Rapid Structural Changes and Acidification of Guard Cell Vacuoles during Stomatal Closure Require Phosphatidylinositol 3,5-Bisphosphate

Bak, Gwangbae; Lee, Eunjung; Lee, Yuree; Kato, Mariko; Segami, Shoji; Sze, Heven; Maeshima, Masayoshi; Hwang, Jae‐Ung; Lee, Youngsook

doi:10.1105/tpc.113.110411

Cited by 120 publications

(123 citation statements)

References 87 publications

(117 reference statements)

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“…This process is best studied in guard cells. Stomatal opening is partly caused by vacuolar convolution (Zouhar and Rojo, 2009;Bak et al, 2013). The conditions that induce stomatal closing result in fragmentation of the central vacuole and loss of guard cell turgor.…”

Section: Discussionmentioning

confidence: 99%

Adjustment of Host Cells for Accommodation of Symbiotic Bacteria: Vacuole Defunctionalization, HOPS Suppression, and TIP1g Retargeting in Medicago

et al. 2014

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In legume-rhizobia symbioses, the bacteria in infected cells are enclosed in a plant membrane, forming organelle-like compartments called symbiosomes. Symbiosomes remain as individual units and avoid fusion with lytic vacuoles of host cells. We observed changes in the vacuole volume of infected cells and thus hypothesized that microsymbionts may cause modifications in vacuole formation or function. To examine this, we quantified the volumes and surface areas of plant cells, vacuoles, and symbiosomes in root nodules of Medicago truncatula and analyzed the expression and localization of VPS11 and VPS39, members of the HOPS vacuole-tethering complex. During the maturation of symbiosomes to become N 2 -fixing organelles, a developmental switch occurs and changes in vacuole features are induced. For example, we found that expression of VPS11 and VPS39 in infected cells is suppressed and host cell vacuoles contract, permitting the expansion of symbiosomes. Trafficking of tonoplast-targeted proteins in infected symbiotic cells is also altered, as shown by retargeting of the aquaporin TIP1g from the tonoplast membrane to the symbiosome membrane. This retargeting appears to be essential for the maturation of symbiosomes. We propose that these alterations in the function of the vacuole are key events in the adaptation of the plant cell to host intracellular symbiotic bacteria.

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Section: Discussionmentioning

confidence: 99%

Adjustment of Host Cells for Accommodation of Symbiotic Bacteria: Vacuole Defunctionalization, HOPS Suppression, and TIP1g Retargeting in Medicago

et al. 2014

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“…For instance, the perturbation of PIP5K2 (Stenzel et al, 2012) or PIP5K10 and PIP5K11 (Ischebeck et al, 2011) results in altered actin dynamics and the loss of cellular polarity. Yet a different category of phenotypes indicates that 3-phosphorylated PIs, which are perturbed by altered levels of VPS34 (Lee et al, 2008a,b), Fab1-like proteins (Bak et al, 2013) or SAC2-SAC5 (Novakova et al, 2014), might be involved in endomembrane trafficking and the control of vacuolar functions. The overall scheme suggests that PIs are involved in controlling the central machinery for membrane trafficking and protein sorting in plants.…”

Section: Pi Functions In Plantsmentioning

confidence: 99%

Phosphoinositide signaling in plant development

2016

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The membranes of eukaryotic cells create hydrophobic barriers that control substance and information exchange between the inside and outside of cells and between cellular compartments. Besides their roles as membrane building blocks, some membrane lipids, such as phosphoinositides (PIs), also exert regulatory effects. Indeed, emerging evidence indicates that PIs play crucial roles in controlling polarity and growth in plants. Here, I highlight the key roles of PIs as important regulatory membrane lipids in plant development and function.

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“…Impairment of genes implicated in PtdIns(3,5)P 2 metabolism has deleterious consequences in yeast, plants, and mammals (8, 15-19), demonstrating an essential function of this minor phospholipid. Recent observations also hint at a role for PPIs in plant vacuoles (18)(19)(20), but the data are scarce and remain inconclusive.Advances in deciphering various cellular roles of PIs include insights into the phosphatases responsible for hydrolyzing PPIs. A group of phosphatases, designated suppressor of actin (SAC) domain phosphatases, has been identified in lower eukaryotes, mammals, and plants (21).…”

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confidence: 99%

SAC phosphoinositide phosphatases at the tonoplast mediate vacuolar function in Arabidopsis

Nováková

Hirsch

Feraru

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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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.membrane lipids | epidermal cells | membrane fusion and fission P olyphosphoinositides (PPIs) are a class of signaling membrane lipids, comprising the phosphorylated products of phosphatidylinositol (PtdIns). PPIs perform a dual function as scaffolding signals and precursors for other molecular messengers, which, together with their specific distribution at different intracellular membranes, makes PPIs important mediators of a wide variety of cellular processes, such as membrane trafficking and homeostasis, cytoskeleton organization, nuclear signaling, and stress responses (1-5). The metabolism of PPIs is regulated by specific kinases, phosphatases, and phospholipases to tightly control the concentration and intracellular localization of different lipid pools (2, 6, 7).In yeast, two phosphoinositide (PI) types, PtdIns3P and PtdIns (3,5)P 2 , and their interconversion have been shown to play crucial roles in trafficking toward the vacuole, regulation of vacuolar pH, and vacuolar membrane fusion and fission (8-11). In yeast and mammals, production and degradation of PtdIns(3,5)P 2 involve the PtdIns3P 5-kinase Fab1p/PIKfyve and the antagonistic phosphatase factor-induced gene/suppressor of actin 3 (Fig4/ Sac3), respectively (8,(12)(13)(14). Impairment of genes implicated in PtdIns(3,5)P 2 metabolism ...

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Rapid Structural Changes and Acidification of Guard Cell Vacuoles during Stomatal Closure Require Phosphatidylinositol 3,5-Bisphosphate

Cited by 120 publications

References 87 publications

Adjustment of Host Cells for Accommodation of Symbiotic Bacteria: Vacuole Defunctionalization, HOPS Suppression, and TIP1g Retargeting in Medicago

Adjustment of Host Cells for Accommodation of Symbiotic Bacteria: Vacuole Defunctionalization, HOPS Suppression, and TIP1g Retargeting in Medicago

Phosphoinositide signaling in plant development

SAC phosphoinositide phosphatases at the tonoplast mediate vacuolar function in Arabidopsis

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