Home LiteratureArticle Details
PMID: 26002867 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The Arabidopsis R-SNARE VAMP721 Interacts with KAT1 and KC1 K+ Channels to Moderate K+ Current at the Plasma Membrane.

The Plant cell ·Vol. 27 ·No. 6 ·2015-06-00 ·Pages 1697-717

Zhang B, Karnik R, Wang Y, Wallmeroth N, Blatt MR, Grefen C

Abstract

SNARE (soluble N-ethylmaleimide-sensitive factor protein attachment protein receptor) proteins drive vesicle traffic, delivering membrane and cargo to target sites within the cell and at its surface. They contribute to cell homeostasis, morphogenesis, and pathogen defense. A subset of SNAREs, including the Arabidopsis thaliana SNARE SYP121, are known also to coordinate solute uptake via physical interactions with K(+) channels and to moderate their gating at the plasma membrane. Here, we identify a second subset of SNAREs that interact to control these K(+) channels, but with opposing actions on gating. We show that VAMPs (vesicle-associated membrane proteins), which target vesicles to the plasma membrane, also interact with and suppress the activities of the inward-rectifying K(+) channels KAT1 and KC1. Interactions were evident in yeast split-ubiquitin assays, they were recovered in vivo by ratiometric bimolecular fluorescence complementation, and they were sensitive to mutation of a single residue, Tyr-57, within the longin domain of VAMP721. Interaction was also recovered on exchange of the residue at this site in the homolog VAMP723, which normally localizes to the endoplasmic reticulum and otherwise did not interact. Functional analysis showed reduced channel activity and alterations in voltage sensitivity that are best explained by a physical interaction with the channel gates. These actions complement those of SYP121, a cognate SNARE partner of VAMP721, and lead us to propose that the channel interactions reflect a "hand-off" in channel control between the two SNARE proteins that is woven together with vesicle fusion.

MeSH Terms
Arabidopsis/metabolism,physiology Arabidopsis Proteins/physiology Cell Membrane/physiology Membrane Potentials/physiology Potassium Channels/physiology Potassium Channels, Inwardly Rectifying/physiology R-SNARE Proteins/physiology Symporters/physiology
Chemicals
Arabidopsis Proteins KAT1 protein, Arabidopsis Potassium Channels Potassium Channels, Inwardly Rectifying R-SNARE Proteins Symporters VAMP721 protein, Arabidopsis potassium-chloride symporters
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Zhang Ben
Laboratory of Plant Physiology and Biophysics, University of Glasgow, Glasgow G12 8QQ, United Kingdom.
Karnik Rucha
Laboratory of Plant Physiology and Biophysics, University of Glasgow, Glasgow G12 8QQ, United Kingdom.
Wang Yizhou
Laboratory of Plant Physiology and Biophysics, University of Glasgow, Glasgow G12 8QQ, United Kingdom.
Wallmeroth Niklas
ZMBP Developmental Genetics, D-72076 Tuebingen, Germany.
Blatt Michael R
Laboratory of Plant Physiology and Biophysics, University of Glasgow, Glasgow G12 8QQ, United Kingdom michael.blatt@glasgow.ac.uk.
Grefen Christopher
ZMBP Developmental Genetics, D-72076 Tuebingen, Germany.
References (91)
91 references, click to expand
  1. The syntaxin SYP132 contributes to plant resistance against bacteria and secretion of pathogenesis-related protein 1.
    Proc Natl Acad Sci U S A. 2007 Jul 10;104(28):11850-5 PMID: 17592123
  2. SNARE complexes of different composition jointly mediate membrane fusion in Arabidopsis cytokinesis.
    Mol Biol Cell. 2013 May;24(10):1593-601 PMID: 23515225
  3. Regulation of voltage dependence of the KAT1 channel by intracellular factors.
    J Gen Physiol. 1995 Mar;105(3):309-28 PMID: 7769379
  4. Formation of the full SNARE complex eliminates interactions of its individual protein components with the Kv2.1 channel.
    Biochemistry. 2008 Aug 12;47(32):8342-9 PMID: 18636750
  5. SNAREs--engines for membrane fusion.
    Nat Rev Mol Cell Biol. 2006 Sep;7(9):631-43 PMID: 16912714
  6. Voltage-sensor transitions of the inward-rectifying K+ channel KAT1 indicate a latching mechanism biased by hydration within the voltage sensor.
