Funct. Plant Biol. 17, 601–613 (1990).

    Article  Google Scholar 

  38. Peaucelle, A., Wightman, R. & Höfte, H. The control of growth symmetry breaking in the Arabidopsis hypocotyl. Curr. Biol. 25, 1746–1752 (2015).

    Article  CAS  PubMed  Google Scholar 

  39. Denninger, P. et al. Distinct RopGEFs successively drive polarization and outgrowth of root hairs. Curr. Biol. 29, 1854–1865.e1855 (2019).

    Article  CAS  PubMed  Google Scholar 

  40. Michniewicz, M., Brewer, P. B. & Friml, J. Polar auxin transport and asymmetric auxin distribution. Arabidopsis Book 5, e0108 (2007).

    PubMed  PubMed Central  Google Scholar 

  41. Scacchi, E. et al. Dynamic, auxin-responsive plasma membrane-to-nucleus movement of Arabidopsis BRX. Development 136, 2059–2067 (2009).

    Article  CAS  PubMed  Google Scholar 

  42. Truernit, E., Bauby, H., Belcram, K., Barthélémy, J. & Palauqui, J.-C. OCTOPUS, a polarly localised membrane-associated protein, regulates phloem differentiation entry in Arabidopsis thaliana. Development 139, 1306–1315 (2012).

    Article  CAS  PubMed  Google Scholar 

  43. Miwa, K. et al. Plants tolerant of high boron levels. Science 318, 1417 (2007).

    Article  CAS  PubMed  Google Scholar 

  44. Takano, J. et al. Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. Proc. Natl Acad. Sci. USA 107, 200910744 (2010).

    Article  Google Scholar 

  45. Campos, R., Goff, J., Rodriguez-Furlan, C. & Van Norman, J. M. The Arabidopsis receptor kinase IRK is polarized and represses specific cell divisions in roots. Dev. Cell 52, 183–195.e184 (2020).

    Article  CAS  PubMed  Google Scholar 

  46. Le, P. Y. & Ambrose, C. CLASP promotes stable tethering of endoplasmic microtubules to the cell cortex to maintain cytoplasmic stability in Arabidopsis meristematic cells. PLoS ONE 13, e0198521 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  48. Kusumi, A. et al. Dynamic organizing principles of the plasma membrane that regulate signal transduction: commemorating the fortieth anniversary of Singer and Nicolson’s fluid-mosaic model. Annu. Rev. Cell Dev. Biol. 28, 215–250 (2012).

    Article  CAS  PubMed  Google Scholar 

  49. Malinsky, J., Opekarová, M., Grossmann, G. & Tanner, W. Membrane microdomains, rafts, and detergent-resistant membranes in plants and fungi. Annu. Rev. Plant Biol. 64, 501–529 (2013).

    Article  CAS  PubMed  Google Scholar 

  50. Boutté, Y. & Grebe, M. Cellular processes relying on sterol function in plants. Curr. Opin. Plant Biol. 12, 705–713 (2009).

    Article  PubMed  Google Scholar 

  51. Levental, I., Grzybek, M. & Simons, K. Greasing their way: lipid modifications determine protein association with membrane rafts. Biochemistry 49, 6305–6316 (2010).

    Article  CAS  PubMed  Google Scholar 

  52. Levental, I., Lingwood, D., Grzybek, M., Coskun, Ü. & Simons, K. Palmitoylation regulates raft affinity for the majority of integral raft proteins. Proc. Natl Acad. Sci. USA 107, 22050–22054 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Van Den Bogaart, G. et al. Membrane protein sequestering by ionic protein–lipid interactions. Nature 479, 552–555 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  54. Lingwood, D. & Simons, K. Lipid rafts as a membrane-organizing principle. Science 327, 46–50 (2010).

    Article  CAS  PubMed  Google Scholar 

  55. Daněk, M., Valentová, O. & Martinec, J. Flotillins, erlins, and HIRs: from animal base camp to plant new horizons. Crit. Rev. Plant Sci. 35, 191–214 (2016).

