A putative TRAPPII tethering factor is required for cell plate assembly during cytokinesis in Arabidopsis

New Phytologist

Volumn 187, Issue 3, 2010, Pages 751-763

  Jaber, Emad ^a   Thiele, Knut ^a   Kindzierski, Viktoria ^a   Loderer, Christoph ^a   Rybak, Katarzyna ^a   Jürgens, Gerd ^b   Mayer, Ulrike ^b   Söllner, Rosemarie ^a   Wanner, Gerhard ^c   Assaad, Farhah F ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY OF MUNICH   (Germany)

Author keywords

Arabidopsis; Cell plate biogenesis; Club; Cytokinesis; Tethering complex; TRAPPII

Indexed keywords

ARABIDOPSIS PROTEIN; MULTIPROTEIN COMPLEX; PROTEIN SUBUNIT;

CELL ORGANELLE; CYTOLOGY; GENETIC ANALYSIS; HERB; MEMBRANE; MICROSCOPY; MUTATION; PHENOTYPE;

ALLELE; ARABIDOPSIS; ARTICLE; CYTOKINESIS; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; MERISTEM; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLANT SEED; POLLEN; PRENATAL DEVELOPMENT; SEEDLING; ULTRASTRUCTURE; EMBRYOLOGY; PROTEIN SUBUNIT;

ALLELES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CONSERVED SEQUENCE; CYTOKINESIS; MERISTEM; MULTIPROTEIN COMPLEXES; MUTAGENESIS, INSERTIONAL; MUTATION; PHENOTYPE; POLLEN; PROTEIN SUBUNITS; SEEDLING; SEEDS;

ARABIDOPSIS;

EID: 77955164216     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2010.03331.x     Document Type: Article

References (68)

1. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R. Genomewide insertional mutagenesis of Arabidopsis thaliana. Science 2003, 301:653-657.
2. Assaad FF. Of weeds and men: what genomes teach us about plant cell biology. Current Opinion in Plant Biology 2001a, 4:478-487.
3. Assaad FF. Plant cytokinesis. Exploring the links. Plant Physiology 2001b, 126:509-516.
4. Assaad FF. The membrane dynamics of root hair morphogenesis. Root hairs 2009, 65-84. Emons AMCKetelar T. eds, Heidelberg, Germany, Springer Verlag
5. Assaad FF, Huet Y, Mayer U, Jürgens G. The cytokinesis gene KEULE encodes a Sec1 protein that binds the syntaxin KNOLLE. Journal of Cell Biology 2001, 152:531-543.
6. Assaad FF, Mayer U, Wanner G, Jürgens G. The KEULE gene is involved in cytokinesis in Arabidopsis. Molecular and General Genetics 1996, 253:267-277.
7. Azimzadeh J, Nacry P, Christodoulidou A, Drevensek S, Camilleri C, Amiour N, Parcy F, Pastuglia M, Bouchez D. Arabidopsis TONNEAU1 proteins are essential for preprophase band formation and interact with centrin. The Plant Cell 2008, 8:2146-2159.
8. Cai H, Reinisch K, Ferro-Novick S. Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Developmental Cell 2007, 12:671-682.
9. Cai H, Zhang Y, Pypaert M, Walker L, Ferro-Novick S. Mutants in trs120 disrupt traffic from the early endosome to the late Golgi. Journal of Cell Biology 2005, 171:823-833.
10. Cai Y, Chin HF, Lazarova D, Menon S, Fu C, Cai H, Sclafani A, Rodgers DW, De La Cruz EM, Ferro-Novick S. The structural basis for activation of the Rab Ypt1p by the TRAPP membrane-tethering complexes. Cell 2008, 133:1202-1213.
11. Cannon MC, Terneus K, Hall Q, Tan L, Wang Y, Wegenhart BL, Chen L, Lamport DT, Chen Y, Kieliszewski MJ. Self-assembly of the plant cell wall requires an extensin scaffold. Proceedings of the National Academy of Sciences, USA 2008, 12:2226-2231.
12. Chow CM, Neto H, Foucart C, Moore I. Rab-A2 and Rab-A3 GTPases define a trans-golgi endosomal membrane domain in Arabidopsis that contributes substantially to the cell plate. The Plant Cell 2008, 20:101-123.
13. Conibear E, Cleck JN, Stevens TH. Vps51p mediates the association of the GARP (Vps52/53/54) complex with the late Golgi t-SNARE Tlg1p. Molecular Biology of the Cell 2003, 14:1610-1623.
14. Cox R, Chen SH, Yoo E, Segev N. Conservation of the TRAPPII-specific subunits of a Ypt/Rab exchanger complex. BMC Evolutionary Biology 2007, 7:12.
15. Dettmer J, Hong-Hermesdorf A, Stierhof YD, Schumacher K. Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. The Plant Cell 2006, 18:715-730.
16. Dhonukshe P, Baluska F, Schlicht M, Hlavacka A, Samaj J, Friml J, Gadella TW. Endocytosis of cell surface material mediates cell plate formation during plant cytokinesis. Developmental Cell 2006, 10:137-150.
17. Fagard M, Desnos T, Desprez T, Goubet F, Refregier G, Mouille G, McCann M, Rayon C, Vernhettes S, Höfte H. PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. The Plant Cell 2000, 12:2409-2424.
18. Fujimoto M, Arimura S, Nakazono M, Tsutsumi N. Arabidopsis dynamin-related protein DRP2B is co-localized with DRP1A on the leading edge of the forming cell plate. Plant Cell Reports 2008, 27:1581-1586.
19. Grosshans BL, Ortiz D, Novick P. Rabs and their effectors: achieving specificity in membrane traffic. Proceedings of the National Academy of Sciences, USA 2006, 103:11821-11827.
20. Guermonprez H, Smertenko A, Crosnier MT, Durandet M, Vrielynck N, Guerche P, Hussey PJ, Satiat-Jeunemaitre B, Bonhomme S. The POK/AtVPS52 protein localizes to several distinct post-Golgi compartments in sporophytic and gametophytic cells. Journal of Experimental Botany 2008, 59:3087-3098.
21. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P. Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Advances in Bioinformatics 2008, 420747
22. Jander G, Norris SR, Rounsley SD, Bush DF, Levin IM, Last RL. Arabidopsis map-based cloning in the post-genome era. Plant Physiology 2002, 129:440-450.
23. Jones S, Newman C, Liu F, Segev N. The TRAPP complex is a nucleotide exchanger for Ypt1 and Ypt31/32. Molecular Biology of the Cell 2000, 11:4403-4411.
24. Jürgens G. Plant cytokinesis: fission by fusion. Trends in Cell Biology 2005, 15:277-283.
