The Plant Cell, Vol. 14, 387-406,
February 2002, Copyright © 2002,
American Society of Plant Biologists
The Abscisic Acid–Related SNARE Homolog NtSyr1 Contributes to Secretion and Growth
Evidence from Competition with Its Cytosolic Domain
Danny Geelen1,2,,a,
Barbara Leyman1,3,,a,
Henri Batokob,
Gian-Pietro Di Sansebastianoa,
Ian Mooreb and
Michael R. Blatt4,5,a
a Laboratory of Plant Physiology and Biophysics, Imperial College of Science, Technology, and Medicine at Wye, Kent TN25 5AH, United Kingdom
b Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3RB, United Kingdom
5 To whom correspondence should be addressed. E-mail m.blatt{at}bio.gla.ac.uk; fax 44-0-141-330-4447
Syntaxins and other SNARE proteins are crucial for intracellular vesicle trafficking, fusion, and secretion. Previously, we isolated the syntaxin-related protein NtSyr1 (NtSyp121) from tobacco in a screen for abscisic acid–related signaling elements, demonstrating its role in determining the abscisic acid sensitivity of K+ and Cl- channels in stomatal guard cells. NtSyr1 is localized to the plasma membrane and is expressed normally throughout the plant, especially in root tissues, suggesting that it might contribute to cellular homeostasis as well as to signaling. To explore its functions in vivo further, we examined stably transformed lines of tobacco that expressed various constructs of NtSyr1, including the full-length protein and a truncated fragment, Sp2, corresponding to the cytosolic domain shown previously to be active in suppressing ion channel response to abscisic acid. Constitutively overexpressing NtSyr1 yielded uniformly high levels of protein (>10 times the wild-type levels) and was associated with a significant enhancement of root growth in seedlings but not with any obvious phenotype in mature, well-watered plants. Similar transformations with constructs encoding the Sp2 fragment of NtSyr1 showed altered leaf morphology but gave only low levels of Sp2 fragment, suggesting a strong selective pressure against plants expressing this protein. High expression of the Sp2 fragment was achieved in stable transformants under the control of a dexamethasone-inducible promoter. Sp2 expression was correlated positively with altered cellular and tissue morphology in leaves and roots and with a cessation of growth in seedlings. Overexpression of the full-length NtSyr1 protein rescued the wild-type phenotype, even in plants expressing high levels of the Sp2 fragment, supporting the idea that the Sp2 fragment interfered specifically with NtSyr1 function by competing with NtSyr1 for its binding partners. To explore NtSyr1 function in secretion, we used a green fluorescent protein (GFP)–based section assay. When a secreted GFP marker was coexpressed with Sp2 in tobacco leaves, GFP fluorescence was retained in cytosolic reticulate and punctate structures. In contrast, in plants coexpressing secreted GFP and NtSyr1 or secreted GFP alone, no GFP fluorescence accumulated within the cells. A new yellow fluorescent protein–based secretion marker was used to show that the punctate structures labeled in the presence of Sp2 colocalized with a Golgi marker. These structures were not labeled in the presence of a dominant Rab1 mutant that inhibited transport from the endoplasmic reticulum to the Golgi. We propose that NtSyr1 functions as an element in SNARE-mediated vesicle trafficking to the plasma membrane and is required for cellular growth and homeostasis.
This article has been cited by other articles:
|
|
|
|
 
D. C. Bassham and M. R. Blatt
SNAREs: Cogs and Coordinators in Signaling and Development
Plant Physiology,
August 1, 2008;
147(4):
1504 - 1515.
