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PMID: 16698946 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

SCARFACE encodes an ARF-GAP that is required for normal auxin efflux and vein patterning in Arabidopsis.

The Plant cell ·Vol. 18 ·No. 6 ·2006-06-00 ·Pages 1396-411

Sieburth LE, Muday GK, King EJ, Benton G, Kim S, Metcalf KE, Meyers L, Seamen E, Van Norman JM

Abstract

To identify molecular mechanisms controlling vein patterns, we analyzed scarface (sfc) mutants. sfc cotyledon and leaf veins are largely fragmented, unlike the interconnected networks in wild-type plants. SFC encodes an ADP ribosylation factor GTPase activating protein (ARF-GAP), a class with well-established roles in vesicle trafficking regulation. Quadruple mutants of SCF and three homologs (ARF-GAP DOMAIN1, 2, and 4) showed a modestly enhanced vascular phenotype. Genetic interactions between sfc and pinoid and between sfc and gnom suggest a possible function for SFC in trafficking of auxin efflux regulators. Genetic analyses also revealed interaction with cotyledon vascular pattern2, suggesting that lipid-based signals may underlie some SFC ARF-GAP functions. To assess possible roles for SFC in auxin transport, we analyzed sfc roots, which showed exaggerated responses to exogenous auxin and higher auxin transport capacity. To determine whether PIN1 intracellular trafficking was affected, we analyzed PIN1:green fluorescent protein (GFP) dynamics using confocal microscopy in sfc roots. We found normal PIN1:GFP localization at the apical membrane of root cells, but treatment with brefeldin A resulted in PIN1 accumulating in smaller and more numerous compartments than in the wild type. These data suggest that SFC is required for normal intracellular transport of PIN1 from the plasma membrane to the endosome.

