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A Sec14p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thaliana root hairs.

Vincent P, Chua M, Nogue F, Fairbrother A, Mekeel H, Xu Y, Allen N, Bibikova TN, Gilroy S, Bankaitis VA - J. Cell Biol. (2005)

Bottom Line: Derangement of tip-directed Ca2+ gradients is also apparent and results from isotropic influx of Ca2+ from the extracellular milieu.We propose AtSfh1p regulates intracellular and plasma membrane phosphoinositide polarity landmarks that focus membrane trafficking, Ca2+ signaling, and cytoskeleton functions to the growing root hair apex.We further suggest that Sec14p-nodulin domain proteins represent a family of regulators of polarized membrane growth in plants.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell and Developmental Biology, Michael Hooker Microscopy Facility, University of North Carolina School of Medicine, Chapel Hill, NC 27599, USA. patrick_vincent@med.unc.edu

ABSTRACT
Phosphatidylinositol (PtdIns) transfer proteins (PITPs) regulate signaling interfaces between lipid metabolism and membrane trafficking. Herein, we demonstrate that AtSfh1p, a member of a large and uncharacterized Arabidopsis thaliana Sec14p-nodulin domain family, is a PITP that regulates a specific stage in root hair development. AtSfh1p localizes along the root hair plasma membrane and is enriched in discrete plasma membrane domains and in the root hair tip cytoplasm. This localization pattern recapitulates that visualized for PtdIns(4,5)P2 in developing root hairs. Gene ablation experiments show AtSfh1p izygosity compromises polarized root hair expansion in a manner that coincides with loss of tip-directed PtdIns(4,5)P2, dispersal of secretory vesicles from the tip cytoplasm, loss of the tip f-actin network, and manifest disorganization of the root hair microtubule cytoskeleton. Derangement of tip-directed Ca2+ gradients is also apparent and results from isotropic influx of Ca2+ from the extracellular milieu. We propose AtSfh1p regulates intracellular and plasma membrane phosphoinositide polarity landmarks that focus membrane trafficking, Ca2+ signaling, and cytoskeleton functions to the growing root hair apex. We further suggest that Sec14p-nodulin domain proteins represent a family of regulators of polarized membrane growth in plants.

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A model for AtSfh1p-mediated control of polarized membrane growth in developing A. thaliana root hairs. AtSfh1p stimulates PIP synthesis on secretory vesicles and thereby drives f-actin assembly for polarized trafficking to the root hair tip. We propose this PIP synthesis involves a coupling of AtSfh1p with PtdIns kinases or PLD and PtdIns-4-phosphate 5-kinase, or both. Polarized vesicle trafficking generates a tip-directed plasma membrane PtdIns(4,5)P2 gradient and localized Ca2+ influx at the tip plasma membrane, presumably due to tip-restricted insertion of secretory vesicles carrying Ca2+ channels. The Ca2+ gradient guides spatial organization of cortical MTs in consolidation of tip growth. We posit the primary (1°) defect in Atsfh1::T-DNA root hairs is collapse of this PtdIns(4,5)P2/f-actin control of polarized membrane trafficking. This secondarily (2°) results in isotropic Ca2+ influx into the root hair. Disorganization of tip-directed cytoplasmic Ca2+ gradients deranges the cortical MT cytoskeleton as a tertiary effect (3°).
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fig9: A model for AtSfh1p-mediated control of polarized membrane growth in developing A. thaliana root hairs. AtSfh1p stimulates PIP synthesis on secretory vesicles and thereby drives f-actin assembly for polarized trafficking to the root hair tip. We propose this PIP synthesis involves a coupling of AtSfh1p with PtdIns kinases or PLD and PtdIns-4-phosphate 5-kinase, or both. Polarized vesicle trafficking generates a tip-directed plasma membrane PtdIns(4,5)P2 gradient and localized Ca2+ influx at the tip plasma membrane, presumably due to tip-restricted insertion of secretory vesicles carrying Ca2+ channels. The Ca2+ gradient guides spatial organization of cortical MTs in consolidation of tip growth. We posit the primary (1°) defect in Atsfh1::T-DNA root hairs is collapse of this PtdIns(4,5)P2/f-actin control of polarized membrane trafficking. This secondarily (2°) results in isotropic Ca2+ influx into the root hair. Disorganization of tip-directed cytoplasmic Ca2+ gradients deranges the cortical MT cytoskeleton as a tertiary effect (3°).

Mentions: Root hair development requires polarized membrane growth from a precise position on the root epidermal cell plasma membrane. Herein, we demonstrate that loss of AtSfh1p, a PtdCho- and PtdIns-binding/transfer protein with the ability to regulate PIP metabolism, deranges root hair growth. AtSfh1p dysfunction compromises tip-directed plasma membrane PtdIns(4,5)P2 and Ca2+ gradients, elicits tip actin defects, and disorganizes root hair MT networks. The result is a derangement of polarized membrane growth after the site of root hair emergence has been correctly specified. We propose the primary function of AtSfh1p is to generate PIP landmarks that couple to components of the f-actin cytoskeleton, thereby focusing membrane delivery to the root hair tip plasma membrane. The polarized secretory pathway restricts insertion of cargo (e.g., ion channels) to the root hair apex, thereby establishing a tip-directed Ca2+ gradient. This gradient cues an organized MT assembly that further reinforces and maintains tip-directed membrane trafficking (Fig. 9).


A Sec14p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thaliana root hairs.