25. Kim YG, Raunser S, Munger C, Wagner J, Song YL, Cygler M, Walz T, Oh BH, Sacher M. The architecture of the multisubunit TRAPP I complex suggests a model for vesicle tethering. Cell 2006, 127:817-830.
26. Koumandou VL, Dacks JB, Coulson RM, Field MC. Control systems for membrane fusion in the ancestral eukaryote; evolution of tethering complexes and SM proteins. BMC Evolutionary Biology 2007, 7:29.
27. Krupnova T, Sasabe M, Ghebreghiorghis L, Gruber CW, Hamada T, Dehmel V, Strompen G, Stierhof YD, Lukowitz W, Kemmerling B. Microtubule-associated kinase-like protein RUNKEL needed [corrected] for cell plate expansion in Arabidopsis cytokinesis. Current Biology 2009, 19:518-523.
28. Lam SK, Siu CL, Hillmer S, Jang S, An G, Robinson DG, Jiang L. Rice SCAMP1 defines clathrin-coated, trans-golgi-located tubular-vesicular structures as an early endosome in tobacco BY-2 cells. The Plant Cell 2007, 19:296-319.
29. Lauber MH, Waizenegger I, Steinmann T, Schwarz H, Mayer U, Hwang I, Lukowitz W, Jürgens G. The Arabidopsis KNOLLE Protein is a cytokinesis-specific syntaxin. The Journal of Cell Biology 1997, 139:1485-1493.
30. Liu C, Johnson S, Wang TL. Cyd, a mutant of pea that alters embryo morphology is defective in cytokinesis. Developmental Genetics 1995, 16:321-331.
31. Lobstein E, Guyon A, Férault M, Twell D, Pelletier G, Bonhomme S. The putative Arabidopsis homolog of yeast vps52p is required for pollen tube elongation, localizes to Golgi, and might be involved in vesicle trafficking. Plant Physiology 2004, 135:1480-1490.
32. Lukowitz W, Gillmor CS, Scheible WR. Positional cloning in Arabidopsis. Why it feels good to have a genome initiative working for you. Plant Physiology 2000, 123:795-805.
33. Lukowitz W, Mayer U, Jürgens G. Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell 1996, 84:61-71.
34. Mayer U, Ruiz RAT, Berleth T, Misera S, Jürgens G. Mutations affecting body organization in the Arabidopsis embryo. Nature 1991, 353:402-407.
35. Mellman I, Warren G. The road taken: past and future foundations of membrane traffic. Cell 2000, 100:99-112.
36. Morozova N, Liang Y, Tokarev AA, Chen SH, Cox R, Andrejic J, Lipatova Z, Sciorra VA, Emr SD, Segev N. TRAPPII subunits are required for the specificity switch of a Ypt-Rab GEF. Nature Cell Biology 2006, 8:1263-1269.
37. Müller S, Smertenko A, Wagner V, Heinrich M, Hussey PJ, Hauser MT. The plant microtubule-associated protein AtMAP65-3/PLE is essential for cytokinetic phragmoplast function. Current Biology 2004, 14:412-417.
38. Nickle TC, Meinke DW. A cytokinesis-defective mutant of Arabidopsis (cyt1) characterized by embryonic lethality, incomplete cell walls, and excessive callose accumulation. Plant Journal 1998, 15:321-332.
39. Nicol F, His I, Jauneau A, Vernhettes S, Canut H, Höfte H. A plasma membrane-bound putative endo-1,4-beta-D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO Journal 1998, 17:5563-5576.
40. Otegui MS, Spitzer C. Endosomal functions in plants. Traffic 2008, 9:1589-1598.
41. Reichardt I, Stierhof YD, Mayer U, Richter S, Schwarz H, Schumacher K, Jürgens G. Plant cytokinesis requires de novo secretory trafficking but not endocytosis. Current Biology 2007, 17:2047-2053.
42. Rojo E, Gillmor CS, Kovaleva V, Somerville CR, Raikhel NV. VACUOLELESS1 is an essential gene required for vacuole formation and morphogenesis in Arabidopsis. Developmental Cell 2001, 1:303-310.
43. Rojo E, Zouhar J, Kovaleva V, Hong S, Raikhel NV. The AtC-VPS protein complex is localized to the tonoplast and the prevacuolar compartment in arabidopsis. Molecular Biology of the Cell 2003, 14:361-369.
44. Sacher M, Kim YG, Lavie A, Oh BH, Segev N. The TRAPP complex: insights into its architecture and function. Traffic 2008, 12:2032-2042.
45. Samuels AL, Giddings TH, Staehelin LA. Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. The Journal of Cell Biology 1995, 130:1345-1357.
46. Sanderfoot AA, Assaad FF, Raikhel NV. The Arabidopsis genome. An abundance of soluble N-ethylmaleimide-sensitive factor adaptor protein receptors. Plant Physiology 2000, 124:1558-1569.
47. Schellmann S, Pimpl P. Coats of endosomal protein sorting: retromer and ESCRT. Current Opinion in Plant Biology 2009, 12:670-676.
48. Scholl RL, May ST, Ware DH. Seed and molecular resources for Arabidopsis. Plant Physiology 2000, 124:1477-1480.
49. Schumann U, Prestele J, O'Geen H, Brueggeman R, Wanner G, Gietl C. Requirement of the C3HC4 zinc RING finger of the Arabidopsis PEX10 for photorespiration and leaf peroxisome contact with chloroplasts. Proceedings of the National Academy of Sciences, USA 2007, 104:1069-1074.
50. Seguí-Simarro JM, Austin JR, White EA, Staehelin LA. Electron tomographic analysis of somatic cell plate formation in meristematic cells of Arabidopsis preserved by high-pressure freezing. The Plant Cell 2004, 16:836-856.
51. Shen J, Tareste DC, Paumet F, Rothman JE, Melia TJ. Selective activation of cognate SNAREpins by Sec1/Munc18 proteins. Cell 2007, 128:183-195.
52. Söllner R, Glasser G, Wanner G, Somerville CR, Jürgens G, Assaad FF. Cytokinesis-defective mutants of Arabidopsis. Plant Physiology 2002, 129:678-690.
53. Spitzer C, Reyes FC, Buono R, Sliwinski MK, Haas TJ, Otegui MS. The ESCRT-related CHMP1A and B proteins mediate multivesicular body sorting of auxin carriers in Arabidopsis and are required for plant development. The Plant Cell 2009, 21:749-766.
54. Spitzer C, Schellmann S, Sabovljevic A, Shahriari M, Keshavaiah C, Bechtold N, Herzog M, Müller S, Hanisch FG, Hülskamp M. The Arabidopsis elch mutant reveals functions of an ESCRT component in cytokinesis. Development 2006, 133:4679-4689.
55. Staehelin LA, Kang BH. Nanoscale architecture of endoplasmic reticulum export sites and of Golgi membranes as determined by electron tomography. Plant Physiology 2008, 147:1454-1468.
56. Strompen G, El Kasmi F, Richter S, Lukowitz W, Assaad FF, Jürgens G, Mayer U. The Arabidopsis HINKEL gene encodes a kinesin-related protein involved in cytokinesis and is expressed in a cell cycle-dependent manner. Currrent Biology 2002, 12:153-158.
57. Swarbreck D, Wilks C, Lamesch P, Berardini TZ, Garcia-Hernandez M, Foerster H, Li D, Meyer T, Muller R, Ploetz L. The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucleic Acids Research 2008, 36:1009-1014.
58. Thiele K, Wanner G, Kindzierski V, Jürgens G, Mayer U, Pachl F, Assaad FF. The timely deposition of callose is essential for cytokinesis in Arabidopsis. Plant Journal 2009, 58:13-26.
59. Torres-Ruiz RA, Jürgens G. Mutations in the FASS gene uncouple pattern formation and morphogenesis in Arabidopsis development. Development 1994, 10:2967-2978.
60. Vernoud V, Horton AC, Yang Z, Nielsen E. Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiology 2003, 131:1191-1208.
61. Völker A, Stierhof YD, Jürgens G. Cell cycle-independent expression of the Arabidopsis cytokinesis-specific syntaxin KNOLLE results in mistargeting to the plasma membrane and is not sufficient for cytokinesis. Journal of Cell Science 2001, 114:3001-3012.
62. Waizenegger I, Lukowitz W, Assaad FF, Schwarz H, Jürgens G, Mayer U. The Arabidopsis KNOLLE and KEULE genes interact to promote fusion of cytokinetic vesicles during cell plate formation. Current Biology 2000, 10:1371-1374.
63. Walker KL, Müller S, Moss D, Ehrhardt DW, Smith LG. Arabidopsis TANGLED identifies the division plane throughout mitosis and cytokinesis. Current Biology 2007, 17:1827-1836.
64. Williamson RE, Burn JE, Birch R, Baskin TI, Arioli T, Betzner AS, Cork A. Morphology of rsw1, a cellulose-deficient mutant of Arabidopsis thaliana. Protoplasma 2001, 215:116-127.
65. Wright AJ, Gallagher K, Smith LG. Discordia1 and alternate discordia1 function redundantly at the cortical division site to promote preprophase band formation and orient division planes in maize. The Plant Cell 2009, 21:234-247.
66. Yamasaki A, Menon S, Yu S, Barrowman J, Meerloo T, Oorschot V, Klumperman J, Satoh A, Ferro-Novick S. mTrs130 is a component of a mammalian TRAPPII complex, a Rab1 GEF that binds to COPI-coated vesicles. Molecular Biology of the Cell 2009, 19:4205-4215.
67. Yu S, Satoh A, Pypaert M, Mullen K, Hay JC, Ferro-Novick S. mBet3p is required for homotypic COPII vesicle tethering in mammalian cells. The Journal of Cell Biology 2006, 174:359-368.
68. Zheng H, Bednarek SY, Sanderfoot AA, Alonso J, Ecker JR, Raikhel NV. NPSN11 is a cell plate-associated SNARE protein that interacts with the syntaxin KNOLLE. Plant Physiology 2002, 129:530-539.