SAC phosphoinositide phosphatases at the tonoplast mediate vacuolar function in Arabidopsis

Petra Nováková, Sibylle Hirsch, Elena Feraru, Ricardo Tejos, Ringo Van Wijk, Tom Viaene, Mareike Heilmann, Jennifer Lerche, Riet De Rycke, Mugurel I. Feraru, Peter Grones, Marc Van Montagu*, Ingo Heilmann, Teun Munnik, Jirí Frimla

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

58 Citations (Scopus)

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.
Original languageEnglish
Pages (from-to)2818-2823
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume111
Issue number7
DOIs
Publication statusPublished - 18 Feb 2014
Externally publishedYes

Keywords

  • Epidermal cells
  • Membrane fusion and fission
  • Membrane lipids

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