Year: 2010
Type: review
Abstract: 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). ↑, induction of; ↓, suppression of; as, antisense suppression; ASR, abiotic stress resistance; AXS, UDP-apiose/UDP-xylose synthase; CalS, callose synthase; CD, cell death, both programmed and necrotic; CE, cellulose; CesA, cellulose synthase catalytic subunit; CH, carbohydrates; DCB, 2,6-dichlorobenzonitrile; DR, disease resistance and reduced pathogen susceptibility; ET, ethylene; EXT, extensin; GM, glucomannan; GMD, GDP-d-mannose 4,6-dehydratase; HSR, hypersensitive to sugar; JA, jasmonic acid; PE, pectin; PME, pectin methyl esterase; SA, salicylic acid. ↑, induction of; ↓, suppression of; as, antisense suppression; ASR, abiotic stress resistance; AXS, UDP-apiose/UDP-xylose synthase; CalS, callose synthase; CD, cell death, both programmed and necrotic; CE, cellulose; CesA, cellulose synthase catalytic subunit; CH, carbohydrates; DCB, 2,6-dichlorobenzonitrile; DR, disease resistance and reduced pathogen susceptibility; ET, ethylene; EXT, extensin; GM, glucomannan; GMD, GDP-d-mannose 4,6-dehydratase; HSR, hypersensitive to sugar; JA, jasmonic acid; PE, pectin; PME, pectin methyl esterase; SA, salicylic acid. 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 levels to restore cell wall structure and performance to the “correct” parameters. Superimposed influences of cell cycle, cell type, cellular context, and developmental stage that determine the correct parameters have been deliberately omitted to emphasize the circular nature of this control system. Ψp, Turgor pressure. The cell wall provides countless potential sources of information. High-M r 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-M r 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. 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 and The binding of an extracellular a alteration to the activation of the protein a cascade of signal transduction are involved in aspects of cell wall structure and the of kinases are known at present to directly bind to a cell wall initially (Kohorn et al., to the cell wall and is specifically at the plasma wall et al., In are to pectic homogalacturonan and bind to OGs in vitro and 2005), important factors involved in normal of the with cell et al., and et al., and for and et al., 2003; et al., 2005), and pathogen resistance and et al., 2009). important biological the to their of are their and is required for growth (Kohorn et al., and the growth is by or and by expression of the role of in normal growth with and osmotic control. is required for the normal expression of an and from This might that cues regarding cell wall properties into the control that the correct of carbohydrates required for growth both as and as compounds (Kohorn et al., might be the and it be transduced to The is by the of pectin to in a (Kohorn et al., 2009), that the degree of pectin binding might determine The that factors influencing the conformation of pectin determine pectin binding to the extracellular domain in vitro and Cabrera et al., might that sense pectin conformation in However, the nature of the between and the cell wall is (Kohorn et al., In it that to the cell is in an in a related to the this is the cellular site the is to be of depends on biosynthesis that is required for or AGPs but for the of a order structure into the wall matrix polymer family of receptor proteins in cell wall signaling is termed as its Arabidopsis a extracellular domain to et al., 2004). are a of extracellular proteins of the with most glycosylated by to are in the by et al., 2008), and to pectin and AGPs by to the of with might of the of However, with of are from the extracellular domain of alteration of expression influences growth and cell wall et al., is specifically required for the of and for normal in and The protein is an protein kinase at the plasma and its from plant is by et al., 2009). The present that might with cell wall polymers and also in cell wall and growth regulator signaling at the receptor level as to of signal transduction roles of genes remain to be The of in The and and genes have been with functions in cell wall integrity control and growth in a et al., 2007; et al., 2009). other of the by the and the of a role related to but also related to cell wall integrity control et al., et al., 2009). mutations of the cell and in cellulose while the that might be a of cell wall function and integrity control et al., 2007). the roles of and for cell to be is for cell the growth of mutants. of in suppression of growth than in that might act as for other et al., 2009). to the genetic also plays an important role in the to growth et al., 2007). Hence, at and can act both as and of cell on the genetic It is to this by the that cell wall performance and integrity control acts cell walls are damaged but also during normal at in the Arabidopsis genome, receptor kinases the largest the of receptor-like kinases and 2003). genes for as as et al., and et al., most for are and are of family that a functional kinase domain et al., 2007; et al., 2009). in and loci to developmental defects and in of various genes related to cell wall growth regulator and abiotic It that and loci might function in or pathways involved in cell wall integrity control et al., 2009). in cell wall biosynthesis and function to their