MeSH Terms
ADP-Ribosylation Factors/chemistry,genetics,metabolism Alleles Amino Acid Sequence Arabidopsis/anatomy & histology,growth & development,metabolism Arabidopsis Proteins/chemistry,genetics,metabolism Biological Transport Cotyledon/cytology GTPase-Activating Proteins/chemistry,genetics,metabolism Gene Expression Regulation, Plant Genes, Plant/genetics Indoleacetic Acids/metabolism Membrane Transport Proteins/metabolism Molecular Sequence Data Mutation/genetics Plant Leaves/cytology,physiology Plant Roots/cytology RNA, Messenger/genetics,metabolism
Chemicals
Arabidopsis Proteins GTPase-Activating Proteins Indoleacetic Acids Membrane Transport Proteins PIN1 protein, Arabidopsis RNA, Messenger VAN3 protein, Arabidopsis ADP-Ribosylation Factors
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Sieburth Leslie E
Department of Biology, University of Utah, Salt Lake City, Utah, 84112, USA. sieburth@biology.utah.edu
Muday Gloria K
King Edward J
Benton Geoff
Kim Sun
Metcalf Kasee E
Meyers Lindsay
Seamen Emylie
Van Norman Jaimie M
References (56)
56 references, click to expand
  1. Activation of phospholipase C gamma by PI 3-kinase-induced PH domain-mediated membrane targeting.
    EMBO J. 1998 Jan 15;17(2):414-22 PMID: 9430633
  2. Auxin signaling in Arabidopsis leaf vascular development.
    Plant Physiol. 2003 Mar;131(3):1327-39 PMID: 12644682
  3. EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana.
    Genes Dev. 1998 Jul 15;12(14):2175-87 PMID: 9679062
  4. Genetic and chemical reductions in protein phosphatase activity alter auxin transport, gravity response, and lateral root growth.
    Plant Cell. 2001 Jul;13(7):1683-97 PMID: 11449059
  5. A gene expression map of the Arabidopsis root.
    Science. 2003 Dec 12;302(5652):1956-60 PMID: 14671301
  6. Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1.
    Plant J. 2005 Oct;44(2):179-94 PMID: 16212599
  7. The Arf GTPase-activating protein ASAP1 regulates the actin cytoskeleton.
    Proc Natl Acad Sci U S A. 2000 Apr 11;97(8):4011-6 PMID: 10725410
  8. A regulatory role for ARF6 in receptor-mediated endocytosis.
    Science. 1995 Feb 24;267(5201):1175-8 PMID: 7855600
  9. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue.
    Science. 1998 Dec 18;282(5397):2226-30 PMID: 9856939
  10. LOP1: a gene involved in auxin transport and vascular patterning in Arabidopsis.
    Development. 1996 Jun;122(6):1811-9 PMID: 8674420
  11. Responses of plant vascular systems to auxin transport inhibition.
    Development. 1999 Jul;126(13):2979-91 PMID: 10357941
  12. A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux.
    Science. 2004 Oct 29;306(5697):862-5 PMID: 15514156
  13. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements.
    Plant Cell. 1997 Nov;9(11):1963-71 PMID: 9401121
  14. Brassinolide induces IAA5, IAA19, and DR5, a synthetic auxin response element in Arabidopsis, implying a cross talk point of brassinosteroid and auxin signaling.
    Plant Physiol. 2003 Dec;133(4):1843-53 PMID: 14605219
  15. ACAP1 promotes endocytic recycling by recognizing recycling sorting signals.
    Dev Cell. 2004 Nov;7(5):771-6 PMID: 15525538
  16. Genetic regulation of vascular tissue patterning in Arabidopsis.
    Plant Cell. 1999 Nov;11(11):2123-37 PMID: 10559439
  17. A series of novel mutants of Arabidopsis thaliana that are defective in the formation of continuous vascular network: calling the auxin signal flow canalization hypothesis into question.
    Development. 2000 Aug;127(15):3197-204 PMID: 10887076
  18. hydra Mutants of Arabidopsis are defective in sterol profiles and auxin and ethylene signaling.
    Plant Cell. 2002 May;14(5):1017-31 PMID: 12034894
  19. Regulation of auxin response by the protein kinase PINOID.
    Cell. 2000 Feb 18;100(4):469-78 PMID: 10693763
  20. Auxin transport.
    Curr Opin Plant Biol. 2005 Oct;8(5):494-500 PMID: 16054428
  21. Brefeldin A: deciphering an enigmatic inhibitor of secretion.
    Plant Physiol. 2002 Nov;130(3):1102-8 PMID: 12427977
  22. VAN3 ARF-GAP-mediated vesicle transport is involved in leaf vascular network formation.
    Development. 2005 Apr;132(7):1699-711 PMID: 15743878
  23. Auxin is required for leaf vein pattern in Arabidopsis.
    Plant Physiol. 1999 Dec;121(4):1179-90 PMID: 10594105
  24. EMB30 is essential for normal cell division, cell expansion, and cell adhesion in Arabidopsis and encodes a protein that has similarity to Sec7.
    Cell. 1994 Jul 1;77(7):1051-62 PMID: 8020095
  25. Auxin inhibits endocytosis and promotes its own efflux from cells.
    Nature. 2005 Jun 30;435(7046):1251-6 PMID: 15988527
  26. Cotyledon vascular pattern2-mediated inositol (1,4,5) triphosphate signal transduction is essential for closed venation patterns of Arabidopsis foliar organs.
