Visualization of highly dynamic F-actin plus ends in growing phaseolus vulgaris root hair cells and their responses to rhizobium etli nod factors

Plant and Cell Physiology

Volumn 55, Issue 3, 2014, Pages 580-592

  Zepeda, Isaac ^a   Sánchez López, Rosana ^a   Kunkel, Joseph G ^a   Bañuelos, Luis A ^a   Hernández Barrera, Alejandra ^a   Sánchez, Federico ^a   Quinto, Carmen ^a   Cárdenas, Luis ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

Author keywords

Fluorescently labeled cytochalasin D; Infection thread; Nodulation; Root hair; Tip growth

Indexed keywords

ACTIN; LIPOPOLYSACCHARIDE; NOD FACTOR, RHIZOBIUM ETLI;

ACTIN FILAMENT; DRUG EFFECTS; METABOLISM; PHASEOLUS; PLANT ROOT;

ACTIN CYTOSKELETON; ACTINS; LIPOPOLYSACCHARIDES; PHASEOLUS; PLANT ROOTS;

EID: 84899080498     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pct202     Document Type: Article

References (59)

1. Arrighi, J.F., Godfroy, O., de Billy, F., Saurat, O., Jauneau, A. and Gough, C. (2008) The RPG gene of Medicago truncatula controls Rhizobium-directed polar growth during infection. Proc. Natl Acad. Sci. USA 105: 9817-9822
2. Augustine, R.C., Vidali, L., Kleinman, K.P. and Bezanilla, M. (2008) Actin Depolymerizing factor is essential for viability in plants, and its phosphoregulation is important for tip growth. Plant J. 54: 863-875
3. Baluska, F., Salaj, J., Mathur, J., Braun, M., Jasper, F., Samaj, J. et al. (2000) 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. 227: 618-632
4. Blanco, F.A., Meschini, E.P., Zanetti, M.E. and Aguilar, O.M. (2009) A small GTPase of the Rab family is required for root hair formation and preinfection stages of the common bean-Rhizobium symbiotic association. Plant Cell 21: 2797-2810
5. Braun, M., Hauslage, J., Czogalla, A. and Limbach, C. (2004) Tiplocalized actin polymerization and remodeling, reflected by the localization of ADF, profilin and villin, are fundamental for gravity-sensing and polar growth in characean rhizoids. Planta 219: 379-388
6. Brewin, N. (2004) Plant cell wall remodelling in the Rhizobium-legume. Crit. Rev. Plant Sci. 23: 293-316
7. Cárdenas, L., Dominguez, J., Quinto, C., Lopez-Lara, I.M., Lugtenberg, B.J., Spaink, H.P. et al. (1995) Isolation, chemical structures and biological activity of the lipo-chitin oligosaccharide nodulation signals from Rhizobium etli. Plant Mol. Biol. 29: 453-464
8. Cárdenas, L., Holdaway-Clarke, T.L., Sanchez, F., Quinto, C., Feijo, J.A., Kunkel, J.G. et al. (2000) Ion changes in legume root hairs responding to Nod factors. Plant Physiol. 123: 443-452
9. Cárdenas, L., Lovy-Wheeler, A., Wilsen, K.L. and Hepler, P.K. (2005) Actin polymerization promotes the reversal of streaming in the apex of pollen tubes. Cell Motil. Cytoskel. 61: 112-127
10. Cárdenas, L. and Quinto, C. (2008) Reactive oxygen species (ROS) as early signals in root hair cells responding to rhizobial nodulation factors. Plant Signal. Behav. 3: 1101-1102
11. Cárdenas, L. (2009) New findings in the mechanisms regulating polar growth in root hair cells. Plant Signal Behav. 4: 4-8
12. Cárdenas, L., Vidali, L., Domínguez, J., Pérez, H., Sánchez, F., Hepler, P.K. et al. (1998) Rearrangement of actin microfilaments in plant root hairs responding to Rhizobium etli nodulation signals. Plant Physiol. 116: 871-877
13. Clifford, P., Richardson, S. and Hémon, D. (1989) Assessing the significance of the correlation between two spatial processes. Biometrics 45: 123-134
14. Chen, C.Y., Cheung., A.Y. and Wu, H.M. (2003) Actin-depolymerizing factor mediates Rac/Rop GTPase-regulated pollen tube growth. Plant Cell 15: 237-249
15. Chen, C.Y., Wong, E.I., Vidali, L., Estavillo, A., Hepler, P.K., Wu, H.M. et al. (2002) The regulation of actin organization by actindepolymerizing factor in elongating pollen tubes. Plant Cell 14: 2175-2190
16. Davidson, A.L. and Newcomb, H. (2001) Changes in actin microfilament arrays in Developing pea root nodule cells. Can. J. Bot. 79: 767-776
