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.
This is a preview of subscription content, access via your institution
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Rent or buy this article
Prices vary by article type
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
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).
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).
Wolf, S. Plant cell wall signaling and receptor-like kinases. Biochem. J. 474, 471–492 (2017).
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).
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).
Höfte, H. & Voxeur, A. Plant cell walls. Curr. Biol. 27, R865–R870 (2017).
Watanabe, Y. et al. Cellulose synthase complexes display distinct dynamic behaviors during xylem transdifferentiation. Proc. Natl Acad. Sci. USA 115, E6366–E6374 (2018).
Sánchez-Rodríguez, C. et al. The cellulose synthases are cargo of the TPLATE adaptor complex. Mol. Plant 11, 346–349 (2018).
Paredez, A. R. Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312, 1491–1495 (2006).
Liu, Z. et al. Cellulose-microtubule uncoupling proteins prevent lateral displacement of microtubules during cellulose synthesis in Arabidopsis. Dev. Cell 38, 305–315 (2016).
Endler, A. et al. A Mechanism for sustained cellulose synthesis during salt stress. Cell 162, 1353–1364 (2015).
Schneider, R. et al. Two complementary mechanisms underpin cell wall patterning during xylem vessel development. Plant Cell 29, 2433–2449 (2017).
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).
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).
Bischoff, V. et al. Phytochrome regulation of cellulose synthesis in Arabidopsis. Curr. Biol. 21, 1822–1827 (2011).
Hu, Z. et al. Mitochondrial defects confer tolerance against cellulose deficiency. Plant Cell 28, 2276–2290 (2016).
Takenaka, Y. et al. Pectin RG-I rhamnosyltransferases represent a novel plant-specific glycosyltransferase family. Nat. Plants 4, 669–676 (2018).
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).
Hocq, L., Pelloux, J. & Lefebvre, V. Connecting homogalacturonan-type pectin remodeling to acid growth. Trends Plant Sci. 22, 20–29 (2017).
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).
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).
Francoz, E. et al. Pectin Demethylesterification generates platforms that anchor peroxidases to remodel plant cell wall domains. Dev. Cell 48, 261–276 (2019).
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).
Denoux, C. et al. Activation of defense response pathways by OGs and Flg22 elicitors in Arabidopsis seedlings. Mol. Plant 1, 423–445 (2008).
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).
Anderson, C. M. et al. WAKs: cell wall-associated kinases linking the cytoplasm to the extracellular matrix. Plant Mol. Biol. 47, 197–206 (2001).
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).
Feng, W. et al. The FERONIA Receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. Curr. Biol. 28, 666–675 (2018).
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).
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).
Lee, Y., Rubio, M. C., Alassimone, J. & Geldner, N. A mechanism for localized lignin deposition in the endodermis. Cell 153, 402–412 (2013).
Roppolo, D. et al. A novel protein family mediates Casparian strip formation in the endodermis. Nature 473, 380–383 (2011).
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).
Liu, Q., Luo, L. & Zheng, L. Lignins: biosynthesis and biological functions in plants. Int. J. Mol. Sci. 19, 335 (2018).
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).
Elsayad, K. et al. Mapping the subcellular mechanical properties of live cells in tissues with fluorescence emission-Brillouin imaging. Sci. Signal. 9, rs5 (2016).
Routier-Kierzkowska, A.-L. et al. Cellular force microscopy for in vivo measurements of plant tissue mechanics. Plant Physiol. 158, 1514–1522 (2012).
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).
Barbier de Reuille, P. et al. MorphoGraphX: a platform for quantifying morphogenesis in 4D. eLife 4, e05864 (2015).
Mravec, J. et al. Tracking developmentally regulated post-synthetic processing of homogalacturonan and chitin using reciprocal oligosaccharide probes. Development 141, 4841–4850 (2014).
Sampathkumar, A. & Wightman, R. in Plant Cell Expansion Vol. 1242 (ed. Estevez, J.) 133–141 (Springer, 2015).
Hamant, O. et al. Developmental patterning by mechanical signals in Arabidopsis. Science 322, 1650–1655 (2008).
Shi, B. & Vernoux, T. Patterning at the shoot apical meristem and phyllotaxis. Curr. Top. Dev. Biol. 131, 81–107 (2019).
Zhou, Y. et al. HAIRY MERISTEM with WUSCHEL confines CLAVATA3 expression to the outer apical meristem layers. Science 361, 502–506 (2018).
Landrein, B. et al. Mechanical stress contributes to the expression of the STM homeobox gene in Arabidopsis shoot meristems. eLife 4, e07811 (2015).
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).
Gälweiler, L. et al. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226–2230 (1998).
Li, T. et al. Calcium signals are necessary to establish auxin transporter polarity in a plant stem cell niche. Nat. Commun. 10, 726 (2019).
Xu, T. et al. Cell surface- and Rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143, 99–110 (2010).
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).
Lin, D. et al. Rho GTPase signaling activates microtubule severing to promote microtubule ordering in Arabidopsis. Curr. Biol. 23, 290–297 (2013).
