• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of plntphysLink to Publisher's site
Plant Physiol. Jun 2010; 153(2): 467–478.
Published online Feb 12, 2010. doi:  10.1104/pp.110.153940
PMCID: PMC2879813
Focus Issue on Plant Cell Walls

Irritable Walls: The Plant Extracellular Matrix and Signaling1

CELL WALLS AFFECT CELL PHYSIOLOGY

The plant cell wall is a dynamic network of carbohydrates and proteins of enormous structural complexity that plays crucial roles in all aspects of plant life. Advances in molecular physiology and genetics have shed light on the relations between structure and function of various cell wall constituents. The application of compounds interfering with plant cell wall structure and biosynthesis as well as molecular genetics as a commonly used tool in plant science have generated several paradigms for the roles of various cell wall polymers in the living organism. Many mutants defective in cellulose, pectin, hemicellulose, lignin, or cell wall and cell surface proteins are available (Table I; Humphrey et al., 2007). Drugs interfering with cellulose biosynthesis, such as isoxaben (Scheible et al., 2001), thaxtomin A (Scheible et al., 2003), and 2,6-dichlorobenzonitrile (DCB; Peng et al., 2001), or β-glucosyl-Yariv dyes (βGlcY; Yariv et al., 1962) that specifically bind to arabinogalactan proteins (AGPs), are used to study the biological roles of specific cell wall polymers in wild-type plants and cell cultures. Phenotypes such as stunted growth, abnormal cellular shape, and altered tensile strength are suggestive of the cell wall's undisputed mechanical role (Willats and Knox, 1996; Fagard et al., 2000; Bouton et al., 2002; Ryden et al., 2003; Pena et al., 2004; Derbyshire et al., 2007). However, a second look at mutant physiology gives strong hints to a central regulatory network that monitors and controls cell wall performance and integrity (Somerville et al., 2004). Many mutants initially selected for altered disease or abiotic stress response or for constitutively expressing abiotic and biotic stress markers primarily affect cell wall biosynthesis (Table I; for review, see Pilling and Höfte, 2003). Other mutants reveal unexpected genetic interactions between different cell wall polymers (Bosca et al., 2006; Diet et al., 2006; Gille et al., 2009). Finally, nonadditive genetic interactions between cell wall defects and second site mutations in regulatory loci (Seifert et al., 2004; Hématy et al., 2007; Xu et al., 2008; Hamann et al., 2009) may pinpoint parts of the genetic system underlying cell wall performance and integrity control. In principle, this system detects functional and structural alterations in the extracellular matrix occurring throughout the normal life cycle of a plant and translates them into an appropriate corrective response. The alterations have to be detected by a specific sensorium that is most likely set to respond to deviations from a “correct” level. As in a multicellular plant, many types of cell walls exist and it can be expected that the control machinery including the correct level of set parameters underlie developmental control. Primary stimuli from the cell wall have to be transduced and integrated with other cues in order to bring about the due response, be it the repair of damaged structures or the modulation of mechanical properties in the cell wall itself or adaptive responses such as the production of antimicrobial metabolites or the restoration of osmotic balance. Such responses often involve a rapid modulation of already existing cellular machinery by posttranslational modifications as well as more long-term alterations of gene expression (Fig. 1). In most reviews on plant cell wall performance and integrity control, comparisons with the well-studied yeast pathway are invoked (Somerville et al., 2004; Humphrey et al., 2007; Hématy and Höfte, 2008; Hématy et al., 2009). Extrapolating from yeast (Levin, 2005), plant cells are expected to sense cell wall polymer structure as well as its mechanical performance that is closely linked to turgor pressure. Activated trans-plasma membrane sensor proteins might trigger a cascade of signal transduction events interwoven with other pathways that might modulate cellular functions by the activation or inhibition of specific transcription factors as well as by affecting posttranscriptional and posttranslational control of gene expression and protein function (Fig. 1). Hence, a symptomatic signature predicted for cell wall performance and integrity control is a drastic alteration in the expression of genes related to cell wall biosynthesis and remodeling (Fig. 1; Table I). There are no apparent plant orthologs to the proteins involved in yeast cell wall integrity control, leaving this area a painstaking but fascinating battleground for original discovery, and most present ideas on early events of “cell wall signaling” depend on interpolations and extrapolations from observations of cell wall polymer mutants and more direct mechanistic studies of other signaling paradigms (Humphrey et al., 2007; Hématy and Höfte, 2008; Hématy et al., 2009) and on the serendipitous identification of novel signaling components (Kohorn et al., 1992; Xu et al., 2008).

Table I.
Indirect physiological alterations induced in cell wall-defective mutants or after transgenic or pharmacological interference with cell wall biosynthesis or structure
Figure 1.
Components of the plant cell wall integrity and performance control system. Differentials in cell wall structure and mechanical performance are detected at the plasma membrane and translated into a compensatory response at the transcriptional and posttranslational ...

THE SIGNALS

The cell wall provides countless potential sources of information. High-Mr cell wall matrix polymers such as hemicellulose, pectin, and glycoproteins display an enormous degree of structural complexity that is amenable to modulation during its biosynthesis and by remodeling in muro. One of the key areas of investigation in plant cell wall research is to establish the relationship between the structural complexity of cell wall polymers and their biological function. Therefore, it is vital to know if stimuli regarding the structural variation of cell wall polymers are perceived by specific receptors. Alternatively, the secondary consequences, such as altered mechanical stiffness or turgor pressure, might represent crucial signals. As in yeast (Levin, 2005), both scenarios are likely to play a role (Fig. 1). The modulation of responses to cellulose biosynthesis inhibition by osmotic support indicates that turgor sensors are likely to be involved in cell wall stress signaling (Hamann et al., 2009). Historically, the typical cell wall signals are relatively low-Mr microbial degradation products such as pectin-derived oligogalacturonides (OGs; Galletti et al., 2009) and cellodextrins (Aziz et al., 2007) acting as potent elicitors of innate immunity. This class of elicitors has been termed host-associated molecular patterns (Galletti et al., 2009) or damage-associated molecular patterns (Zipfel, 2009), in analogy to pathogen-associated molecular patterns (PAMPs; for review, see Zipfel, 2009). It has been observed that cell wall carbohydrate fragments can also act as signals influencing developmental processes. Such bioactive oligosaccharides, whose activity can be quite specific, have been generally termed oligosaccharins (Albersheim et al., 1983). The biological activity of OGs depends on their degrees of polymerization, methylation, and conformation (compare with Cabrera et al., 2008), while side chain fucosylation of xyloglucan (XG)-derived oligosaccharins is important for their auxin-antagonizing effect (Fry et al., 1990). However, it is unclear at present if oligosaccharins act during normal development or if the responses such as modulation of growth regulator signaling (Fry et al., 1990; Bellincampi et al., 1996; Ferrari et al., 2008; Zabotin et al., 2009) represent an artificial adaptation to a perceived pathogen attack, as can be observed in numerous cell wall mutants.

Xylogen is a 50- to 100-kD highly glycosylated cell wall molecule that directly acts as an extracellular developmental signal (Motose et al., 2004). Xylogen promotes tracheid differentiation in vitro and, together with its paralogs, is required for normal vascular differentiation in planta. Xylogen is a hybrid glycosylphosphatidylinositol lipid (GPI)-anchored AGP and nonspecific lipid transfer protein (Motose et al., 2004). AGPs might act as paracrine and autocrine signals in many biological processes (for review, see Seifert and Roberts, 2007; see also article by Ellis et al., 2010). Their potential to bind to β-glycan polymers (for review, see Nothnagel, 1997) together with their plasma membrane localization via GPI anchors put them in a strategic position to mediate between cell wall polymers and cell signaling. However, available studies are too crude to annotate specific signaling roles to individual AGP species. Cell surface receptor binding to xylogen and most other cell wall-derived elicitors and potential signaling molecules remain to be identified. However, as discussed in the following section, pectic homogalacturonan and OGs are known to bind to specific cell surface receptors.

