title: The IQD Family of Calmodulin-Binding Proteins Links Calcium Signaling to Microtubules, Membrane Subdomains, and the Nucleus.
abstract: Calcium (Ca2+) signaling and dynamic reorganization of the cytoskeleton are essential processes for the coordination and control of plant cell shape and cell growth. Calmodulin (CaM) and closely related calmodulin-like (CML) polypeptides are principal sensors of Ca2+signals. CaM/CMLs decode and relay information encrypted by the second messenger via differential interactions with a wide spectrum of targets to modulate their diverse biochemical activities. The plant-specific IQ67 DOMAIN (IQD) family emerged as possibly the largest class of CaM-interacting proteins with undefined molecular functions and biological roles. Here, we show that the 33 members of the IQD family in Arabidopsis (Arabidopsis thaliana) differentially localize, using green fluorescent protein (GFP)-tagged proteins, to multiple and distinct subcellular sites, including microtubule (MT) arrays, plasma membrane subdomains, and nuclear compartments. Intriguingly, the various IQD-specific localization patterns coincide with the subcellular patterns of IQD-dependent recruitment of CaM, suggesting that the diverse IQD members sequester Ca2+-CaM signaling modules to specific subcellular sites for precise regulation of Ca2+-dependent processes. Because MT localization is a hallmark of most IQD family members, we quantitatively analyzed GFP-labeled MT arrays inNicotiana benthamianacells transiently expressing GFP-IQD fusions and observed IQD-specific MT patterns, which point to a role of IQDs in MT organization and dynamics. Indeed, stable overexpression of select IQD proteins in Arabidopsis altered cellular MT orientation, cell shape, and organ morphology. Because IQDs share biochemical properties with scaffold proteins, we propose that IQD families provide an assortment of platform proteins for integrating CaM-dependent Ca2+signaling at multiple cellular sites to regulate cell function, shape, and growth.
authors.affiliation: Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, 06120 Halle (Saale), Germany (K.B., R.P., G.S., D.M., S.A.); katharina.buerstenbinder@ipb-halle.de.|Institute of Computer Science (B.M.), Biocenter (G.H.), and Institute of Biochemistry and Biotechnology (S.A.), Martin Luther University Halle-Wittenberg, 06120 Halle (Saale), Germany; and katharina.buerstenbinder@ipb-halle.de.|Department of Plant Sciences, University of California, Davis, California 95616 (S.A.) katharina.buerstenbinder@ipb-halle.de.
authors.forename: Katharina
authors.identifier: 0000-0002-3493-4800
authors.initials: K
authors.lastname: Bürstenbinder
authors.affiliation: Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, 06120 Halle (Saale), Germany (K.B., R.P., G.S., D.M., S.A.).|Institute of Computer Science (B.M.), Biocenter (G.H.), and Institute of Biochemistry and Biotechnology (S.A.), Martin Luther University Halle-Wittenberg, 06120 Halle (Saale), Germany; and.|Department of Plant Sciences, University of California, Davis, California 95616 (S.A.).
authors.forename: Birgit
authors.identifier: 0000-0002-7146-043X
authors.initials: B
authors.lastname: Möller
authors.affiliation: Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, 06120 Halle (Saale), Germany (K.B., R.P., G.S., D.M., S.A.).|Institute of Computer Science (B.M.), Biocenter (G.H.), and Institute of Biochemistry and Biotechnology (S.A.), Martin Luther University Halle-Wittenberg, 06120 Halle (Saale), Germany; and.|Department of Plant Sciences, University of California, Davis, California 95616 (S.A.).
authors.forename: Romina
authors.initials: R
authors.lastname: Plötner
authors.affiliation: Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, 06120 Halle (Saale), Germany (K.B., R.P., G.S., D.M., S.A.).|Institute of Computer Science (B.M.), Biocenter (G.H.), and Institute of Biochemistry and Biotechnology (S.A.), Martin Luther University Halle-Wittenberg, 06120 Halle (Saale), Germany; and.|Department of Plant Sciences, University of California, Davis, California 95616 (S.A.).
authors.forename: Gina
authors.initials: G
authors.lastname: Stamm
authors.affiliation: Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, 06120 Halle (Saale), Germany (K.B., R.P., G.S., D.M., S.A.).|Institute of Computer Science (B.M.), Biocenter (G.H.), and Institute of Biochemistry and Biotechnology (S.A.), Martin Luther University Halle-Wittenberg, 06120 Halle (Saale), Germany; and.|Department of Plant Sciences, University of California, Davis, California 95616 (S.A.).
authors.forename: Gerd
authors.initials: G
authors.lastname: Hause
authors.affiliation: Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, 06120 Halle (Saale), Germany (K.B., R.P., G.S., D.M., S.A.).|Institute of Computer Science (B.M.), Biocenter (G.H.), and Institute of Biochemistry and Biotechnology (S.A.), Martin Luther University Halle-Wittenberg, 06120 Halle (Saale), Germany; and.|Department of Plant Sciences, University of California, Davis, California 95616 (S.A.).
authors.forename: Dipannita
authors.initials: D
authors.lastname: Mitra
authors.affiliation: Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, 06120 Halle (Saale), Germany (K.B., R.P., G.S., D.M., S.A.).|Institute of Computer Science (B.M.), Biocenter (G.H.), and Institute of Biochemistry and Biotechnology (S.A.), Martin Luther University Halle-Wittenberg, 06120 Halle (Saale), Germany; and.|Department of Plant Sciences, University of California, Davis, California 95616 (S.A.).
authors.forename: Steffen
authors.initials: S
authors.lastname: Abel
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D002118:Calcium / Q000378:metabolism; D020013:Calcium Signaling; D002147:Calmodulin / Q000235:genetics / Q000378:metabolism; D002148:Calmodulin-Binding Proteins / Q000235:genetics / Q000378:metabolism*; D002467:Cell Nucleus / Q000235:genetics / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant; D049452:Green Fluorescent Proteins / Q000235:genetics / Q000378:metabolism; D021962:Membrane Microdomains / Q000378:metabolism*; D018613:Microscopy, Confocal; D008870:Microtubules / Q000378:metabolism*; D005810:Multigene Family; D018515:Plant Leaves / Q000235:genetics / Q000378:metabolism; D030821:Plants, Genetically Modified; D011485:Protein Binding; D020133:Reverse Transcriptase Polymerase Chain Reaction
chemical_list: D029681:Arabidopsis Proteins; D002147:Calmodulin; D002148:Calmodulin-Binding Proteins; C503424:IQD1 protein, Arabidopsis; D049452:Green Fluorescent Proteins; D002118:Calcium