Arabidopsis Synaptotagmin 1 Is Required for the Maintenance of Plasma Membrane Integrity and Cell Viability[W]

Plasma membrane repair in animal cells uses synaptotagmin 7, a Ca2+-activated membrane fusion protein that mediates delivery of intracellular membranes to wound sites by a mechanism resembling neuronal Ca2+-regulated exocytosis. Here, we show that loss of function of the homologous Arabidopsis thaliana Synaptotagmin 1 protein (SYT1) reduces the viability of cells as a consequence of a decrease in the integrity of the plasma membrane. This reduced integrity is enhanced in the syt1-2 null mutant in conditions of osmotic stress likely caused by a defective plasma membrane repair. Consistent with a role in plasma membrane repair, SYT1 is ubiquitously expressed, is located at the plasma membrane, and shares all domains characteristic of animal synaptotagmins (i.e., an N terminus-transmembrane domain and a cytoplasmic region containing two C2 domains with phospholipid binding activities). Our analyses support that membrane trafficking mediated by SYT1 is important for plasma membrane integrity and plant fitness.

[1]  M. Uemura,et al.  Calcium-Dependent Freezing Tolerance in Arabidopsis Involves Membrane Resealing via Synaptotagmin SYT1[W] , 2008, The Plant Cell Online.

[2]  M. Zhang,et al.  Dolichol Biosynthesis and Its Effects on the Unfolded Protein Response and Abiotic Stress Resistance in Arabidopsis[W][OA] , 2008, The Plant Cell Online.

[3]  D. Toomre,et al.  Repair of injured plasma membrane by rapid Ca2+-dependent endocytosis , 2008, The Journal of cell biology.

[4]  D. Takezawa,et al.  Long- and short-term freezing induce different types of injury in Arabidopsis thaliana leaf cells , 2007, Planta.

[5]  Filip Rolland,et al.  A central integrator of transcription networks in plant stress and energy signalling , 2007, Nature.

[6]  M. Craxton.  Evolutionary genomics of plant genes encoding N-terminal-TM-C2 domain proteins and the similar FAM62 genes and synaptotagmin genes of metazoans , 2007, BMC Genomics.

[7]  R. Sagi-Eisenberg.  The mast cell: where endocytosis and regulated exocytosis meet , 2007, Immunological reviews.

[8]  Jianhua Zhu,et al.  An Enhancer Mutant of Arabidopsis salt overly sensitive 3 Mediates both Ion Homeostasis and the Oxidative Stress Response , 2007, Molecular and Cellular Biology.

[9]  Andrew G. Clark,et al.  Rehabilitation and the single cell. , 2007, Current opinion in cell biology.

[10]  A. Harfouche,et al.  The Arabidopsis Tetratricopeptide Repeat-Containing Protein TTL1 Is Required for Osmotic Stress Responses and Abscisic Acid Sensitivity1[W] , 2006, Plant Physiology.

[11]  Thomas C. Südhof,et al.  A Complexin/Synaptotagmin 1 Switch Controls Fast Synaptic Vesicle Exocytosis , 2006, Cell.

[12]  O. Borsani,et al.  ABA- and ethylene-mediated responses in osmotically stressed tomato are regulated by the TSS2 and TOS1 loci. , 2006, Journal of experimental botany.

[13]  F. Baluška,et al.  Cytokinesis in plant and animal cells: endosomes 'shut the door'. , 2006, Developmental biology.

[14]  K. S. Deshpande,et al.  Human protein reference database—2006 update , 2005, Nucleic Acids Res..

[15]  N. Andrews,et al.  There's more to life than neurotransmission: the regulation of exocytosis by synaptotagmin VII. , 2005, Trends in cell biology.

[16]  F. Baluška,et al.  The endocytic network in plants. , 2005, Trends in cell biology.

[17]  T. Kirchhausen,et al.  An emergency response team for membrane repair , 2005, Nature Reviews Molecular Cell Biology.

[18]  N. Andrews.  Membrane Resealing: Synaptotagmin VII Keeps Running the Show , 2005, Science's STKE.

[19]  Frantisek Baluska,et al.  Plant synapses: actin-based domains for cell-to-cell communication. , 2005, Trends in plant science.

