Apical myosin XI anticipates F-actin during polarized growth of Physcomitrella patens cells

Plant Journal

Volumn 73, Issue 3, 2013, Pages 417-428

  Furt, Fabienne ^a   Liu, Yen Chun ^a   Bibeau, Jeffrey P ^a   Tüzel, Erkan ^a   Vidali, Luis ^a  

^a Life Science and Bioengineering Center   (United States)

Author keywords

Actin; cross correlation; Myosin; Physcomitrella patens; tip growth; vesicles

Indexed keywords

ACTIN; CROSS CORRELATIONS; MYOSIN; PHYSCOMITRELLA PATENS; TIP GROWTH; VESICLES;

CELL GROWTH; CELLS; CYTOLOGY; GROWTH KINETICS; MACHINERY; PLANTS (BOTANY); POLYMERIZATION;

PROTEINS;

ACTIN; MYOSIN;

ARTICLE; BRYOPSIDA; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

ACTINS; BRYOPSIDA; MYOSINS;

BRYOPHYTA; BRYOPHYTES; PHYSCOMITRELLA; PHYSCOMITRELLA PATENS;

EID: 84873059624     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12039     Document Type: Article

References (64)

1. 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.
2. Bridgman, P.C., (1999) Myosin Va movements in normal and dilute-lethal axons provide support for a dual filament motor complex. J. Cell Biol. 146, 1045-1060.
3. Cai, G., and, Cresti, M., (2009) Organelle motility in the pollen tube: a tale of 20 years. J. Exp. Bot. 60, 495-508.
4. Campellone, K.G., and, Welch, M.D., (2010) A nucleator arms race: cellular control of actin assembly. Nat. Rev. Mol. Cell Biol. 11, 237-251.
5. Cardenas, L., Lovy-Wheeler, A., Kunkel, J.G., and, Hepler, P.K., (2008) Pollen tube growth oscillations and intracellular calcium levels are reversibly modulated by actin polymerization. Plant Physiol. 146, 1611-1621.
6. Chen, T., Teng, N., Wu, X., Wang, Y., Tang, W., Samaj, J., Baluska, F., and, Lin, J., (2007) Disruption of actin filaments by latrunculin B affects cell wall construction in Picea meyeri pollen tube by disturbing vesicle trafficking. Plant Cell Physiol. 48, 19-30.
7. Cheney, R.E., O'Shea, M.K., Heuser, J.E., Coelho, M.V., Wolenski, J.S., Espreafico, E.M., Forscher, P., Larson, R.E., and, Mooseker, M.S., (1993) Brain myosin-V is a two-headed unconventional myosin with motor activity. Cell, 75, 13-23.
8. Cole, R.A., and, Fowler, J.E., (2006) Polarized growth: maintaining focus on the tip. Curr. Opin. Plant Biol. 9, 579-588.
9. Eklund, D.M., Svensson, E.M., and, Kost, B., (2010) Physcomitrella patens: a model to investigate the role of RAC/ROP GTPase signalling in tip growth. J. Exp. Bot. 61, 1917-1937.
10. Eppinga, R.D., Peng, I.F., Lin, J.L., Wu, C.F., and, Lin, J.J., (2008) Opposite effects of overexpressed myosin Va or heavy meromyosin Va on vesicle distribution, cytoskeleton organization, and cell motility in nonmuscle cells. Cell Motil. Cytoskeleton, 65, 197-215.
11. Evans, L.L., Lee, A.J., Bridgman, P.C., and, Mooseker, M.S., (1998) Vesicle-associated brain myosin-V can be activated to catalyze actin-based transport. J. Cell Sci. 111 (Pt 14), 2055-2066.
12. Fasshauer, D., Sutton, R.B., Brunger, A.T., and, Jahn, R., (1998) Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc. Natl. Acad. Sci. USA, 95, 15781-15786.