transcriptional with cell genes et al., 2007). The family is involved in many different aspects of development (for review, see et al., 2009). of and act in an as by the effect of and et al., is required for cell wall during the wild-type response a pathogen and, in for normal cell wall et al., 2009). This that might be involved in cell wall performance and integrity control of the of cell wall but is that might sense cell wall fragments by pathogen et al., 2009). In a genetic investigation of family of the of of and to display and cell defects et al., 2008), of various cell wall structural mutants such as et al., 2005), et al., et al., and et al., 2003). and mutants from in mutants display the as the and This nonadditive as and acting in the pathway as et al., 2003). It that the is with the and that both proteins with the unexpected observations that proteins play a role in cell wall as between cell wall and signal might be by an and act as a novel second The between and to be binding between the domain of and the domain of of the on the and a between the and cell wall polymers on the other might and cell wall Many are with AGPs while several are in et al., that also AGPs et al., are generally to represent membrane lipid (for review, see and 2010). Hence, the between and AGPs might be by their into lipid A of potential cell wall sensors are the and 2009) by a family of Arabidopsis several to bind the et al., a present in various extracellular matrix proteins but in plant cell wall of this plasma membrane during et al., the in cell wall It might be to binding of the extracellular domain to cell wall carbohydrates; this as in the proteins are and 2009). Hence, of remain to be As the plasma membrane is to the cell wall by turgor pressure, the of mechanical at the plasma wall might be a to cell wall integrity and performance to the cell for cell wall stress might be into a signal is of receptor on cell wall polymers to the extracellular matrix protein and 2009). In principle, or other receptor kinases might be to this A more of turgor is the in response to plasma membrane or Arabidopsis to the and the gene and are for plasma membrane in a role of the genes for plant growth and the specific have to be et al., 2008). A involved in plasma membrane is and its et al., 2007). the in a and its expression in plant is with plasma membrane and is required for into with mechanical It is to that alterations in mechanical cell wall properties during growth and abiotic stress might be as a in plasma membrane and proteins are the for molecular components of the plasma membrane system. is known on the molecular of receptor kinases plants et al., et al., 2009), genetic in many signaling from receptor kinases to protein kinase et al., act in the signal transduction of extracellular stimuli in all and of types of protein In response to stimuli such as growth abiotic and developmental an kinase kinase and a kinase that in a various such as transcription level of protein kinases is to act on of the of is relatively the of signaling at the transcriptional level is an (for review, see and 2008). There is that the of pectin or pectin fragments by signaling. The protein kinase of are is for the rapid activation of and for alterations in including activation of the (Kohorn et al., 2009). this might of a the of on the response to pectin in the mutant is quite (Kohorn et al., potential at the cellular or the plant level. a of a more growth that is by a (Kohorn et al., of by pectin in a are transcription involved in protein or related to cell wall biosynthesis and The in response to pectin of wild-type and relatively in with of cells with OGs et al., One for this might in the that with while cells stress might affect pectin conformation by the cell wall and in a and an osmotic Hence, a that can be from the available might pectin to to the activation of other such as its most closely related via and and in the activation of transcription factors stress osmotic and cell wall biosynthesis and this of events from of cell wall structure to signal transduction to transcription to modulation of signal signal osmotic cell wall biosynthesis, and remodeling an of a regulatory of cell wall integrity control as in the (Fig. 1). the activation of and can be detected by of are also at the level. Therefore, it is that studies different aspects of cell wall integrity control, application of OGs et al., or with AGP integrity by and Nothnagel, specific of cascade components and and and of while for of and and in both studies cells used and at a the might be for the observed However, it is to that in to the stress response by the activation of specific of and is required for the of the responses to different types of cell wall protein kinase acting in cell wall stress signal transduction is et al., 2004). is by It is also by and by the expression it a level. expression or more between and of kinase activity also by and and levels and a occurring with is required for and activation of and et al., 2004). The more activation by with might be due to roles of in the et al., and might be in the as well as host-associated molecular patterns such as the to cellulose structure to turgor might be a molecules such as and various other and can act as of or second often by binding to and specific proteins such as or in cell wall integrity such as