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).
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).
Peaucelle, A. et al. Pectin-induced changes in cell wall mechanics underlie organ initiation in. Arab. Curr. Biol. 21, 1720–1726 (2011).
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).
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).
Toyota, M. et al. Glutamate triggers long-distance, calcium-based plant defense signaling. Science 361, 1112–1115 (2018).
Yamanaka, T. et al. MCA1 and MCA2 that mediate Ca2+ uptake have distinct and overlapping roles in Arabidopsis. Plant Physiol. 152, 1284–1296 (2010).
Yuan, F. et al. OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514, 367–371 (2014).
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).
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).
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).
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).
Stegmann, M. et al. The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. Science 355, 287–289 (2017).
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).
Gonneau, M. et al. Receptor kinase THESEUS1 is a rapid alkalinization factor 34 receptor in. Arab. Curr. Biol. 28, 2452–2458 (2018).
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).
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).
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).
Polyn, S., Willems, A. & De Veylder, L. Cell cycle entry, maintenance, and exit during plant development. Curr. Opin. Plant Biol. 23, 1–7 (2015).
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).
Shi, L., Wu, Y. & Sheen, J. TOR signaling in plants: conservation and innovation. Development 145, dev160887 (2018).
Zebell, S. G. & Dong, X. Cell-cycle regulators and cell death in immunity. Cell Host Microbe 18, 402–407 (2015).
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).
Sablowski, R. Coordination of plant cell growth and division: collective control or mutual agreement? Curr. Opin. Plant Biol. 34, 54–60 (2016).
Chen, H.-W., Persson, S., Grebe, M. & McFarlane, H. E. Cellulose synthesis during cell plate assembly. Physiol. Plant. 164, 17–26 (2018).
Moreno-Layseca, P. & Streuli, C. H. Signaling pathways linking integrins with cell cycle progression. Matrix Biol. 34, 144–153 (2014).
Alcaino, C., Farrugia, G. & Beyder, A. Mechanosensitive Piezo channels in the gastrointestinal tract. Curr. Top. Membr. 79, 219–244 (2017).
Levin, D. E. Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 189, 1145–1175 (2011).
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).
Davì, V. et al. Mechanosensation dynamically coordinates polar growth and cell wall assembly to promote cell survival. Dev. Cell 45, 170–182 (2018).
Gigli-Bisceglia, N. & Hamann, T. Outside-in control — does plant cell wall integrity regulate cell cycle progression? Physiol. Plant. 164, 82–94 (2018).
Sampathkumar, A. et al. Primary wall cellulose synthase regulates shoot apical meristem mechanics and growth. Development 146, dev179036 (2019).
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).
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).
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).
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).
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).
Nishimura, M. T. et al. Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301, 969–972 (2003).
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).
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).
Hander, T. et al. Damage on plants activates Ca 2+-dependent metacaspases for release of immunomodulatory peptides. Science 363, eaar7486 (2019).
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).
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).
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).
Li, C., Wu, H.-M. & Cheung, A. Y. FERONIA and her pals: functions and mechanisms. Plant Physiol. 171, 2379–2392 (2016).
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).
Masachis, S. et al. A fungal pathogen secretes plant alkalinizing peptides to increase infection. Nat. Microbiol. 1, 16043 (2016).
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).
Mecchia, M. A. et al. RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis. Science 358, 1600–1603 (2017).
Ringer, P., Colo, G., Fässler, R. & Grashoff, C. Sensing the mechano-chemical properties of the extracellular matrix. Matrix Biol. 64, 6–16 (2017).
Gall, H. L. et al. Cell wall metabolism in response to abiotic stress. Plants 4, 112–166 (2015).
Zhu, J. K. Abiotic stress signaling and responses in plants. Cell 167, 313–324 (2016).
Tenhaken, R. Cell wall remodeling under abiotic stress. Front. Plant Sci. 5, 771 (2014).
Haswell, E. S. & Verslues, P. E. The ongoing search for the molecular basis of plant osmosensing. J. Gen. Physiol. 145, 389–394 (2015).
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).
Kohorn, B. D. et al. An Arabidopsis cell wall-associated kinase required for invertase activity and cell growth. Plant J. 46, 307–316 (2006).
Hamant, O. & Haswell, E. S. Life behind the wall: sensing mechanical cues in plants. BMC Biol. 15, 59 (2017).
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).
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).
The authors gratefully acknowledge financial support from NTNU (to J.S.) and the Finnish Cultural Foundation (to L.V.).
The authors declare no competing interests.
Peer review information: Nature Plants thanks A. Cheung, A. Molina 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.
About this article
Cite this article
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
This article is cited by
Nature Plants (2023)
Transcriptome analysis of resistant and susceptible grapes reveals molecular mechanisms underlying resistance of white rot disease
Horticulture Advances (2023)
Journal of Plant Growth Regulation (2023)
Metabolomics targets tissue-specific responses in alleviating the negative effects of salinity in tef (Eragrostis tef) during germination
Nature Plants (2023)