    Article  Google Scholar 

  56. Raffaele, S., Mongrand, S., Gamas, P., Niebel, A. & Ott, T. Genome-wide annotation of remorins, a plant-specific protein family: evolutionary and functional perspectives. Plant Physiol. 145, 593–600 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Jarsch, I. K. et al. Plasma membranes are subcompartmentalized into a plethora of coexisting and diverse microdomains in Arabidopsis and Nicotiana benthamiana. Plant Cell 26, 1698–1711 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Demir, F. et al. Arabidopsis nanodomain-delimited ABA signaling pathway regulates the anion channel SLAH3. Proc. Natl Acad. Sci. USA 110, 8296–8301 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Bücherl, C. A. et al. Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains. eLife 6, e25114 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  60. Martiniere, A. et al. Osmotic stress activates two reactive oxygen species pathways with distinct effects on protein nanodomains and diffusion. Plant Physiol. 179, 1581–1593 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Platre, M. P. et al. Developmental control of plant Rho GTPase nano-organization by the lipid phosphatidylserine. Science 364, 57–62 (2019).

    Article  CAS  PubMed  Google Scholar 

  62. Jaillais, Y. & Ott, T. The nanoscale organization of the plasma membrane and its importance in signaling: a proteolipid perspective. Plant Physiol. 182, 1682–1696 (2020).

    Article  CAS  PubMed  Google Scholar 

  63. Groves, J. T. & Kuriyan, J. Molecular mechanisms in signal transduction at the membrane. Nat. Struct. Mol. Biol. 17, 659–665 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Sadegh, S., Higgins, J. L., Mannion, P. C., Tamkun, M. M. & Krapf, D. Plasma membrane is compartmentalized by a self-similar cortical actin meshwork. Phys. Rev. 7, 011031 (2017).

    Article  Google Scholar 

  65. Szymanski, W. G. et al. Cytoskeletal components define protein location to membrane microdomains. Mol. Cell. Proteom. 14, 2493–2509 (2015).

    Article  CAS  Google Scholar 

  66. Liang, P. et al. Symbiotic root infections in Medicago truncatula require remorin-mediated receptor stabilization in membrane nanodomains. Proc. Natl Acad. Sci. USA 115, 5289–5294 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Yanagisawa, M., Alonso, J. M. & Szymanski, D. B. Microtubule-dependent confinement of a cell signaling and actin polymerization control module regulates polarized cell growth. Curr. Biol. 28, 2459–2466.e2454 (2018).

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  69. McKenna, J. F. et al. The cell wall regulates dynamics and size of plasma-membrane nanodomains in Arabidopsis. Proc. Natl Acad. Sci. USA 116, 12857–12862 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Daněk, M. et al. Cell wall contributes to the stability of plasma membrane nanodomain organization of Arabidopsis thaliana FLOTILLIN2 and HYPERSENSITIVE INDUCED REACTION1 proteins. Plant J. 101, 619–636 (2020).

    Article  PubMed  Google Scholar 

  71. Pan, X. et al. Auxin-induced signaling protein nanoclustering contributes to cell polarity formation. Nat. Commun. 11, 3914 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Sampathkumar, A. Mechanical feedback-loop regulation of morphogenesis in plants. Development 147, dev177964 (2020).

    Article  CAS  PubMed  Google Scholar 

  73. Hamant, O. & Haswell, E. S. Life behind the wall: sensing mechanical cues in plants. BMC Biol. 15, 59 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  74. Paradez, A., Wright, A. & Ehrhardt, D. W. Microtubule cortical array organization and plant cell morphogenesis. Curr. Opin. Plant Biol. 9, 571–578 (2006).

    Article  CAS  PubMed  Google Scholar 

  75. Hamant, O., Inoue, D., Bouchez, D., Dumais, J. & Mjolsness, E. Are microtubules tension sensors? Nat. Commun. 10, 2360 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  76. Buschmann, H. & Lloyd, C. W. Arabidopsis mutants and the network of microtubule-associated functions. Mol. Plant 1, 888–898 (2008).

    Article  CAS  PubMed  Google Scholar 

  77. Mirabet, V. et al. The self-organization of plant microtubules inside the cell volume yields their cortical localization, stable alignment, and sensitivity to external cues. PLoS Comput. Biol. 14, e1006011 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  78. Durand-Smet, P., Spelman, T. A., Meyerowitz, E. M. & Jönsson, H. Cytoskeletal organization in isolated plant cells under geometry control. Proc. Natl Acad. Sci. USA 117, 17399–17408 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Li, S., Lei, L., Somerville, C. R. & Gu, Y. Cellulose synthase interactive protein 1 (CSI1) links microtubules and cellulose synthase complexes. Proc. Natl Acad. Sci. USA 109, 185–190 (2012).

