The reorganization of actin filaments is required for vacuolar fusion of guard cells during stomatal opening in Arabidopsis

Plant, Cell and Environment

Volumn 36, Issue 2, 2013, Pages 484-497

  Li, Li Juan ^a   Ren, Fei ^a   Gao, Xin Qi ^b   Wei, Peng Cheng ^a   Wang, Xue Chen ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b SHANDONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

Actin related protein 2 3 complex; Stomatal movement; Vacuole

Indexed keywords

ACTIN; ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 3; ARABIDOPSIS PROTEIN; ARP2 PROTEIN, ARABIDOPSIS; CYTOCHALASIN D; DIS1 PROTEIN, ARABIDOPSIS; GREEN FLUORESCENT PROTEIN; PHALLOIDIN;

CELL ORGANELLE; CYTOLOGY; DICOTYLEDON; MEMBRANE; MUTATION; PHYSIOLOGY; PHYTOCHEMISTRY; PROTEIN; STOMATA;

ACTIN FILAMENT; ARABIDOPSIS; ARTICLE; CELL VACUOLE; CYTOLOGY; DRUG EFFECT; GENETICS; LIGHT; MEMBRANE FUSION; METABOLISM; MUTATION; PHYSIOLOGY; PLANT STOMA; POLYMERIZATION; RADIATION EXPOSURE; TIME LAPSE IMAGING;

ACTIN CYTOSKELETON; ACTIN-RELATED PROTEIN 2; ACTIN-RELATED PROTEIN 3; ACTINS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CYTOCHALASIN D; GREEN FLUORESCENT PROTEINS; LIGHT; MEMBRANE FUSION; MUTATION; PHALLOIDINE; PLANT STOMATA; POLYMERIZATION; TIME-LAPSE IMAGING; VACUOLES;

ARABIDOPSIS;

EID: 84871926629     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2012.02592.x     Document Type: Article

References (50)

