Inositol Polyphosphate Phosphatidylinositol 5-Phosphatase9 (At5PTase9) Controls Plant Salt Tolerance by Regulating Endocytosis

• Published in: Molecular plant 2013-11, Vol.6 (6), p.1781-1794
• Main Authors: Golani, Yael, Kaye, Yuval, Gilhar, Omri, Ercetin, Mustafa, Gillaspy, Glenda, Levine, Alex
• Format: Article
• Language: English
• Subjects: abiotic/environmental stress; Adaptation, Physiological; Arabidopsis; Arabidopsis - enzymology; Arabidopsis - genetics; Arabidopsis - physiology; Calcium - metabolism; Endocytosis; Gene expression; Gene Expression Regulation, Enzymologic; Gene Expression Regulation, Plant; Ion Transport; Mutation; Osmotic Pressure; oxidative and photo-oxidative stress; Oxygen; Phosphoric Monoester Hydrolases - genetics; Phosphoric Monoester Hydrolases - metabolism; protein traffic and secretion; Reactive Oxygen Species - metabolism; salinity; Sodium Chloride
• ISSN: 1674-2052; 1752-9867
• DOI: 10.1093/mp/sst072

Phosphatidylinositol 5-phosphatases (5PTases) that hydrolyze the 5’ position of the inositol ring are key components of membrane trafficking system. Recently, we reported that mutation in At5PTase7 gene reduced production of reactive oxygen species (ROS) and decreased expression of stress-responsive genes, resulting in increased salt sensitivity. Here, we describe an even more salt-sensitive 5ptase mutant, At5ptase9, which also hydrolyzes the 5’ phosphate groups specifically from membrane-bound phosphatidylinositides. Interestingly, the mutants were more tolerant to osmotic stress. We analyzed the main cellular processes that may be affected by the mutation, such as production of ROS, influx of calcium, and induction of salt-response genes. The At5ptase9 mutants showed reduced ROS production and Ca2+ influx, as well as decreased fluid-phase endocytosis. Inhibition of endocytosis by phenylarsine oxide or Tyrphostin A23 in wild-type plants blocked these responses. Induction of salt-responsive genes in wild-type plants was also suppressed by the endocytosis inhibitors. Thus, inhibition of endocytosis in wild-type plants mimicked the salt stress responses, observed in the At5ptase9 mutants. In summary, our results show a key non-redundant role of At5PTase7 and 9 isozymes, and underscore the localization of membrane-bound PtdIns in regulating plant salt tolerance by coordinating the endocytosis, ROS production, Ca2+ influx, and induction of stress-responsive genes. The paper reveals a critical and essential role of specific membrane-associated phosphatidylinositol 5-phosphatases (5PTases) in regulating plant adaptation to abiotic stresses. We show that these 5PTases control membrane trafficking and production of reactive oxygen species, as well as stress gene expression.