Disarrangement of actin filaments and Ca2+ gradient by CdCl2 alters cell wall construction in Arabidopsis thaliana root hairs by inhibiting vesicular trafficking

Journal of Plant Physiology

Volumn 168, Issue 11, 2011, Pages 1157-1167

  Fan, Jun Ling ^a,b   Wei, Xue Zhi ^b   Wan, Li Chuan ^a   Zhang, Ling Yun ^c   Zhao, Xue Qin ^a,b   Liu, Wei Zhong ^b   Hao, Huai Qin ^a   Zhang, Hai Yan ^a  

^a INSTITUTE OF BOTANY   (China)

^b SHANXI NORMAL UNIVERSITY   (China)

^c BEIJING FORESTRY UNIVERSITY   (China)

Author keywords

Actin filaments; Ca2+ gradient; Cadmium; Cell wall; Root hair

Indexed keywords

CADMIUM CHLORIDE; CALCIUM; CALCIUM CHANNEL; PECTIN;

ARABIDOPSIS; ARTICLE; CELL VACUOLE; CELL WALL; CONFOCAL MICROSCOPY; CYTOPLASM; DRUG EFFECT; FLUORESCENCE; GROWTH, DEVELOPMENT AND AGING; INFRARED SPECTROSCOPY; METABOLISM; MICROFILAMENT; PLANT ROOT; PLANT SEED; SEEDLING; ULTRASTRUCTURE;

ARABIDOPSIS; CADMIUM CHLORIDE; CALCIUM; CALCIUM CHANNELS; CELL WALL; CYTOPLASM; FLUORESCENCE; MICROFILAMENTS; MICROSCOPY, CONFOCAL; PECTINS; PLANT ROOTS; SEEDLING; SEEDS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; VACUOLES;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 79956368023     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2011.01.031     Document Type: Article

References (54)