17. de Ruijter, N.C.A., Bisseling, T. and Emons, A. (1999) Rhizobium Nod factors induce an increase in sub-Apical fine bundles of actin filaments in Vicia sativa root hairs within minutes. Mol. Plant Microbe Interact. 12: 829-832
18. Fahraeus, G. (1957) The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J. Gen. Microbiol. 16: 374-381
19. Fan, X., Hou, J., Chen, X., Chaudhry, F., Staiger, C.J. and Ren, H. (2004) Identification and characterization of a Ca2+-dependent actin filament-severing protein from lily pollen. Plant Physiol. 136: 3979-3989
20. Fischer, U., Men, S. and Grebe, M. (2004) Lipid function in plant cell polarity. Curr. Opin. Plant Biol. 7: 670-676
21. Fisher, R.F. and Long, S.R. (1992) Rhizobium-plant signal exchange. Nature 357: 655-660
22. Foreman, J., Demidchik, V., Bothwell, J.H., Mylona, P., Miedema, H., Torres, M.A. et al. (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422: 442-446
23. Fournier, J., Timmers, A.C., Sieberer, B.J., Jauneau, A., Chabaud, M. and Barker, D.G. (2008) Mechanism of infection thread elongation in root hairs of Medicago truncatula and dynamic interplay with associated rhizobial colonization. Plant Physiol. 148: 1985-1995
24. Fricke, R., Gohl, C., Dharmalingam, E., Grevelhorster, A., Zahedi, B., Harden, N. et al. (2009) Drosophila Cip4/Toca-1 integrates membrane trafficking and actin Dynamics through WASP and SCAR/ WAVE. Curr. Biol. 19: 1429-1437
25. Gao, X.Q., Wang, X.L., Ren, F., Chen, J. and Wang, X.C. (2009) Dynamics of vacuoles and actin filaments in guard cells and their roles in stomatal movement. Plant Cell Environ. 32: 1108-1116
26. Gibbon, B.C., Kovar, D.R. and Staiger, C.J. (1999) Latrunculin B has different effects on pollen germination and tube growth. Plant Cell 11: 2349-2363
27. Hable, W.E., Miller, N.R. and Kropf, D.L. (2003) Polarity establishment requires dynamic actin in fucoid zygotes. Protoplasma 221: 193-204
28. He, X., Liu, Y.M., Wang, W. and Li, Y. (2006) Distribution of G-Actin is related to root hair growth of wheat. Ann. Bot. 98: 49-55
29. Hepler, P.K., Vidali, L. and Cheung, A.Y. (2001) Polarized cell growth in higher plants. Annu. Rev. Cell Dev. Biol. 17: 159-187
30. Hussey, P.J., Ketelaar, T. and Deeks, M.J. (2006) Control of the actin cytoskeleton in plant cell growth. Annu. Rev. Plant Biol. 57: 109-125
31. Jones, M.A., Raymond, M.J. and Smirnoff, N. (2006) Analysis of the root-hair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in Arabidopsis. Plant J. 45: 83-100
32. Ketelaar, T., de Ruijter, N.C. and Emons, A.M. (2003) Unstable F-Actin specifies the area and microtubule direction of cell expansion in Arabidopsis root hairs. Plant Cell 15: 285-292
33. Lhuissier, F., De Ruijter, N., Sieberer, B., Esseling, J.J. and Emons, A. (2001) Time course of cell biological events evoked in legume root hairs by Rhizobium Nod factors: State of the art. Ann. Bot. 87: 289-302
34. Lloyd, C.W., Pearce, K.J., Rawlins, D.J., Ridge, R.W. and Shaw, P.J. (1987) Endoplasmic microtubules connect the advancing nucleus to the tip of legume root hairs, but F-Actin is involved in basipetal migration. Cell Motil. Cytoskel. 8: 27-36
35. McKenna, S.T., Kunkel, J.G., Bosch, M., Rounds, C.M., Vidali, L., Winship, L.J. et al. (2009) Exocytosis precedes and predicts the increase in growth in oscillating pollen tubes. Plant Cell 21: 3026-3040
36. Miller, D.D., de Ruijter, N.C.A., Bisseling, T. and Emons, A.M. (1999) The role of actin in root hair morphogenesis: Studies with lipochitooligosaccharide as a growth stimulator and cytochalasin as an actin perturbing drug. Plant J. 17: 141-154
37. Miller, D.D., Leferink-Ten Klooster, H.B. and Emons, A.M. (2000) Lipochito-oligosaccharide nodulation factors stimulate cytoplasmic polarity with longitudinal endoplasmic reticulum and vesicles at the tip in vetch root hairs. Mol. Plant Microbe Interact. 13: 1385-1390