1. Avisar D., Prokhnevsky A.I., Makarova K.S., Koonin E.V. & Dolja V.V. (2008) Myosin XI-K is required for rapid trafficking of Golgi stacks, peroxisomes, and mitochondria in leaf cells of Nicotiana benthamiana. Plant Physiology 146, 1098-1108.
2. Bick I., Thiel G. & Homann U. (2001) Cytochalasin D attenuates the desensitisation of pressure-stimulated vesicle fusion in guard cell protoplasts. European Journal of Cell Biology 80, 521-526.
3. Blatt M.R. (2000) Cellular signaling and volume control in stomatal movements in plants. Annual Review of Cell and Developmental Biology 16, 221-241.
4. Buchanan B., Gruissem W. & Jones R. (2000) Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists, Rockville, MD.
5. Carter C., Pan S., Zouhar J., Avila E.L., Girke T. & Raikhel N.V. (2004) The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. The Plant Cell 16, 3285-3303.
6. Chen N.Z. (2007) Functional analysis of ARP2 and ARP3 in response to salt and oxidative stress in Arabidopsis. Doctoral Dissertation, China Agricultural University, Beijing, China.
7. Choi Y., Lee Y., Jeon B.W., Staiger C.J. & Lee Y. (2008) Phosphatidylinositol 3- and 4-phosphate modulate actin filament reorganization in guard cells of day flower. Plant, Cell & Environment 31, 366-377.
8. Drengk A., Fritsch J., Schmauch C., Ruhling H. & Maniak M. (2003) A coat of filamentous actin prevents clustering of late-endosomal vacuoles in vivo. Current Biology 13, 1814-1819.
9. Eitzen G., Wang L., Thorngren N. & Wickner W. (2002) Remodeling of organelle-bound actin is required for yeast vacuole fusion. The Journal of Cell Biology 158, 669-679.
10. Eun S.O. & Lee Y. (1997) Actin filaments of guard cells are reorganized in response to light and abscisic acid. Plant Physiology 115, 1491-1498.
11. Eun S.O. & Lee Y. (2000) Stomatal opening by fusicoccin is accompanied by depolymerization of actin filaments in guard cells. Planta 210, 1014-1017.
12. Gao X.Q., Li C.G., Wei P.C., Zhang X.Y., Chen J. & Wang X.C. (2005) The dynamic changes of tonoplasts in guard cells are important for stomatal movement in Vicia faba. Plant Physiology 139, 1207-1216.
13. Gao X.Q., Chen J., Wei P.C., Ren F., Chen J. & Wang X.C. (2008) Array and distribution of actin filaments in guard cells contribute to the determination of stomatal aperture. Plant Cell Reports 27, 1655-1665.
14. Gao X.Q., Wang X.L., Ren F., Chen J. & Wang X.C. (2009) Dynamics of vacuoles and actin filaments in guard cells and their roles in stomatal movement. Plant, Cell & Environment 32, 1108-1116.
15. Higaki T., Kutsuna N., Okubo E., Sano T. & Hasezawa S. (2006) Actin microfilaments regulate vacuolar structures and dynamics: dual observation of actin microfilaments and vacuolar membrane in living tobacco BY-2 cells. Plant and Cell Physiology 47, 839-852.
16. Higaki T., Kutsuna N., Sano T., Kondo N. & Hasezawa S. (2009) Quantification and cluster analysis of actin cytoskeletal structures in plant cells: role of actin bundling in stomatal movement during diurnal cycles in Arabidopsis guard cells. The Plant Journal 61, 156-165.
17. Hoffmann A. & Nebenführ A. (2004) Dynamic rearrangements of transvacuolar strands in BY-2 cells imply a role of myosin in remodeling the plant actin cytoskeleton. Protoplasma 224, 201-210.
18. Holweg C.L. (2007) Living markers for actin block myosin-dependent motility of plant organelles and auxin. Cell Motility and the Cytoskeleton 64, 69-81.
19. Huang R.F., Wang X.C. & Lou C.H. (2000) Cytoskeletal inhibitors suppress the stomatal opening of Vicia faba L. induced by fusicoccin and IAA. Plant Science 156, 65-71.
20. Hunter P.R., Craddock C.P., Di Benedetto S., Roberts L.M. & Frigerio L. (2007) Fluorescent reporter proteins for the tonoplast and the vacuolar lumen identify a single vacuolar compartment in Arabidopsis cells. Plant Physiology 145, 1371-1382.
21. +-channel activities in guard cells of Vicia faba L. Plant Physiology 115, 335-342.
22. Hwang J.-U., Eun S.-O. & Lee Y. (2000) Structure and function of actin filaments in mature guard cells. In Actin: A Dynamic Framework for Multiple Plant Cell Functions (eds C.J. Staiger, F. Baluska, D. Volkmann & P.W. Barlow ), pp. 427-436. Kluwer Academic Publishers, Dordrecht.
23. Kim M., Hepler P.K., Eun S.O., Ha K.S. & Lee Y. (1995) Actin filaments in mature guard cells are radially distributed and involved in stomatal movement. Plant Physiology 109, 1077-1084.
24. Kutsuna N., Kumagai F., Sato M.H. & Hasezawa S. (2003) Three-dimensional reconstruction of tubular structure of vacuolar membrane throughout mitosis in living tobacco cells. Plant Cell Physiology 44, 1045-1054.