    Article  CAS  PubMed  Google Scholar 

  80. Bringmann, M. et al. POM-POM2/cellulose synthase interacting1 is essential for the functional association of cellulose synthase and microtubules in Arabidopsis. Plant Cell 24, 163–177 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Gardiner, J. C. et al. A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane. Plant Cell 13, 2143–2158 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Oda, Y. Emerging roles of cortical microtubule–membrane interactions. J. Plant Res. 131, 5–14 (2018).

    Article  CAS  PubMed  Google Scholar 

  83. Nakamura, M., Ehrhardt, D. W. & Hashimoto, T. Microtubule and katanin-dependent dynamics of microtubule nucleation complexes in the acentrosomal Arabidopsis cortical array. Nat. Cell Biol. 12, 1064–1070 (2010).

    Article  CAS  PubMed  Google Scholar 

  84. Heisler, M., Hamant, O., Krupinski, P., Uyttewaal, M. & Ohno, C. Alignment between PIN1 polarity and microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport. PLoS Biol. 8, e1000516 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  85. Eren, E. C., Dixit, R. & Gautam, N. A three-dimensional computer simulation model reveals the mechanisms for self-organization of plant cortical microtubules into oblique arrays. Mol. Biol. Cell 21, 2674–2684 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Ambrose, J. C., Shoji, T., Kotzer, A. M., Pighin, J. A. & Wasteneys, G. O. The Arabidopsis CLASP gene encodes a microtubule-associated protein involved in cell expansion and division. Plant Cell 19, 2763–2775 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Verger, S., Long, Y., Boudaoud, A. & Hamant, O. A tension–adhesion feedback loop in plant epidermis. eLife 7, e34460 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  88. Routier-Kierzkowska, A.-L. et al. Cellular force microscopy for in vivo measurements of plant tissue mechanics. Plant Physiol. 158, 1514–1522 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Chan, J. Microtubule and cellulose microfibril orientation during plant cell and organ growth. J. Microsc. 247, 23–32 (2012).

    Article  CAS  PubMed  Google Scholar 

  90. Crowell, E. F. et al. Differential regulation of cellulose orientation at the inner and outer face of epidermal cells in the Arabidopsis hypocotyl. Plant Cell 23, 2592–2605 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Robinson, S. & Kuhlemeier, C. Global compression reorients cortical microtubules in Arabidopsis hypocotyl epidermis and promotes growth. Curr. Biol. 28, 1794–1802.e1792 (2018).

    Article  CAS  PubMed  Google Scholar 

  92. Geitmann, A., Hush, J. & Overall, R. Inhibition of ethylene biosynthesis does not block microtubule re-orientation in wounded pea roots. Protoplasma 198, 135–142 (1997).

    Article  CAS  Google Scholar 

  93. Hejnowicz, Z., Rusin, A. & Rusin, T. Tensile tissue stress affects the orientation of cortical microtubules in the epidermis of sunflower hypocotyl. J. Plant Growth Regul. 19, 31–44 (2000).

    Article  CAS  PubMed  Google Scholar 

  94. Jacques, E., Verbelen, J.-P. & Vissenberg, K. Mechanical stress in Arabidopsis leaves orients microtubules in a ‘continuous’ supracellular pattern. BMC Plant Biol. 13, 163 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  95. Colin, L. et al. Cortical tension overrides geometrical cues to orient microtubules in confined protoplasts. Proc. Natl Acad. Sci. USA 117, 32731–32738 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Yu, M. et al. mDia1 senses both force and torque during F-actin filament polymerization. Nat. Commun. 8, 1650 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  97. Risca, V. I. et al. Actin filament curvature biases branching direction. Proc. Natl Acad. Sci. USA 109, 2913–2918 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Chugh, P. et al. Actin cortex architecture regulates cell surface tension. Nat. Cell Biol. 19, 689–697 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Simon, C., Caorsi, V., Campillo, C. & Sykes, C. Interplay between membrane tension and the actin cytoskeleton determines shape changes. Phys. Biol. 15, 065004 (2018).

