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SAC phosphoinositide phosphatases at the tonoplast mediate vacuolar function in Arabidopsis

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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)P-2 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)P-2, 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.
Keywords
PROTEIN, PLANT-CELLS, THALIANA, STRESS, ROOT GRAVITROPISM, MULTIVESICULAR BODY, MEMBRANE HOMEOSTASIS, PREVACUOLAR COMPARTMENTS, AUXIN EFFLUX CARRIER, 5-BISPHOSPHATE, PHOSPHATIDYLINOSITOL 3, membrane fusion and fission, epidermal cells, membrane lipids

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MLA
Novakova, Petra, et al. “SAC Phosphoinositide Phosphatases at the Tonoplast Mediate Vacuolar Function in Arabidopsis.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, vol. 111, no. 7, 2014, pp. 2818–23, doi:10.1073/pnas.1324264111.
APA
Novakova, P., Hirsch, S., Feraru, E., Tejos Ulloa, R., van Wijk, R., Viaene, T., … Friml, J. (2014). SAC phosphoinositide phosphatases at the tonoplast mediate vacuolar function in Arabidopsis. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 111(7), 2818–2823. https://doi.org/10.1073/pnas.1324264111
Chicago author-date
Novakova, Petra, Sibylle Hirsch, Elena Feraru, Ricardo Tejos Ulloa, Ringo van Wijk, Tom Viaene, Mareike Heilmann, et al. 2014. “SAC Phosphoinositide Phosphatases at the Tonoplast Mediate Vacuolar Function in Arabidopsis.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 111 (7): 2818–23. https://doi.org/10.1073/pnas.1324264111.
Chicago author-date (all authors)
Novakova, Petra, Sibylle Hirsch, Elena Feraru, Ricardo Tejos Ulloa, Ringo van Wijk, Tom Viaene, Mareike Heilmann, Jennifer Lerche, Riet De Rycke, Ioan Mugurel Feraru, Peter Grones, Marc Van Montagu, Ingo Heilmann, Teun Munnik, and Jiri Friml. 2014. “SAC Phosphoinositide Phosphatases at the Tonoplast Mediate Vacuolar Function in Arabidopsis.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 111 (7): 2818–2823. doi:10.1073/pnas.1324264111.
Vancouver
1.
Novakova P, Hirsch S, Feraru E, Tejos Ulloa R, van Wijk R, Viaene T, et al. SAC phosphoinositide phosphatases at the tonoplast mediate vacuolar function in Arabidopsis. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 2014;111(7):2818–23.
IEEE
[1]
P. Novakova et al., “SAC phosphoinositide phosphatases at the tonoplast mediate vacuolar function in Arabidopsis,” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, vol. 111, no. 7, pp. 2818–2823, 2014.
@article{4362717,
  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)P-2 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)P-2, 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.}},
  author       = {{Novakova, Petra and Hirsch, Sibylle and Feraru, Elena and Tejos Ulloa, Ricardo and van Wijk, Ringo and Viaene, Tom and Heilmann, Mareike and Lerche, Jennifer and De Rycke, Riet and Feraru, Ioan Mugurel and Grones, Peter and Van Montagu, Marc and Heilmann, Ingo and Munnik, Teun and Friml, Jiri}},
  issn         = {{0027-8424}},
  journal      = {{PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA}},
  keywords     = {{PROTEIN,PLANT-CELLS,THALIANA,STRESS,ROOT GRAVITROPISM,MULTIVESICULAR BODY,MEMBRANE HOMEOSTASIS,PREVACUOLAR COMPARTMENTS,AUXIN EFFLUX CARRIER,5-BISPHOSPHATE,PHOSPHATIDYLINOSITOL 3,membrane fusion and fission,epidermal cells,membrane lipids}},
  language     = {{eng}},
  number       = {{7}},
  pages        = {{2818--2823}},
  title        = {{SAC phosphoinositide phosphatases at the tonoplast mediate vacuolar function in Arabidopsis}},
  url          = {{http://dx.doi.org/10.1073/pnas.1324264111}},
  volume       = {{111}},
  year         = {{2014}},
}

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