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Regulation of ROP signaling in cell division and cell expansion by a small ROPGAP family

Applicant Dr. Sabine Müller
Subject Area Plant Cell and Developmental Biology
Term from 2015 to 2024
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 277031791
 
Final Report Year 2024

Final Report Abstract

A fundamental property of life is control over cell shape, which is essential for the morphology and physiology across diverse organisms. In plants, the key factors of cellular morphogenesis are the orientation of cell division and the direction/polarity of cell expansion. These cellular processes provide the basis of complex, three-dimensional organ development, tissue functionality, and adaptation to changing environmental conditions. The cytoskeleton, a dynamically organized internal scaffolding structure, directly or indirectly via feedback mechanisms involving the cell wall, determine cell shape. The cytoskeleton plays an important role in cell division and growth by establishing division planes, separating chromosomes, and coordinating directional vesicle transport during cytokinesis. In addition, the cytoskeleton supports unidirectional (anisotropic) and multipolar cell growth in interphase. Over the years, my group has significantly contributed to the understanding of division plane orientation in plants, a long-standing research question captivating scientists since 19th century. In the root meristem of Arabidopsis thaliana, we have characterized the function and localization of PLECKSTRIN HOMOLOGY GTPase ACTIVATING (PHGAP) proteins. We showed that they control the placement of kinesin-12 class motor proteins PHRAGMOPLAST ORIENTING KINESIN 1 (POK1) and POK2. These are key components of the division zone at the cell cortex, that guide the cytokinetic apparatus during late cytokinesis. We were able to confirm PHGAPs somewhat surprising involvement in cell division, as well as reveal their canonical functions during leave epidermal cell development. We documented for the first time the function of PHGAPs in cell division and polarized cell expansion, implying that plant cells utilize similar polarization mechanisms in both processes. Beyond doubt, we establish PHGAPs as genuine and specific regulators of Rho related of plants 2 (ROP2). A fascinating and yet unexplored facet of PHGAPs is their remarkable specificity for ROP2 over ROP6 in the context of polarized growth of pavement cells. In addition, we gained insight into the phospho-regulation of PHGAPs by the activity of Brassinosteroid regulated kinases, BIN2 and Arabidopsis thaliana SHAGGY/GSK3-like kinase (AtSK). During leaf development, their activity stabilizes PHGAPs at the plasma membrane, thereby promoting localized ROP2 inhibition on commencing indentations of the undulating pavement cells. Intriguingly, our results indicate that plant cells utilize polarization modules involving PHGAPs in cell division and during cell expansion. Collectively, our work contributes to a better understanding of the molecular mechanisms that determine cell morphology and helps to understand their impact on plant development and morphology.

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