    Article  PubMed  Google Scholar 

  100. Zhang, L., Xing, J. & Lin, J. At the intersection of exocytosis and endocytosis in plants. N. Phytol. 224, 1479–1489 (2019).

    Article  CAS  Google Scholar 

  101. Houk, A. R. et al. Membrane tension maintains cell polarity by confining signals to the leading edge during neutrophil migration. Cell 148, 175–188 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Thottacherry, J. J. et al. Mechanochemical feedback control of dynamin independent endocytosis modulates membrane tension in adherent cells. Nat. Commun. 9, 4217 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  103. Wen, P. J. et al. Actin dynamics provides membrane tension to merge fusing vesicles into the plasma membrane. Nat. Commun. 7, 12604 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Stewart, M. P. et al. Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding. Nature 469, 226–230 (2011).

    Article  CAS  PubMed  Google Scholar 

  105. Basu, R. et al. Cytotoxic T cells use mechanical force to potentiate target cell killing. Cell 165, 100–110 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Ranade, S. S., Syeda, R. & Patapoutian, A. Mechanically activated ion channels. Neuron 87, 1162–1179 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Singer, S. J. & Nicolson, G. L. The fluid mosaic model of the structure of cell membranes. Science 175, 720–731 (1972).

    Article  CAS  PubMed  Google Scholar 

  108. Diz-Muñoz, A., Fletcher, D. A. & Weiner, O. D. Use the force: membrane tension as an organizer of cell shape and motility. Trends Cell Biol. 23, 47–53 (2013).

    Article  PubMed  Google Scholar 

  109. Shi, Z. & Baumgart, T. Membrane tension and peripheral protein density mediate membrane shape transitions. Nat. Commun. 6, 5974 (2015).

    Article  CAS  PubMed  Google Scholar 

  110. Kusumi, A. et al. Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. Annu. Rev. Biophys. Biomol. Struct. 34, 351–378 (2005).

    Article  CAS  PubMed  Google Scholar 

  111. Fogelson, B. & Mogilner, A. Computational estimates of membrane flow and tension gradient in motile cells. PLoS ONE 9, e84524 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  112. Lieber, A. D., Schweitzer, Y., Kozlov, M. M. & Keren, K. Front-to-rear membrane tension gradient in rapidly moving cells. Biophys. J. 108, 1599–1603 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Schweitzer, Y., Lieber, A. D., Keren, K. & Kozlov, M. M. Theoretical analysis of membrane tension in moving cells. Biophys. J. 106, 84–92 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Shi, Z., Graber, Z. T., Baumgart, T., Stone, H. A. & Cohen, A. E. Cell membranes resist flow. Cell 175, 1769–1779.e1713 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. García-Sáez, A. J., Chiantia, S. & Schwille, P. Effect of line tension on the lateral organization of lipid membranes. J. Biol. Chem. 282, 33537–33544 (2007).

    Article  PubMed  Google Scholar 

  116. Oglęcka, K., Rangamani, P., Liedberg, B., Kraut, R. S. & Parikh, A. N. Oscillatory phase separation in giant lipid vesicles induced by transmembrane osmotic differentials. eLife 3, e03695 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  117. Ho, J. C., Rangamani, P., Liedberg, B. & Parikh, A. N. Mixing water, transducing energy, and shaping membranes: autonomously self-regulating giant vesicles. Langmuir 32, 2151–2163 (2016).

    Article  CAS  PubMed  Google Scholar 

  118. Oglecka, K., Sanborn, J., Parikh, A. N. & Kraut, R. S. Osmotic gradients induce bio-reminiscent morphological transformations in giant unilamellar vesicles. Front. Physiol. 3, 120 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Colom, A. et al. A fluorescent membrane tension probe. Nat. Chem. 1, 1118–1125 (2018).

    Article  Google Scholar 

  120. Riggi, M. et al. Decrease in plasma membrane tension triggers PtdIns (4, 5) P 2 phase separation to inactivate TORC2. Nat. Cell Biol. 20, 1043–1051 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Michels, L. et al. Complete microviscosity maps of living plants cells and tissues with a toolbox of targeting mechanoprobes. Proc. Natl Acad. Sci. USA 117, 18110–18118 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Homann, U. Fusion and fission of plasma-membrane material accommodates for osmotically induced changes in the surface area of guard-cell protoplasts. Planta 206, 329–333 (1998).