Vincent P, Chua M, Nogue F, Fairbrother A, Mekeel H, Xu Y, Allen N, Bibikova TN, Gilroy S, Bankaitis VA - J. Cell Biol. (2005)

A model for AtSfh1p-mediated control of polarized membrane growth in developing A. thaliana root hairs. AtSfh1p stimulates PIP synthesis on secretory vesicles and thereby drives f-actin assembly for polarized trafficking to the root hair tip. We propose this PIP synthesis involves a coupling of AtSfh1p with PtdIns kinases or PLD and PtdIns-4-phosphate 5-kinase, or both. Polarized vesicle trafficking generates a tip-directed plasma membrane PtdIns(4,5)P2 gradient and localized Ca2+ influx at the tip plasma membrane, presumably due to tip-restricted insertion of secretory vesicles carrying Ca2+ channels. The Ca2+ gradient guides spatial organization of cortical MTs in consolidation of tip growth. We posit the primary (1°) defect in Atsfh1::T-DNA root hairs is collapse of this PtdIns(4,5)P2/f-actin control of polarized membrane trafficking. This secondarily (2°) results in isotropic Ca2+ influx into the root hair. Disorganization of tip-directed cytoplasmic Ca2+ gradients deranges the cortical MT cytoskeleton as a tertiary effect (3°).
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2171805&req=5

fig9: A model for AtSfh1p-mediated control of polarized membrane growth in developing A. thaliana root hairs. AtSfh1p stimulates PIP synthesis on secretory vesicles and thereby drives f-actin assembly for polarized trafficking to the root hair tip. We propose this PIP synthesis involves a coupling of AtSfh1p with PtdIns kinases or PLD and PtdIns-4-phosphate 5-kinase, or both. Polarized vesicle trafficking generates a tip-directed plasma membrane PtdIns(4,5)P2 gradient and localized Ca2+ influx at the tip plasma membrane, presumably due to tip-restricted insertion of secretory vesicles carrying Ca2+ channels. The Ca2+ gradient guides spatial organization of cortical MTs in consolidation of tip growth. We posit the primary (1°) defect in Atsfh1::T-DNA root hairs is collapse of this PtdIns(4,5)P2/f-actin control of polarized membrane trafficking. This secondarily (2°) results in isotropic Ca2+ influx into the root hair. Disorganization of tip-directed cytoplasmic Ca2+ gradients deranges the cortical MT cytoskeleton as a tertiary effect (3°).
Mentions: Root hair development requires polarized membrane growth from a precise position on the root epidermal cell plasma membrane. Herein, we demonstrate that loss of AtSfh1p, a PtdCho- and PtdIns-binding/transfer protein with the ability to regulate PIP metabolism, deranges root hair growth. AtSfh1p dysfunction compromises tip-directed plasma membrane PtdIns(4,5)P2 and Ca2+ gradients, elicits tip actin defects, and disorganizes root hair MT networks. The result is a derangement of polarized membrane growth after the site of root hair emergence has been correctly specified. We propose the primary function of AtSfh1p is to generate PIP landmarks that couple to components of the f-actin cytoskeleton, thereby focusing membrane delivery to the root hair tip plasma membrane. The polarized secretory pathway restricts insertion of cargo (e.g., ion channels) to the root hair apex, thereby establishing a tip-directed Ca2+ gradient. This gradient cues an organized MT assembly that further reinforces and maintains tip-directed membrane trafficking (Fig. 9).

Bottom Line: Derangement of tip-directed Ca2+ gradients is also apparent and results from isotropic influx of Ca2+ from the extracellular milieu.We propose AtSfh1p regulates intracellular and plasma membrane phosphoinositide polarity landmarks that focus membrane trafficking, Ca2+ signaling, and cytoskeleton functions to the growing root hair apex.We further suggest that Sec14p-nodulin domain proteins represent a family of regulators of polarized membrane growth in plants.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell and Developmental Biology, Michael Hooker Microscopy Facility, University of North Carolina School of Medicine, Chapel Hill, NC 27599, USA. patrick_vincent@med.unc.edu

ABSTRACT
Phosphatidylinositol (PtdIns) transfer proteins (PITPs) regulate signaling interfaces between lipid metabolism and membrane trafficking. Herein, we demonstrate that AtSfh1p, a member of a large and uncharacterized Arabidopsis thaliana Sec14p-nodulin domain family, is a PITP that regulates a specific stage in root hair development. AtSfh1p localizes along the root hair plasma membrane and is enriched in discrete plasma membrane domains and in the root hair tip cytoplasm. This localization pattern recapitulates that visualized for PtdIns(4,5)P2 in developing root hairs. Gene ablation experiments show AtSfh1p izygosity compromises polarized root hair expansion in a manner that coincides with loss of tip-directed PtdIns(4,5)P2, dispersal of secretory vesicles from the tip cytoplasm, loss of the tip f-actin network, and manifest disorganization of the root hair microtubule cytoskeleton. Derangement of tip-directed Ca2+ gradients is also apparent and results from isotropic influx of Ca2+ from the extracellular milieu. We propose AtSfh1p regulates intracellular and plasma membrane phosphoinositide polarity landmarks that focus membrane trafficking, Ca2+ signaling, and cytoskeleton functions to the growing root hair apex. We further suggest that Sec14p-nodulin domain proteins represent a family of regulators of polarized membrane growth in plants.

Show MeSH
Related in: MedlinePlus