Signaling in cell expansion and morphogenesis

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Project Summary The integrity of cells is tightly controlled to keep organisms alive in the face of environmental change. The normal process of growth, however, requires that cells partly disrupt cellular structures that provide stability. These conflicting cellular priorities create challenges for cells in balancing integrity and extensibility. The root of Arabidopsis is adept at dynamically regulating growth in response to stressful environments such as salinity and provides a model developmental system where growth is localized to a specific region of the organ that is accessible to high-resolution imaging. Recent work has revealed that cell integrity during salt stress is maintained through the mechano-sensitive receptor-like kinase FERONIA. Identification of this essential regulatory pathway provides opportunities to understand the mechanism cells use to integrate information on cellular mechanics into decisions that control the biosynthesis of the extracellular matrix, which determines the growth potential of cells. Current understanding of how growth is organized in plants has largely focused on cellular contexts where tip- growth is predominant and wall biosynthesis is localized to a discrete focal area in the cell. This process is thought to be distinct from the major mode of cell growth in organs where delivery of new wall materials occurs in a distributed manner across the cell. New work presented here identifies an essential function for the FERONIA (FER) kinase in regulating the mechanical properties of the wall and cell integrity under salt stress. These findings suggest that dynamic regulation of wall biosynthesis by mechanical cues may be necessary to maintain cell integrity during stress. The project aims to elucidate the cellular mechanisms by which salinity disrupts cell integrity and the role of FERONIA in reorganizing the biosynthesis of the extracellular matrix to permit growth while maintaining cell integrity. To achieve this goal we will use high-resolution imaging approaches including light and force measurements and advanced proteomic methods that enable molecular insight into the biochemical pathways that link wall mechanics to intracellular signaling, cytoskeletal dynamics and ECM biosynthesis. Specifically we aim to 1) Understand the role of FER in regulating vesicle trafficking and dynamical properties of the actin and microtubule-based cytoskeleton to understand how these processes affect delivery of cargo for wall biosynthesis during stress. 2) FER-dependent intracellular calcium transients will be used as beacons of signaling activity to determine the cell-autonomy of FER function with respect to cell integrity and vesicle trafficking. 3) Quantitative phosphoproteomics will identify signaling components that directly interact with FER and the Rho-GTPase from Plants (ROPs) to link receptor activity to wall biosynthesis and calcium signaling. The proposed research is significant as it will advance our understanding of cellular homeostasis mechanisms that integrate mechanical and environmental stress cues using root growth as a model.