Feedback from the wall
Introduction
The cell walls of higher plants provide mechanical strength, define cell shape and thus overall plant morphology, and protect against pathogen attack. The complex polysaccharide structure of wall must therefore combine strength with the plasticity that is required for cell expansion and plant growth. In addition to controlling the mechanical aspects of plant development, the cell wall must also posses inherent signalling properties. These properties are essential not only for the role of the cell wall in defence but also for the co-ordination of wall synthesis and expansion between adjacent cells, and thus the development of entire plant organs. Pien et al. [1•] have already shown that the role of the cell wall in plant morphogenesis stretches far beyond supplying the physical constraints that control the direction of cell expansion. Local increases in the expression of expansin, a cell wall protein that facilitates growth by promoting wall loosening (see [2]), are sufficient to trigger the formation of an entire leaf, indicating that local changes in cell wall extensibility within the meristem set in motion the entire cascade of leaf development. Several recent studies have provided evidence that changes in wall composition can also be perceived by the cell, activate feedback-signalling networks, and thus provide a sensing mechanism through which growth responses can be co-ordinated or altered appropriately.
Section snippets
A role for the cell wall in signalling?
The recent characterisation of several cell wall mutants has revealed a causal link between cell wall synthesis and structure and the jasmonate (JA) and ethylene signalling pathways. These mutants, eli1 (ectopic lignification1) and cev1 (constitutive expression of VEGETATIVE STORAGE PROTEINS1 [VSP1]), were originally isolated from screens for ectopic lignin production and defence responses 3., 4.. Recently, further characterisation has revealed that the mutations responsible for these
Miniaturised analytical techniques for studying cell walls
Little is known about the cellular machinery that underlies cell wall synthesis and deposition. Mutants have been very instructive in elucidating the molecular machinery underlying these processes, but the analysis of cell wall changes remains a major bottleneck. Recently, major advances have been achieved in the miniaturisation of techniques for the analysis of polysaccharides and in the adaptation of micro-spectroscopic techniques to interpret complex mixtures of polymers found in the cell
Conclusions
The discovery that the plant cell wall appears to constitute an integral component of multiple signalling pathways suggests that the cell wall properties of plants, like those of yeast, are constantly sensed to co-ordinate growth and defence responses. Virtually nothing is known about how changes in cell wall properties are perceived and how these signals are transduced. Feedback signalling may well involve stress sensors akin to WSC1 and MID2, which have been identified in yeast. Vital
Note added in proof
Recently, further characterisation of the pmr4 mutant has suggested that callose, which is normally deposited at wound sites following pathogen invasion, may also be involved in feedback signalling from the wall. Surprisingly, Nishimura et al. [47••] showed that pmr4 mutants display increased resistance to pathogen attack, despite their lack of the callose synthase gene that is responsible for the production of callose in response to biotic and abiotic stress. The analysis of double mutants and
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
- •
of special interest
- ••
of outstanding interest
Acknowledgements
Thanks to Marie-Theres Hauser and M Pauly for contributing information before publication, Grégory Mouille for interesting discussions concerning this publication and Stéphane Mesnage for critical reading of the manuscript. The work in the authors’ laboratory related to this review was funded in part by Action concertée Incitative 2000 (grant 47), the EEC framework 5 projects GEMINI and EUROPECTIN, and GENOPLANTE grants (1999025 and 2001035).
References (47)
- et al.
Coordination of the mating and cell integrity mitogen-activated protein kinase pathways in Saccharomyces cerevisiae
Mol. Cell Biol.
(1997) - et al.
Mid2 is a putative sensor for cell integrity signaling in Saccharomyces cerevisiae
Mol. Cell Biol.
(1999) - et al.
A comparison of oligogalacturonide- and auxin-induced extracellular alkalinization and growth responses in roots of intact cucumber seedlings
Plant Physiol.
(2002) - et al.
The Arabidopsis SOS5 locus encodes a putative cell surface adhesion protein and is required for normal cell expansion
Plant Cell
(2003) - et al.
Local expression of expansin induces the entire process of leaf development and modifies leaf shape
Proc. Natl Acad. Sci. USA
(2001) Loosening of plant cell walls by expansins
Nature
(2000)- et al.
The eli1 mutation reveals a link between cell expansion and secondary cell wall formation in Arabidopsis thaliana
Development
(2000) - et al.
The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens
Plant Cell
(2001) - et al.
Reduced cellulose synthesis invokes lignification and defense responses in Arabidopsis thaliana
Plant J.
(2003) - et al.