13. Finka, A., Schaefer, D.G., Saidi, Y., Goloubinoff, P., and, Zryd, J.P., (2007) In vivo visualization of F-actin structures during the development of the moss Physcomitrella patens. New Phytol. 174, 63-76.
14. Fu, Y., Wu, G., and, Yang, Z., (2001) Rop GTPase-dependent dynamics of tip-localized F-actin controls tip growth in pollen tubes. J. Cell Biol. 152, 1019-1032.
15. Furt, F., Lemoi, K., Tuzel, E., and, Vidali, L., (2012) Quantitative analysis of organelle distribution and dynamics in Physcomitrella patens protonemal cells. BMC Plant Biol. 12, 70.
16. Ghil, M., Allen, M.R., Dettinger, M.D., et al,. (2002) Advanced spectral methods for climatic time series. Rev. Geophys. 40, 1003.
17. Gilroy, S., and, Jones, D.L., (2000) Through form to function: root hair development and nutrient uptake. Trends Plant Sci. 5, 56-60.
18. Gouin, E., Welch, M.D., and, Cossart, P., (2005) Actin-based motility of intracellular pathogens. Curr. Opin. Microbiol. 8, 35-45.
19. Govindan, B., Bowser, R., and, Novick, P., (1995) The role of Myo2, a yeast class V myosin, in vesicular transport. J. Cell Biol. 128, 1055-1068.
20. Haglund, C.M., Choe, J.E., Skau, C.T., Kovar, D.R., and, Welch, M.D., (2010) Rickettsia Sca2 is a bacterial formin-like mediator of actin-based motility. Nat. Cell Biol. 12, 1057-1063.
21. Harries, P.A., Pan, A., and, Quatrano, R.S., (2005) Actin-related protein2/3 complex component ARPC1 is required for proper cell morphogenesis and polarized cell growth in Physcomitrella patens. Plant Cell, 17, 2327-2339.
22. Heckman, D.S., Geiser, D.M., Eidell, B.R., Stauffer, R.L., Kardos, N.L., and, Hedges, S.B., (2001) Molecular evidence for the early colonization of land by fungi and plants. Science, 293, 1129-1133.
23. Heindl, J.E., Saran, I., Yi, C.R., Lesser, C.F., and, Goldberg, M.B., (2010) Requirement for formin-induced actin polymerization during spread of Shigella flexneri. Infect. Immun. 78, 193-203.
24. Hepler, P.K., Vidali, L., and, Cheung, A.Y., (2001) Polarized cell growth in higher plants. Annu. Rev. Cell Dev. Biol. 17, 159-187.
25. HoldawayClarke, T.L., Feijo, J.A., Hackett, G.R., Kunkel, J.G., and, Hepler, P.K., (1997) Pollen tube growth and the intracellular cytosolic calcium gradient oscillate in phase while extracellular calcium influx is delayed. Plant Cell, 9, 1999-2010.
26. Hong, W., (2005) SNAREs and traffic. Biochim. Biophys. Acta, 1744, 493-517.
27. Hwang, J.U., Gu, Y., Lee, Y.J., and, Yang, Z.B., (2005) Oscillatory ROP GTPase activation leads the oscillatory polarized growth of pollen tubes. Mol. Biol. Cell, 16, 5385-5399.
28. Kenrick, P., and, Crane, P.R., (1997) The origin and early evolution of plants on land. Nature, 389, 33-39.
29. Liu, Y.C., and, Vidali, L., (2011) Efficient polyethylene glycol (PEG) mediated transformation of the moss Physcomitrella patens. J. Vis. Exp. 50, 2560.
30. Ma, L., Cantley, L.C., Janmey, P.A., and, Kirschner, M.W., (1998) Corequirement of specific phosphoinositides and small GTP-binding protein Cdc42 in inducing actin assembly in Xenopus egg extracts. J. Cell Biol. 140, 1125-1136.
31. McKenna, S.T., Kunkel, J.G., Bosch, M., Rounds, C.M., Vidali, L., Winship, L.J., and, Hepler, P.K., (2009) Exocytosis precedes and predicts the increase in growth in oscillating pollen tubes. Plant Cell, 21, 3026-3040.
