Arabidopsis pavement cell shape formation involves spatially confined ROPGAP regulators

• Published in: Current biology 2022-02, Vol.32 (3), p.532-544.e7
• Main Authors: Lauster, Theresa, Stöckle, Dorothee, Gabor, Katharina, Haller, Theresa, Krieger, Natalie, Lotz, Pia, Mayakrishnan, Ravikumar, Späth, Ellen, Zimmermann, Steffi, Livanos, Pantelis, Müller, Sabine
• Format: Article
• Language: English
• Subjects: Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; cell polarity signaling; Cell Shape; cytoskeleton; GTPase activating protein; microtubule; Microtubules - metabolism; morphogenesis; pavement cell; PHGAP; Plant Leaves - metabolism; rho GTP-Binding Proteins - genetics; rho GTP-Binding Proteins - metabolism; Rho-related GTPases from plants; ROP
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2021.12.042

In many plant species, pavement cell development relies on the coordinated formation of interdigitating lobes and indentations. Polarity signaling via the activity of antagonistic Rho-related GTPases from plants (ROPs) was implicated in pavement cell development, but the spatiotemporal regulation remained unclear. Here, we report on the role of the PLECKSTRIN HOMOLOGY GTPase ACTIVATING PROTEINS (PHGAPS) during multipolar growth in pavement cell shape establishment. Loss of function in phgap1phgap2 double mutants severely affected the shape of Arabidopsis leaf epidermal pavement cells. Predominantly, PHGAPs interacted with ROP2 and displayed a distinct and microtubule-dependent enrichment along the anticlinal cell face and transfacial boundary of pavement cell indentation regions. This localization was established upon undulation initiation and was maintained throughout the expansion of the cell. Our data suggest that PHGAP1/REN2 and PHGAP2/REN3 are key players in the establishment of ROP2 activity gradients and underscore the importance of locally controlled ROP activity for the orchestrated establishment of multipolarity in epidermal cells. •Two PHGAPs/RENs are required for multipolar pavement cell shape formation•Loss of PHGAPs elevates active ROP2 levels•Enrichment of PHGAPs on anticlinal faces of indentations is microtubule dependent•The distinct enrichment of PHGAPs requires their carboxyl-terminal domain How cells acquire complex shapes is a fundamental question in biology. Lauster et al. show that PHGAP/RENs associate with cortical microtubules preferentially along anticlinal cell faces, and they facilitate the spatially distinct deactivation of ROP2 in indentations. This interplay is essential for multipolarity of epidermal pavement cells.