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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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Tissue-specific AtSfh1p expression. Otherwise wild-type transgenic plants stained for GUS expressed from a promoterless construct (A) or the AtSFH1 promoter (PAtSFH1::GUS) (B). (C) PAtSFH1::GUS expression is robust in root. Arrows denote GUS-active trichoblast cell files. (D) Root hair producing epidermal cell files (arrows) exhibit robust PAtSFH1::GUS expression. (E) GUS activity is recorded both in trichoblast cell bodies and root hairs. Arrows denote cell plates. PAtSFH1::GUS activity in cotyledon hydathodes (F), apical shoot meristem (G), and apical cells of the root cap (H). Bars: (A and B) 0.12 cm; (C–H) 50 μm.
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fig3: Tissue-specific AtSfh1p expression. Otherwise wild-type transgenic plants stained for GUS expressed from a promoterless construct (A) or the AtSFH1 promoter (PAtSFH1::GUS) (B). (C) PAtSFH1::GUS expression is robust in root. Arrows denote GUS-active trichoblast cell files. (D) Root hair producing epidermal cell files (arrows) exhibit robust PAtSFH1::GUS expression. (E) GUS activity is recorded both in trichoblast cell bodies and root hairs. Arrows denote cell plates. PAtSFH1::GUS activity in cotyledon hydathodes (F), apical shoot meristem (G), and apical cells of the root cap (H). Bars: (A and B) 0.12 cm; (C–H) 50 μm.

Mentions: Sec14p-nodulin domain proteins are uncharacterized and expansion of this family suggests tissue-specific functions for its members. AtSfh1p was chosen for detailed analysis because the AtSfh1p-LBD is most homologous to Sec14p. RT-PCR analyses indicated essentially root-specific expression of AtSFH1 (unpublished data), a result in accord with microarray data (http://www.cbs.umn.edu/arabidopsis/). β-Glucuronidase (GUS) histochemical staining confirmed and extended these results. AtSFH1 was expressed solely in root trichoblast cell files engaged in root hair growth (Fig. 3, C–E), hydathodes, shoot apical meristem, and apical cells of the root cap (Fig. 3, F–H).


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)

Tissue-specific AtSfh1p expression. Otherwise wild-type transgenic plants stained for GUS expressed from a promoterless construct (A) or the AtSFH1 promoter (PAtSFH1::GUS) (B). (C) PAtSFH1::GUS expression is robust in root. Arrows denote GUS-active trichoblast cell files. (D) Root hair producing epidermal cell files (arrows) exhibit robust PAtSFH1::GUS expression. (E) GUS activity is recorded both in trichoblast cell bodies and root hairs. Arrows denote cell plates. PAtSFH1::GUS activity in cotyledon hydathodes (F), apical shoot meristem (G), and apical cells of the root cap (H). Bars: (A and B) 0.12 cm; (C–H) 50 μm.
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Related In: Results  -  Collection

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fig3: Tissue-specific AtSfh1p expression. Otherwise wild-type transgenic plants stained for GUS expressed from a promoterless construct (A) or the AtSFH1 promoter (PAtSFH1::GUS) (B). (C) PAtSFH1::GUS expression is robust in root. Arrows denote GUS-active trichoblast cell files. (D) Root hair producing epidermal cell files (arrows) exhibit robust PAtSFH1::GUS expression. (E) GUS activity is recorded both in trichoblast cell bodies and root hairs. Arrows denote cell plates. PAtSFH1::GUS activity in cotyledon hydathodes (F), apical shoot meristem (G), and apical cells of the root cap (H). Bars: (A and B) 0.12 cm; (C–H) 50 μm.
Mentions: Sec14p-nodulin domain proteins are uncharacterized and expansion of this family suggests tissue-specific functions for its members. AtSfh1p was chosen for detailed analysis because the AtSfh1p-LBD is most homologous to Sec14p. RT-PCR analyses indicated essentially root-specific expression of AtSFH1 (unpublished data), a result in accord with microarray data (http://www.cbs.umn.edu/arabidopsis/). β-Glucuronidase (GUS) histochemical staining confirmed and extended these results. AtSFH1 was expressed solely in root trichoblast cell files engaged in root hair growth (Fig. 3, C–E), hydathodes, shoot apical meristem, and apical cells of the root cap (Fig. 3, F–H).

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