32. Menand, B., Calder, G., and, Dolan, L., (2007) Both chloronemal and caulonemal cells expand by tip growth in the moss Physcomitrella patens. J. Exp. Bot. 58, 1843-1849.
33. Messerli, M.A., Creton, R., Jaffe, L.F., and, Robinson, K.R., (2000) Periodic increases in elongation rate precede increases in cytosolic Ca2+ during pollen tube growth. Dev. Biol. 222, 84-98.
34. 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.
35. Monshausen, G.B., Messerli, M.A., and, Gilroy, S., (2008) Imaging of the Yellow Cameleon 3.6 indicator reveals that elevations in cytosolic Ca2+ follow oscillating increases in growth in root hairs of Arabidopsis. Plant Physiol. 147, 1690-1698.
36. Ojangu, E.L., Järve, K., Paves, H., and, Truve, E., (2007) Arabidopsis thaliana myosin XIK is involved in root hair as well as trichome morphogenesis on stems and leaves. Protoplasma, 230, 193-202.
37. Peremyslov, V.V., Prokhnevsky, A.I., Avisar, D., and, Dolja, V.V., (2008) Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis. Plant Physiol. 146, 1109-1116.
38. Peremyslov, V.V., Prokhnevsky, A.I., and, Dolja, V.V., (2010) Class XI myosins are required for development, cell expansion, and F-Actin organization in Arabidopsis. Plant Cell, 22, 1883-1897.
39. Peremyslov, V.V., Klocko, A.L., Fowler, J.E., and, Dolja, V.V., (2012) Arabidopsis myosin XI-K localizes to the motile endomembrane vesicles associated with F-actin. Front. Plant Sci. 3, 184.
40. Perroud, P.F., and, Quatrano, R.S., (2006) The role of ARPC4 in tip growth and alignment of the polar axis in filaments of Physcomitrella patens. Cell Motil. Cytoskeleton, 63, 162-171.
41. Perroud, P.F., and, Quatrano, R.S., (2008) BRICK1 is required for apical cell growth in filaments of the moss Physcomitrella patens but not for gametophore morphology. Plant Cell, 20, 411-422.
42. Prekeris, R., and, Terrian, D.M., (1997) Brain myosin V is a synaptic vesicle-associated motor protein: evidence for a Ca2+-dependent interaction with the synaptobrevin-synaptophysin complex. J. Cell Biol. 137, 1589-1601.
43. Prokhnevsky, A.I., Peremyslov, V.V., and, Dolja, V.V., (2008) Overlapping functions of the four class XI myosins in Arabidopsis growth, root hair elongation, and organelle motility. Proc. Natl Acad. Sci. USA, 105, 19744-19749.
44. Reck-Peterson, S.L., Novick, P.J., and, Mooseker, M.S., (1999) The tail of a yeast class V myosin, myo2p, functions as a localization domain. Mol. Biol. Cell, 10, 1001-1017.
45. Rossi, G., and, Brennwald, P., (2011) Yeast homologues of lethal giant larvae and type V myosin cooperate in the regulation of Rab-dependent vesicle clustering and polarized exocytosis. Mol. Biol. Cell, 22, 842-857.
46. Sanderfoot, A., (2007) Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants. Plant Physiol. 144, 6-17.
47. Santiago-Tirado, F.H., Legesse-Miller, A., Schott, D., and, Bretscher, A., (2011) PI4P and Rab inputs collaborate in myosin-V-dependent transport of secretory compartments in yeast. Dev. Cell, 20, 47-59.