The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses
Plant Cell
(2002)
The Arabidopsis det3 mutant reveals a central role for the vacuolar H+-ATPase in plant growth and development
Genes Dev.
Two cinnamoyl-CoA reductase (CCR) genes from Arabidopsis thaliana are differentially expressed during development and in response to infection with pathogenic bacteria
Phytochemistry
The protein kinase C-activated MAP kinase pathway of Saccharomyces cerevisiae mediates a novel aspect of the heat shock response
Genes Dev.
A second osmosensing signal transduction pathway in yeast. Hypotonic shock activates the PKC1 protein kinase-regulated cell integrity pathway
J. Biol. Chem.
Characterization of the Wsc1 protein, a putative receptor in the stress response of Saccharomyces cerevisiae
Genetics
Wsc1 and Mid2 are cell surface sensors for cell wall integrity signaling that act through Rom2, a guanine nucleotide exchange factor for Rho1
Mol. Cell Biol.
Rho1p, a yeast protein at the interface between cell polarization and morphogenesis
Science
Identification of yeast Rho1p GTPase as a regulatory subunit of 1,3-beta-glucan synthase
Science
Cell wall stress depolarizes cell growth via hyperactivation of RHO1
J. Cell Biol.
Wall-associated kinases are expressed throughout plant development and are required for cell expansion
Plant Cell
Requirement for the induced expression of a cell wall associated receptor kinase for survival during the pathogen response
Plant J.
Antisense expression of a cell wall-associated protein kinase, WAK4, inhibits cell elongation and alters morphology
Plant Cell
Pectins: structure, biosynthesis, and oligogalacturonide-related signaling
Phytochemistry
Cited by (88)
4-Nitrophenol at environmentally relevant concentrations mediates reproductive toxicity in Caenorhabditis elegans via metabolic disorders-induced estrogen signaling pathway
2025, Journal of Environmental Sciences (China)Jasmonate signaling and remodeling of cell wall metabolism induced by boron deficiency in pea shoots
2022, Environmental and Experimental BotanyCitation Excerpt :Upregulation of transcripts coding for GTs, PGs, pectate lyases, PMAs, EXTs, EXPs and XTHs is observed in the present study (Fig. 4), which suggests that B deficiency may affect cell wall biosynthesis by regulating gene expression levels and related enzyme activity. Deficiency of B apparently compromises cell wall structure and function, triggering a series of compensatory mechanisms to respond to B deficiency through biosynthesis and modification of the cell wall (Pilling and Höfte, 2003). As an example, we can consider the XTH family including both xyloglucan endotransglucosylase (XET) and xyloglucan endohydrolase (XEH) enzymes, both of which have distinct effects on cell wall structure (Eklöf and Brumer, 2010).
Sensing environmental and developmental signals via cellooligomers
2018, Journal of Plant PhysiologyCitation Excerpt :These studies demonstrate that COM perception represents a novel surveillance system, preferentially active in roots, that synergistically operates with other stimuli (such as flg22, oligogalacturonides or chitooligomers) to inform the cell about the integrity of the cell wall (Souza et al., 2017; Johnson et al., 2018). Signaling systems informing the cell or the entire plant body about the integrity and state of the cell wall and events occuring in the apoplast have been often described (Pilling and Höfte, 2003; Vorwerk et al., 2004; Hématy et al., 2007, 2009; Cheung and Wu, 2011; Denness et al., 2011; Ramírez et al., 2011; Trouvelot et al., 2014; Bolouri Moghaddam and Van den Ende, 2012; Wolf et al., 2012). COMs as breakdown products of cell wall material or released by microbes might play a crucial role as apoplastic signals.
Computational study of FaEXPA1, a strawberry alpha expansin protein, through molecular modeling and molecular dynamics simulation studies
2018, Computational Biology and ChemistryCitation Excerpt :Plant cell walls are a complex and dynamic supra-molecular assembly composed of crystalline cellulose microfibrils surrounded by an amorphous matrix of polysaccharides such as hemicellulose and pectins as well as inorganic molecules and proteins (Chundawat et al., 2011; Johansson et al., 2004; Vaaje-Kolstad et al., 2010). The plant cell wall regulates growth and development, mechanical support, and cell shape and acts as a barrier against biotic and abiotic stresses (Pilling and Höfte, 2003; Nardi et al., 2015), and changes in cell wall architecture have been well described (Marga et al., 2005). Regarding plant cell wall metabolism, disassembly is the main process that leads to fruit softening during ripening and postharvest (Vicente et al., 2007).
Regulation of cell wall remodeling in grapevine (Vitis vinifera L.) callus under individual mineral stress deficiency
2016, Journal of Plant Physiology