THE SENSORS

The Wall-Associated Kinase Family

Sensors for extracellular molecules consisting of an extracellular ligand-binding domain, a single trans-plasma membrane domain, and a cytosolic protein kinase domain have been termed receptor-like kinases (RLKs) and, with more than 610 genes in the Arabidopsis (Arabidopsis thaliana) genome, constitute the largest family of receptor-like proteins in plant genomes (Shiu and Bleecker, 2001a, 2001b). The binding of an extracellular ligand induces a conformational alteration leading to the activation of the protein kinase, thereby initiating a cascade of subsequent signal transduction events. Several RLKs are potentially involved in reporting sensing aspects of cell wall structure and function; however, only the subfamily of wall-associated kinases (WAKs) are known at present to directly bind to a cell wall carbohydrate. Its initially identified member, WAK1 (Kohorn et al., 1992), binds to the cell wall extremely tightly and is specifically localized at the plasma membrane-cell wall interface (He et al., 1996). In plants, WAKs are covalently bound to pectic homogalacturonan (Wagner and Kohorn, 2001); however, they bind noncovalently to Ca2+-cross-linked OGs in vitro (Decreux and Messiaen, 2005), pointing toward important endogenous factors involved in normal assembly of the WAK-pectin supramolecular structure. Genetic evidence implicates WAKs with cell elongation (Lally et al., 2001; Wagner and Kohorn, 2001; Kohorn et al., 2006b), tolerance and sensing for metals and minerals, respectively (Sivaguru et al., 2003; Hou et al., 2005), and pathogen resistance (Diener and Ausubel, 2005; Li et al., 2009). Without doubt, WAKs fulfill important biological roles, raising the stakes to uncover their mode of action. What are their physiological ligands and downstream substrates? WAK2 is required for sugar-independent growth (Kohorn et al., 2006b), and the wak2 growth phenotype is rescued by external sugar or sorbitol and by ectopic expression of Suc-6-P synthase, implicating the role of WAK2 in normal growth with sugar metabolism and osmotic control. Crucially, WAK2 is required for the normal expression of vacuolar invertase, an enzyme releasing Glc and Fru from Suc. This might mean that WAK2 feeds cues regarding cell wall properties into the control module that maintains the correct balance of carbohydrates required for optimal growth both as energy source and as osmotically active compounds (Kohorn et al., 2006b). What might be the stimulus, and how could it be transduced to activate invertase transcription? The vacuolar invertase promoter is activated by the external addition of pectin to protoplasts in a WAK2-dependent fashion (Kohorn et al., 2009), indicating that the degree of pectin binding might determine WAK activity. The observation that factors influencing the Ca2+-induced so-called egg-box conformation of pectin determine pectin binding to the WAK1 extracellular domain in vitro (Decreux and Messiaen, 2005; Cabrera et al., 2008) might mean that WAKs could sense pectin conformation in vivo. However, the nature of the interaction between WAKs and the cell wall is still somewhat ominous (Kohorn et al., 2006a). In fact, it appears that en route to the cell wall, WAK2 is retained in an insoluble complex in a secretory compartment related to the Golgi. Whether this is the cellular site where the WAK2-pectin association is formed remains to be investigated. Intriguingly, intracellular retention of WAK2 depends on l-Fuc biosynthesis that is required for rhamnogalacturonan II, XG, or AGPs but not for homogalacturonan, indicating the recruitment of a higher order structure into the WAK2-cell wall matrix polymer complex.

The Pro-Rich Extensin-Like Receptor Kinase Family

Another family of receptor kinase-like proteins recently implicated in cell wall signaling is termed PERK, as its 11 Arabidopsis members contain a Pro-rich region extracellular domain similar to extensin (EXT; Nakhamchik et al., 2004). EXTs are a group of Hyp-rich, rod-shaped extracellular proteins typically containing repeats of the Ser-Hyp(3–5) motif, with most Hyp residues typically being glycosylated by one to four Ara residues (Showalter, 1993). EXTs are mostly insoluble once secreted in the wall, cross-linked by di-isodityrosine bonds (Cannon et al., 2008), and ionically bound to pectin and AGPs by basic amino acids (Showalter, 1993). Due to the presence of Ser-Hyp(3–5) motifs sometimes interspersed with basic residues, PERKs might share some of the features of EXTs. However, peptide motifs previously implicated with di-isodityrosin-dependent cross-linking of EXTs are absent from the extracellular domain of PERKs. While transgenic alteration of PERK expression influences growth and cell wall deposition (Haffani et al., 2006), PERK4 is specifically required for the abscisic acid (ABA)-dependent influx of Ca2+ and for normal ABA sensitivity in seeds and roots. The PERK4 protein is an active protein kinase localized at the plasma membrane, and its extraction from plant material is increased by pectinase treatment (Bai et al., 2009). The present data suggest that PERK4 might interact with cell wall polymers and also participate in ABA perception, potentially linking cell wall and growth regulator signaling at the receptor level as opposed to cross talk of signal transduction cascades. Additional roles of PERK genes remain to be investigated.

The Catharanthus roseus-Like Receptor-Like Kinase 1-Like Family

The group of Catharanthus roseus-like RLKs (CrRLK1L) contains 16 members in Arabidopsis. The THESEUS1 (THE1), FERONIA (FER), and HERKULES1 and -2 (HERK) genes have recently been implicated with functions in cell wall integrity control and growth in a partially overlapping manner (Hématy et al., 2007; Guo et al., 2009). Two other members of the family, encoded by the ANXUR1 and ANXUR2 loci, suppress the premature rupture of germinated pollen tubes, a role not apparently related to elongation but potentially also related to cell wall integrity control (Boisson-Dernier et al., 2009; Miyazaki et al., 2009). Loss-of-function (LOF) mutations of THE1 partially suppress the cell elongation defect and ectopic lignification in cellulose synthase-defective backgrounds while overexpression increases the responses, suggesting that THE1 might be a component of cell wall function and integrity control (Hématy et al., 2007). Although the roles of THE1, HERK1, and HERK2 for cell elongation appear to be largely overlapping, FER is essential for cell elongation, preventing the growth of fer full LOF mutants. Knockdown of FER results in stronger suppression of growth than in the1 herk1 herk2 triple mutants, suggesting that FER might act as mandatory heterodimerization partner for other RLKs (Guo et al., 2009). To add to the genetic complexity, FER also plays an important role in the female gametophyte to restrict pollen tube growth (Escobar-Restrepo et al., 2007). Hence, at least two CrRLK1L genes, THE1 and FER, can act both as repressors and promoters of cell elongation depending on the genetic background. It is tempting to explain this seemingly paradoxical behavior by the assertion that cell wall performance and integrity control acts not only when cell walls are damaged but also during unstressed normal development.

Leu-Rich Repeat Receptor Kinases

Containing at least 220 members in the Arabidopsis genome, leucine-rich repeat receptor kinases (LRR-RLKs) form the largest group among the superfamily of receptor-like kinases (Shiu and Bleecker, 2003). LRR-RLK genes encode receptors for ligands as diverse as brassinosteroid (Kinoshita et al., 2005) and bacterial peptide elicitor fls22 (Gomez-Gomez et al., 2001); however, most ligands for LRR-RLKs are unknown. STRUBBELIG (SUB) and SUB RECEPTOR FAMILY (SRF) are members of LRR-RLK family V that lack a functional kinase domain (Eyuboglu et al., 2007; Fulton et al., 2009). Mutations in SUB and SUB-LIKE MUTANT (SLM) loci lead to comparable pleiotropic developmental defects and changes in transcript abundance of various genes related to cell wall biogenesis, growth regulator signaling, and abiotic stress. It was proposed that SUB and SLM loci might function in identical or convergent pathways potentially involved in cell wall integrity control (Fulton et al., 2009). Several SRFs were implicated in cell wall biosynthesis and function owing to their transcriptional cofluctuation with cell wall-related genes (Eyuboglu et al., 2007).

