Irritable Walls: The Plant Extracellular Matrix and Signaling

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 resistanc