    Plant Physiol. 2014 Oct;166(2):960-75 PMID: 25185120
  7. Selective mobility and sensitivity to SNAREs is exhibited by the Arabidopsis KAT1 K+ channel at the plasma membrane.
    Plant Cell. 2006 Apr;18(4):935-54 PMID: 16531497
  8. Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells.
    Cell Struct Funct. 2004 Apr;29(2):49-65 PMID: 15342965
  9. AtKC1, a conditionally targeted Shaker-type subunit, regulates the activity of plant K+ channels.
    Plant J. 2008 Jan;53(1):115-23 PMID: 17976154
  10. An exocyst complex functions in plant cell growth in Arabidopsis and tobacco.
    Plant Cell. 2008 May;20(5):1330-45 PMID: 18492870
  11. Isolation and proteomic analysis of the SYP61 compartment reveal its role in exocytic trafficking in Arabidopsis.
    Cell Res. 2012 Feb;22(2):413-24 PMID: 21826108
  12. Selective regulation of maize plasma membrane aquaporin trafficking and activity by the SNARE SYP121.
    Plant Cell. 2012 Aug;24(8):3463-81 PMID: 22942383
  13. Increased activity of the vesicular soluble N-ethylmaleimide-sensitive factor attachment protein receptor TI-VAMP/VAMP7 by tyrosine phosphorylation in the Longin domain.
    J Biol Chem. 2013 Apr 26;288(17):11960-72 PMID: 23471971
  14. VAMP subfamilies identified by specific R-SNARE motifs.
    Biol Cell. 2004 May;96(4):251-6 PMID: 15145528
  15. The potassium channel KAT1 is activated by plant and animal 14-3-3 proteins.
    J Biol Chem. 2006 Nov 24;281(47):35735-41 PMID: 16990282
  16. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  17. Exocytosis and cell polarity in plants - exocyst and recycling domains.
    New Phytol. 2009;183(2):255-72 PMID: 19496948
  18. Differential expression control and polarized distribution of plasma membrane-resident SYP1 SNAREs in Arabidopsis thaliana.
    Plant Cell Physiol. 2009 Feb;50(2):280-9 PMID: 19098073
  19. SDM-Assist software to design site-directed mutagenesis primers introducing "silent" restriction sites.
    BMC Bioinformatics. 2013;14:105 PMID: 23522286
  20. A 2in1 cloning system enables ratiometric bimolecular fluorescence complementation (rBiFC).
    Biotechniques. 2012 Nov;53(5):311-14 PMID: 23066669
  21. Functional differentiation of endosomes in Arabidopsis cells.
    Plant J. 2004 Dec;40(5):783-9 PMID: 15546360
  22. A novel motif essential for SNARE interaction with the K(+) channel KC1 and channel gating in Arabidopsis.
    Plant Cell. 2010 Sep;22(9):3076-92 PMID: 20884800
  23. A bicistronic, Ubiquitin-10 promoter-based vector cassette for transient transformation and functional analysis of membrane transport demonstrates the utility of quantitative voltage clamp studies on intact Arabidopsis root epidermis.
    Plant Cell Environ. 2011 Apr;34(4):554-64 PMID: 21251017
  24. A genomic perspective on membrane compartment organization.
    Nature. 2001 Feb 15;409(6822):839-41 PMID: 11237004
  25. A role for the AKT1 potassium channel in plant nutrition.
    Science. 1998 May 8;280(5365):918-21 PMID: 9572739
  26. Arabidopsis Sec1/Munc18 protein SEC11 is a competitive and dynamic modulator of SNARE binding and SYP121-dependent vesicle traffic.
    Plant Cell. 2013 Apr;25(4):1368-82 PMID: 23572542
  27. Structure and function of SNARE and SNARE-interacting proteins.
    Q Rev Biophys. 2005 Feb;38(1):1-47 PMID: 16336742
  28. A SNARE complex containing SGR3/AtVAM3 and ZIG/VTI11 in gravity-sensing cells is important for Arabidopsis shoot gravitropism.