The family XIII LRR-RLK ERECTA (ER) is involved in many different aspects of development (for review, see van Zanten et al., 2009). Family XIII contains seven members, three of which, ER, ERECTA-LIKE1 (ERL1), and ERL2, act in an overlapping manner, as evidenced by the synergistic effect of er, erl1, and erl2 LOF alleles (Shpak et al., 2003, 2004, 2005). Interestingly, ER is required for cell wall reinforcement during the wild-type defense response against a fungal pathogen and, in fact, for normal cell wall composition (Sanchez-Rodriguez et al., 2009). This phenotype suggests that ERECTA might be involved in cell wall performance and integrity control upstream of the regulation of cell wall structure. An alternative but not mutually exclusive interpretation is that ER might sense cell wall fragments released by pathogen attack (Sanchez-Rodriguez et al., 2009). In a reverse genetic investigation of family XIII of LRR-RLKs, the combination of LOF alleles of FEI1 and FEI2 was found to display Suc- and salt-sensitive cell expansion defects (Xu et al., 2008), reminiscent of various cell wall structural mutants such as cobra (Roudier et al., 2005), sabre (Aeschbacher et al., 1995), rsw1 (Arioli et al., 1998), and sos5 (Shi et al., 2003). Like cobra and rsw1, fei1 fei2 double mutants suffer from severe deficiency in crystalline cellulose. Interestingly, fei1 fei2 sos5 triple mutants display the same phenotype as the fei1 fei2 and sos5 parental lines. This nonadditive interaction was interpreted as FEI1 and FEI2 acting redundantly in the same pathway as SOS5/FLA4 (Shi et al., 2003). It was found that the fei1 fei2 phenotype is partially suppressed with the ethylene biosynthetic inhibitor α-amino-isobutyric acid and that both FEI proteins interact with the ethylene biosynthetic enzyme ACS5. These unexpected observations suggested that FEI proteins play a role in cell wall architecture, possibly as mediators between cell wall and signal transduction. 1-Aminocyclopropane-1-carboxylic acid might be produced locally by an activated FEI ACS complex and act as a novel second messenger. The physical relation between FEI1/2 and FLA4 remains to be studied; however, hypothetical binding between the protein-protein interaction fasciclin domain of FLA4 and the LRR domain of either of the FEI RLKs on the one hand and a carbohydrate-carbohydrate interaction between the FLA4 AG moiety and cell wall polymers on the other hand might physically connect protein-binding RLK and cell wall carbohydrates. Many LRR-RLK transcripts are coregulated with AGPs (G.J. Seifert, unpublished data), while several members are enriched in detergent-resistant membranes (Shahollari et al., 2004) that also contain GPI-anchored AGPs (Borner et al., 2005). Detergent-resistant membranes are generally hypothesized to represent biochemically distinct nanoscale membrane domains sometimes called lipid rafts (for review, see Lingwood and Simons, 2010). Hence, the speculative interaction between LRR-RLKs and GPI-anchored AGPs might be promoted by their subcompartmentalization into lipid domains.

Leguminous l-Type Lectin RLKs

A group of potential cell wall sensors are the leguminous l-type lectin RLKs (Bouwmeester and Govers, 2009) encoded by a large family of 46 Arabidopsis loci. Interestingly, several l-lectin RLKs were found to bind peptides containing the Arg-Gly-Asp (RGD) tripeptide (Gouget et al., 2006), a sequence present in various animal extracellular matrix proteins but so far not identified in any plant cell wall proteins. Addition of this peptide facilitates plasma membrane detachment during plasmolysis (Canut et al., 1998), implicating the identified RGD-binding RLKs in cell wall adhesion. It might be tempting to invoke binding of the extracellular lectin domain to cell wall carbohydrates; however, this seems unlikely, as sugar-binding residues in the identified proteins are insufficiently conserved (Bouwmeester and Govers, 2009). Hence, native ligands of RGD-binding l-lectin RLKs remain to be proposed.

Mechanosensitive Receptors and Ion Channels

As the plasma membrane is mechanically connected to the cell wall by turgor pressure, the perception of mechanical force at the plasma membrane-cell wall interface might be a global mechanism to report cell wall integrity and performance to the cell interior. An interesting hypothetical mechanism for how cell wall stress might be turned into a signal is deformation-dependent exposure of previously masked receptor recognition sites on cell wall polymers analogous to the animal extracellular matrix protein fibronectin (Monshausen and Gilroy, 2009). In principle, WAKs or other transmembrane receptor kinases might be activated according to this speculative concept. A more traditional type of turgor pressure gauge is the mechanosensitive (MS) ion channel, which opens in response to plasma membrane stretching or warping. Several Arabidopsis homologs to the prokaryotic and eukaryotic MscS/MSC1 MS channels form the MSL gene family. Although MSL9 and MSL10 are necessary for plasma membrane stretch-induced ion conductance in root protoplasts, a role of the MSL genes for plant growth and the specific substrate ion have yet to be established (Haswell et al., 2008). A locus involved in stretch-induced plasma membrane Ca2+ conductivity is MCA1 and possibly its paralog MCA2 (Nakagawa et al., 2007). Plant MCA1 complements the yeast-lethal mutation mid1 in a putative stretch-activated Ca2+ channel-encoding locus, and its expression in plant tissues is correlated with Ca2+ influx upon plasma membrane distortion and is required for root penetration into medium with heterogeneous mechanical properties. It is intriguing to speculate that alterations in mechanical cell wall properties during growth and abiotic stress might be sensed as a change in plasma membrane tension, thereby modulating transmembrane Ca2+ current. Both MSL and MCA proteins are the first candidates for molecular components of the plasma membrane MS ion channel system.

SIGNAL TRANSDUCTION

Phosphorylation Cascades

Surprisingly little is known on the molecular targets of receptor kinases plants (De Smet et al., 2009; Tor et al., 2009), although genetic evidence in many cases suggests signaling from receptor kinases to mitogen-activated protein kinase (MAPK) cascades (Nakagami et al., 2005). MAPK cascades act in the signal transduction of extracellular stimuli in all eukaryotes and consist of three types of protein kinases. In response to stimuli such as growth regulators, abiotic stress, oxidative stress, PAMPs, and developmental cues, an active MAPK kinase kinase (MAP3K) phosphorylates and thereby activates a MAPK kinase (MAP2K) that in turn activates a MAPK. Active MAPKs potentially phosphorylate various substrates such as transcription factors. Another level of protein kinases is understood to act on top of MAP3Ks. Because the number of MAPKs is relatively small, the specificity of signaling at the transcriptional level is an intriguing problem (for review, see Colcombet and Hirt, 2008).

There is accumulating evidence that the perception of pectin or pectin fragments by WAKs involves MAPK signaling. The immediate protein kinase substrates of WAK2 are unknown; however, WAK2 is necessary for the rapid pectin-triggered activation of MAPK3 and for pectin-induced alterations in transcript levels, including activation of the vacuolar invertase promoter (Kohorn et al., 2009). Hypothetically, this might place WAK2 upstream of a MAPK cascade. Despite the dramatic influence of WAK2 on the response to externally applied pectin in protoplasts, the wak2 mutant phenotype is quite subtle (Kohorn et al., 2006b), invoking potential redundancy at the cellular or the whole plant level. Consistently, a dominant negative version of WAK2 causes a more dramatic growth phenotype that is synergistically enhanced by a mapk3 LOF allele (Kohorn et al., 2006b). Families of transcripts influenced by pectin in a WAK2-dependent manner are transcription factors, defense related, involved in protein phosphorylation, or related to cell wall biosynthesis and remodeling. The transcript profile in response to pectin treatment of wild-type and wak2 protoplasts displayed relatively few differences in comparison with short-term treatment of suspension cells with OGs (Moscatiello et al., 2006). One reason for this discrepancy might lie in the fact that protoplasts were kept with osmoprotectants while suspension cells were not. Osmotic stress might indirectly affect pectin conformation by mechanically stressing the primary cell wall and thereby synergistically activating WAKs in a pectin-dependent and an osmotic stress-dependent fashion. Hence, a possible scheme that can be crudely outlined from the available data might link pectin conformation/osmotic balance to WAK2/WAK1 activation, leading to the activation of MAPK3 (and possibly other MAPKs, such as its most closely related ortholog MAPK6) via unknown MAP3Ks and MAP2Ks and resulting in the activation of transcription factors regulating stress management, osmotic balance, and cell wall biosynthesis and remodeling. Generally, this cyclical sequence of events from sensing of cell wall structure to signal transduction to transcription to modulation of signal sensing, signal transduction, osmotic balance, cell wall biosynthesis, and remodeling constitutes an example of a regulatory module of cell wall integrity control as outlined in the introduction (Fig. 1).

Although the initial activation of MAPKs takes place within minutes and can be detected by phosphorylation of generic substrates, some MAPKs are also induced at the transcript level. Therefore, it is interesting that two independent studies addressing different aspects of cell wall integrity control, application of OGs (Moscatiello et al., 2006) or interference with AGP integrity by βGlcY (Guan and Nothnagel, 2004), found specific sets of MAPK cascade components transcriptionally up-regulated. MAPK3, -5, and -11 and MAP3K15 and -16 were induced after 1 h of βGlcY treatment, while OG treatment for 2 h induced MAPK3, two isoforms of MAPK4, MAP2K9, and MAP3K8 and -19. Although in both studies suspension cells were used and sampled at a similar time interval after the treatment, there might be technical explanations for the observed differences. However, it is tempting to speculate that in addition to the general stress response node represented by MAPK3/MAPK6, the activation of specific sets of MAPKs, MAP2Ks, and MAP3Ks is required for the precise tuning of the responses to different types of cell wall stresses.

