Comparative analyses of extracellular matrix proteome: an under-explored area in plant research

Abstract

Within their social milieu, cells are petite and deformable, enclosed in a flimsy plasma membrane which swerves from their default spherical shape to more polar shapes due to the local deposition, complex interactions and the remodelling of the extracellular matrix (ECM). Consequently, multicellularity has evolved, albeit independently in plants and animals. Although animals are truly multicellular, plants are supracellular organisms because their immobile cells divide via phragmoplast-based incomplete cytokinesis, which results in the formation of cytoplasmic cell-to-cell channels known as plasmodesmata (Baluska et al., 2003). The ECM in plants, often referred as the cell wall, is integrated into the apoplast—a structurally coherent superstructure extending throughout the plant body. In lieu, plant cells are not fully separated and both the plasma membrane and endoplasmic reticulum traverse cellular borders through plasmodesmata (Baluska et al., 2003; Fincher, G. 2009.). The ECM is a fundamental component of the microenvironment of both animal and plant cells that has been substantially expanded during evolution. Throughout the plant kingdom, the formation and regulation of the ECM architecture has been shown to have the potential to influence many conduits of development, position-dependent differentiation, patterning and totipotent cell niches, besides environmental stress response and pathobiology (Brownlee & Berger, 1995; Degenhardt & Gimmer, 2000; Wilson, 2010). Furthermore, it has been reported that the ECM plays an important morphoregulatory role during somatic embryogenesis and organogenesis in plants, besides its pivotal role in cellular osmo- and volume-regulation (Šamaj et al., 1999; Rose et al., 2004). The plant ECM has biomechanical and morphogenetic functions with the immense ability to turn cells into hydraulic machines which establish a crucial functional difference between cell walls and other cellular surface structures. It encloses the cell hermetically and constrains the hydrostatic pressure evoked by osmotic gradients between the cell and its environment which controls cellular osmo- and volume-regulation (Peters et al., 2000; Cosgrove, D. J. 2005). Plasticity in the ECM allows the cellular uptake of massive amounts of water into a central vacuole while rigidity in the ECM determines the conductance of enormous amounts of water and dissolved solutes through vascular bundles. The secretion of an ECM by one cell can also influence the neighbouring cells, conceivably the best exemplified paracrine interaction known in the plant kingdom (for a review, see Brownlee, 2002). Beyond their paramount importance in the generation of form, cell walls are frequently considered ‘growth-controlling’ (Wolf et al., 2009). Cells devoid of the ECM inevitably lose their polar shape and the loss of cellular polarisation prevents cell-to-cell interactions and communication. The ECM/cell wall is evolutionary and inherently bestowed with information that can be both stored and relayed to cell interior via templating processes. It serves as the first line mediator in cell signalling for perceiving and transmitting extra- and intercellular signals in many cellular pathways. Communication between the cytoplasm and the cell wall is necessary and evident because of events such as cell expansion (Cosgrove, 1997, Schröder, F et al 2009), mechanical stress (Kumar et al., 2006; Telewski, 2006), environmental perturbation (Gail McLean et al., 1997; Thelen, J. and Peck, S. 2007) and pathogen infection (Hammond- Kosack & Jones, 1996) which lead to altered biosynthesis and the modification of wall components and downstream cytoplasmic events. In addition, it can act as a substrate for migration and has also been recognised as a surrogate for providing inputs into cell behaviour (Hall et al., 2002), although the available data is rather scarce for higher plants and critical linker molecules between the cytoskeleton and the ECM are still missing. Thus, the ECM/cell wall primarily serves a dual function, as a cell support system and for signalling during development and stress. The ECM/cell wall must therefore be dynamic as cells divide and elongate, modulating its composition and architecture during its synthesis and after it has been deposited. The wall function is a multi-step, complex process and the underlying mechanisms governing these steps are not fully understood.