25. Le J., El-Assal Sel D., Basu D., Saad M.E. & Szymanski D.B. (2003) Requirements for Arabidopsis ATARP2 and ATARP3 during epidermal development. Current Biology 13, 1341-1347.
26. Li S., Blanchoin L., Yang Z. & Lord E.M. (2003) The putative Arabidopsis arp2/3 complex controls leaf cell morphogenesis. Plant Physiology 132, 2034-2044.
27. Li Y., Sorefan K., Hemmann G. & Bevan M.W. (2004) Arabidopsis NAP and PIR regulate actin-based cell morphogenesis and multiple developmental processes. Plant Physiology 136, 3616-3627.
28. + channels as targets of osmosensing in guard cells. The Plant Cell 10, 1957-1970.
29. MacRobbie E.A. & Kurup S. (2007) Signalling mechanisms in the regulation of vacuolar ion release in guard cells. New Phytologist 175, 630-640.
30. Maisch J., Fišerová J., Fischer L. & Nick P. (2009) Tobacco Arp3 is localized to actin-nucleating sites in vivo. The Journal of Experimental Botany 60, 603-614.
31. Marty F. (1999) Plant vacuoles. The Plant Cell 11, 587-600.
32. Mathur J., Mathur N., Kernebeck B. & Hulskamp M. (2003) Mutations in actin-related proteins 2 and 3 affect cell shape development in Arabidopsis. The Plant Cell 15, 1632-1645.
33. Ostrowicz C.W., Meiringer C.T. & Ungermann C. (2008) Yeast vacuole fusion: a model system for eukaryotic endomembrane dynamics. Autophagy 4, 5-19.
34. Ovecka M., Lang I., Baluska F., Ismail A., Illes P. & Lichtscheidl I.K. (2005) Endocytosis and vesicle trafficking during tip growth of root hairs. Protoplasma 226, 39-54.
35. Pandey S., Zhang W. & Assmann S.M. (2007) Roles of ion channels and transporters in guard cell signal transduction. FEBS Letters 581, 2325-2336.
36. Pollard T.D. (2007) Regulation of actin filament assembly by Arp2/3 complex and formins. Annual Review of Biophysics and Biomolecular Structure 36, 451-477.
37. Qualmann B., Kessels M.M. & Kelly R.B. (2000) Molecular links between endocytosis and the actin cytoskeleton. The Journal of Cell Biology 150, F111-F116.
38. Rauchenberger R., Hacker U., Murphy J., Niewohner J. & Maniak M. (1997) Coronin and vacuolin identify consecutive stages of a late, actin-coated endocytic compartment in Dictyostelium. Current Biology 7, 215-218.
39. Roelfsema M.R. & Hedrich R. (2005) In the light of stomatal opening: new insights into 'the Watergate'. New Phytologist 167, 665-691.
40. Schroeder J.I., Allen G.J., Hugouvieux V., Kwak J.M. & Waner D. (2001) Guard cell signal transduction. Annual Review of Plant Physiology and Plant Molecular Biology 52, 627-658.
41. Sheahan M.B., Rose R.J. & McCurdy D.W. (2007) Actin-filament-dependent remodeling of the vacuole in cultured mesophyll protoplasts. Protoplasma 230, 141-152.
42. Staiger C.J., Sheahan M.B., Khurana P., Wang X., McCurdy D.W. & Blanchoin L. (2009) Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array. The Journal of Cell Biology 184, 269-280.
43. Tanaka Y., Kutsuna N., Kanazawa Y., Kondo N., Hasezawa S. & Sano T. (2007) Intra-vacuolar reserves of membranes during stomatal closure: the possible role of guard cell vacuoles estimated by 3-D reconstruction. Plant and Cell Physiology 48, 1159-1169.
44. Uemura T., Yoshimura S.H., Takeyasu K. & Sato M.H. (2002) Vacuolar membrane dynamics revealed by GFP-AtVam3 fusion protein. Genes to Cells 7, 743-753.
45. Vitale M.L., Rodriguez Del Castillo A., Tchakarov L. & Trifaro J.M. (1991) Cortical filamentous actin disassembly and scinderin redistribution during chromaffin cell stimulation precede exocytosis, a phenomenon not exhibited by gelsolin. The Journal of Cell Biology 113, 1057-1067.
46. Wada M. & Suetsugu N. (2004) Plant organelle positioning. Current Opinion in Plant Biology 7, 626-631.
47. Wang Y.S., Yoo C.M. & Blancaflor E.B. (2007) Improved imaging of actin filaments in transgenic Arabidopsis plants expressing a green fluorescent protein fusion to the C- and N-termini of the fimbrin actin-binding domain 2. New Phytologist 177, 525-536.
48. Yoneda A., Kutsuna N., Higaki T., Oda Y., Sano T. & Hasezawa S. (2007) Recent progress in living cell imaging of plant cytoskeleton and vacuole using fluorescent-protein transgenic lines and three-dimensional imaging. Protoplasma 230, 129-139.
49. Zhang C., Mallery E.L., Schlueter J., Huang S., Fan Y., Brankle S., Staiger C.J. & Szymanski D.B. (2008) Arabidopsis SCARs function interchangeably to meet actin-related protein 2/3 activation thresholds during morphogenesis. The Plant Cell 20, 995-1011.
50. Zhang W., Fan L.M. & Wu W.H. (2007) Osmo-sensitive and stretch-activated calcium-permeable channels in Vicia faba guard cells are regulated by actin dynamics. Plant Physiology 143, 1140-1151.