1. Apostolova M.D., Christova T., Templeton D.M. Involvement of gelsolin in cadmium-induced disruption of the mesangial cell cytoskeleton. Toxicol Sci 2006, 89:465-474.
2. Baluska F., Salaj J., Mathur J., Braun M., Jasper F., Samaj J., et al. Root hair formation: F-actin-dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges. Dev Biol 2000, 227:618-632.
3. Bove J., Vaillancourt B., Kroeger J., Hepler P.K., Wiseman P.W., Geitmann A. Magnitude and direction of vesicle dynamics in growing pollen tubes using spatiotemporal image correlation spectroscopy and fluorescence recovery after photobleaching. Plant Physiol 2008, 147:1646-1658.
4. Brown D.M., Zeef L.A.H., Ellis J., Goodacre R., Turner S.R. Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 2005, 17:2281-2295.
5. Carol R.J., Dolan L. Building a hair: tip growth in Arabidopsis thaliana root hairs. Philos Trans R Soc Lond B Biol Sci 2002, 357:815-821.
6. Chaoui A., El Ferjani E. Effects of cadmium and copper on antioxidant capacities, lignification and auxin degradation in leaves of pea (Pisum sativum L.) seedlings. C R Biol 2005, 328:23-31.
7. Chen L., Carpita N.C., Reiter W.D., Wilson R.H., Jeffries C., McCann M.C. A rapid method to screen for cell-wall mutants using discriminant analysis of Fourier transform infrared spectra. Plant J 1998, 16:385-392.
8. Chen T., Teng N.J., Wu X.Q., Wang Y.H., Tang W., Samaj J., et al. Disruption of AFs by latrunculin B affects cell wall construction in Picea meyeri pollen tube by disturbing vesicle trafficking. Plant Cell Physiol 2007, 48:19-30.
9. Clemens S., Antosiewicz D.M., Ward J.M., Schachtman D.P., Schroeder J.I. The plant cDNA LCT1 mediates the uptake of calcium and cadmium in yeast. Proc Natl Acad Sci 1998, 95:12043-12048.
10. Crdenas L., Vidali L., Domnguez J., Prez H., Snchez F., Hepler P.K., et al. Rearrangement of actin microfilaments in plant root hairs responding to rhizobium etli nodulation signals. Plant Physiol 1998, 116:871-877.
11. Douchiche O., Rihouey C., Schaumann A., Driouich A., Morvan C. Cadmium-induced alterations of the structural features of pectins in flax hypocotyl. Planta 2007, 225:1301-1312.
12. Felle H.H., Hepler P.K. The Cytosolic Ca2+ Concentration gradient of Sinapis alba root hairs as revealed by Ca2+-selective microelectrode tests and Fura-Dextran ratio imaging. Plant Physiol 1997, 114:39-45.
13. Garcia-Rios V., Freile-Pelegrin Y., Robledo D., Mendoza-Cozatl D., Moreno-Sanchez R., Gold-Bouchot G. Cell wall composition affects Cd2+ accumulation and intracellular thiol peptides in marine red algae. Aquat Toxicol 2007, 81:65-72.
14. Garnier L., Simon-Plas F., Thuleau P., Agnel J.P., Blein J.P., Ranjeva R., et al. Cadmium affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity. Plant Cell Environ 2006, 29:1956-1969.
15. González-Guerrero M., Melville L.H., Ferrol N., Lott J.N., Azcón-Aguilar C., Peterson R.L. Ultrastructural localization of heavy metals in the extraradical mycelium and spores of the arbuscular mycorrhizal fungus Glomus intraradices. Can J Microbiol 2008, 54:103-110.
16. Hall J.L. Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 2002, 53:1-11.
17. Halperin S.J., Gilroy S., Lynch J.P. Sodium chloride reduces growth and cytosolic calcium, but does not affect cytosolic pH, in root hairs of Arabidopsis thaliana L. J Exp Bot 2003, 54:1269-1280.
18. Holdaway-Clarke T.L., Feijo J.A., Hackett G.R., Kunkel J.G., Hepler P.K. Pollen tube growth and the intracellular cytosolic calcium gradient oscillate in phase while extracellular calcium influx is delayed. Plant Cell 1997, 9:1999-2010.
19. Kazmirski S.L., Isaacson R.L., An C., Buckle A., Johnson C.M., Daggett V., et al. Loss of a metal-binding site in gelsolin leads to familial amyloidosis. Nat Struct Biol 2002, 9:112-116.
20. Khaitlina S., Hinssen H. Ca-dependent binding of actin to gelsolin. FEBS Lett. 2002, 521:14-18.
21. Kohorn B.D. Plasma membrane-cell wall contacts. Plant Physiol 2000, 124:31-38.
22. Lee Y.J., Szumlanski A., Nielsen E., Yang Z. Rho-GTPase-dependent filamentous actin dynamics coordinate vesicle targeting and exocytosis during tip growth. J Cell Biol 2008, 181:1155-1168.
23. Leshem Y., Melamed-Book N., Cagnac O., Ronen G., Nishri Y., Solomon M., et al. Suppression of Arabidopsis vesicle-SNARE expression inhibited fusion of H2O2-containing vesicles with tonoplast and increased salt tolerance. Proc Natl Acad Sci 2006, 103:18008-18013.
24. Leshem Y., Seri L., Levine A. Induction of phosphatidylinositol 3-kinase-mediated endocytosis by salt stress leads to intracellular production of reactive oxygen species and salt tolerance. Plant J 2007, 51:185-197.
25. Mathur J., Hulskamp M. Cell growth: how to grow and where to grow. Curr Biol 2001, 11:R402-R404.
26. Mikes J., Siglova M., Cejkova A., Masak J., Jirku V. The influence of heavy metals on the production of extracellular polymer substances in the processes of heavy metal ions elimination. Water Sci Technol 2005, 52:151-156.