48. Schott, D., Ho, J., Pruyne, D., and, Bretscher, A., (1999) The COOH-terminal domain of Myo2p, a yeast myosin V, has a direct role in secretory vesicle targeting. J. Cell Biol. 147, 791-808.
49. Schuh, M., (2011) An actin-dependent mechanism for long-range vesicle transport. Nat. Cell Biol. 13, 1431-1436.
50. Sparkes, I.A., (2010) Motoring around the plant cell: insights from plant myosins. Biochem. Soc. Trans. 38, 833-838.
51. Sutton, R.B., Fasshauer, D., Jahn, R., and, Brunger, A.T., (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature, 395, 347-353.
52. Tauhata, S.B., dos Santos, D.V., Taylor, E.W., Mooseker, M.S., and, Larson, R.E., (2001) High affinity binding of brain myosin-Va to F-actin induced by calcium in the presence of ATP. J. Biol. Chem. 276, 39812-39818.
53. Taunton, J., Rowning, B.A., Coughlin, M.L., Wu, M., Moon, R.T., Mitchison, T.J., and, Larabell, C.A., (2000) Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP. J. Cell Biol. 148, 519-530.
54. Ueda, H., Yokota, E., Kutsuna, N., Shimada, T., Tamura, K., Shimmen, T., Hasezawa, S., Dolja, V.V., and, Hara-Nishimura, I., (2010) Myosin-dependent endoplasmic reticulum motility and F-actin organization in plant cells. Proc. Natl. Acad. Sci. USA, 107, 6894-6899.
55. Uemura, T., Ueda, T., Ohniwa, R.L., Nakano, A., Takeyasu, K., and, Sato, M.H., (2004) Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells. Cell Struct. Funct. 29, 49-65.
56. Verchot-Lubicz, J., and, Goldstein, R.E., (2010) Cytoplasmic streaming enables the distribution of molecules and vesicles in large plant cells. Protoplasma, 240, 99-107.
57. Vidali, L., McKenna, S.T., and, Hepler, P.K., (2001) Actin polymerization is essential for pollen tube growth. Mol. Biol. Cell, 12, 2534-2545.
58. Vidali, L., Augustine, R.C., Kleinman, K.P., and, Bezanilla, M., (2007) Profilin is essential for tip growth in the moss Physcomitrella patens. Plant Cell, 19, 3705-3722.
59. Vidali, L., Rounds, C.M., Hepler, P.K., and, Bezanilla, M., (2009a) Lifeact-mEGFP reveals a dynamic apical F-actin network in tip growing plant cells. PLoS ONe, 4, e5744.
60. Vidali, L., van Gisbergen, P.A.C., Guerin, C., Franco, P., Li, M., Burkart, G.M., Augustine, R.C., Blanchoin, L., and, Bezanilla, M., (2009b) Rapid formin-mediated actin-filament elongation is essential for polarized plant cell growth. Proc. Natl. Acad. Sci. USA, 106, 13341-13346.
61. Vidali, L., Burkart, G.M., Augustine, R.C., Kerdavid, E., Tuzel, E., and, Bezanilla, M., (2010) Myosin XI is essential for tip growth in Physcomitrella patens. Plant Cell, 22, 1868-1882.
62. Zang, J.H., and, Spudich, J.A., (1998) Myosin II localization during cytokinesis occurs by a mechanism that does not require its motor domain. Proc. Natl. Acad. Sci. USA 95, 13652-13657.
63. Zarsky, V., Cvrckova, F., Potocky, M., and, Hala, M., (2009) Exocytosis and cell polarity in plants-exocyst and recycling domains. New Phytol. 183, 255-272.
64. Zilberman, Y., Alieva, N.O., Miserey-Lenkei, S., Lichtenstein, A., Kam, Z., Sabanay, H., and, Bershadsky, A., (2011) Involvement of the Rho-mDia1 pathway in the regulation of Golgi complex architecture and dynamics. Mol. Biol. Cell, 22, 2900-2911.