    Plant Cell. 2004 May;16(5):1263-75 PMID: 15100402
  27. Arabidopsis map-based cloning in the post-genome era.
    Plant Physiol. 2002 Jun;129(2):440-50 PMID: 12068090
  28. Phosphoinositide-dependent activation of the ADP-ribosylation factor GTPase-activating protein ASAP1. Evidence for the pleckstrin homology domain functioning as an allosteric site.
    J Biol Chem. 2000 Mar 31;275(13):9653-63 PMID: 10734117
  29. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem.
    Curr Biol. 2005 Nov 8;15(21):1899-911 PMID: 16271866
  30. The arabidopsis thaliana AGRAVITROPIC 1 gene encodes a component of the polar-auxin-transport efflux carrier.
    Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):15112-7 PMID: 9844024
  31. ACAPs are arf6 GTPase-activating proteins that function in the cell periphery.
    J Cell Biol. 2000 Oct 30;151(3):627-38 PMID: 11062263
  32. Arf GAPs: multifunctional proteins that regulate membrane traffic and actin remodelling.
    Cell Signal. 2004 Apr;16(4):401-13 PMID: 14709330
  33. VARICOSE, a WD-domain protein, is required for leaf blade development.
    Development. 2003 Dec;130(26):6577-88 PMID: 14660546
  34. The SCARFACE gene is required for cotyledon and leaf vein patterning.
    Development. 2000 Aug;127(15):3205-13 PMID: 10887077
  35. Cell polarity and PIN protein positioning in Arabidopsis require STEROL METHYLTRANSFERASE1 function.
    Plant Cell. 2003 Mar;15(3):612-25 PMID: 12615936
  36. Genome-wide insertional mutagenesis of Arabidopsis thaliana.
    Science. 2003 Aug 1;301(5633):653-7 PMID: 12893945
  37. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure.
    Science. 2004 Jan 23;303(5657):495-9 PMID: 14645856
  38. A critical role of sterols in embryonic patterning and meristem programming revealed by the fackel mutants of Arabidopsis thaliana.
    Genes Dev. 2000 Jun 15;14(12):1485-97 PMID: 10859167
  39. BIG: a calossin-like protein required for polar auxin transport in Arabidopsis.
    Genes Dev. 2001 Aug 1;15(15):1985-97 PMID: 11485992
  40. Specific and high-affinity binding of inositol phosphates to an isolated pleckstrin homology domain.
    Proc Natl Acad Sci U S A. 1995 Nov 7;92(23):10472-6 PMID: 7479822
  41. The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport.
    Development. 2001 Oct;128(20):4057-67 PMID: 11641228
  42. Requirement of the Auxin Polar Transport System in Early Stages of Arabidopsis Floral Bud Formation.
    Plant Cell. 1991 Jul;3(7):677-684 PMID: 12324609
  43. Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF.
    Science. 1999 Oct 8;286(5438):316-8 PMID: 10514379
  44. Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana.
    Plant Cell. 2004 Jul;16(7):1898-911 PMID: 15208397
  45. The identification of CVP1 reveals a role for sterols in vascular patterning.
    Plant Cell. 2002 Sep;14(9):2045-58 PMID: 12215504
  46. Partial loss-of-function alleles reveal a role for GNOM in auxin transport-related, post-embryonic development of Arabidopsis.
    Development. 2004 Jan;131(2):389-400 PMID: 14681187
  47. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking.
    Nature. 2001 Sep 27;413(6854):425-8 PMID: 11574889
  48. Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development.
    Plant Cell. 2001 Nov;13(11):2441-54 PMID: 11701880
  49. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis.
    Nature. 2002 Feb 14;415(6873):806-9 PMID: 11845211
  50. The PIN auxin efflux facilitators: evolutionary and functional perspectives.
    Trends Plant Sci. 2005 Apr;10(4):170-7 PMID: 15817418
  51. Phosphatidylinositol 4,5-bisphosphate and Arf6-regulated membrane traffic.
    J Cell Biol. 2001 Sep 3;154(5):1007-17 PMID: 11535619
  52. Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3718-23 PMID: 10737809
  53. Analysis of the small GTPase gene superfamily of Arabidopsis.
    Plant Physiol. 2003 Mar;131(3):1191-208 PMID: 12644670
  54. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth.
    Cell. 2003 Jan 24;112(2):219-30 PMID: 12553910
  55. The POLARIS gene of Arabidopsis encodes a predicted peptide required for correct root growth and leaf vascular patterning.
    Plant Cell. 2002 Aug;14(8):1705-21 PMID: 12172017
  56. Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis.
    Planta. 2003 Mar;216(5):841-53 PMID: 12624772
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
DOI
10.1105/tpc.105.039008
Email
sieburth@biology.utah.edu
Published
2006-06-00
Epub
2006-00-12
Pages
1396-411
Language
English
Region
England
NLM ID
9208688
PMCID
PMC1475492
Subset
IM
Databases
RefSeq
NM_100962, NM_104767, NM_121333, NM_125591
External Links
PubMed source DOI: 10.1105/tpc.105.039008 PMC Full Text View journal details
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