27. Mouille G., Robin S., Lecomte M., Pagant S., Hofte H. Classification and identification of Arabidopsis cell wall mutants using Fourier-Transform InfraRed (FT-IR) microspectroscopy. Plant J 2003, 35:393-404.
28. Mouille G., Witucka-Wall H., Bruyant M.P., Loudet O., Pelletier S., Rihouey C., et al. Quantitative trait loci analysis of primary cell wall composition in Arabidopsis. Plant Physiol 2006, 141:1035-1044.
29. Mutwil M., Debolt S., Persson S. Cellulose synthesis. A complex complex. Curr Opin Plant Biol 2008, 11:352-357.
30. O'Neill M.A., Ishii T., Albersheim P., Darvill A.G. Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. Annu Rev Plant Biol 2004, 55:9-39.
31. Orvar B.L., Sangwan V., Omann F., Dhindsa R.S. Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. Plant J 2000, 23:785-794.
32. Ovecka M., Lang I., Baluska F., Ismail A., Illes P., Lichtscheidl I.K. Endocytosis and vesicle trafficking during tip growth of root hairs. Protoplasma 2005, 226:39-54.
33. Perfus-Barbeoch L., Leonhardt N., Vavasseur A., Forestier C. Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant J 2002, 32:539-548.
34. Powlin S.S., Keng P.C., Miller R.K. Toxicity of cadmium in human trophoblast cells (JAr choriocarcinoma): role of calmodulin and the calmodulin inhibitor, zaldaride maleate. Toxicol Appl Pharmacol 1997, 144:225-234.
35. Pribyl P., Cepák V., Zachleder V. Cytoskeletal alterations in interphase cells of the green alga Spirogyra decimina in response to heavy metals exposure. I: The effect of cadmium. Protoplasma 2005, 226:231-240.
36. Prozialeck W.C., Niewenhuis R.J. Cadmium (Cd2+) disrupts Ca2+-dependent cell-cell junctions and alters the pattern of E-cadherin immunofluorescence in LLC-PK1 cells. Biochem Biophys Res Commun 1991, 181:1118-1124.
37. Raize O., Argaman Y., Yannai S. Mechanisms of biosorption of different heavy metals by brown marine macroalgae. Biotechnol Bioeng 2004, 87:451-458.
38. Ringli C., Baumberger N., Diet A., Frey B., Keller B. ACTIN2 is essential for bulge site selection and tip growth during root hair development of Arabidopsis. Plant Physiol 2002, 129:1464-1472.
39. Roy S.J., Holdaway-Clarke T.L., Hackett G.R., Kunkel J.G., Lord E.M., Hepler P.K. Uncoupling secretion and tip growth in lily pollen tubes: evidence for the role of calcium in exocytosis. Plant J 1999, 19:379-386.
40. Samaj J., Muller J., Beck M., Bohm N., Menzel D. Vesicular trafficking, cytoskeleton and signalling in root hairs and pollen tubes. Trends Plant Sci 2006, 11:594-600.
41. Sherrier D.J., VandenBosch K.A. Secretion of cell wall polysaccharides in Vicia root hairs. Plant J 1994, 5:185-195.
42. Stohs S.J., Bagchi D., Hassoun E., Bagchi M. Oxidative mechanisms in the toxicity of chromium and cadmium ions. J Environ Pathol Toxicol Oncol 2000, 19:201-213.
43. Suzuki Y., Chao S.-H., Zysk J.R., Cheung W.Y. Stimulation of calmodulin by cadmium ion. Arch Toxicol 1985, 57:205-211.
44. Taylor L.P., Hepler P.K. Pollen germination and tube growth. Annu Rev Plant Physiol Plant Mol Biol 1997, 48:461-491.
45. Vassilieva E.V., Nusrat A. Vesicular trafficking: molecular tools and targets. Methods Mol Biol 2008, 440:3-14.
46. Verma K., Shekhawat G.S., Sharma A., Mehta S.K., Sharma V. Cadmium induced oxidative stress and changes in soluble and ionically bound cell wall peroxidase activities in roots of seedling and 3-4 leaf stage plants of Brassica juncea (L.) czern. Plant Cell Rep 2008, 27:1261-1269.
47. Voigt B., Timmers A.C., Samaj J., Muller J., Baluska F., Menzel D. GFP-FABD2 fusion construct allows in vivo visualization of the dynamic actin cytoskeleton in all cells of Arabidopsis seedlings. Eur J Cell Biol 2005, 84:595-608.
48. Wang Z., Templeton D.M. Cellular factors mediate cadmium-dependent actin depolymerization. Toxicol Appl Pharmacol 1996, 139:115-121.
49. Wightman R., Turner S.R. The roles of the cytoskeleton during cellulose deposition at the secondary cell wall. Plant J 2008, 54:794-805.
50. Willats W.G.T., McCartney L., Knox J.P. In situ analysis of pectic polysaccharides in seed mucilage and at the root surface of Arabidopsis thaliana. Planta 2001, 213:37-44.
51. Wymer C.L., Bibikova T.N., Gilroy S. Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. Plant J 1997, 12:427-439.
52. Zhang H., Qu X., Bao C., Khurana P., Wang Q., Xie Y., et al. Arabidopsis VILLIN5, an actin filament bundling and severing protein, is necessary for normal pollen tube growth. Plant Cell 2010, 22:2749-2767.
53. Zhang H.Y., Jiang Y.N., He Z.Y., Ma M. Cadmium accumulation and oxidative burst in garlic (Allium sativum). J Plant Physiol 2005, 162:977-984.
54. Zhang W.H., Rengel Z., Kuo J. Determination of intracellular Ca2+ in cells of intact wheat roots: loading of acetoxymethyl ester of Fluo-3 under low temperature. Plant J 1998, 15:147-151.