An intracellular protein kinase potentially acting in cell wall stress signal transduction is OXI1 (Rentel et al., 2004). OXI1 transcript is induced by reactive oxygen species (ROS). It is also induced by cellulase treatment and transiently by wounding. Thirty minutes after the wounding stimulus, OXI1 expression was induced; however, another 30 min later, it again reached a lower level. OXI1 expression after hydrogen peroxide (H2O2) or cellulase treatment was more sustained, still increasing between 1 and 3 h of treatment. OXI1 kinase activity was also strongly stimulated by H2O2 and cellulase, peaking 5 min after H2O2 treatment and obtaining higher levels and a later occurring peak after treatment with cellulase. OXI1 is required for full H2O2- and cellulase-stimulated activation of MAPK3 and MAPK6 (Rentel et al., 2004). The more efficient activation by cellulase compared with H2O2 might be due to multiple roles of cellulase in the stimulation process (Rentel et al., 2004), and these might be PAMPs in the cellulase peptide as well as host-associated molecular patterns such as the released cellodextrins. Third, damage to cellulose structure leading to turgor instability might be a trigger.

Ca2+ and ROS

Numerous small molecules such as protons and various other ions, ROS, nucleotides, lipids, and sugars can act as intracellular transmitters of information, or second messengers, often by binding to and reshaping specific transducer proteins such as calmodulin or hexokinase.

Drastic experimental interventions in cell wall integrity such as binding of βGlcY to AGPs trigger rapid elevation of intracellular Ca2+ (Roy et al., 1999; Pickard and Fujiki, 2005). Moreover, Ca2+ partially transmits the intracellular response to cell wall-derived OG elicitors (Moscatiello et al., 2006). On the other hand, the respiratory burst oxidase homolog isoform D (AtRBOHD), encoding an enzyme that produces superoxide anions, is required for the responses to cellulose biosynthesis inhibition (Hamann et al., 2009), and various inhibitors of ROS suppress cell death triggered by genetic and chemical interference with AGP structure (G.J. Seifert, unpublished data). Experimentally, far less tractable than genes, mRNAs, or proteins, the very dynamic intracellular fluxes of second messengers in response to specific structural stimuli coming in from the cell wall under natural conditions remain to be explored under less artificial conditions. Some understanding of how second messengers might be involved in cell wall signaling might be obtained from developmental models. Root hair initiation and growth have been studied physiologically and genetically. Hair initiation involves the selection of the appropriate position for the future hair close to the base of the trichoblast and cell wall remodeling to allow the formation of an outward bulge of precise shape and size. Hair growth requires the continuous tip-focused deposition of new cell wall material and subsequent cell wall remodeling at the flanks of the hair (Dolan, 2001; Carol and Dolan, 2002). Quite obviously, both the initiation and growth processes have to be responsive to the actual state of cell wall structure and stability. Interestingly, root hair growth follows an oscillatory pattern that might reflect bursts of cell wall expansion. Ca2+ and ROS together with extracellular pH oscillate in a manner similar to hair growth but trailing its peak by 4 and 8 s, respectively (Monshausen et al., 2007, 2008). One interpretation for this behavior is that a phase of rapid cell wall expansion is sensed at the level of the plasma membrane, causing an increase of intracellular Ca2+ followed by the production of ROS and alkalinization of the apoplast. The Ca2+ signal might limit cell wall expansion, preventing catastrophic failure. Consistently, suppression of both Ca2+ influx and ROS production can cause hair cells to burst (Foreman et al., 2003; Monshausen et al., 2008). Ca2+ fluxes might initially be stimulated by MS channels that respond to increased membrane stretch in a cell wall growth phase. As ROS and Ca2+ act in a positive feedback loop during root hair growth (Takeda et al., 2008), an increase of Ca2+ enhances ROS production that might vice versa increase intracellular Ca2+, possibly by activating a hyperpolarization-activated Ca2+ channel (Foreman et al., 2003) until cell wall expansion is supplanted by cell wall rigidification. As opposed to previously discussed stress signaling pathways but consistent with the short time scale of the observed oscillations, this type of growth control might act rapidly on a posttranslational level. However, it is quite clear that cell wall signals also involve Ca2+ and ROS in a manner that depends on gene expression. One example is the addition of OGs to cultured cells, which induces Ca2+-dependent as well as Ca2+-independent alterations in the transcript profile (Moscatiello et al., 2006). Another example is the observation that responses in transcripts induced by H2O2 and cell wall stress show considerable overlap (Duval and Beaudoin, 2009).

Modulation by Sugar Signaling

Sugars such as Glc and Suc act as intercellular signals independently from their role in metabolism (for review, see Hanson and Smeekens, 2009). Sugar signaling is partially conserved among kingdoms and interacts with all major signaling networks such as growth regulator and light signal transduction in plants. Therefore, it is not surprising that sugar signaling also interacts with cell wall performance and integrity control. That the cell wall matrix structural mutants mur4, mur1, and mur3 are sugar hyperresponsive suggested such a link (Li et al., 2007). External Glc or Suc is required for many responses to pharmacological inhibition of cellulose biosynthesis. Interestingly, metabolically inactive Glc and Suc analogs stimulated most of the Glc/Suc-dependent responses to cellulose biosynthesis inhibition, while Fru did not (Hamann et al., 2009). This behavior is reminiscent of the role of the HEXOKINASE1 (HXK1) locus that mediates many responses to Glc, even in the absence of Glc-phosphorylating activity (Moore et al., 2003). HXK1-dependent sugar signaling modulates the signaling of numerous growth regulators (Moore et al., 2003); however, its role in cell wall performance and integrity control remains to be investigated. Another gene important for sugar signaling is PLEIOTROPIC REGULATORY LOCUS1 (PRL1), which, similar to HXK, has a widespread regulatory role, influencing growth regulator response (Nemeth et al., 1998) and innate immunity (Palma et al., 2007) and response to singlet oxygen (Baruah et al., 2009). Sugar hypersensitivity of mur4, assayed as inhibition of dark-grown hypocotyl elongation, depended on PRL1 (Li et al., 2007). By contrast, only a minor proportion of genes differentially regulated in the mur4 background was influenced by PRL1. This is consistent with the observation that many transcription factor genes, induced by interference with AGPs (Guan and Nothnagel, 2004) or by inhibition of cellulose synthesis (Duval and Beaudoin, 2009), are also induced by singlet oxygen, albeit independently of PRL1 (Baruah et al., 2009). Taken together, this suggests that sugar signaling via PRL1, and possibly via HXK1, might modulate cell wall signaling without being essential.

Interactions with Growth Regulator Signaling and Other Factors

The isolation of cell wall mutants from forward genetic screens that were initially directed at other questions such as disease resistance mechanisms or sugar and growth regulator signaling was extremely important to highlight the integral role of cell wall structure in various aspects of signaling. Sustained defects in cell wall polymers often lead to the constitutive activation or modulation of numerous stress responses such as ethylene, jasmonate, or ABA-responsive genes and resistance to various pathogens (Table I). The unexpected diversity of observed responses might have several explanations that are not mutually exclusive: (1) diversity of plant materials; (2) differential sensitivity of cell types to chemicals or mutations; (3) diversity of cell wall stress stimuli, such as genetic or chemical inhibition with cellulose, hemicellulose, pectin, or AGPs; (4) combination with other relevant stimuli, such as light, water supply, or external carbohydrate and osmotically active compounds that modulate outcome; and (5) different time scopes of the various experiments, from relatively short-term drug experiments that can have immediate actions to mutant studies producing sustained effects. The significance of these individual parameters has not been systematically addressed so far. Moreover, it will be interesting to genetically dissect the role of growth regulator signaling pathways for the downstream responses such as transcriptional and posttranscriptional regulation of cell wall biosynthesis and remodeling.

THE OUTPUT

From the preceding discussion, it becomes clear that the typical fingerprint of an activated cell wall integrity and performance control machinery is the large-scale alteration of transcriptional activities related to cell wall biosynthesis and remodeling (Table I). However, most of what is known at present about the transcriptional regulation of cell wall biosynthesis or remodeling comes from developmentally regulated systems such as xylogenesis (Zhong et al., 2006; Demura and Fukuda, 2007; Lasserre et al., 2008; for review, see Zhong et al., 2007) or is based on the assumption that genes involved in a given metabolic process are (transcriptionally) coregulated (Brown et al., 2005; Persson et al., 2005). Evidence for posttranslational modulation of cell wall biosynthesis is generally only circumstantial (Winter and Huber, 2000; Nuhse et al., 2004; Seifert, 2004; Jacob-Wilk et al., 2006). The identification of transcription factors and posttranslational processes regulating cell wall biosynthesis and remodeling is an important field of future research.

