Diffuse Growth of Plant Cell Walls

Abstract

The primary wall of a growing cell is a versatile, subtle, and dynamic structure, with unique properties and functions in the life of the plant (Burton et al., 2010). When a cell grows, its wall stretches irreversibly as the cell enlarges in volume. Cells can start and stop this process quickly, in less than a minute in some cases, revealing that the molecular processes underlying irreversible wall expansion are dynamically controlled. Such dynamic behavior may be mediated, at least in part, by changes in wall pH (Hager, 2003; Barbez et al., 2017), which modulates the wall-loosening action of expansins (Cosgrove, 2015) and potentially other wall-modifying agents. Wall pH in turn is dynamically modulated by plasma membrane H+-ATPase activity (Haruta et al., 2014, 2015) and other processes in the wall. Because growing cell walls are thin and in close physical contact with plasma membranes, wall pH can be rapidly modulated (Bibikova et al., 1998; Monshausen et al., 2007; Barbez et al., 2017). As a result of the pH-dependent activity of expansins, the growing cell wall behaves like a “smart material”—one whose properties (extensibility in this case) reversibly and rapidly change with environment (e.g. pH). Slower changes in wall structure that influence the wall’s ability to expand also occur as part of the natural course of cell development, e.g. as cells are displaced through the elongation zone of a stem (Phyo et al., 2017), or in response to external perturbations, e.g. Sahaf and Sharon (2016). These slower changes may include changes in mechanics, such as wall stiffening, and in the density or accessibility of sites where expansins or other proteins can loosen the wall. The wall itself is synthesized in a team effort: mobile cellulose synthesis complexes (Paredez et al., 2006; Li et al., 2016b) produce long, thin, strong, stiff cellulose microfibrils at the cell surface, while matrix polysaccharides and glycoproteins are deposited to the cell surface via the secretory apparatus (Zhu et al., 2015; Kim and Brandizzi, 2016). The cytoskeleton guides the wall synthesis machinery to supply wall components to appropriate locations on the cell surface (Szymanski and Staiger, 2017), where the components assemble to form an organized, mechanically strong structure that can withstand the in-plane tensile forces generated by the outward push of cell turgor pressure yet is able to expand in a controlled manner. The structural requirements for orderly expansion of the cell wall are not well defined at this time. Moreover, except with the possible exception of tip-growing cells (Dumais et al., 2006; Rojas et al., 2011), synthesis, secretion, and wall assembly are only distantly coupled to the wall extension process itself. For instance, cellulose synthesis in carbon-limited Arabidopsis (Arabidopsis thaliana) hypocotyls was temporally distinct from cell expansion (Ivakov et al., 2017); likewise, wall deposition did not keep up with cell expansion in dark-grown hypocotyls, resulting in substantial wall thinning (Refrégier et al., 2004). On the other hand, gradients in wall thickness in the growing trichome of Arabidopsis precisely matched predictions for mechanical stability of the wall, implying good coordination between local wall deposition and expansion (Yanagisawa et al., 2015). We still have much to learn about how plant cells build a stable yet extensible wall. When the normal molecular assembly of the cell wall is disturbed, for instance, by mutations that affect synthesis of cellulose (Fagard et al., 2000), xyloglucan (Cavalier et al., 2008), or pectic polysaccharides (Mouille et al., 2007), cell expansion may be disrupted in unpredictable ways. Genetic results suggest that errors in wall assembly trigger surface receptor-like kinases such as FERONIA that may act as sensors of cell wall integrity (CWI; Humphrey et al., 2007; Höfte, 2015) and mechanosensation (Hamant and Haswell, 2017). The ensuing responses, which include production of reactive oxygen species and inactivation of the plasma membrane H+-ATPase, likely give rise to some of the complex phenotypes that originate from rather simple modifications of wall polysaccharides (Voxeur and Höfte, 2016). For example, growth defects stemming from mutation of a cellulose synthase gene in Arabidopsis were partially suppressed by mutation of THESEUS1 (Hématy et al., 2007), another member of the same receptor kinase family as FERONIA (Cheung and Wu, 2011; Li et al., 2016a). Evidently, CWI responses compound and confound the direct effects of cell wall defects. Defects in pectin metabolism appear particularly prone to trigger CWI responses that activate the brassinosteroid pathway, leading to diverse growth phenotypes (Wolf et al., 2012, 2014). On the other hand, FERONIA and its extracellular peptide ligand (“rapid alkalinization factor”) are also required for normal root growth and auxin responses (Haruta et al., 2014; Shih et al., 2014; Velasquez et al., 2016; Barbez