    Article  CAS  Google Scholar 

  123. Fricke, W., Jarvis, M. C. & Brett, C. T. Turgor pressure, membrane tension and the control of exocytosis in higher plants. Plant Cell Environ. 23, 999–1003 (2000).

    Article  Google Scholar 

  124. Wolfe, J. & Steponkus, P. L. Mechanical properties of the plasma membrane of isolated plant protoplasts: mechanism of hyperosmotic and extracellular freezing injury. Plant Physiol. 71, 276–285 (1983).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Apodaca, G. Modulation of membrane traffic by mechanical stimuli. Am. J. Physiol. Renal Physiol. 282, F179–F190 (2002).

    Article  PubMed  Google Scholar 

  126. Asnacios, A. & Hamant, O. The mechanics behind cell polarity. Trends Cell Biol. 22, 584–591 (2012).

    Article  CAS  PubMed  Google Scholar 

  127. Sorre, B. et al. Curvature-driven lipid sorting needs proximity to a demixing point and is aided by proteins. Proc. Natl Acad. Sci. USA 106, 5622–5626 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Subramaniam, A. B., Lecuyer, S., Ramamurthi, K. S., Losick, R. & Stone, H. A. Particle/fluid interface replication as a means of producing topographically patterned polydimethylsiloxane surfaces for deposition of lipid bilayers. Adv. Mater. 22, 2142–2147 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Feriani, L., Cristofolini, L. & Cicuta, P. Soft pinning of liquid domains on topographical hemispherical caps. Chem. Phys. Lipids 185, 78–87 (2015).

    Article  CAS  PubMed  Google Scholar 

  130. Rinaldin, M., Fonda, P., Giomi, L. & Kraft, D. J. Geometric pinning and antimixing in scaffolded lipid vesicles. Nat. Commun. 11, 4314 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Ren, C. et al. Leukocyte cytoskeleton polarization is initiated by plasma membrane curvature from cell attachment. Dev. Cell 49, 206–219.e207 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Chan, J., Mansfield, C., Clouet, F., Dorussen, D. & Coen, E. Intrinsic cell polarity coupled to growth axis formation in tobacco BY-2 cells. Curr. Biol. 30, 4999–5006 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Zhao, H. et al. Membrane-sculpting BAR domains generate stable lipid microdomains. Cell Rep. 4, 1213–1223 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Simunovic, M. et al. Friction mediates scission of tubular membranes scaffolded by BAR proteins. Cell 170, 172–184.e111 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Altartouri, B. et al. Pectin chemistry and cellulose crystallinity govern pavement cell morphogenesis in a multi-step mechanism. Plant Physiol. 181, 127–141 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Bidhendi, A. J., Altartouri, B., Gosselin, F. P. & Geitmann, A. Mechanical stress initiates and sustains the morphogenesis of wavy leaf epidermal cells. Cell Rep. 28, 1237–1250.e1236 (2019).

    Article  CAS  PubMed  Google Scholar 

  137. Sassi, M. et al. An auxin-mediated shift toward growth isotropy promotes organ formation at the shoot meristem in Arabidopsis. Curr. Biol. 24, 2335–2342 (2014).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Work on cell polarity in D.W.’s lab is supported by an Advanced Grant from the European Research Council (ERC; ‘DIRNDL’, contract number 833867) and seed funding from the inter-university alliance Utrecht/Eindhoven/Wageningen. The work of J.S. is part of the CATCH project funded by the European Research Council (ERC Consolidator Grant).

Author information

Authors and Affiliations

Authors

Contributions

V.G., J.S. and D.W. conceptualized the project. V.G. designed the artwork. J.S. and D.W. acquired the funding. D.W. supervised the project. V.G. wrote the original draft. J.S. and D.W. reviewed and edited the manuscript.

Corresponding author

Correspondence to Dolf Weijers.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Plants thanks Andrew Muroyama, Dominique Bergmann and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gorelova, V., Sprakel, J. & Weijers, D. Plant cell polarity as the nexus of tissue mechanics and morphogenesis. Nat. Plants 7, 1548–1559 (2021). https://doi.org/10.1038/s41477-021-01021-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-021-01021-w

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing