Syntaxin of plant proteins SYP123 and SYP132 mediate root hair tip growth in Arabidopsis thaliana.

Root hairs are fast-growing tubular protrusions on root epidermal cells that play important roles in water and nutrient uptake in plants. The tip-focused polarized growth of root hairs is accomplished by the secretion of newly synthesized materials to the tip via the polarized membrane trafficking mechanism. Here, we report the function of two different types of plasma membrane (PM) Qa-SNAREs (soluble N-ethylmaleimide-sensitive factor attachment protein receptors), SYP123 and SYP132, in the growth of root hair in Arabidopsis. We found that SYP123, but not SYP132, localizes in the tip region of root hairs by recycling between the brefeldin A (BFA)-sensitive endosomes and the PM of the expanding tip in an F-actin-dependent manner. The vesicle-associated membrane proteins VAMP721/722/724 also exhibited tip-focused localization in root hairs and formed ternary SNARE complexes with both SYP123 and SYP132. These results demonstrate that SYP123 and SYP132 act in a coordinated fashion to mediate tip-focused membrane trafficking for root hair tip growth.

[1]  G. Jürgens,et al.  SNARE complexes of different composition jointly mediate membrane fusion in Arabidopsis cytokinesis , 2013, Molecular biology of the cell.

[2]  P. Schulze-Lefert,et al.  Requirement of vesicle-associated membrane protein 721 and 722 for sustained growth during immune responses in Arabidopsis , 2013, Molecules and cells.

[3]  Do-Hyung Kim,et al.  dRAGging amino Acid-mTORC1 signaling by SH3BP4 , 2013, Molecules and cells.

[4]  G. Jürgens,et al.  Mechanisms of Functional Specificity Among Plasma‐Membrane Syntaxins in Arabidopsis , 2011, Traffic.

[5]  A. Nakano,et al.  A membrane trafficking pathway regulated by the plant-specific RAB GTPase ARA6 , 2011, Nature Cell Biology.

[6]  R. Malhó,et al.  Localization of Arabidopsis SYP125 syntaxin in the plasma membrane sub-apical and distal zones of growing pollen tubes , 2011, Plant signaling & behavior.

[7]  Naohiro Kato,et al.  Expression, localization and interaction of SNARE proteins in Arabidopsis are selectively altered by the dark , 2010 .

[8]  F. Baluška,et al.  Structural Sterols Are Involved in Both the Initiation and Tip Growth of Root Hairs in Arabidopsis thaliana[W] , 2010, Plant Cell.

[9]  G. Di Sansebastiano,et al.  Asymmetric localization of Arabidopsis SYP124 syntaxin at the pollen tube apical and sub-apical zones is involved in tip growth , 2010, BMC Plant Biology.

[10]  Naohiro Kato,et al.  Luminescence detection of SNARE–SNARE interaction in Arabidopsis protoplasts , 2010, Plant Molecular Biology.

[11]  A. Nakano,et al.  Differential expression control and polarized distribution of plasma membrane-resident SYP1 SNAREs in Arabidopsis thaliana. , 2009, Plant & cell physiology.

[12]  P. Schulze-Lefert,et al.  Activity Determinants and Functional Specialization of Arabidopsis PEN1 Syntaxin in Innate Immunity* , 2008, Journal of Biological Chemistry.

[13]  M. Sauer,et al.  ARF GEF-Dependent Transcytosis and Polar Delivery of PIN Auxin Carriers in Arabidopsis , 2008, Current Biology.

[14]  G. Jürgens,et al.  Co-option of a default secretory pathway for plant immune responses , 2008, Nature.

[15]  Detlef Weigel,et al.  Gene silencing in plants using artificial microRNAs and other small RNAs. , 2008, The Plant journal : for cell and molecular biology.

[16]  R. Panstruga,et al.  SNARE-ware: the role of SNARE-domain proteins in plant biology. , 2007, Annual review of cell and developmental biology.

[17]  Nicholas J. Provart,et al.  An “Electronic Fluorescent Pictograph” Browser for Exploring and Analyzing Large-Scale Biological Data Sets , 2007, PloS one.

[18]  Naohiro Kato,et al.  Split luciferase complementation assay to study protein-protein interactions in Arabidopsis protoplasts. , 2007, The Plant journal : for cell and molecular biology.

[19]  K. Findlay,et al.  The syntaxin SYP132 contributes to plant resistance against bacteria and secretion of pathogenesis-related protein 1 , 2007, Proceedings of the National Academy of Sciences.

[20]  A. Sanderfoot Increases in the Number of SNARE Genes Parallels the Rise of Multicellularity among the Green Plants1[W][OA] , 2007, Plant Physiology.

[21]  K. Czymmek,et al.  Medicago truncatula syntaxin SYP132 defines the symbiosome membrane and infection droplet membrane in root nodules , 2007, Planta.

[22]  J. Šamaj,et al.  Vesicular trafficking, cytoskeleton and signalling in root hairs and pollen tubes. , 2006, Trends in plant science.

