Journal Article

POLAR-guided signalling complex assembly and localization drive asymmetric cell division

Boeren, Sjef, Mena, Montaña, Russinova, Eugenia, de Marcos Serrano, Alberto, Zhang, Cheng, Gudesblat, Gustavo E., Houbaert, Anaxi, Wang, Kun, Betti, Camilla, Eeckhout, Dominique, Karimi, Mansour, Urs, Mounashree J., Jacobs, Thomas, Savatin, Daniel V., Zhiponova, Miroslava K., Fenoll, Carmen, De Jaeger, Geert, Tiwari, Manish, Vanhoutte, Isabelle, de Vries, Sacco

2018

Overview

Stomatal cell lineage is an archetypal example of asymmetric cell division (ACD), which is necessary for plant survival 1 – 4 . In Arabidopsis thaliana , the GLYCOGEN SYNTHASE KINASE3 (GSK3)/SHAGGY-like kinase BRASSINOSTEROID INSENSITIVE 2 (BIN2) phosphorylates both the mitogen-activated protein kinase (MAPK) signalling module 5 , 6 and its downstream target, the transcription factor SPEECHLESS (SPCH) 7 , to promote and restrict ACDs, respectively, in the same stomatal lineage cell. However, the mechanisms that balance these mutually exclusive activities remain unclear. Here we identify the plant-specific protein POLAR as a stomatal lineage scaffold for a subset of GSK3-like kinases that confines them to the cytosol and subsequently transiently polarizes them within the cell, together with BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE (BASL), before ACD. As a result, MAPK signalling is attenuated, enabling SPCH to drive ACD in the nucleus. Moreover, POLAR turnover requires phosphorylation on specific residues, mediated by GSK3. Our study reveals a mechanism by which the scaffolding protein POLAR ensures GSK3 substrate specificity, and could serve as a paradigm for understanding regulation of GSK3 in plants. POLAR, identified in a survey of the protein interactome of BRASSINOSTEROID INSENSITIVE 2 in Arabidopsis thaliana , has a key role in coordinating cell polarity and enabling asymmetric cell division.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 14/35 / 14/63 / 631/449 / 631/449/2124 / 64 / 82 / 82/80 / 82/83 / Arabidopsis / Arabidopsis - cytology / Arabidopsis - enzymology / Arabidopsis - metabolism / Arabidopsis Proteins - metabolism / Arabidopsis thaliana / Asymmetric Cell Division / Asymmetry / Basic Helix-Loop-Helix Transcription Factors - metabolism / Biochemie / Biochemistry / Cell cycle / Cell Cycle Proteins - metabolism / Cell division / Cell Lineage / Cell Polarity / Cloning / CRISPR / Cytosol / Cytosol - enzymology / Cytosol - metabolism / Genomes / Glycogen / Glycogen synthase kinase 3 / Glycogen Synthase Kinase 3 - metabolism / Glycogen synthesis / Humanities and Social Sciences / Kinases / Letter / Localization / MAP kinase / MAP Kinase Signaling System / Mitogens / multidisciplinary / Multiprotein Complexes - chemistry / Multiprotein Complexes - metabolism / Observations / Phenotype / Phosphorylation / Physiological aspects / Plant cells / Plant Stomata - cytology / Polysaccharides / Protein Binding / Protein kinase / Protein kinases / Protein Kinases - metabolism / Proteins / Scaffolding / Science / Science (multidisciplinary) / Signal Transduction / Signaling / Steroids (Organic compounds) / Stomata / Substrate Specificity / Substrates / Transcription factors