Function of WAKs in Regulating Cell Wall Development and Responses to Abiotic Stress

Abstract

Receptor-like kinases (RLKs) are instrumental in regulating plant cell surface sensing and vascular tissue differentiation. Wall-associated kinases (WAKs) are a unique group of RLKs that have been identified as key cell wall integrity (CWI) sensors. WAK signaling is suggested to be activated during growth in response to cell expansion or when the cell wall is damaged, for example, during pathogen attack. WAKs are proposed to interact with pectins or pectin fragments that are enriched in primary walls. Secondary walls have low levels of pectins, yet recent studies have shown important functions of WAKs during secondary wall development. Several wak mutants show defects in secondary wall thickening of the xylem vessels and fibers or the development of vascular bundles. This review will discuss the recent advances in our understanding of WAK functions during plant development and responses to abiotic stresses and the regulation of vascular tissue secondary wall development.

Keywords: cell wall integrity (CWI); oligogalacturonides; pectin; primary cell wall (PCW); secondary cell wall (SCW); wall-associated kinase (WAK).

Figure 1

A model for Arabidopsis and rice WAKs regulating primary and secondary wall signaling in plants. (A) In Arabidopsis, AtWAK1, Glycine-Rich Protein 3 (AtGRP-3), and Kinase-Associated Protein Phosphatase (KAPP) are associated with a multimeric complex of 500 kDa. WAK1 senses pectin fragments of oligogalacturonide (OG) and triggers a defense response that accumulates ROS through activation of NADPH oxidase AtRbohD and MAPK-mediated activation of defense gene expression. Pectin binding activates WAK kinase and the subsequent activation of Mitogen-activated Protein Kinase 3 (MPK3), leading to the regulation of genes involved in cell expansion. MPK6 is either repressed or not activated. AtWAKL4 interacts with and phosphorylates the Cd transporter protein Natural-Resistance-Associated Macrophage Protein 1 (NRAMP1), resulting in enhanced degradation of NRAMP1, which ultimately reduces Cd uptake. (B) AtWAKL14 and AtWAKL8 may interact with cell wall pectin, activating cytoplasmic kinases and downstream signaling pathways to regulate vascular tissue differentiation and SCW development via transcriptional networks, influencing stem and fruit development. (C) In rice, OsWAK11 was found to be capable of binding directly to the BR receptor brassinosteroid insensitive 1 (OsBRI1) and phosphorylate the receptor. OsWAK11 binding is proposed to compete with and prevent binding of the co-receptor Somatic Embryogenesis Receptor-like Kinase 1 (OsSERK1). Inhibition of the kinase Glycogen Synthase Kinase 3 (OsGSK3) allows the accumulation of the transcription factors Brassinazole Resistant 1 (OsBZR1) in a dephosphorylated active form and inhibits its activity. OsWAK11 demonstrated stability under light conditions but underwent degradation under dark conditions, thereby releasing the inhibition of OsBARI activity. OsWAK112 negatively regulates plant salt responses by inhibiting ethylene production, possibly via direct binding with S-adenosyl-L-methionine synthetase (SAMS) 1/2/3 (SAMS1/2/3). (D) OsWAK10 and OsXa4 interact with cell wall pectin, activating cytoplasmic kinases and downstream signaling pathways to regulate vascular tissue differentiation and SCW development via transcriptional networks.

Figure 2

Summary of expression patterns and biological functions of WAKs involved in secondary wall development in Arabidopsis and rice. Expression profiles of WAKs in shoot meristem, flower, silique, stem, leaf, and root, and transgenic plant phenotypes in Arabidopsis (A) and rice (B). Colored cells indicate tissue expression patterns of WAKs in vascular tissues.