PERSPECTIVES

In this article, we have reviewed the accumulating evidence for the involvement of the impact of structural alterations of the plant cell wall on many aspects of plant life. The mechanisms of how fluctuations in cell wall integrity and performance are monitored or how such stimuli are converted into appropriate control responses are expected to be highly complex, and only a few putative components have emerged. Among the different types of receptors, the group of WAK proteins provides the best understood paradigm for cell wall signaling. WAK binds to and is activated by OGs and pectin, leading to the activation of MAPK3 and to transcriptional alterations of cell wall biosynthesis and remodeling as well as stress signaling. Several other candidate receptors are in line to be further characterized for their extracellular ligands and intracellular substrates. The relation of MS ion channels of the MSL and MCA classes to cell wall performance and turgor sensing remains to be experimentally tested. The puzzle of how a limited set of MAPKs can effect the transcription of the correct set of cell wall-modifying and biosynthetic genes remains to be addressed, and cell wall structure-controlling transcription factors have yet to be identified. Because the life and walls of plant cells are far more complex than those of yeast cells, we expect future discoveries of many new receptors, signal transduction components, and transcriptional regulators involved in various aspects of cell wall performance and integrity control

Acknowledgments

We thank Andrea Pitzschke for critical comments on the manuscript.

References

  • Aeschbacher RA, Hauser MT, Feldmann KA, Benfey PN. (1995) The SABRE gene is required for normal cell expansion in Arabidopsis. Genes Dev 9: 330–340 [PubMed]
  • Ahn JW, Verma R, Kim M, Lee JY, Kim YK, Bang JW, Reiter WD, Pai HS. (2006) Depletion of UDP-D-apiose/UDP-D-xylose synthases results in rhamnogalacturonan-II deficiency, cell wall thickening, and cell death in higher plants. J Biol Chem 281: 13708–13716 [PubMed]
  • Albersheim P, Darvill AG, O'Neil M, Valente B, Sharp JK, Nothnagel EA, Davis KR, Yamazaki N, Collin DJ, York WS, et al. (1983) Oligosaccharins, naturally occurring carbohydrates with biological regulatory functions. Ciferri O, Dure L, editors. , , Structure and Function of Plant Genomes. Plenum Press, New York, pp 293–312
  • Arioli T, Peng L, Betzner AS, Burn J, Wittke W, Herth W, Camilleri C, Höfte H, Plazinski J, Birch R, et al. (1998) Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279: 717–720 [PubMed]
  • Aziz A, Gauthier A, Bezier A, Poinssot B, Joubert JM, Pugin A, Heyraud A, Baillieul F. (2007) Elicitor and resistance-inducing activities of beta-1,4 cellodextrins in grapevine, comparison with beta-1,3 glucans and alpha-1,4 oligogalacturonides. J Exp Bot 58: 1463–1472 [PubMed]
  • Bai L, Zhang G, Zhou Y, Zhang Z, Wang W, Du Y, Wu Z, Song CP. (2009) Plasma membrane-associated proline-rich extensin-like receptor kinase 4, a novel regulator of Ca signaling, is required for abscisic acid responses in Arabidopsis thaliana. Plant J 60: 314–327 [PubMed]
  • Baruah A, Simkova K, Hincha DK, Apel K, Laloi C. (2009) Modulation of O-mediated retrograde signaling by the PLEIOTROPIC RESPONSE LOCUS 1 (PRL1) protein, a central integrator of stress and energy signaling. Plant J 60: 22–32 [PubMed]
  • Bellincampi D, Cardarelli M, Zaghi D, Serino G, Salvi G, Gatz C, Cervone F, Altamura MM, Costantino P, Lorenzo GD. (1996) Oligogalacturonides prevent rhizogenesis in rolB-transformed tobacco explants by inhibiting auxin-induced expression of the rolB gene. Plant Cell 8: 477–487 [PMC free article] [PubMed]
  • Bischoff V, Cookson SJ, Wu S, Scheible WR. (2009) Thaxtomin A affects CESA-complex density, expression of cell wall genes, cell wall composition, and causes ectopic lignification in Arabidopsis thaliana seedlings. J Exp Bot 60: 955–965 [PMC free article] [PubMed]
  • Boisson-Dernier A, Roy S, Kritsas K, Grobei MA, Jaciubek M, Schroeder JI, Grossniklaus U. (2009) Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge. Development 136: 3279–3288 [PMC free article] [PubMed]
  • Borner GH, Sherrier DJ, Weimar T, Michaelson LV, Hawkins ND, Macaskill A, Napier JA, Beale MH, Lilley KS, Dupree P. (2005) Analysis of detergent-resistant membranes in Arabidopsis: evidence for plasma membrane lipid rafts. Plant Physiol 137: 104–116 [PMC free article] [PubMed]
  • Bosca S, Barton CJ, Taylor NG, Ryden P, Neumetzler L, Pauly M, Roberts K, Seifert GJ. (2006) Interactions between MUR10/CesA7 dependent secondary cellulose biosynthesis and primary cell wall structure. Plant Physiol 142: 1353–1363 [PMC free article] [PubMed]
  • Bouton S, Leboeuf E, Mouille G, Leydecker MT, Talbotec J, Granier F, Lahaye M, Höfte H, Truong HN. (2002) QUASIMODO1 encodes a putative membrane-bound glycosyltransferase required for normal pectin synthesis and cell adhesion in Arabidopsis. Plant Cell 14: 2577–2590 [PMC free article] [PubMed]
  • Bouwmeester K, Govers F. (2009) Arabidopsis L-type lectin receptor kinases: phylogeny, classification, and expression profiles. J Exp Bot 60: 4383–4396 [PubMed]
  • Brocard-Gifford I, Lynch TJ, Garcia ME, Malhotra B, Finkelstein RR. (2004) The Arabidopsis thaliana ABSCISIC ACID-INSENSITIVE8 encodes a novel protein mediating abscisic acid and sugar responses essential for growth. Plant Cell 16: 406–421 [PMC free article] [PubMed]
  • Brown DM, Zeef LA, Ellis J, Goodacre R, Turner SR. (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17: 2281–2295 [PMC free article] [PubMed]
  • Cabrera JC, Boland A, Messiaen J, Cambier P, Van Cutsem P. (2008) Egg box conformation of oligogalacturonides: the time-dependent stabilization of the elicitor-active conformation increases its biological activity. Glycobiology 18: 473–482 [PubMed]
  • Cannon MC, Terneus K, Hall Q, Tan L, Wang Y, Wegenhart BL, Chen L, Lamport DT, Chen Y, Kieliszewski MJ. (2008) Self-assembly of the plant cell wall requires an extensin scaffold. Proc Natl Acad Sci USA 105: 2226–2231 [PMC free article] [PubMed]
  • Cano-Delgado A, Penfield S, Smith C, Catley M, Bevan M. (2003) Reduced cellulose synthesis invokes lignification and defense responses in Arabidopsis thaliana. Plant J 34: 351–362 [PubMed]
  • Canut H, Carrasco A, Galaud JP, Cassan C, Bouyssou H, Vita N, Ferrara P, Pont-Lezica R. (1998) High affinity RGD-binding sites at the plasma membrane of Arabidopsis thaliana links the cell wall. Plant J 16: 63–71 [PubMed]
  • Carol RJ, Dolan L. (2002) Building a hair: tip growth in Arabidopsis thaliana root hairs. Philos Trans R Soc Lond B Biol Sci 357: 815–821 [PMC free article] [PubMed]
  • Chen Z, Hong X, Zhang H, Wang Y, Li X, Zhu JK, Gong Z. (2005) Disruption of the cellulose synthase gene, AtCesA8/IRX1, enhances drought and osmotic stress tolerance in Arabidopsis. Plant J 43: 273–283 [PubMed]
  • Colcombet J, Hirt H. (2008) Arabidopsis MAPKs: a complex signaling network involved in multiple biological processes. Biochem J 413: 217–226 [PubMed]
  • Decreux A, Messiaen J. (2005) Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiol 46: 268–278 [PubMed]
  • Demura T, Fukuda H. (2007) Transcriptional regulation in wood formation. Trends Plant Sci 12: 64–70 [PubMed]
  • Derbyshire P, McCann MC, Roberts K. (2007) Restricted cell elongation in Arabidopsis hypocotyls is associated with a reduced average pectin esterification level. BMC Plant Biol 7: 31. [PMC free article] [PubMed]