    Proc Natl Acad Sci U S A. 2003 Jul 8;100(14):8589-94 PMID: 12815100
  29. SNARE-ware: the role of SNARE-domain proteins in plant biology.
    Annu Rev Cell Dev Biol. 2007;23:147-74 PMID: 17506694
  30. A membrane trafficking pathway regulated by the plant-specific RAB GTPase ARA6.
    Nat Cell Biol. 2011 Jul;13(7):853-9 PMID: 21666683
  31. The 25-kDa synaptosome-associated protein (SNAP-25) binds and inhibits delayed rectifier potassium channels in secretory cells.
    J Biol Chem. 2002 Jun 7;277(23):20195-204 PMID: 11925439
  32. The trafficking protein SYP121 of Arabidopsis connects programmed stomatal closure and K⁺ channel activity with vegetative growth.
    Plant J. 2012 Jan;69(2):241-51 PMID: 21914010
  33. Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants.
    Plant Physiol. 2007 May;144(1):6-17 PMID: 17369437
  34. Binding of SEC11 indicates its role in SNARE recycling after vesicle fusion and identifies two pathways for vesicular traffic to the plasma membrane.
    Plant Cell. 2015 Mar;27(3):675-94 PMID: 25747882
  35. OSM1/SYP61: a syntaxin protein in Arabidopsis controls abscisic acid-mediated and non-abscisic acid-mediated responses to abiotic stress.
    Plant Cell. 2002 Dec;14(12):3009-28 PMID: 12468724
  36. A generalized method for transfecting root epidermis uncovers endosomal dynamics in Arabidopsis root hairs.
    Plant J. 2007 Jul;51(2):322-30 PMID: 17610544
  37. A molecular framework for coupling cellular volume and osmotic solute transport control.
    J Exp Bot. 2011 Apr;62(7):2363-70 PMID: 21115662
  38. A new catch in the SNARE.
    Trends Plant Sci. 2004 Apr;9(4):187-95 PMID: 15063869
  39. A dual mechanism controlling the localization and function of exocytic v-SNAREs.
    Proc Natl Acad Sci U S A. 2003 Jul 22;100(15):9011-6 PMID: 12853575
  40. K(+) channel profile and electrical properties of Arabidopsis root hairs.
    FEBS Lett. 2001 Nov 23;508(3):463-9 PMID: 11728473
  41. The Arabidopsis exocyst complex is involved in cytokinesis and cell plate maturation.
    Plant Cell. 2010 Sep;22(9):3053-65 PMID: 20870962
  42. Heteromeric AtKC1{middle dot}AKT1 channels in Arabidopsis roots facilitate growth under K+-limiting conditions.
    J Biol Chem. 2009 Aug 7;284(32):21288-95 PMID: 19509299
  43. The high road and the low road: trafficking choices in plants.
    Cell. 2007 Sep 21;130(6):977-9 PMID: 17889639
  44. Applications of fluorescent marker proteins in plant cell biology.
    Methods Mol Biol. 2014;1062:487-507 PMID: 24057383
  45. Clustering of syntaxin-1A in model membranes is modulated by phosphatidylinositol 4,5-bisphosphate and cholesterol.
    Biochemistry. 2009 Jun 2;48(21):4617-25 PMID: 19364135
  46. The longin SNARE VAMP7/TI-VAMP adopts a closed conformation.
    J Biol Chem. 2010 Jun 4;285(23):17965-73 PMID: 20378544
  47. H3 domain of syntaxin 1A inhibits KATP channels by its actions on the sulfonylurea receptor 1 nucleotide-binding folds-1 and -2.
