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Cell wall integrity maintenance during plant development and interaction with the environment

Nature Plants volume 5, pages 924–932 (2019)Cite this article

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Abstract

Cell walls are highly dynamic structures that provide mechanical support for plant cells during growth, development and adaptation to a changing environment. Thus, it is important for plants to monitor the state of their cell walls and ensure their functional integrity at all times. This monitoring involves perception of physical forces at the cell wall–plasma membrane interphase. These forces are altered during cell division and morphogenesis, as well as in response to various abiotic and biotic stresses. Mechanisms responsible for the perception of physical stimuli involved in these processes have been difficult to separate from other regulatory mechanisms perceiving chemical signals such as hormones, peptides or cell wall fragments. However, recently developed technologies in combination with more established genetic and biochemical approaches are beginning to open up this exciting field of study. Here, we will review our current knowledge of plant cell wall integrity signalling using selected recent findings and highlight how the cell wall–plasma membrane interphase can act as a venue for sensing changes in the physical forces affecting plant development and stress responses. More importantly, we discuss how these signals may be integrated with chemical signals derived from established signalling cascades to control specific adaptive responses during exposure to biotic and abiotic stresses.

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Fig. 1: A simplified plant cell wall model depicting the main cell wall components as well as physical and chemical stimuli relevant during interactions between plants and their environment.
Fig. 2: Functions of THE1 and FER at the intersection between chemical and physical signalling during the biotic stress response.
Fig. 3: A simplified model summarizing how responses to cell wall–plasma membrane perturbations may be coordinated in a plant cell.

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References

  1. Doblin, M. S., Johnson, K. L., Humphries, J., Newbigin, E. J. & Bacic, A. T. Are designer plant cell walls a realistic aspiration or will the plasticity of the plant’s metabolism win out? Curr. Opin. Biotechnol. 26, 108–114 (2014).

    CAS  PubMed  Google Scholar 

  2. Mahon, E. L. & Mansfield, S. D. Tailor-made trees: engineering lignin for ease of processing and tomorrow’s bioeconomy. Curr. Opin. Biotechnol. 56, 147–155 (2019).

    CAS  PubMed  Google Scholar 

  3. Wolf, S. Plant cell wall signaling and receptor-like kinases. Biochem. J. 474, 471–492 (2017).

    CAS  PubMed  Google Scholar 

  4. Bacete, L., Mélida, H., Miedes, E. & Molina, A. Plant cell wall-mediated immunity: cell wall changes trigger disease resistance responses. Plant J. 93, 614–636 (2018).

    CAS  PubMed  Google Scholar 

  5. Novaković, L., Guo, T., Bacic, A., Sampathkumar, A. & Johnson, K. Hitting the wall—sensing and signaling pathways involved in plant cell wall remodeling in response to abiotic stress. Plants 7, 89 (2018).

    PubMed Central  Google Scholar 

  6. Höfte, H. & Voxeur, A. Plant cell walls. Curr. Biol. 27, R865–R870 (2017).

    PubMed  Google Scholar 

  7. Watanabe, Y. et al. Cellulose synthase complexes display distinct dynamic behaviors during xylem transdifferentiation. Proc. Natl Acad. Sci. USA 115, E6366–E6374 (2018).

    PubMed  Google Scholar 

  8. Sánchez-Rodríguez, C. et al. The cellulose synthases are cargo of the TPLATE adaptor complex. Mol. Plant 11, 346–349 (2018).

    PubMed  Google Scholar 

  9. Paredez, A. R. Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312, 1491–1495 (2006).

    CAS  PubMed  Google Scholar 

  10. Liu, Z. et al. Cellulose-microtubule uncoupling proteins prevent lateral displacement of microtubules during cellulose synthesis in Arabidopsis. Dev. Cell 38, 305–315 (2016).

    PubMed  Google Scholar 

  11. Endler, A. et al. A Mechanism for sustained cellulose synthesis during salt stress. Cell 162, 1353–1364 (2015).

    CAS  PubMed  Google Scholar 

  12. Schneider, R. et al. Two complementary mechanisms underpin cell wall patterning during xylem vessel development. Plant Cell 29, 2433–2449 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Li, S., Lei, L., Yingling, Y. G. & Gu, Y. Microtubules and cellulose biosynthesis: The emergence of new players. Curr. Opin. Plant Biol. 28, 76–82 (2015).

    CAS  PubMed  Google Scholar 

  14. Ivakov, A. A. et al. Cellulose synthesis and cell expansion are regulated by different mechanisms in growing Arabidopsis hypocotyls. Plant Cell 29, 1305–1315 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Bischoff, V. et al. Phytochrome regulation of cellulose synthesis in Arabidopsis. Curr. Biol. 21, 1822–1827 (2011).

    CAS  PubMed  Google Scholar 

  16. Hu, Z. et al. Mitochondrial defects confer tolerance against cellulose deficiency. Plant Cell 28, 2276–2290 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Takenaka, Y. et al. Pectin RG-I rhamnosyltransferases represent a novel plant-specific glycosyltransferase family. Nat. Plants 4, 669–676 (2018).

    CAS  PubMed  Google Scholar 

  18. Ebert, B. et al. The three members of the Arabidopsis glycosyltransferase family 92 are functional β-1,4-galactan synthases. Plant Cell Physiol. 59, 2624–2636 (2018).

    CAS  PubMed  Google Scholar 

  19. Hocq, L., Pelloux, J. & Lefebvre, V. Connecting homogalacturonan-type pectin remodeling to acid growth. Trends Plant Sci. 22, 20–29 (2017).

    CAS  PubMed  Google Scholar 

  20. Willats, W. G. et al. Modulation of the degree and pattern of methyl-esterification of pectic homogalacturonan in plant cell walls. Implications for pectin methyl esterase action, matrix properties, and cell adhesion. J. Biol. Chem. 276, 19404–19413 (2001).

    CAS  PubMed  Google Scholar 

  21. Willats, W. G. T., Gilmartin, P. M., Mikkelsen, J. D. & Knox, J. P. Cell wall antibodies without immunization: generation and use of de-esterified homogalacturonan block-specific antibodies from a naive phage display library. Plant J. 18, 57–65 (1999).

    CAS  PubMed  Google Scholar 

  22. Francoz, E. et al. Pectin Demethylesterification generates platforms that anchor peroxidases to remodel plant cell wall domains. Dev. Cell 48, 261–276 (2019).

    CAS  PubMed  Google Scholar 

  23. De Lorenzo, G., Ferrari, S., Giovannoni, M., Mattei, B. & Cervone, F. Cell wall traits that influence plant development, immunity and bioconversion. Plant J. 97, 134–147 (2018).

    Google Scholar 

  24. Denoux, C. et al. Activation of defense response pathways by OGs and Flg22 elicitors in Arabidopsis seedlings. Mol. Plant 1, 423–445 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Benedetti, M. et al. Plant immunity triggered by engineered in vivo release of oligogalacturonides, damage-associated molecular patterns. Proc. Natl Acad. Sci. USA 112, 5533–5538 (2015).

    CAS  PubMed  Google Scholar 

  26. Anderson, C. M. et al. WAKs: cell wall-associated kinases linking the cytoplasm to the extracellular matrix. Plant Mol. Biol. 47, 197–206 (2001).

    CAS  PubMed  Google Scholar 

  27. Kohorn, B. D., Kohorn, S. L., Saba, N. J. & Martinez, V. M. Requirement for pectin methyl esterase and preference for fragmented over native pectins for wall-associated kinase-activated, EDS1/PAD4-dependent stress response in Arabidopsis. J. Biol. Chem. 289, 18978–18986 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Feng, W. et al. The FERONIA Receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. Curr. Biol. 28, 666–675 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Lin, W., Tang, W., Anderson, C. & Yang, Z. FERONIA’s sensing of cell wall pectin activates ROP GTPase signaling in Arabidopsis. Preprint at https://doi.org/10.1101/269647 (2018).

  30. Naseer, S. et al. Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin. Proc. Natl Acad. Sci. USA 109, 10101–10106 (2012).

    CAS  PubMed  Google Scholar 

  31. Lee, Y., Rubio, M. C., Alassimone, J. & Geldner, N. A mechanism for localized lignin deposition in the endodermis. Cell 153, 402–412 (2013).

    CAS  PubMed  Google Scholar 

  32. Roppolo, D. et al. A novel protein family mediates Casparian strip formation in the endodermis. Nature 473, 380–383 (2011).

    CAS  PubMed  Google Scholar 

  33. Denness, L. et al. Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species- and jasmonic acid-dependent process in Arabidopsis. Plant Physiol. 156, 1364–1374 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Liu, Q., Luo, L. & Zheng, L. Lignins: biosynthesis and biological functions in plants. Int. J. Mol. Sci. 19, 335 (2018).

    PubMed Central  Google Scholar 

  35. Engelsdorf, T. et al. The plant cell wall integrity maintenance and immune signaling systems cooperate to control stress responses in Arabidopsis thaliana. Sci. Signal. 11, eaao3070 (2018).

    PubMed  Google Scholar 

  36. Elsayad, K. et al. Mapping the subcellular mechanical properties of live cells in tissues with fluorescence emission-Brillouin imaging. Sci. Signal. 9, rs5 (2016).

    PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Robinson, S. et al. An automated confocal micro-extensometer enables in vivo quantification of mechanical properties with cellular resolution. Plant Cell 29, 2959–2973 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Barbier de Reuille, P. et al. MorphoGraphX: a platform for quantifying morphogenesis in 4D. eLife 4, e05864 (2015).

    PubMed Central  Google Scholar 

  40. Mravec, J. et al. Tracking developmentally regulated post-synthetic processing of homogalacturonan and chitin using reciprocal oligosaccharide probes. Development 141, 4841–4850 (2014).

    CAS  PubMed  Google Scholar 

  41. Sampathkumar, A. & Wightman, R. in Plant Cell Expansion Vol. 1242 (ed. Estevez, J.) 133–141 (Springer, 2015).

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

    CAS  PubMed  Google Scholar 

  43. Shi, B. & Vernoux, T. Patterning at the shoot apical meristem and phyllotaxis. Curr. Top. Dev. Biol. 131, 81–107 (2019).

    PubMed  Google Scholar 

  44. Zhou, Y. et al. HAIRY MERISTEM with WUSCHEL confines CLAVATA3 expression to the outer apical meristem layers. Science 361, 502–506 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  46. Scofield, S., Dewitte, W., Nieuwland, J. & Murray, J. A. H. The Arabidopsis homeobox gene SHOOT MERISTEMLESS has cellular and meristem-organisational roles with differential requirements for cytokinin and CYCD3 activity. Plant J. 75, 53–66 (2013).

    CAS  PubMed  Google Scholar 

  47. Gälweiler, L. et al. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226–2230 (1998).

    PubMed  Google Scholar 

  48. Li, T. et al. Calcium signals are necessary to establish auxin transporter polarity in a plant stem cell niche. Nat. Commun. 10, 726 (2019).

    PubMed  PubMed Central  Google Scholar 

  49. Xu, T. et al. Cell surface- and Rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143, 99–110 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. 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).

    CAS  PubMed  Google Scholar 

  51. Lin, D. et al. Rho GTPase signaling activates microtubule severing to promote microtubule ordering in Arabidopsis. Curr. Biol. 23, 290–297 (2013).

    CAS  PubMed  Google Scholar 

  52. 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).

    CAS  PubMed  Google Scholar 

  53. Armezzani, A. et al. Transcriptional induction of cell wall remodelling genes is coupled to microtubule-driven growth isotropy at the shoot apex in Arabidopsis. Development 145, dev162255 (2018).

    PubMed  Google Scholar 

  54. Peaucelle, A. et al. Pectin-induced changes in cell wall mechanics underlie organ initiation in. Arab. Curr. Biol. 21, 1720–1726 (2011).

    CAS  Google Scholar 

  55. Pien, S., Wyrzykowska, J., McQueen-Mason, S., Smart, C. & Fleming, A. Local expression of expansin induces the entire process of leaf development and modifies leaf shape. Proc. Natl Acad. Sci. USA 98, 11812–11817 (2001).

    CAS  PubMed  Google Scholar 

  56. Shih, H.-W., DePew, C. L., Miller, N. D. & Monshausen, G. B. The cyclic nucleotide-gated channel CNGC14 regulates root gravitropism in Arabidopsis thaliana. Curr. Biol. 25, 3119–3125 (2015).

    CAS  PubMed  Google Scholar 

  57. Toyota, M. et al. Glutamate triggers long-distance, calcium-based plant defense signaling. Science 361, 1112–1115 (2018).

    CAS  PubMed  Google Scholar 

  58. Yamanaka, T. et al. MCA1 and MCA2 that mediate Ca2+ uptake have distinct and overlapping roles in Arabidopsis. Plant Physiol. 152, 1284–1296 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Yuan, F. et al. OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514, 367–371 (2014).

    CAS  PubMed  Google Scholar 

  60. Nakagawa, Y. et al. Arabidopsis plasma membrane protein crucial for Ca2+ influx and touch sensing in roots. Proc. Natl Acad. Sci. USA 104, 3639–3644 (2007).

    CAS  PubMed  Google Scholar 

  61. Rosa, M. et al. The Maize MID-COMPLEMENTING ACTIVITY homolog CELL NUMBER REGULATOR13/NARROW ODD DWARF coordinates organ growth and tissue patterning. Plant Cell 29, 474–490 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Hematy, K. et al. A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr. Biol. 17, 922–931 (2007).

    CAS  PubMed  Google Scholar 

  63. Franck, C. M., Westermann, J. & Boisson-Dernier, A. Plant malectin-like receptor kinases: from cell wall integrity to immunity and beyond. Annu. Rev. Plant Biol. 69, 301–328 (2018).

    CAS  PubMed  Google Scholar 

  64. Stegmann, M. et al. The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. Science 355, 287–289 (2017).

    CAS  PubMed  Google Scholar 

  65. Shih, H.-W., Miller, N. D., Dai, C., Spalding, E. P. & Monshausen, G. B. The receptor-like kinase FERONIA is required for mechanical signal transduction in Arabidopsis seedlings. Curr. Biol. 24, 1887–1892 (2014).

    CAS  PubMed  Google Scholar 

  66. Gonneau, M. et al. Receptor kinase THESEUS1 is a rapid alkalinization factor 34 receptor in. Arab. Curr. Biol. 28, 2452–2458 (2018).

    CAS  Google Scholar 

  67. Srivastava, R., Liu, J.-X., Guo, H., Yin, Y. & Howell, S. H. Regulation and processing of a plant peptide hormone, AtRALF23, in Arabidopsis. Plant J. 59, 930–939 (2009).

    CAS  PubMed  Google Scholar 

  68. Wolf, S., Rausch, T. & Greiner, S. The N-terminal pro region mediates retention of unprocessed type-I PME in the Golgi apparatus. Plant J. 58, 361–375 (2009).

    CAS  PubMed  Google Scholar 

  69. Duan, Q., Kita, D., Li, C., Cheung, A. Y. & Wu, H.-M. M. FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proc. Natl Acad. Sci. USA 107, 17821–17826 (2010).

    CAS  PubMed  Google Scholar 

  70. Polyn, S., Willems, A. & De Veylder, L. Cell cycle entry, maintenance, and exit during plant development. Curr. Opin. Plant Biol. 23, 1–7 (2015).

    CAS  PubMed  Google Scholar 

  71. Reitz, M. U., Gifford, M. L. & Schäfer, P. Hormone activities and the cell cycle machinery in immunity-triggered growth inhibition. J. Exp. Bot. 66, 2187–2197 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Shi, L., Wu, Y. & Sheen, J. TOR signaling in plants: conservation and innovation. Development 145, dev160887 (2018).

    PubMed  PubMed Central  Google Scholar 

  73. Zebell, S. G. & Dong, X. Cell-cycle regulators and cell death in immunity. Cell Host Microbe 18, 402–407 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Huot, B., Yao, J., Montgomery, B. L. & He, S. Y. Growth–defense tradeoffs in plants: a balancing act to optimize fitness. Mol. Plant 7, 1267–1287 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Sablowski, R. Coordination of plant cell growth and division: collective control or mutual agreement? Curr. Opin. Plant Biol. 34, 54–60 (2016).

    CAS  PubMed  Google Scholar 

  76. Chen, H.-W., Persson, S., Grebe, M. & McFarlane, H. E. Cellulose synthesis during cell plate assembly. Physiol. Plant. 164, 17–26 (2018).

    CAS  PubMed  Google Scholar 

  77. Moreno-Layseca, P. & Streuli, C. H. Signaling pathways linking integrins with cell cycle progression. Matrix Biol. 34, 144–153 (2014).

    CAS  PubMed  Google Scholar 

  78. Alcaino, C., Farrugia, G. & Beyder, A. Mechanosensitive Piezo channels in the gastrointestinal tract. Curr. Top. Membr. 79, 219–244 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Levin, D. E. Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 189, 1145–1175 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Kono, K., Al-Zain, A., Schroeder, L., Nakanishi, M. & Ikui, A. E. Plasma membrane/cell wall perturbation activates a novel cell cycle checkpoint during G1 in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 113, 6910–6915 (2016).

    CAS  PubMed  Google Scholar 

  81. Davì, V. et al. Mechanosensation dynamically coordinates polar growth and cell wall assembly to promote cell survival. Dev. Cell 45, 170–182 (2018).

    PubMed  Google Scholar 

  82. Gigli-Bisceglia, N. & Hamann, T. Outside-in control — does plant cell wall integrity regulate cell cycle progression? Physiol. Plant. 164, 82–94 (2018).

    CAS  PubMed  Google Scholar 

  83. Sampathkumar, A. et al. Primary wall cellulose synthase regulates shoot apical meristem mechanics and growth. Development 146, dev179036 (2019).

    CAS  PubMed  Google Scholar 

  84. Gigli-Bisceglia, N. et al. Cell wall integrity modulates Arabidopsis thaliana cell cycle gene expression in a cytokinin- and nitrate reductase-dependent manner. Development 145, dev166678 (2018).

    PubMed  Google Scholar 

  85. Dewitte, W. et al. Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proc. Natl Acad. Sci. USA 104, 14537–14542 (2007).

    CAS  PubMed  Google Scholar 

  86. Chamizo-Ampudia, A., Sanz-Luque, E., Llamas, A., Galvan, A. & Emilio, F. Nitrate reductase regulates plant nitric oxide homeostasis. Trends Plant Sci. 22, 163–174 (2017).

    CAS  PubMed  Google Scholar 

  87. Van der Does, D. et al. The Arabidopsis leucine-rich repeat receptor kinase MIK2/LRR-KISS connects cell wall integrity sensing, root growth and response to abiotic and biotic stresses. PLoS Genet. 13, e1006832 (2017).

    PubMed  PubMed Central  Google Scholar 

  88. Guo, H. et al. FERONIA receptor kinase contributes to plant immunity by suppressing jasmonic acid signaling in Arabidopsis thaliana. Curr. Biol. 28, 3316–3324 (2018).

    CAS  PubMed  Google Scholar 

  89. Nishimura, M. T. et al. Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301, 969–972 (2003).

    CAS  PubMed  Google Scholar 

  90. Claverie, J. et al. The cell wall-derived xyloglucan is a new DAMP triggering plant immunity in Vitis vinifera and Arabidopsis thaliana. Front. Plant Sci. 9, 1725 (2018).

    PubMed  PubMed Central  Google Scholar 

  91. Souza, C. & de, A. et al. Cellulose-derived oligomers act as damage-associated molecular patterns and trigger defense-like responses. Plant Physiol. 173, 2383–2398 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Hander, T. et al. Damage on plants activates Ca 2+-dependent metacaspases for release of immunomodulatory peptides. Science 363, eaar7486 (2019).

    CAS  PubMed  Google Scholar 

  93. Huffaker, A., Pearce, G. & Ryan, C. A. An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc. Natl Acad. Sci. USA 103, 10098–10103 (2006).