[23]  David A Jones,et al.  Re-organization of the cytoskeleton and endoplasmic reticulum in the Arabidopsis pen1-1 mutant inoculated with the non-adapted powdery mildew pathogen, Blumeria graminis f. sp. hordei. , 2006, Molecular plant pathology.

[24]  M. Blatt,et al.  Selective Mobility and Sensitivity to SNAREs Is Exhibited by the Arabidopsis KAT1 K+ Channel at the Plasma Membrane[W] , 2006, The Plant Cell Online.

[25]  P. Schulze-Lefert,et al.  Nonhost resistance in Arabidopsis-Colletotrichum interactions acts at the cell periphery and requires actin filament function. , 2006, Molecular plant-microbe interactions : MPMI.

[26]  Fumihiko Sato,et al.  PGP4, an ATP Binding Cassette P-Glycoprotein, Catalyzes Auxin Transport in Arabidopsis thaliana Rootsw⃞ , 2005, The Plant Cell Online.

[27]  F. Baluška,et al.  Endocytosis and vesicle trafficking during tip growth of root hairs , 2005, Protoplasma.

[28]  Laurie G. Smith,et al.  Spatial control of cell expansion by the plant cytoskeleton. , 2005, Annual review of cell and developmental biology.

[29]  A. Nakano,et al.  Actin-based motility of endosomes is linked to the polar tip growth of root hairs. , 2005, European journal of cell biology.

[30]  W. Hong SNAREs and traffic. , 2005, Biochimica et biophysica acta.

[31]  Paul Schulze-Lefert,et al.  Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[32]  B. Scheres,et al.  Dissection of Arabidopsis ADP-RIBOSYLATION FACTOR 1 Function in Epidermal Cell Polarityw⃞ , 2005, The Plant Cell Online.

[33]  A. Nakano,et al.  Functional differentiation of endosomes in Arabidopsis cells. , 2004, The Plant journal : for cell and molecular biology.

[34]  Heather Youngs,et al.  The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. , 2004, Molecular biology of the cell.

[35]  M. Preuss,et al.  The Arabidopsis Rab GTPase RabA4b Localizes to the Tips of Growing Root Hair Cells , 2004, The Plant Cell Online.

[36]  A. Nakano,et al.  Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells. , 2004, Cell structure and function.

[37]  T. Boller,et al.  A Plasma Membrane Syntaxin Is Phosphorylated in Response to the Bacterial Elicitor Flagellin* , 2003, Journal of Biological Chemistry.

[38]  Erich Kombrink,et al.  SNARE-protein-mediated disease resistance at the plant cell wall , 2003, Nature.

[39]  R. Sessions,et al.  Tyrphostin A23 Inhibits Internalization of the Transferrin Receptor by Perturbing the Interaction between Tyrosine Motifs and the Medium Chain Subunit of the AP-2 Adaptor Complex* , 2003, The Journal of Biological Chemistry.

[40]  A. Nakano,et al.  The Arabidopsis GNOM ARF-GEF Mediates Endosomal Recycling, Auxin Transport, and Auxin-Dependent Plant Growth , 2003, Cell.

[41]  L. Dolan,et al.  Building a hair: tip growth in Arabidopsis thaliana root hairs. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[42]  M. Blatt,et al.  The abscisic acid-related SNARE homolog NtSyr1 contributes to secretion and growth: evidence from competition with its cytosolic domain. , 2002, The Plant cell.

[43]  R Swarup,et al.  Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. , 2001, Genes & development.

[44]  J. Friml,et al.  Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth , 2001, The EMBO journal.

[45]  N. Chua,et al.  Technical advance: An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. , 2000, The Plant journal : for cell and molecular biology.

[46]  M. Blatt,et al.  A tobacco syntaxin with a role in hormonal control of guard cell ion channels. , 1999, Science.

[47]  A. Brunger,et al.  Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[48]  S. Clough,et al.  Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[49]  I. Waizenegger,et al.  The Arabidopsis KNOLLE Protein Is a Cytokinesis-specific Syntaxin , 1997, The Journal of cell biology.

[50]  L. Staehelin,et al.  Brefeldin A Effects in Plants (Are Different Golgi Responses Caused by Different Sites of Action?) , 1997, Plant physiology.

[51]  B. Satiat-Jeunemaitre,et al.  Brefeldin A effects in plant and fungal cells: something new about vesicle trafficking? , 1996, Journal of microscopy.

[52]  J. Lippincott-Schwartz,et al.  Brefeldin A: insights into the control of membrane traffic and organelle structure , 1992, The Journal of cell biology.

[53]  T. Ueda,et al.  The Role of RAB GTPases and SNARE Proteins in Plant Endocytosis and Post-Golgi Trafficking , 2012 .

[54]  M. Newman,et al.  A SNARE-protein has opposing functions in penetration resistance and defence signalling pathways. , 2007, The Plant journal : for cell and molecular biology.

[55]  S. Chandra,et al.  Endocytosis in Plants , 1994 .