Increasing Plasma Membrane Phosphatidylinositol(4,5)Bisphosphate Biosynthesis Increases Phosphoinositide Metabolism in<i>Nicotiana tabacum</i>

Im, Young Jun; Perera, Imara Y.; Brglez, I.; Davis, Alison; Stevenson-Paulik, Jill; Phillippy, Brian Q.; Johannes, Eva; Allen, Nina S.; Boss, Wendy F.

doi:10.1105/tpc.107.051367

Cited by 67 publications

(79 citation statements)

References 74 publications

(109 reference statements)

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“…Using transgenic tobacco (Nicotiana tabacum) cells expressing a mammalian PIP5K, it was recently shown that PIP5K is the flux-limiting factor in the plant metabolic pathway that leads to PtdIns(4,5)P 2 production (Im et al, 2007b). In our study, reduced PIP5K3 expression levels in the mutant lines or increased levels following inducible overexpression caused significantly shorter or longer root hairs, respectively, than normal.…”

Section: Discussionmentioning

confidence: 57%

TheArabidopsisPhosphatidylinositol Phosphate 5-Kinase PIP5K3 Is a Key Regulator of Root Hair Tip Growth

et al. 2008

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Phosphatidylinositol 4,5-bisphosphate [PtdIns(4,5)P 2 ] functions as a site-specific signal on membranes to promote cytoskeletal reorganization and membrane trafficking. Localization of PtdIns(4,5)P 2 to apices of growing root hairs and pollen tubes suggests that it plays an important role in tip growth. However, its regulation and mode of action remain unclear. We found that Arabidopsis thaliana PIP5K3 (for Phosphatidylinositol Phosphate 5-Kinase 3) encodes a phosphatidylinositol 4-phosphate 5-kinase, a key enzyme producing PtdIns(4,5)P 2 , that is preferentially expressed in growing root hairs. T-DNA insertion mutations that substantially reduced the expression of PIP5K3 caused significantly shorter root hairs than in the wild type. By contrast, overexpression caused longer root hairs and multiple protruding sites on a single trichoblast. A yellow fluorescent protein (YFP) fusion of PIP5K3, driven by the PIP5K3 promoter, complemented the short-root-hair phenotype. PIP5K3-YFP localized to the plasma membrane and cytoplasmic space of elongating root hair apices, to growing root hair bulges, and, notably, to sites about to form root hair bulges. The signal was greatest in rapidly growing root hairs and quickly disappeared when elongation ceased. These results provide evidence that PIP5K3 is involved in localizing PtdIns(4,5)P 2 to the elongating root hair apex and is a key regulator of the machinery that initiates and promotes root hair tip growth.

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Section: Discussionmentioning

confidence: 57%

TheArabidopsisPhosphatidylinositol Phosphate 5-Kinase PIP5K3 Is a Key Regulator of Root Hair Tip Growth

et al. 2008

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“…Similar PI4P distribution was also found in root hairs (Vermeer et al, 2009). In plant cells, PI4P is the most abundant form of phosphoinositide (Im et al, 2007b). Genetic studies of enzymes involved in PI4P synthesis and degradation in root hairs have implicated PI4P in the regulation of polar exocytosis (Preuss et al, 2006;Thole et al, 2008).…”

Section: Pi4p May Participate In a Late Stage Of Clathrin-dependent Ementioning

confidence: 56%

Phosphoinositides Regulate Clathrin-Dependent Endocytosis at the Tip of Pollen Tubes inArabidopsisand Tobacco

