title: SAC phosphoinositide phosphatases at the tonoplast mediate vacuolar function in Arabidopsis.
abstract: Phosphatidylinositol (PtdIns) is a structural phospholipid that can be phosphorylated into various lipid signaling molecules, designated polyphosphoinositides (PPIs). The reversible phosphorylation of PPIs on the 3, 4, or 5 position of inositol is performed by a set of organelle-specific kinases and phosphatases, and the characteristic head groups make these molecules ideal for regulating biological processes in time and space. In yeast and mammals, PtdIns3P and PtdIns(3,5)P2 play crucial roles in trafficking toward the lytic compartments, whereas the role in plants is not yet fully understood. Here we identified the role of a land plant-specific subgroup of PPI phosphatases, the suppressor of actin 2 (SAC2) to SAC5, during vacuolar trafficking and morphogenesis in Arabidopsis thaliana. SAC2-SAC5 localize to the tonoplast along with PtdIns3P, the presumable product of their activity. In SAC gain- and loss-of-function mutants, the levels of PtdIns monophosphates and bisphosphates were changed, with opposite effects on the morphology of storage and lytic vacuoles, and the trafficking toward the vacuoles was defective. Moreover, multiple sac knockout mutants had an increased number of smaller storage and lytic vacuoles, whereas extralarge vacuoles were observed in the overexpression lines, correlating with various growth and developmental defects. The fragmented vacuolar phenotype of sac mutants could be mimicked by treating wild-type seedlings with PtdIns(3,5)P2, corroborating that this PPI is important for vacuole morphology. Taken together, these results provide evidence that PPIs, together with their metabolic enzymes SAC2-SAC5, are crucial for vacuolar trafficking and for vacuolar morphology and function in plants.
authors.affiliation: Institute of Science and Technology Austria, 3400 Klosterneuburg, Austria.
authors.forename: Petra
authors.initials: P
authors.lastname: Nováková
authors.forename: Sibylle
authors.initials: S
authors.lastname: Hirsch
authors.forename: Elena
authors.initials: E
authors.lastname: Feraru
authors.forename: Ricardo
authors.initials: R
authors.lastname: Tejos
authors.forename: Ringo
authors.initials: R
authors.lastname: van Wijk
authors.forename: Tom
authors.initials: T
authors.lastname: Viaene
authors.forename: Mareike
authors.initials: M
authors.lastname: Heilmann
authors.forename: Jennifer
authors.initials: J
authors.lastname: Lerche
authors.forename: Riet
authors.initials: R
authors.lastname: De Rycke
authors.forename: Mugurel I
authors.initials: MI
authors.lastname: Feraru
authors.forename: Peter
authors.initials: P
authors.lastname: Grones
authors.forename: Marc
authors.initials: M
authors.lastname: Van Montagu
authors.forename: Ingo
authors.initials: I
authors.lastname: Heilmann
authors.forename: Teun
authors.initials: T
authors.lastname: Munnik
authors.forename: Jirí
authors.initials: J
authors.lastname: Friml
mesh_terms: D017360:Arabidopsis / Q000201:enzymology* / Q000254:growth & development; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D017931:DNA Primers / Q000235:genetics; D019143:Evolution, Molecular; D046529:Microscopy, Electron, Transmission; D010641:Phenotype; D018129:Phosphatidylinositol Phosphates / Q000378:metabolism; D010749:Phosphoprotein Phosphatases / Q000235:genetics / Q000378:metabolism*; D030821:Plants, Genetically Modified; D060888:Real-Time Polymerase Chain Reaction; D014617:Vacuoles / Q000378:metabolism / Q000502:physiology / Q000648:ultrastructure
chemical_list: D029681:Arabidopsis Proteins; D017931:DNA Primers; D018129:Phosphatidylinositol Phosphates; D010749:Phosphoprotein Phosphatases
keywords: epidermal cells; membrane fusion and fission; membrane lipids