[20]  C. Larsson,et al.  Arabidopsis plasma membrane proteomics identifies components of transport, signal transduction and membrane trafficking. , 2004, Plant & cell physiology.

[21]  P. Zimmermann,et al.  GENEVESTIGATOR. Arabidopsis Microarray Database and Analysis Toolbox1[w] , 2004, Plant Physiology.

[22]  T. Südhof,et al.  Structural basis for the evolutionary inactivation of Ca2+ binding to synaptotagmin 4 , 2004, Nature Structural &Molecular Biology.

[23]  M. Craxton.  Synaptotagmin gene content of the sequenced genomes , 2004, BMC Genomics.

[24]  T. Sūdhof.  The synaptic vesicle cycle. , 2004, Annual review of neuroscience.

[25]  O. Borsani,et al.  Regulation of K+ Transport in Tomato Roots by the TSS1 Locus. Implications in Salt Tolerance1 , 2004, Plant Physiology.

[26]  Kurt W. Marek,et al.  Synaptotagmin I is necessary for compensatory synaptic vesicle endocytosis in vivo , 2003, Nature.

[27]  P. Mcneil,et al.  Plasma membrane disruption: repair, prevention, adaptation. , 2003, Annual review of cell and developmental biology.

[28]  M. Uemura,et al.  Mass spectrometric approach for identifying putative plasma membrane proteins of Arabidopsis leaves associated with cold acclimation. , 2003, The Plant journal : for cell and molecular biology.

[29]  Chien-Chang Chen,et al.  Defective membrane repair in dysferlin-deficient muscular dystrophy , 2003, Nature.

[30]  O. Borsani,et al.  Developing salt tolerant plants in a new century: a molecular biology approach , 2003, Plant Cell, Tissue and Organ Culture.

[31]  Jian-Kang Zhu,et al.  ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. , 2003, Genes & development.

[32]  T. Südhof,et al.  Sr2+ Binding to the Ca2+ Binding Site of the Synaptotagmin 1 C2B Domain Triggers Fast Exocytosis without Stimulating SNARE Interactions , 2003, Neuron.

[33]  O. Borsani,et al.  Tomato tos1 mutation identifies a gene essential for osmotic tolerance and abscisic acid sensitivity. , 2002, The Plant journal : for cell and molecular biology.

[34]  Jianhua Zhu,et al.  OSM1/SYP61: A Syntaxin Protein in Arabidopsis Controls Abscisic Acid–Mediated and Non-Abscisic Acid–Mediated Responses to Abiotic Stress , 2002, The Plant Cell Online.

[35]  T. Südhof,et al.  Structure/Function Analysis of Ca2+ Binding to the C2A Domain of Synaptotagmin 1 , 2002, The Journal of Neuroscience.

[36]  K. Mikoshiba,et al.  Alternative splicing isoforms of synaptotagmin VII in the mouse, rat and human. , 2002, The Biochemical journal.

[37]  T. Südhof.  Synaptotagmins: Why So Many?* , 2002, The Journal of Biological Chemistry.

[38]  T. Südhof,et al.  Three-Dimensional Structure of the Synaptotagmin 1 C2B-Domain Synaptotagmin 1 as a Phospholipid Binding Machine , 2001, Neuron.

[39]  M. Ishitani,et al.  FIERY1 encoding an inositol polyphosphate 1-phosphatase is a negative regulator of abscisic acid and stress signaling in Arabidopsis. , 2001, Genes & development.

[40]  E. Caler,et al.  Plasma Membrane Repair Is Mediated by Ca2+-Regulated Exocytosis of Lysosomes , 2001, Cell.

[41]  L. Xiong,et al.  Abiotic stress signal transduction in plants: Molecular and genetic perspectives. , 2001, Physiologia plantarum.

[42]  T. Südhof,et al.  Synaptotagmin I functions as a calcium regulator of release probability , 2001, Nature.

[43]  C. Hawes,et al.  A Rab1 GTPase Is Required for Transport between the Endoplasmic Reticulum and Golgi Apparatus and for Normal Golgi Movement in Plants , 2000, Plant Cell.