  • De Smet I, Voss U, Jurgens G, Beeckman T. (2009) Receptor-like kinases shape the plant. Nat Cell Biol 11: 1166–1173 [PubMed]
  • Diener AC, Ausubel FM. (2005) RESISTANCE TO FUSARIUM OXYSPORUM 1, a dominant Arabidopsis disease-resistance gene, is not race specific. Genetics 171: 305–321 [PMC free article] [PubMed]
  • Diet A, Link B, Seifert GJ, Schellenberg B, Wagner U, Pauly M, Reiter WD, Ringli C. (2006) The Arabidopsis root hair cell wall formation mutant lrx1 is suppressed by mutations in the RHM1 gene encoding a UDP-l-rhamnose synthase. Plant Cell 18: 1630–1641 [PMC free article] [PubMed]
  • Dolan L. (2001) How and where to build a root hair. Curr Opin Plant Biol 4: 550–554 [PubMed]
  • Duval I, Beaudoin N. (2009) Transcriptional profiling in response to inhibition of cellulose synthesis by thaxtomin A and isoxaben in Arabidopsis thaliana suspension cells. Plant Cell Rep 28: 811–830 [PubMed]
  • Duval I, Brochu V, Simard M, Beaulieu C, Beaudoin N. (2005) Thaxtomin A induces programmed cell death in Arabidopsis thaliana suspension-cultured cells. Planta 222: 820–831 [PubMed]
  • Ellis C, Karafyllidis I, Wasternack C, Turner JG. (2002) The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. Plant Cell 14: 1557–1566 [PMC free article] [PubMed]
  • Ellis M, Egelund J, Schultz CJ, Bacic A. (2010) Arabinogalactan-proteins: key regulators at the cell surface? Plant Physiol 153: 403–419 [PMC free article] [PubMed]
  • Errakhi R, Dauphin A, Meimoun P, Lehner A, Reboutier D, Vatsa P, Briand J, Madiona K, Rona JP, Barakate M, et al. (2008) An early Ca2+ influx is a prerequisite to thaxtomin A-induced cell death in Arabidopsis thaliana cells. J Exp Bot 59: 4259–4270 [PubMed]
  • Escobar-Restrepo JM, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang WC, Grossniklaus U. (2007) The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 317: 656–660 [PubMed]
  • Eyuboglu B, Pfister K, Haberer G, Chevalier D, Fuchs A, Mayer KF, Schneitz K. (2007) Molecular characterisation of the STRUBBELIG-RECEPTOR FAMILY of genes encoding putative leucine-rich repeat receptor-like kinases in Arabidopsis thaliana. BMC Plant Biol 7: 16. [PMC free article] [PubMed]
  • Fagard M, Desnos T, Desprez T, Goubet F, Refregier G, Mouille G, McCann M, Rayon C, Vernhettes S, Höfte H. (2000) PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell 12: 2409–2424 [PMC free article] [PubMed]
  • Ferrari S, Galletti R, Pontiggia D, Manfredini C, Lionetti V, Bellincampi D, Cervone F, De Lorenzo G. (2008) Transgenic expression of a fungal endo-polygalacturonase increases plant resistance to pathogens and reduces auxin sensitivity. Plant Physiol 146: 669–681 [PMC free article] [PubMed]
  • Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, et al. (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422: 442–446 [PubMed]
  • Fry SC, McDougall GJ, Lorences EP, Biggs KJ, Smith RC. (1990) Oligosaccharins from xyloglucan and cellulose: modulators of the action of auxin and H+ on plant growth. Symp Soc Exp Biol 44: 285–298 [PubMed]
  • Fulton L, Batoux M, Vaddepalli P, Yadav RK, Busch W, Andersen SU, Jeong S, Lohmann JU, Schneitz K. (2009) DETORQUEO, QUIRKY, and ZERZAUST represent novel components involved in organ development mediated by the receptor-like kinase STRUBBELIG in Arabidopsis thaliana. PLoS Genet 5: e1000355. [PMC free article] [PubMed]
  • Galletti R, De Lorenzo G, Ferrari S. (2009) Host-derived signals activate plant innate immunity. Plant Signal Behav 4: 33–34 [PMC free article] [PubMed]
  • Gao M, Showalter AM. (1999) Yariv reagent treatment induces programmed cell death in Arabidopsis cell cultures and implicates arabinogalactan protein involvement. Plant J 19: 321–331 [PubMed]
  • Gaspar YM, Nam J, Schultz CJ, Lee LY, Gilson PR, Gelvin SB, Bacic A. (2004) Characterization of the Arabidopsis lysine-rich arabinogalactan-protein AtAGP17 mutant (rat1) that results in a decreased efficiency of Agrobacterium transformation. Plant Physiol 135: 2162–2171 [PMC free article] [PubMed]
  • Gille S, Hansel U, Ziemann M, Pauly M. (2009) Identification of plant cell wall mutants by means of a forward chemical genetic approach using hydrolases. Proc Natl Acad Sci USA 106: 14699–14704 [PMC free article] [PubMed]
  • Gomez-Gomez L, Bauer Z, Boller T. (2001) Both the extracellular leucine-rich repeat domain and the kinase activity of FSL2 are required for flagellin binding and signaling in Arabidopsis. Plant Cell 13: 1155–1163 [PMC free article] [PubMed]
  • Gouget A, Senchou V, Govers F, Sanson A, Barre A, Rouge P, Pont-Lezica R, Canut H. (2006) Lectin receptor kinases participate in protein-protein interactions to mediate plasma membrane-cell wall adhesions in Arabidopsis. Plant Physiol 140: 81–90 [PMC free article] [PubMed]
  • Guan Y, Nothnagel EA. (2004) Binding of arabinogalactan proteins by Yariv phenylglycoside triggers wound-like responses in Arabidopsis cell cultures. Plant Physiol 135: 1346–1366 [PMC free article] [PubMed]
  • Guo H, Ye H, Li L, Yin Y. (2009) A family of receptor-like kinases are regulated by BES1 and involved in plant growth in Arabidopsis thaliana. Plant Signal Behav 4: 784–786 [PMC free article] [PubMed]
  • Haffani YZ, Silva-Gagliardi NF, Sewter SK, Grace Aldea M, Zhao Z, Nakhamchik A, Cameron RK, Goring DR. (2006) Altered expression of PERK receptor kinases in Arabidopsis leads to changes in growth and floral organ formation. Plant Signal Behav 1: 251–260 [PMC free article] [PubMed]
  • Hamann T, Bennett M, Mansfield J, Somerville C. (2009) Identification of cell-wall stress as a hexose-dependent and osmosensitive regulator of plant responses. Plant J 57: 1015–1026 [PubMed]
  • Hanson J, Smeekens S. (2009) Sugar perception and signaling: an update. Curr Opin Plant Biol 12: 562–567 [PubMed]
  • Haswell ES, Peyronnet R, Barbier-Brygoo H, Meyerowitz EM, Frachisse JM. (2008) Two MscS homologs provide mechanosensitive channel activities in the Arabidopsis root. Curr Biol 18: 730–734 [PubMed]
  • He ZH, Fujiki M, Kohorn BD. (1996) A cell wall-associated, receptor-like protein kinase. J Biol Chem 271: 19789–19793 [PubMed]
  • Hématy K, Cherk C, Somerville S. (2009) Host-pathogen warfare at the plant cell wall. Curr Opin Plant Biol 12: 406–413 [PubMed]
  • Hématy K, Höfte H. (2008) Novel receptor kinases involved in growth regulation. Curr Opin Plant Biol 11: 321–328 [PubMed]
  • Hématy K, Sado PE, Van Tuinen A, Rochange S, Desnos T, Balzergue S, Pelletier S, Renou JP, Höfte H. (2007) A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr Biol 17: 922–931 [PubMed]
  • Hernandez-Blanco C, Feng DX, Hu J, Sanchez-Vallet A, Deslandes L, Llorente F, Berrocal-Lobo M, Keller H, Barlet X, Sanchez-Rodriguez C, et al. (2007) Impairment of cellulose synthases required for Arabidopsis secondary cell wall formation enhances disease resistance. Plant Cell 19: 890–903 [PMC free article] [PubMed]
  • Hewezi T, Howe P, Maier TR, Hussey RS, Mitchum MG, Davis EL, Baum TJ. (2008) Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase: cooperative cell wall modification during parasitism. Plant Cell 20: 3080–3093 [PMC free article] [PubMed]
  • Hou X, Tong H, Selby J, Dewitt J, Peng X, He ZH. (2005) Involvement of a cell wall-associated kinase, WAKL4, in Arabidopsis mineral responses. Plant Physiol 139: 1704–1716 [PMC free article] [PubMed]
  • Humphrey TV, Bonetta DT, Goring DR. (2007) Sentinels at the wall: cell wall receptors and sensors. New Phytol 176: 7–21 [PubMed]
  • Jacob-Wilk D, Kurek I, Hogan P, Delmer DP. (2006) The cotton fiber zinc-binding domain of cellulose synthase A1 from Gossypium hirsutum displays rapid turnover in vitro and in vivo. Proc Natl Acad Sci USA 103: 12191–12196 [PMC free article] [PubMed]