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. U. Rehman, E. Stigliano, G. W. Lycett, L. Sticher, F. Sbano, M. Faraco, G. Dalessandro, and G.-P. Di Sansebastiano
Tomato Rab11a Characterization Evidenced a Difference Between SYP121-Dependent and SYP122-Dependent exocytosis
Plant Cell Physiol.,
May 1, 2008;
49(5):
751 - 766.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. L. Avila, M. Brown, S. Pan, R. Desikan, S. J. Neill, T. Girke, M. Surpin, and N. V. Raikhel
Expression analysis of Arabidopsis vacuolar sorting receptor 3 reveals a putative function in guard cells
J. Exp. Bot.,
April 1, 2008;
59(6):
1149 - 1161.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Sokolovski, A. Hills, R. A. Gay, and M. R. Blatt
Functional Interaction of the SNARE Protein NtSyp121 in Ca2+ Channel Gating, Ca2+ Transients and ABA Signalling of Stomatal Guard Cells
Mol Plant,
March 1, 2008;
1(2):
347 - 358.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Sanderfoot
Increases in the Number of SNARE Genes Parallels the Rise of Multicellularity among the Green Plants
Plant Physiology,
May 1, 2007;
144(1):
6 - 17.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Maggio, A. Barbante, F. Ferro, L. Frigerio, and E. Pedrazzini
Intracellular sorting of the tail-anchored protein cytochrome b5 in plants: a comparative study using different isoforms from rabbit and Arabidopsis
J. Exp. Bot.,
April 1, 2007;
58(6):
1365 - 1379.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Campanoni and M. R. Blatt
Membrane trafficking and polar growth in root hairs and pollen tubes
J. Exp. Bot.,
January 1, 2007;
58(1):
65 - 74.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Van Damme, S. Coutuer, R. De Rycke, F.-Y. Bouget, D. Inze, and D. Geelen
Somatic Cytokinesis and Pollen Maturation in Arabidopsis Depend on TPLATE, Which Has Domains Similar to Coat Proteins
PLANT CELL,
December 1, 2006;
18(12):
3502 - 3518.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
O. Foresti, L. L.P. daSilva, and J. Denecke
Overexpression of the Arabidopsis Syntaxin PEP12/SYP21 Inhibits Transport from the Prevacuolar Compartment to the Lytic Vacuole in Vivo
PLANT CELL,
September 1, 2006;
18(9):
2275 - 2293.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. T. Mai, M. Nomura, K. Takegawa, E. Asamizu, S. Sato, T. Kato, S. Tabata, and S. Tajima
Identification of a Sed5-like SNARE Gene LjSYP32-1 that Contributes to Nodule Tissue Formation of Lotus japonicus
Plant Cell Physiol.,
July 1, 2006;
47(7):
829 - 838.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Jou, C.-P. Chiang, G.-Y. Jauh, and H. E. Yen
Functional Characterization of Ice Plant SKD1, an AAA-Type ATPase Associated with the Endoplasmic Reticulum-Golgi Network, and Its Role in Adaptation to Salt Stress
Plant Physiology,
May 1, 2006;
141(1):
135 - 146.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J.-U. Sutter, P. Campanoni, M. Tyrrell, and M. R. Blatt
Selective Mobility and Sensitivity to SNAREs Is Exhibited by the Arabidopsis KAT1 K+ Channel at the Plasma Membrane
PLANT CELL,
April 1, 2006;
18(4):
935 - 954.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Chatre, F. Brandizzi, A. Hocquellet, C. Hawes, and P. Moreau
Sec22 and Memb11 Are v-SNAREs of the Anterograde Endoplasmic Reticulum-Golgi Pathway in Tobacco Leaf Epidermal Cells
Plant Physiology,
November 1, 2005;
139(3):
1244 - 1254.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Heese, A. A. Ludwig, and J. D.G. Jones
Rapid Phosphorylation of a Syntaxin during the Avr9/Cf-9-Race-Specific Signaling Pathway
Plant Physiology,
August 1, 2005;
138(4):
2406 - 2416.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Zheng, L. Camacho, E. Wee, H. Batoko, J. Legen, C. J. Leaver, R. Malho, P. J. Hussey, and I. Moore
A Rab-E GTPase Mutant Acts Downstream of the Rab-D Subclass in Biosynthetic Membrane Traffic to the Plasma Membrane in Tobacco Leaf Epidermis
PLANT CELL,
July 1, 2005;
17(7):
2020 - 2036.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. E. Williams, J. Torabinejad, E. Cohick, K. Parker, E. J. Drake, J. E. Thompson, M. Hortter, and D. B. DeWald
Mutations in the Arabidopsis Phosphoinositide Phosphatase Gene SAC9 Lead to Overaccumulation of PtdIns(4,5)P2 and Constitutive Expression of the Stress-Response Pathway
Plant Physiology,
June 1, 2005;
138(2):
686 - 700.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. M. Kotzer, F. Brandizzi, U. Neumann, N. Paris, I. Moore, and C. Hawes
AtRabF2b (Ara7) acts on the vacuolar trafficking pathway in tobacco leaf epidermal cells
J. Cell Sci.,
December 15, 2004;
117(26):
6377 - 6389.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Van Damme, K. Van Poucke, E. Boutant, C. Ritzenthaler, D. Inze, and D. Geelen
In Vivo Dynamics and Differential Microtubule-Binding Activities of MAP65 Proteins
Plant Physiology,
December 1, 2004;
136(4):
3956 - 3967.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. F. Assaad, J.-L. Qiu, H. Youngs, D. Ehrhardt, L. Zimmerli, M. Kalde, G. Wanner, S. C. Peck, H. Edwards, K. Ramonell, et al.