    CAS  PubMed  Google Scholar 

  94. Jing, Y. et al. Danger-associated peptides interact with PIN-dependent local auxin distribution to inhibit root growth in Arabidopsis. Plant Cell https://doi.org/10.1105/tpc.18.00757 (2019).

    PubMed  Google Scholar 

  95. Qu, S., Zhang, X., Song, Y., Lin, J. & Shan, X. THESEUS1 positively modulates plant defense responses against Botrytis cinerea through GUANINE EXCHANGE FACTOR4 signaling: THE1 functions in plant defense responses. J. Integr. Plant Biol. 59, 797–804 (2017).

    CAS  PubMed  Google Scholar 

  96. Li, C., Wu, H.-M. & Cheung, A. Y. FERONIA and her pals: functions and mechanisms. Plant Physiol. 171, 2379–2392 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Haruta, M., Sabat, G., Stecker, K., Minkoff, B. B. & Sussman, M. R. A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343, 408–411 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Masachis, S. et al. A fungal pathogen secretes plant alkalinizing peptides to increase infection. Nat. Microbiol. 1, 16043 (2016).

    CAS  PubMed  Google Scholar 

  99. Dünser, K. et al. Extracellular matrix sensing by FERONIA and leucine‐rich repeat extensins controls vacuolar expansion during cellular elongation in Arabidopsis thaliana. EMBO J. 38, e100353 (2019).

    PubMed  PubMed Central  Google Scholar 

  100. Mecchia, M. A. et al. RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis. Science 358, 1600–1603 (2017).

    CAS  PubMed  Google Scholar 

  101. Ringer, P., Colo, G., Fässler, R. & Grashoff, C. Sensing the mechano-chemical properties of the extracellular matrix. Matrix Biol. 64, 6–16 (2017).

    CAS  PubMed  Google Scholar 

  102. Gall, H. L. et al. Cell wall metabolism in response to abiotic stress. Plants 4, 112–166 (2015).

    PubMed  PubMed Central  Google Scholar 

  103. Zhu, J. K. Abiotic stress signaling and responses in plants. Cell 167, 313–324 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  104. Tenhaken, R. Cell wall remodeling under abiotic stress. Front. Plant Sci. 5, 771 (2014).

    PubMed  Google Scholar 

  105. Haswell, E. S. & Verslues, P. E. The ongoing search for the molecular basis of plant osmosensing. J. Gen. Physiol. 145, 389–394 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  106. Hamann, T., Bennett, M., Mansfield, J. & Somerville, C. Identification of cell-wall stress as a hexose-dependent and osmosensitive regulator of plant responses. Plant J. 57, 1015–1026 (2009).

    CAS  PubMed  Google Scholar 

  107. Kohorn, B. D. et al. An Arabidopsis cell wall-associated kinase required for invertase activity and cell growth. Plant J. 46, 307–316 (2006).

    CAS  PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  109. Yu, F. et al. FERONIA receptor kinase pathway suppresses abscisic acid signaling in Arabidopsis by activating ABI2 phosphatase. Proc. Natl Acad. Sci. USA 109, 14693–14698 (2012).

    CAS  PubMed  Google Scholar 

  110. Honkanen, S. et al. The mechanism forming the cell surface of tip-growing rooting cells is conserved among land plants. Curr. Biol. 26, 3238–3244 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors gratefully acknowledge financial support from NTNU (to J.S.) and the Finnish Cultural Foundation (to L.V.).

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  1. Department of Biology, Faculty of Natural Sciences, Norwegian University of Science and Technology, Trondheim, Norway

    Lauri Vaahtera, Julia Schulz & Thorsten Hamann

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  1. Lauri Vaahtera
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L.V., J.S. and T.H. contributed equally to the concept, outline and writing of the manuscript, including the generation of the figures.

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Vaahtera, L., Schulz, J. & Hamann, T. Cell wall integrity maintenance during plant development and interaction with the environment. Nat. Plants 5, 924–932 (2019). https://doi.org/10.1038/s41477-019-0502-0

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