    J Biol Chem. 2004 Dec 17;279(51):53259-65 PMID: 15485808
  48. A tobacco syntaxin with a role in hormonal control of guard cell ion channels.
    Science. 1999 Jan 22;283(5401):537-40 PMID: 9915701
  49. SNARE protein trafficking in polarized MDCK cells.
    Traffic. 2000 Jul;1(7):553-60 PMID: 11208143
  50. Functional impact of syntaxin on gating of N-type and Q-type calcium channels.
    Nature. 1995 Dec 7;378(6557):623-6 PMID: 8524397
  51. SGR2, a phospholipase-like protein, and ZIG/SGR4, a SNARE, are involved in the shoot gravitropism of Arabidopsis.
    Plant Cell. 2002 Jan;14(1):33-46 PMID: 11826297
  52. A SNARE-protein has opposing functions in penetration resistance and defence signalling pathways.
    Plant J. 2007 Jan;49(2):302-12 PMID: 17241452
  53. TWIK-2, a new weak inward rectifying member of the tandem pore domain potassium channel family.
    J Biol Chem. 1999 Mar 19;274(12):7887-92 PMID: 10075682
  54. Reduced expression of the v-SNAREs AtVAMP71/AtVAMP7C gene family in Arabidopsis reduces drought tolerance by suppression of abscisic acid-dependent stomatal closure.
    J Exp Bot. 2010 Jun;61(10):2615-22 PMID: 20423938
  55. The longin domain regulates subcellular targeting of VAMP7 in Arabidopsis thaliana.
    FEBS Lett. 2005 May 23;579(13):2842-6 PMID: 15876431
  56. Functional interaction of the SNARE protein NtSyp121 in Ca2+ channel gating, Ca2+ transients and ABA signalling of stomatal guard cells.
    Mol Plant. 2008 Mar;1(2):347-58 PMID: 19825544
  57. A SNARE complex unique to seed plants is required for protein storage vacuole biogenesis and seed development of Arabidopsis thaliana.
    Plant Cell. 2008 Nov;20(11):3006-21 PMID: 18984676
  58. Kv2.1 channel activation and inactivation is influenced by physical interactions of both syntaxin 1A and the syntaxin 1A/soluble N-ethylmaleimide-sensitive factor-25 (t-SNARE) complex with the C terminus of the channel.
    Mol Pharmacol. 2005 Feb;67(2):480-8 PMID: 15525758
  59. The photoreversible fluorescent protein iLOV outperforms GFP as a reporter of plant virus infection.
    Proc Natl Acad Sci U S A. 2008 Dec 16;105(50):20038-43 PMID: 19060199
  60. VAMP2 interacts directly with the N terminus of Kv2.1 to enhance channel inactivation.
    Pflugers Arch. 2008 Sep;456(6):1121-36 PMID: 18542995
  61. Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs.
    Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15781-6 PMID: 9861047
  62. Localization and control of expression of Nt-Syr1, a tobacco SNARE protein.
    Plant J. 2000 Nov;24(3):369-81 PMID: 11069710
  63. Suppression of Arabidopsis vesicle-SNARE expression inhibited fusion of H2O2-containing vesicles with tonoplast and increased salt tolerance.
    Proc Natl Acad Sci U S A. 2006 Nov 21;103(47):18008-13 PMID: 17101982
  64. The determination of protein-protein interactions by the mating-based split-ubiquitin system (mbSUS).
    Methods Mol Biol. 2009;479:217-33 PMID: 19083185
  65. A glucocorticoid-mediated transcriptional induction system in transgenic plants.
    Plant J. 1997 Mar;11(3):605-12 PMID: 9107046
  66. A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis.
    Cell. 2006 Jun 30;125(7):1347-60 PMID: 16814720
  67. A silicon transporter in rice.
    Nature. 2006 Mar 30;440(7084):688-91 PMID: 16572174
  68. Anatomy and dynamics of a supramolecular membrane protein cluster.
    Science. 2007 Aug 24;317(5841):1072-6 PMID: 17717182
  69. Reconstitution of the vital functions of Munc18 and Munc13 in neurotransmitter release.
    Science. 2013 Jan 25;339(6118):421-5 PMID: 23258414
  70. Co-option of a default secretory pathway for plant immune responses.
    Nature. 2008 Feb 14;451(7180):835-40 PMID: 18273019
  71. Arabidopsis SNAREs SYP61 and SYP121 coordinate the trafficking of plasma membrane aquaporin PIP2;7 to modulate the cell membrane water permeability.
    Plant Cell. 2014 Jul;26(7):3132-47 PMID: 25082856
  72. SNAREs: cogs and coordinators in signaling and development.
    Plant Physiol. 2008 Aug;147(4):1504-15 PMID: 18678742
  73. What makes a gate? The ins and outs of Kv-like K+ channels in plants.
    Trends Plant Sci. 2009 Jul;14(7):383-90 PMID: 19540150
  74. The abscisic acid-related SNARE homolog NtSyr1 contributes to secretion and growth: evidence from competition with its cytosolic domain.