et al. 2010

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Using the tip-growing pollen tube of Arabidopsis thaliana and Nicotiana tabacum as a model to investigate endocytosis mechanisms, we show that phosphatidylinositol-4-phosphate 5-kinase 6 (PIP5K6) regulates clathrin-dependent endocytosis in pollen tubes. Green fluorescent protein-tagged PIP5K6 was preferentially localized to the subapical plasma membrane (PM) in pollen tubes where it apparently converts phosphatidylinositol 4-phosphate (PI4P) to phosphatidylinositol 4,5-bisphosphate [PI(4,5)P 2 ]. RNA interference-induced suppression of PIP5K6 expression impaired tip growth and inhibited clathrin-dependent endocytosis in pollen tubes. By contrast, PIP5K6 overexpression induced massive aggregation of the PM in pollen tube tips. This PM abnormality was apparently due to excessive clathrin-dependent membrane invagination because this defect was suppressed by the expression of a dominant-negative mutant of clathrin heavy chain. These results support a role for PI(4,5)P 2 in promoting early stages of clathrin-dependent endocytosis (i.e., membrane invagination). Interestingly, the PIP5K6 overexpression-induced PM abnormality was partially suppressed not only by the overexpression of PLC2, which breaks down PI(4,5)P 2 , but also by that of PI4Kb1, which increases the pool of PI4P. Based on these observations, we propose that a proper balance between PI4P and PI(4,5)P 2 is required for clathrin-dependent endocytosis in the tip of pollen tubes.

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“…Data previously published on the effects of pollen-expressed PLCs on polar tip growth (Dowd et al, 2006;Helling et al, 2006) indicate that a balance between synthesis and degradation of PtdIns(4,5) P 2 must be maintained for formation of the dynamic PtdIns(4,5)P 2 microdomain and for proper pollen tube elongation. In addition, data from in vivo labeling experiments indicate that PtdIns(4,5)P 2 is turned over very rapidly (Perera et al, 2002;Im et al, 2007;Krinke et al, 2007), and that increased abundance of PI4P 5-kinases should, thus, unbalance the system and have immediate effects on pollen tube growth.…”

Section: Discussionmentioning

confidence: 99%

Type B Phosphatidylinositol-4-Phosphate 5-Kinases MediateArabidopsisandNicotiana tabacumPollen Tube Growth by Regulating Apical Pectin Secretion

Ischebeck¹,

Stenzel²,

Heilmann³

2008

The Plant Cell

177

262

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Phosphatidylinositol-4,5-bisphosphate [PtdIns(4,5)P 2 ] occurs in the apical plasma membrane of growing pollen tubes. Because enzymes responsible for PtdIns(4,5)P 2 production at that location are uncharacterized, functions of PtdIns(4,5)P 2 in pollen tube tip growth are unresolved. Two candidate genes encoding pollen-expressed Arabidopsis thaliana phosphatidylinositol-4-phosphate 5-kinases (PI4P 5-kinases) of Arabidopsis subfamily B were identified (PIP5K4 and PIP5K5), and their recombinant proteins were characterized as being PI4P 5-kinases. Pollen of T-DNA insertion lines deficient in both PIP5K4 and PIP5K5 exhibited reduced pollen germination and defects in pollen tube elongation. Fluorescence-tagged PIP5K4 and PIP5K5 localized to an apical plasma membrane microdomain in Arabidopsis and tobacco (Nicotiana tabacum) pollen tubes, and overexpression of either PIP5K4 or PIP5K5 triggered multiple tip branching events. Further studies using the tobacco system revealed that overexpression caused massive apical pectin deposition accompanied by plasma membrane invaginations. By contrast, callose deposition and cytoskeletal structures were unaltered in the overexpressors. Morphological effects depended on PtdIns(4,5)P 2 production, as an inactive enzyme variant did not produce any effects. The data indicate that excessive PtdIns(4,5)P 2 production by type B PI4P 5-kinases disturbs the balance of membrane trafficking and apical pectin deposition. Polar tip growth of pollen tubes may thus be modulated by PtdIns(4,5)P 2 via regulatory effects on membrane trafficking and/or apical pectin deposition.

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Increasing Plasma Membrane Phosphatidylinositol(4,5)Bisphosphate Biosynthesis Increases Phosphoinositide Metabolism inNicotiana tabacum

Cited by 67 publications

References 74 publications

TheArabidopsisPhosphatidylinositol Phosphate 5-Kinase PIP5K3 Is a Key Regulator of Root Hair Tip Growth

TheArabidopsisPhosphatidylinositol Phosphate 5-Kinase PIP5K3 Is a Key Regulator of Root Hair Tip Growth

Phosphoinositides Regulate Clathrin-Dependent Endocytosis at the Tip of Pollen Tubes inArabidopsisand Tobacco

Type B Phosphatidylinositol-4-Phosphate 5-Kinases MediateArabidopsisandNicotiana tabacumPollen Tube Growth by Regulating Apical Pectin Secretion

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