binding of to AGPs trigger rapid of et al., and the response to cell wall-derived elicitors et al., the other the an that is required for the responses to cellulose biosynthesis inhibition (Hamann et al., 2009), and various of cell by genetic and with AGP structure than or the dynamic of second in response to specific structural stimuli in from the cell wall remain to be artificial of second might be involved in cell wall signaling might be from developmental and growth have been and the of the appropriate position for the to the of the and cell wall remodeling to the of an of and growth the of cell wall and cell wall remodeling at the of the and both the and growth processes have to be to the of cell wall structure and growth an that might of cell wall and together with extracellular in a to growth but its by and et al., 2008). One for this is that a of rapid cell wall is at the level of the plasma an of by the production of and of the The signal might cell wall suppression of both and production can cells to et al., 2003; et al., 2008). might initially be by that respond to membrane in a cell wall growth As and act in a during growth et al., 2008), an of production that might by a et al., cell wall is by cell wall As to discussed stress signaling pathways but with the of the observed this of growth control might act on a posttranslational level. However, it is quite that cell wall signals also involve and in a that depends on gene One is the of OGs to as well as alterations in the et al., is the that responses in by and cell wall stress and 2009). such as and act as signals from their role in (for review, see and 2009). signaling is and with all signaling such as growth regulator and light signal transduction in Therefore, it is that signaling also with cell wall performance and integrity control. the cell wall matrix structural mutants and are such a et al., 2007). or is required for many responses to inhibition of cellulose and most of the responses to cellulose biosynthesis while (Hamann et al., 2009). This is of the role of the that many responses to in the of activity et al., 2003). signaling the signaling of numerous growth et al., its role in cell wall performance and integrity control to be gene important for signaling is to has a regulatory influencing growth regulator response et al., and innate et al., 2007) and response to et al., 2009). of as inhibition of on et al., 2007). a of genes in the by This is with the that many transcription by with AGPs and Nothnagel, or by inhibition of cellulose and 2009), are also by of et al., 2009). this that signaling via and via might modulate cell wall signaling The of cell wall mutants from genetic that initially at other such as disease resistance or and growth regulator signaling important to the role of cell wall structure in various aspects of signaling. defects in cell wall polymers often to the activation or modulation of numerous stress responses such as or genes and resistance to various (Table I). The unexpected of observed responses might have several that are of plant of cell types to or of cell wall stress such as genetic or inhibition with cellulose, hemicellulose, pectin, or with other such as or carbohydrate and compounds that modulate and different of the various from relatively that can have to mutant studies The of individual parameters has been it be to the role of growth regulator signaling pathways for the responses such as transcriptional and posttranscriptional of cell wall biosynthesis and the it that the typical of an cell wall integrity and performance control machinery is the alteration of transcriptional related to cell wall biosynthesis and remodeling (Table I). However, most of is known at present about the transcriptional of cell wall biosynthesis or remodeling from such as et al., 2006; and 2007; et al., 2008; for review, see et al., 2007) or is on the that genes involved in a are et al., et al., for posttranslational modulation of cell wall biosynthesis is generally and 2000; et al., 2004; 2004; et al., The identification of transcription factors and posttranslational processes cell wall biosynthesis and remodeling is an important of In this have the for the of the of structural alterations of the plant cell wall on many aspects of plant life. The of in cell wall integrity and performance are or such stimuli are into appropriate control responses are expected to be highly and a components have the different types of the of proteins provides the for cell wall signaling. to and is by OGs and pectin, to the activation of and to transcriptional alterations of cell wall biosynthesis and remodeling as well as stress signaling. other are in to be for their extracellular and The of of the and to cell wall performance and turgor to be The of a set of can effect the transcription of the correct set of cell and genes to be and cell wall transcription factors have to be identified. the life and walls of plant cells are more than of yeast of many signal transduction and transcriptional involved in various aspects of cell wall performance and integrity control for on the
Source: PLANT PHYSIOLOGY
Authors: Georg J. Seifert, Claudia Blaukopf
Institution: BOKU University
Language: English
Subfield: Plant Science
Domain: Life Sciences
Open Access status: bronze
Funder: Austrian Science Fund
OpenAlex ID: W2111283875