  • Kinoshita T, Cano-Delgado A, Seto H, Hiranuma S, Fujioka S, Yoshida S, Chory J. (2005) Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433: 167–171 [PubMed]
  • Kohorn BD, Johansen S, Shishido A, Todorova T, Martinez R, Defeo E, Obregon P. (2009) Pectin activation of MAP kinase and gene expression is WAK2 dependent. Plant J 8: 8 [PMC free article] [PubMed]
  • Kohorn BD, Kobayashi M, Johansen S, Friedman HP, Fischer A, Byers N. (2006a) Wall-associated kinase 1 (WAK1) is crosslinked in endomembranes, and transport to the cell surface requires correct cell-wall synthesis. J Cell Sci 119: 2282–2290 [PubMed]
  • Kohorn BD, Kobayashi M, Johansen S, Riese J, Huang LF, Koch K, Fu S, Dotson A, Byers N. (2006b) An Arabidopsis cell wall-associated kinase required for invertase activity and cell growth. Plant J 46: 307–316 [PubMed]
  • Kohorn BD, Lane S, Smith TA. (1992) An Arabidopsis serine/threonine kinase homologue with an epidermal growth factor repeat selected in yeast for its specificity for a thylakoid membrane protein. Proc Natl Acad Sci USA 89: 10989–10992 [PMC free article] [PubMed]
  • Lally D, Ingmire P, Tong HY, He ZH. (2001) Antisense expression of a cell wall-associated protein kinase, WAK4, inhibits cell elongation and alters morphology. Plant Cell 13: 1317–1331 [PMC free article] [PubMed]
  • Lasserre E, Jobet E, Llauro C, Delseny M. (2008) AtERF38 (At2g35700), an AP2/ERF family transcription factor gene from Arabidopsis thaliana, is expressed in specific cell types of roots, stems and seeds that undergo suberization. Plant Physiol Biochem 46: 1051–1061 [PubMed]
  • Levin DE. (2005) Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 69: 262–291 [PMC free article] [PubMed]
  • Li H, Zhou SY, Zhao WS, Su SC, Peng YL. (2009) A novel wall-associated receptor-like protein kinase gene, OsWAK1, plays important roles in rice blast disease resistance. Plant Mol Biol 69: 337–346 [PubMed]
  • Li Y, Smith C, Corke F, Zheng L, Merali Z, Ryden P, Derbyshire P, Waldron K, Bevan MW. (2007) Signaling from an altered cell wall to the nucleus mediates sugar-responsive growth and development in Arabidopsis thaliana. Plant Cell 19: 2500–2515 [PMC free article] [PubMed]
  • Lingwood D, Simons K. (2010) Lipid rafts as a membrane-organizing principle. Science 327: 46–50 [PubMed]
  • Manfield IW, Orfila C, McCartney L, Harholt J, Bernal AJ, Scheller HV, Gilmartin PM, Mikkelsen JD, Paul Knox J, Willats WG. (2004) Novel cell wall architecture of isoxaben-habituated Arabidopsis suspension-cultured cells: global transcript profiling and cellular analysis. Plant J 40: 260–275 [PubMed]
  • Meimoun P, Tran D, Baz M, Errakhi R, Dauphin A, Lehner A, Briand J, Biligui B, Madiona K, Beaulieu C, et al. (2009) Two different signaling pathways for thaxtomin A-induced cell death in Arabidopsis and tobacco BY2. Plant Signal Behav 4: 142–144 [PMC free article] [PubMed]
  • Melida H, Garcia-Angulo P, Alonso-Simon A, Encina A, Alvarez J, Acebes JL. (2009) Novel type II cell wall architecture in dichlobenil-habituated maize calluses. Planta 229: 617–631 [PubMed]
  • Miyazaki S, Murata T, Sakurai-Ozato N, Kubo M, Demura T, Fukuda H, Hasebe M. (2009) ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization. Curr Biol 19: 1327–1331 [PubMed]
  • Monshausen GB, Bibikova TN, Messerli MA, Shi C, Gilroy S. (2007) Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc Natl Acad Sci USA 104: 20996–21001 [PMC free article] [PubMed]
  • Monshausen GB, Gilroy S. (2009) Feeling green: mechanosensing in plants. Trends Cell Biol 19: 228–235 [PubMed]
  • Monshausen GB, Messerli MA, Gilroy S. (2008) Imaging of the Yellow Cameleon 3.6 indicator reveals that elevations in cytosolic Ca2+ follow oscillating increases in growth in root hairs of Arabidopsis. Plant Physiol 147: 1690–1698 [PMC free article] [PubMed]
  • Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J. (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300: 332–336 [PubMed]
  • Moscatiello R, Mariani P, Sanders D, Maathuis FJ. (2006) Transcriptional analysis of calcium-dependent and calcium-independent signaling pathways induced by oligogalacturonides. J Exp Bot 57: 2847–2865 [PubMed]
  • Motose H, Sugiyama M, Fukuda H. (2004) A proteoglycan mediates inductive interaction during plant vascular development. Nature 429: 873–878 [PubMed]
  • Nakagami H, Pitzschke A, Hirt H. (2005) Emerging MAP kinase pathways in plant stress signaling. Trends Plant Sci 10: 339–346 [PubMed]
  • Nakagawa Y, Katagiri T, Shinozaki K, Qi Z, Tatsumi H, Furuichi T, Kishigami A, Sokabe M, Kojima I, Sato S, et al. (2007) Arabidopsis plasma membrane protein crucial for Ca2+ influx and touch sensing in roots. Proc Natl Acad Sci USA 104: 3639–3644 [PMC free article] [PubMed]
  • Nakhamchik A, Zhao Z, Provart NJ, Shiu SH, Keatley SK, Cameron RK, Goring DR. (2004) A comprehensive expression analysis of the Arabidopsis proline-rich extensin-like receptor kinase gene family using bioinformatic and experimental approaches. Plant Cell Physiol 45: 1875–1881 [PubMed]
  • Nemeth K, Salchert K, Putnoky P, Bhalerao R, Koncz-Kalman Z, Stankovic-Stangeland B, Bako L, Mathur J, Okresz L, Stabel S, et al. (1998) Pleiotropic control of glucose and hormone responses by PRL1, a nuclear WD protein, in Arabidopsis. Genes Dev 12: 3059–3073 [PMC free article] [PubMed]
  • Nishimura MT, Stein M, Hou BH, Vogel JP, Edwards H, Somerville SC. (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301: 969–972 [PubMed]
  • Nothnagel EA. (1997) Proteoglycans and related components in plant cells. Int Rev Cytol 174: 195–291 [PubMed]
  • Nuhse TS, Stensballe A, Jensen ON, Peck SC. (2004) Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. Plant Cell 16: 2394–2405 [PMC free article] [PubMed]
  • Palma K, Zhao Q, Cheng YT, Bi D, Monaghan J, Cheng W, Zhang Y, Li X. (2007) Regulation of plant innate immunity by three proteins in a complex conserved across the plant and animal kingdoms. Genes Dev 21: 1484–1493 [PMC free article] [PubMed]
  • Pena MJ, Ryden P, Madson M, Smith AC, Carpita NC. (2004) The galactose residues of xyloglucan are essential to maintain mechanical strength of the primary cell walls in Arabidopsis during growth. Plant Physiol 134: 443–451 [PMC free article] [PubMed]
  • Peng L, Xiang F, Roberts E, Kawagoe Y, Greve LC, Kreuz K, Delmer DP. (2001) The experimental herbicide CGA 325′615 inhibits synthesis of crystalline cellulose and causes accumulation of non-crystalline β-1,4-glucan associated with CesA protein. Plant Physiol 126: 981–992 [PMC free article] [PubMed]
  • Persson S, Wei H, Milne J, Page GP, Somerville CR. (2005) Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proc Natl Acad Sci USA 102: 8633–8638 [PMC free article] [PubMed]
  • Pickard BG, Fujiki M. (2005) Ca2+ pulsation in BY-2 cells and evidence for control of mechanosensory Ca2+-selective channels by the plasmalemmal reticulum. Funct Plant Biol 32: 863–879
  • Pilling E, Höfte H. (2003) Feedback from the wall. Curr Opin Plant Biol 6: 1–6 [PubMed]
  • Rentel MC, Lecourieux D, Ouaked F, Usher SL, Petersen L, Okamoto H, Knight H, Peck SC, Grierson CS, Hirt H, et al. (2004) OXI1 kinase is necessary for oxidative burst-mediated signaling in Arabidopsis. Nature 427: 858–861 [PubMed]
  • Roudier F, Fernandez AG, Fujita M, Himmelspach R, Borner GH, Schindelman G, Song S, Baskin TI, Dupree P, Wasteneys GO, et al. (2005) COBRA, an Arabidopsis extracellular glycosyl-phosphatidyl inositol-anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. Plant Cell 17: 1749–1763 [PMC free article] [PubMed]
