Cell wall damage attenuates root hair patterning and tissue morphogenesis mediated by the receptor kinase STRUBBELIG

Abstract

Cell wall remodeling is essential for the control of growth and development as well as the regulation of stress responses. However, the underlying cell wall monitoring mechanisms remain poorly understood. Regulation of root hair fate and flower development in Arabidopsis thaliana requires signaling mediated by the atypical receptor kinase STRUBBELIG (SUB). Furthermore, SUB is involved in cell wall integrity signaling and regulates the cellular response to reduced levels of cellulose, a central component of the cell wall. Here, we show that continuous exposure to sub-lethal doses of the cellulose biosynthesis inhibitor isoxaben results in altered root hair patterning and floral morphogenesis. Genetically impairing cellulose biosynthesis also results in root hair patterning defects. We further show that isoxaben exerts its developmental effects through the attenuation of SUB signaling. Our evidence indicates that downregulation of SUB is a multi-step process and involves changes in SUB complex architecture at the plasma membrane, enhanced removal of SUB from the cell surface, and downregulation of SUB transcript levels. The results provide molecular insight into how the cell wall regulates cell fate and tissue morphogenesis.

The Arabidopsis MCTP member QUIRKY regulates the formation of the STRUBBELIG receptor kinase complex

“…QKY -mediated stabilization of SUB at the cell surface (Song et al , 2019; Chaudhary et al , 2021) (Fig. 6) counteracts the constitutive endocytosis and degradation of SUB (Gao et al , 2019; Song et al , 2019).…”

“…SUB controls root hair patterning, leaf development, floral organ shape, and ovule development (Chevalier et al, 2005;Kwak et al, 2005;Fulton et al, 2009;Lin et al, 2012). Recently, SUB has also been shown to be required for the stress response elicited by a reduction in cellulose biosynthesis (Chaudhary et al, 2020(Chaudhary et al, , 2021. Genetic evidence suggested that SUB functions as a scaffold protein in several cell surface signaling complexes (Vaddepalli et al, 2011;Chaudhary et al, 2021).…”

“…Recently, SUB has also been shown to be required for the stress response elicited by a reduction in cellulose biosynthesis (Chaudhary et al, 2020(Chaudhary et al, , 2021. Genetic evidence suggested that SUB functions as a scaffold protein in several cell surface signaling complexes (Vaddepalli et al, 2011;Chaudhary et al, 2021). In support of this notion SUB harbors an ECD with only six LRRs (Vaddepalli et al, 2011) and thus is akin to the ECD of known co-receptors, such as BRI1-ASSOCIATED RECEPTOR KINASE 1/SOMATIC EMBROYGENESIS RECEPTOR-LIKE KINASE 3 (BAK1/SERK3) that carries five LRRs (Li et al, 2002;Nam & Li, 2002).…”

“…Several lines of evidence suggest that QKY and SUB are components of a complex (Trehin et al , 2013; Vaddepalli et al , 2014; Song et al , 2019) and physically interact at plasmodesmata (PD) in epidermal root cells of young Arabidopsis seedlings (Vaddepalli et al , 2014). SUB undergoes constitutive clathrin-dependent endocytosis followed by degradation in the vacuole (Gao et al , 2019; Song et al , 2019) and QKY is also required for the stabilization of SUB at the cell surface (Song et al , 2019; Chaudhary et al , 2021). Apart from its function in SUB-dependent signaling, QKY has been reported to play other roles in growth and development.Genetic evidence indicates that QKY and its maize homolog Carbohydrate Partitioning Defective33 ( cpd33 ) play a role in sugar export from leaves and thus carbohydrate partitioning (Tran et al , 2019).…”

The regulation of the cell wall by glycosylphosphatidylinositol-anchored proteins in Arabidopsis

“…SUB is a non-cell-autonomous atypical Receptor-Like Kinase that controls tissue morphogenesis and responses to damaged cell wall integrity. Interestingly, the intracellular kinase domain is not required for its functions (Cha udhary et al, 2020;Chaudhary et al, 2021). Loss of function of ZET results in severe defection in the outer integuments development, floral organs morphogenesis, and stems anisotropic elongation, for which altered cell wall composition and structure might be responsible (Vaddepalli et al, 2017).…”