The PEN1 Syntaxin Defines a Novel Cellular Compartment upon Fungal Attack and Is Required for the Timely Assembly of Papillae
Mol. Biol. Cell,
November 1, 2004;
15(11):
5118 - 5129.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Lefebvre, H. Batoko, G. Duby, and M. Boutry
Targeting of a Nicotiana plumbaginifolia H+-ATPase to the Plasma Membrane Is Not by Default and Requires Cytosolic Structural Determinants
PLANT CELL,
July 1, 2004;
16(7):
1772 - 1789.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Wang, G. Holroyd, A. M. Hetherington, and C. K-Y. Ng
Seeing 'cool' and 'hot'--infrared thermography as a tool for non-invasive, high-throughput screening of Arabidopsis guard cell signalling mutants
J. Exp. Bot.,
June 1, 2004;
55(400):
1187 - 1193.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Kuliawat, E. Kalinina, J. Bock, L. Fricker, T. E. McGraw, S. R. Kim, J. Zhong, R. Scheller, and P. Arvan
Syntaxin-6 SNARE Involvement in Secretory and Endocytic Pathways of Cultured Pancreatic {beta}-Cells
Mol. Biol. Cell,
April 1, 2004;
15(4):
1690 - 1701.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Mazel, Y. Leshem, B. S. Tiwari, and A. Levine
Induction of Salt and Osmotic Stress Tolerance by Overexpression of an Intracellular Vesicle Trafficking Protein AtRab7 (AtRabG3e)
Plant Physiology,
January 1, 2004;
134(1):
118 - 128.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. S. Nuhse, T. Boller, and S. C. Peck
A Plasma Membrane Syntaxin Is Phosphorylated in Response to the Bacterial Elicitor Flagellin
J. Biol. Chem.,
November 14, 2003;
278(46):
45248 - 45254.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Pimpl, S. L. Hanton, J. P. Taylor, L. L. Pinto-daSilva, and J. Denecke
The GTPase ARF1p Controls the Sequence-Specific Vacuolar Sorting Route to the Lytic Vacuole
PLANT CELL,
May 1, 2003;
15(5):
1242 - 1256.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
P. Wick, X. Gansel, C. Oulevey, V. Page, I. Studer, M. Durst, and L. Sticher
The Expression of the t-SNARE AtSNAP33 Is Induced by Pathogens and Mechanical Stimulation
Plant Physiology,
May 1, 2003;
132(1):
343 - 351.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Zhu, Z. Gong, C. Zhang, C.-P. Song, B. Damsz, G. Inan, H. Koiwa, J.-K. Zhu, P. M. Hasegawa, and R. A. Bressan
OSM1/SYP61: A Syntaxin Protein in Arabidopsis Controls Abscisic Acid-Mediated and Non-Abscisic Acid-Mediated Responses to Abiotic Stress
PLANT CELL,
December 1, 2002;
14(12):
3009 - 3028.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. A. Eckardt
Specificity and Cross-Talk in Plant Signal Transduction: January 2002 Keystone Symposium
PLANT CELL,
May 1, 2002;
14(90001):
S9 - 14.
[Full Text]
[PDF]
|
|
|
|
|
