Wall-Associated Kinases Are Expressed throughout Plant Development and Are Required for Cell Expansion

Abstract

The mechanism by which events in the angiosperm cell wall are communicated to the cytoplasm is not well characterized. A family of five Arabidopsis wall-associated kinases (WAKs) have the potential to provide a physical and signaling continuum between the cell wall and the cytoplasm. The WAKs have an active cytoplasmic protein kinase domain, span the plasma membrane, and contain an N terminus that binds the cell wall. We show here that WAK s are expressed at organ junctions, in shoot and root apical meristems, in expanding leaves, and in response to wall disturbances. Leaves expressing an antisense WAK gene have reduced WAK protein levels and exhibit a loss of cell expansion. WAKs are covalently bound to pectin in the cell wall, providing evidence that the binding of a structural carbohydrate by a receptor-like kinase may have significance in the control of cell expansion. INTRODUCTIONIn animal, fungal, and algal systems, the physical connection and the communication between the extracellular matrix (ECM) and the cell plays a fundamental role in cell growth and division (Fowler and Quatrano, 1997;Lukashev and Werb, 1998;Tsai, 1998). Similarly, the plant cell wall forms an ECM of carbohydrate and protein that provides structure for individual cells and whole organs. The cell wall must be dynamic as cells divide and elongate, and modulation of its composition and architecture is required during its synthesis and after it has been deposited (Cosgrove, 1997;Reiter, 1998). The wall must therefore be considered in the context of modulating plant development (Kohorn, 2000). Communication between the cytoplasm and the cell wall is necessary and evident because events like cell expansion (Cosgrove, 1997) and pathogen infection (Hammond-Kosack and Jones, 1996) lead to altered biosynthesis and modification of cell wall components and downstream cytoplasmic events such as systemic acquired resistance. How the dynamics and synthesis of the cell wall are coordinated with cytoplasmic events is largely uncharacterized.Developing cells have walls that are composed of cellulose, hemicellulose, pectin, and proteins. Cellulose is directly secreted by cellulose synthase into the ECM, where it assembles with hemicelluloses and pectins, which are produced in the endomembrane system and secreted by vesicles. The cell wall also includes endoglucanases (Hayashi et al., 1984; Zuo et al., 2000), xyloglucan endotransglycosylases (Fry et al., 1992;Vissenberg et al., 2000), expansins (McQueen-Mason et al., 1992; Cho and Cosgrove, 2000), and a number of other glycosyl transferases that alter carbohydrate linkages and modify secreted cell wall components. Other cell wall proteins, some of which are heavily glycosylated, have been proposed as structural cell wall components or have been implicated in mediating multiple aspects of plant development (reviewed in: Showalter, 1993; Cosgrove, 1997;Kohorn, 2000). These include the families of proline-rich proteins, glycine-rich proteins, hydroxyprolinerich glycoproteins, and arabinogalactan proteins...

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