[44]  H. Shi,et al.  The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[45]  H. Bohnert,et al.  PLANT CELLULAR AND MOLECULAR RESPONSES TO HIGH SALINITY. , 2000, Annual review of plant physiology and plant molecular biology.

[46]  C. Kim,et al.  The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[47]  C. Xiang,et al.  A mini binary vector series for plant transformation , 1999, Plant Molecular Biology.

[48]  John A. Faulkner,et al.  Progressive Muscular Dystrophy in α-Sarcoglycan–deficient Mice , 1998, The Journal of cell biology.

[49]  T. Südhof,et al.  Ca2+ binding to synaptotagmin: how many Ca2+ ions bind to the tip of a C2‐domain? , 1998, The EMBO journal.

[50]  Jiping Liu,et al.  A calcium sensor homolog required for plant salt tolerance. , 1998, Science.

[51]  M. Ishitani,et al.  Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis: interactions and convergence of abscisic acid-dependent and abscisic acid-independent pathways. , 1997, The Plant cell.

[52]  D. Prasher,et al.  Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[53]  F. Baluška,et al.  Immunofluorescence Detection of F-actin on Low Melting Point Wax Sections from Plant Tissues , 1997, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[54]  T. Südhof,et al.  Bipartite Ca2+-Binding Motif in C2 Domains of Synaptotagmin and Protein Kinase C , 1996, Science.

[55]  J. Mathur,et al.  Enhanced green fluorescence by the expression of an Aequorea victoria green fluorescent protein mutant in mono- and dicotyledonous plant cells. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[56]  K. Miyake,et al.  Vesicle accumulation and exocytosis at sites of plasma membrane disruption , 1995, The Journal of cell biology.

[57]  G. Bi,et al.  Calcium-regulated exocytosis is required for cell membrane resealing , 1995, The Journal of cell biology.

[58]  S. Sprang,et al.  Structure of the first C2 domain of synaptotagmin I: A novel Ca2+/phospholipid-binding fold , 1995, Cell.

[59]  Yaoguang Liu,et al.  Thermal asymmetric interlaced PCR: automatable amplification and sequencing of insert end fragments from P1 and YAC clones for chromosome walking. , 1995, Genomics.

[60]  T. Südhof,et al.  Synaptotagmin I: A major Ca2+ sensor for transmitter release at a central synapse , 1994, Cell.

[61]  P. Sealy,et al.  Emergency response team. , 1994, The Canadian nurse.

[62]  G. Bi,et al.  Cell membrane resealing by a vesicular mechanism similar to neurotransmitter release. , 1994, Science.

[63]  T. Südhof,et al.  Synaptotagmin: a calcium sensor on the synaptic vesicle surface. , 1992, Science.

[64]  J. Dixon,et al.  Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. , 1991, Analytical biochemistry.

[65]  J. Ervasti,et al.  Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle , 1990, Nature.

[66]  M. Bevan,et al.  GUS fusions: beta‐glucuronidase as a sensitive and versatile gene fusion marker in higher plants. , 1987, The EMBO journal.

[67]  A. Ullrich,et al.  Multiple, distinct forms of bovine and human protein kinase C suggest diversity in cellular signaling pathways. , 1986, Science.

[68]  K. Schumaker,et al.  A Ca/H Antiport System Driven by the Proton Electrochemical Gradient of a Tonoplast H-ATPase from Oat Roots. , 1985, Plant physiology.

[69]  M. M. Bradford.  A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[70]  F. Baluška,et al.  Endocytosis of cell surface material mediates cell plate formation during plant cytokinesis. , 2006, Developmental cell.

[71]  R. Bressan,et al.  Identification of plant stress-responsive determinants in Arabidopsis by large-scale forward genetic screens. , 2006, Journal of experimental botany.

[72]  Natalie Wilson.  Human Protein Reference Database , 2004, Nature Reviews Genetics.

[73]  Natalie Wilson,et al.  Human Protein Reference Database , 2004, Nature Reviews Molecular Cell Biology.

[74]  Jian-Kang Zhu,et al.  Salt and drought stress signal transduction in plants. , 2002, Annual review of plant biology.

[75]  E. Haber.  The Cell Membrane , 1984, Springer US.

[76]  Koorie Dhoulagarle,et al.  There's more to life , 1979 .