38. Miyahara, A., Richens, J., Starker, C., Morieri, G., Smith, L., Long, S. et al. (2010) Conservation in function of a SCAR/WAVE component during infection thread and root hair growth in Medicago truncatula. Mol. Plant Microbe Interact. 23: 1553-1562
39. Monshausen, G.B., Bibikova, T.N., Messerli, M.A., Shi, C. and Gilroy, S. (2007) Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc. Natl Acad. Sci. USA 104: 20996-21001
40. Montiel, J., Nava, N., Cardenas, L., Sanchez-Lopez, R., Arthikala, M.K., Santana, O. et al. (2012) A Phaseolus vulgaris NADPH oxidase gene is required for root infection by Rhizobia. Plant Cell Physiol. 53: 1751-1767
41. Münter, S., Enninga, J., Vazquez-Martinez, R., Delbarre, E., David-Watine, B., Nehrbass, U. et al. (2006) Actin polymerisation at the cytoplasmic face of eukaryotic nuclei. BMC Cell Biol. 7: 1-13
42. Nutman, P.S. (1959) Some observations on root-hair infection by nodule bacteria. J. Exp. Bot. 10: 250-263
43. Pappas, C., Bhattacharya, N., Cooper, J. and Gregorio, C. (2008) Nebulin interacts with CapZ and regulates thin filament architecture within the Z-disc. Mol. Biol. Cell 19: 1837-1847
44. Peleg-Grossman, S., Volpin, H. and Levine, A. (2007) Root hair curling and Rhizobium infection in Medicago truncatula are mediated by phosphatidylinositide-regulated endocytosis and reactive oxygen species. J. Exp. Bot. 58: 1637-1649
45. R Development Core Team (2013) Manual of R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria
46. Sangiorgio, V., Pitto, M., Palestini, P. and Masserini, M. (2004) GPIanchored proteins and lipid rafts. Ital. J. Biochem. 53: 98-111
47. Schafer, D.A. (2002) Coupling actin Dynamics and membrane dynamics during endocytosis. Curr. Opin. Cell Biol. 14: 76-81
48. Schindelman, G., Morikami, A., Jung, J., Baskin, T.I., Carpita, N.C., Derbyshire, P. et al. (2001) COBRA encodes a putative GPI-Anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. Genes Dev. 15: 1115-1127
49. Shaw, S.L. and Long, S.R. (2003) Nod factor elicits two separable calcium responses in Medicago truncatula root hair cells. Plant Physiol. 131: 976-984
50. Sieberer, B.J., Timmers, A.C., Lhuissier, F.G. and Emons, A.M. (2002) Endoplasmic microtubules configure the subapical cytoplasm and are required for fast growth of Medicago truncatula root hairs. Plant Physiol. 130: 977-988
51. Takeda, S., Gapper, C., Kaya, H., Bell, E., Kuchitsu, K. and Dolan, L. (2008) Local positive feedback regulation Determines cell shape in root hair cells. Science 319: 1241-1244
52. Torralba, S., Raudaskoski, M., Pedregosa, A.M. and Laborda, F. (1998) Effect of cytochalasin A on apical growth, actin cytoskeleton organization and enzyme secretion in Aspergillus nidulans. Microbiology 144: 45-53
53. van Brussel, A.A., Bakhuizen, R., van Spronsen, P.C., Spaink, H.P., Tak, T., Lugtenberg, B.J. et al. (1992) Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipooligosaccharides of Rhizobium. Science 257: 70-72
54. Vidali, L., McKenna, S.T. and Hepler, P.K. (2001) Actin polymerization is essential for pollen tube growth. Mol. Biol. Cell 12: 2534-2545
55. Wang, Y.F., Fan, L.M., Zhang, W.Z., Zhang, W. and Wu, W.H. (2004) Ca2+-permeable channels in the plasma membrane of Arabidopsis pollen are regulated by actin microfilaments. Plant Physiol. 136: 3892-3904
56. Wasteneys, G.O. and Galway, M.E. (2003) Remodeling the cytoskeleton for growth and form: An overview with some new views. Annu. Rev. Plant Biol. 54: 691-722
57. Wymer, C.L., Bibikova, T.N. and Gilroy, S. (1997) Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. Plant J. 12: 427-439
58. Yang, Z. (1998) Signaling tip growth in plants. Curr. Opin. Plant. Biol. 1: 525-530
59. Yokota, K., Fukai, E., Madsen, L.H., Jurkiewicz, A., Rueda, P., Radutoiu, S. et al. (2009) Rearrangement of actin cytoskeleton mediates invasion of lotus japonicus roots by Mesorhizobium loti. Plant Cell 21: 267-284