  • Roy SJ, Holdaway-Clarke TL, Hackett GR, Kunkel JG, Lord EM, Hepler PK. (1999) Uncoupling secretion and tip growth in lily pollen tubes: evidence for the role of calcium in exocytosis. Plant J 19: 379–386 [PubMed]
  • Ryden P, Sugimoto-Shirasu K, Smith AC, Findlay K, Reiter WD, McCann MC. (2003) Tensile properties of Arabidopsis cell walls depend on both a xyloglucan cross-linked microfibrillar network and rhamnogalacturonan II-borate complexes. Plant Physiol 132: 1033–1040 [PMC free article] [PubMed]
  • Sanchez-Rodriguez C, Estevez JM, Llorente F, Hernandez-Blanco C, Jorda L, Pagan I, Berrocal M, Marco Y, Somerville S, Molina A. (2009) The ERECTA receptor-like kinase regulates cell wall-mediated resistance to pathogens in Arabidopsis thaliana. Mol Plant Microbe Interact 22: 953–963 [PubMed]
  • Scheible WR, Eshed R, Richmond T, Delmer D, Somerville C. (2001) Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis Ixr1 mutants. Proc Natl Acad Sci USA 98: 10079–10084 [PMC free article] [PubMed]
  • Scheible WR, Fry B, Kochevenko A, Schindelasch D, Zimmerli L, Somerville S, Loria R, Somerville CR. (2003) An Arabidopsis mutant resistant to thaxtomin A, a cellulose synthesis inhibitor from Streptomyces species. Plant Cell 15: 1781–1794 [PMC free article] [PubMed]
  • Seifert GJ. (2004) Nucleotide sugar interconversions and cell wall biosynthesis: how to bring the inside to the outside. Curr Opin Plant Biol 7: 277–284 [PubMed]
  • Seifert GJ, Barber C, Wells B, Roberts K. (2004) Growth regulators and the control of nucleotide sugar flux. Plant Cell 16: 723–730 [PMC free article] [PubMed]
  • Seifert GJ, Roberts K. (2007) The biology of arabinogalactan proteins. Annu Rev Plant Biol 58: 137–161 [PubMed]
  • Shahollari B, Peskan-Berghofer T, Oelmuller R. (2004) Receptor kinases with leucine-rich repeats are enriched in Triton X-100 insoluble plasma membrane microdomains from plants. Physiol Plant 122: 397–403
  • Shi H, Kim Y, Guo Y, Stevenson B, Zhu JK. (2003) The Arabidopsis SOS5 locus encodes a putative cell surface adhesion protein and is required for normal cell expansion. Plant Cell 15: 19–32 [PMC free article] [PubMed]
  • Shiu SH, Bleecker AB. (2001a) Plant receptor-like kinase gene family: diversity, function, and signaling. Sci STKE 2001: RE22. [PubMed]
  • Shiu SH, Bleecker AB. (2001b) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA 98: 10763–10768 [PMC free article] [PubMed]
  • Shiu SH, Bleecker AB. (2003) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132: 530–543 [PMC free article] [PubMed]
  • Showalter AM. (1993) Structure and function of plant-cell wall proteins. Plant Cell 5: 9–23 [PMC free article] [PubMed]
  • Shpak ED, Berthiaume CT, Hill EJ, Torii KU. (2004) Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation. Development 131: 1491–1501 [PubMed]
  • Shpak ED, Lakeman MB, Torii KU. (2003) Dominant-negative receptor uncovers redundancy in the Arabidopsis ERECTA leucine-rich repeat receptor-like kinase signaling pathway that regulates organ shape. Plant Cell 15: 1095–1110 [PMC free article] [PubMed]
  • Shpak ED, McAbee JM, Pillitteri LJ, Torii KU. (2005) Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309: 290–293 [PubMed]
  • Sivaguru M, Ezaki B, He ZH, Tong H, Osawa H, Baluska F, Volkmann D, Matsumoto H. (2003) Aluminum-induced gene expression and protein localization of a cell wall-associated receptor kinase in Arabidopsis. Plant Physiol 132: 2256–2266 [PMC free article] [PubMed]
  • Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osborne E, Paredez A, Persson S, Raab T, et al. (2004) Toward a systems approach to understanding plant cell walls. Science 306: 2206–2211 [PubMed]
  • Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L. (2008) Local positive feedback regulation determines cell shape in root hair cells. Science 319: 1241–1244 [PubMed]
  • Tedman-Jones JD, Lei R, Jay F, Fabro G, Li X, Reiter WD, Brearley C, Jones JD. (2008) Characterization of Arabidopsis mur3 mutations that result in constitutive activation of defence in petioles, but not leaves. Plant J 56: 691–703 [PubMed]
  • Tor M, Lotze MT, Holton N. (2009) Receptor-mediated signaling in plants: molecular patterns and programmes. J Exp Bot 60: 3645–3654 [PMC free article] [PubMed]
  • van Hengel AJ, Roberts K. (2003) AtAGP30, an arabinogalactan-protein in the cell walls of the primary root, plays a role in root regeneration and seed germination. Plant J 36: 256–270 [PubMed]
  • van Zanten M, Snoek LB, Proveniers MC, Peeters AJ. (2009) The many functions of ERECTA. Trends Plant Sci 14: 214–218 [PubMed]
  • Vogel JP, Raab TK, Schiff C, Somerville SC. (2002) PMR6, a pectate lyase-like gene required for powdery mildew susceptibility in Arabidopsis. Plant Cell 14: 2095–2106 [PMC free article] [PubMed]
  • Vogel JP, Raab TK, Somerville CR, Somerville SC. (2004) Mutations in PMR5 result in powdery mildew resistance and altered cell wall composition. Plant J 40: 968–978 [PubMed]
  • Wagner TA, Kohorn BD. (2001) Wall-associated kinases are expressed throughout plant development and are required for cell expansion. Plant Cell 13: 303–318 [PMC free article] [PubMed]
  • Willats WG, Knox JP. (1996) A role for arabinogalactan-proteins in plant cell expansion: evidence from studies on the interaction of β-glucosyl Yariv reagent with seedlings of Arabidopsis thaliana. Plant J 9: 919–925 [PubMed]
  • Winter H, Huber SC. (2000) Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Crit Rev Biochem Mol Biol 35: 253–289 [PubMed]
  • Xu SL, Rahman A, Baskin TI, Kieber JJ. (2008) Two leucine-rich repeat receptor kinases mediate signaling, linking cell wall biosynthesis and ACC synthase in Arabidopsis. Plant Cell 20: 3065–3079 [PMC free article] [PubMed]
  • Yang J, Sardar HS, McGovern KR, Zhang Y, Showalter AM. (2007) A lysine-rich arabinogalactan protein in Arabidopsis is essential for plant growth and development, including cell division and expansion. Plant J 49: 629–640 [PubMed]
  • Yariv J, Rapport MM, Graf L. (1962) The interaction of glycosides and saccharides with antibody to the corresponding phenylazo glycosides. Biochem J 85: 383–388 [PMC free article] [PubMed]
  • Zabotin AI, Barisheva TS, Trofimova OI, Toroschina TE, Larskaya IA, Zabotina OA. (2009) Oligosaccharin and ABA synergistically affect the acquisition of freezing tolerance in winter wheat. Plant Physiol Biochem 47: 854–858 [PubMed]
  • Zhong R, Demura T, Ye ZH. (2006) SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 18: 3158–3170 [PMC free article] [PubMed]
  • Zhong R, Kays SJ, Schroeder BP, Ye ZH. (2002) Mutation of a chitinase-like gene causes ectopic deposition of lignin, aberrant cell shapes, and overproduction of ethylene. Plant Cell 14: 165–179 [PMC free article] [PubMed]
  • Zhong R, Richardson EA, Ye ZH. (2007) The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell 19: 2776–2792 [PMC free article] [PubMed]
  • Zhu Y, Nam J, Carpita NC, Matthysse AG, Gelvin SB. (2003) Agrobacterium-mediated root transformation is inhibited by mutation of an Arabidopsis cellulose synthase-like gene. Plant Physiol 133: 1000–1010 [PMC free article] [PubMed]
  • Zipfel C. (2009) Early molecular events in PAMP-triggered immunity. Curr Opin Plant Biol 12: 414–420 [PubMed]

Articles from Plant Physiology are provided here courtesy of American Society of Plant Biologists
PubReader format: click here to try

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...