    Plant Cell. 2002 Feb;14(2):387-406 PMID: 11884682
  75. A tripartite SNARE-K+ channel complex mediates in channel-dependent K+ nutrition in Arabidopsis.
    Plant Cell. 2009 Sep;21(9):2859-77 PMID: 19794113
  76. Interactions between Rabs, tethers, SNAREs and their regulators in exocytosis.
    Biochem Soc Trans. 2006 Nov;34(Pt 5):683-6 PMID: 17052174
  77. Selective targeting of plasma membrane and tonoplast traffic by inhibitory (dominant-negative) SNARE fragments.
    Plant J. 2007 Sep;51(6):1099-115 PMID: 17662029
  78. Arabidopsis R-SNARE proteins VAMP721 and VAMP722 are required for cell plate formation.
    PLoS One. 2011;6(10):e26129 PMID: 22022536
  79. Abscisic acid triggers the endocytosis of the arabidopsis KAT1 K+ channel and its recycling to the plasma membrane.
    Curr Biol. 2007 Aug 21;17(16):1396-402 PMID: 17683934
  80. Molecular determinants of the functional interaction between syntaxin and N-type Ca2+ channel gating.
    Proc Natl Acad Sci U S A. 2000 Dec 5;97(25):13943-8 PMID: 11087812
  81. Involvement of the vacuoles of the endodermis in the early process of shoot gravitropism in Arabidopsis.
    Plant Cell. 2002 Jan;14(1):47-56 PMID: 11826298
  82. The voltage-dependent potassium channel subunit Kv2.1 regulates insulin secretion from rodent and human islets independently of its electrical function.
    Diabetologia. 2012 Jun;55(6):1709-20 PMID: 22411134
  83. SNAREs and traffic.
    Biochim Biophys Acta. 2005 Jun 30;1744(2):120-44 PMID: 15893389
  84. A ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies.
    Plant J. 2010 Oct;64(2):355-65 PMID: 20735773
  85. K+ channel interactions detected by a genetic system optimized for systematic studies of membrane protein interactions.
    Proc Natl Acad Sci U S A. 2004 Aug 17;101(33):12242-7 PMID: 15299147
  86. EZ-Rhizo: integrated software for the fast and accurate measurement of root system architecture.
    Plant J. 2009 Mar;57(5):945-56 PMID: 19000163
  87. SNAREs--molecular governors in signalling and development.
    Curr Opin Plant Biol. 2008 Dec;11(6):600-9 PMID: 18945636
  88. Requirement of vesicle-associated membrane protein 721 and 722 for sustained growth during immune responses in Arabidopsis.
    Mol Cells. 2013 Jun;35(6):481-8 PMID: 23661365
  89. The FAST technique: a simplified Agrobacterium-based transformation method for transient gene expression analysis in seedlings of Arabidopsis and other plant species.
    Plant Methods. 2009 May 20;5:6 PMID: 19457242
  90. SNARE-protein-mediated disease resistance at the plant cell wall.
    Nature. 2003 Oct 30;425(6961):973-7 PMID: 14586469
  91. False interaction of syntaxin 1A with a Ca(2+)-activated K(+) channel revealed by co-immunoprecipitation and pull-down assays: implications for identification of protein-protein interactions.
    Neuropharmacology. 2003 May;44(6):817-27 PMID: 12681380
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1532-298X
Published
2015-06-00
Epub
2015-00-22
Pages
1697-717
Language
English
Region
England
NLM ID
9208688
PMCID
PMC4498211
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · BB/F001630/1 · United Kingdom
Biotechnology and Biological Sciences Research Council · BB/H0024867/1 · United Kingdom
Biotechnology and Biological Sciences Research Council · BB/I024496/1 · United Kingdom
Biotechnology and Biological Sciences Research Council · BB/L001276/1 · United Kingdom
Biotechnology and Biological Sciences Research Council · BB/K015893/1 · United Kingdom
Biotechnology and Biological Sciences Research Council · BB/M01133X/1 · United Kingdom
Biotechnology and Biological Sciences Research Council · BB/H009817/1 · United Kingdom
Corrections
ErratumIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com