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Phosphoinositide-dependent regulation of VAN3 ARF-GAP localization and activity essential for vascular tissue continuity in plants

Satoshi Naramoto UGent, Shinichiro Sawa, Koji Koizumi, Tomohiro Uemura, Jiri Friml UGent, Akihiko Nakano and Hiroo Fukuda (2009) DEVELOPMENT. 136(9). p.1529-1538
abstract
ACAP-type ARF GTPase activating proteins (ARF-GAPs) regulate multiple cellular processes, including endocytosis, secretion, phagocytosis, cell adhesion and cell migration. However, the regulation of ACAP functions by other cellular proteins is poorly understood. We have reported previously that a plant ACAP, VAN3, plays a pivotal role in plant venation continuity. Here, we report on newly identified VAN3 regulators: the CVP2 (cotyledon vascular pattern 2) 5 PTase, which is considered to degrade IP3 and also to produce PtdIns(4) P from PtdIns(4,5) P-2; and a PH domain-containing protein, VAB (VAN3 binding protein). Combinational mutations of both CVP2 and its closest homologue CVL1 (CVP2 like 1) phenocopied the strong allele of van3 mutants, showing severe vascular continuity. The phenotype of double mutants between van3, cvp2 and vab suggested that VAN3, CVP2 and VAB function in vascular pattern formation in the same pathway. Localization analysis revealed that both CVP2 and VAB colocalize with VAN3 in the trans-Golgi network (TGN), supporting their functions in the same pathway. The subcellular localization of VAN3 was dependent on its PH domain, and mislocalization of VAN3 was induced in cvp2 or vab mutants. These results suggest that CVP2 and VAB cooperatively regulate the subcellular localization of VAN3 through the interaction between its PH domain and phosphoinositides and/or inositol phosphates. In addition, PtdIns(4) P, to which VAN3 binds preferentially, enhanced the ARF-GAP activity of VAN3, whereas IP3 inhibited it. These results suggest the existence of PtdIns(4) P and/or IP3-dependent subcellular targeting and regulation of VAN3 ACAP activity that governs plant vascular tissue continuity.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
VAN3, Arabidopsis, Vein, ARF-GAP, CVP2, VAB, GTPASE-ACTIVATING PROTEIN, BIMOLECULAR FLUORESCENCE COMPLEMENTATION, ARABIDOPSIS GENE MONOPTEROS, AUXIN TRANSPORT, THALIANA, CELLS, COTYLEDON, ENCODES, NETWORK, EFFLUX
journal title
DEVELOPMENT
Development
volume
136
issue
9
pages
1529 - 1538
Web of Science type
Article
Web of Science id
000265096500013
JCR category
DEVELOPMENTAL BIOLOGY
JCR impact factor
7.194 (2009)
JCR rank
4/35 (2009)
JCR quartile
1 (2009)
ISSN
0950-1991
DOI
10.1242/dev.030098
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
672756
handle
http://hdl.handle.net/1854/LU-672756
date created
2009-05-29 17:41:18
date last changed
2012-12-04 16:58:55
@article{672756,
  abstract     = {ACAP-type ARF GTPase activating proteins (ARF-GAPs) regulate multiple cellular processes, including endocytosis, secretion, phagocytosis, cell adhesion and cell migration. However, the regulation of ACAP functions by other cellular proteins is poorly understood. We have reported previously that a plant ACAP, VAN3, plays a pivotal role in plant venation continuity. Here, we report on newly identified VAN3 regulators: the CVP2 (cotyledon vascular pattern 2) 5 PTase, which is considered to degrade IP3 and also to produce PtdIns(4) P from PtdIns(4,5) P-2; and a PH domain-containing protein, VAB (VAN3 binding protein). Combinational mutations of both CVP2 and its closest homologue CVL1 (CVP2 like 1) phenocopied the strong allele of van3 mutants, showing severe vascular continuity. The phenotype of double mutants between van3, cvp2 and vab suggested that VAN3, CVP2 and VAB function in vascular pattern formation in the same pathway. Localization analysis revealed that both CVP2 and VAB colocalize with VAN3 in the trans-Golgi network (TGN), supporting their functions in the same pathway. The subcellular localization of VAN3 was dependent on its PH domain, and mislocalization of VAN3 was induced in cvp2 or vab mutants. These results suggest that CVP2 and VAB cooperatively regulate the subcellular localization of VAN3 through the interaction between its PH domain and phosphoinositides and/or inositol phosphates. In addition, PtdIns(4) P, to which VAN3 binds preferentially, enhanced the ARF-GAP activity of VAN3, whereas IP3 inhibited it. These results suggest the existence of PtdIns(4) P and/or IP3-dependent subcellular targeting and regulation of VAN3 ACAP activity that governs plant vascular tissue continuity.},
  author       = {Naramoto, Satoshi and Sawa, Shinichiro and Koizumi, Koji and Uemura, Tomohiro and Friml, Jiri and Nakano, Akihiko and Fukuda, Hiroo},
  issn         = {0950-1991},
  journal      = {DEVELOPMENT},
  keyword      = {VAN3,Arabidopsis,Vein,ARF-GAP,CVP2,VAB,GTPASE-ACTIVATING PROTEIN,BIMOLECULAR FLUORESCENCE COMPLEMENTATION,ARABIDOPSIS GENE MONOPTEROS,AUXIN TRANSPORT,THALIANA,CELLS,COTYLEDON,ENCODES,NETWORK,EFFLUX},
  language     = {eng},
  number       = {9},
  pages        = {1529--1538},
  title        = {Phosphoinositide-dependent regulation of VAN3 ARF-GAP localization and activity essential for vascular tissue continuity in plants},
  url          = {http://dx.doi.org/10.1242/dev.030098},
  volume       = {136},
  year         = {2009},
}

Chicago
Naramoto, Satoshi, Shinichiro Sawa, Koji Koizumi, Tomohiro Uemura, Jiri Friml, Akihiko Nakano, and Hiroo Fukuda. 2009. “Phosphoinositide-dependent Regulation of VAN3 ARF-GAP Localization and Activity Essential for Vascular Tissue Continuity in Plants.” Development 136 (9): 1529–1538.
APA
Naramoto, S., Sawa, S., Koizumi, K., Uemura, T., Friml, J., Nakano, A., & Fukuda, H. (2009). Phosphoinositide-dependent regulation of VAN3 ARF-GAP localization and activity essential for vascular tissue continuity in plants. DEVELOPMENT, 136(9), 1529–1538.
Vancouver
1.
Naramoto S, Sawa S, Koizumi K, Uemura T, Friml J, Nakano A, et al. Phosphoinositide-dependent regulation of VAN3 ARF-GAP localization and activity essential for vascular tissue continuity in plants. DEVELOPMENT. 2009;136(9):1529–38.
MLA
Naramoto, Satoshi, Shinichiro Sawa, Koji Koizumi, et al. “Phosphoinositide-dependent Regulation of VAN3 ARF-GAP Localization and Activity Essential for Vascular Tissue Continuity in Plants.” DEVELOPMENT 136.9 (2009): 1529–1538. Print.