Arabidopsis villins promote actin turnover at pollen tube tips and facilitate the construction of actin collars

Plant Cell

Volumn 25, Issue 5, 2013, Pages 1803-1817

  Qu, Xiaolu ^a   Zhang, Hua ^a   Xie, Yurong ^a   Wang, Juan ^a   Chen, Naizhi ^a   Huang, Shanjin ^a,b  

^a INSTITUTE OF BOTANY   (China)

^b INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84879488409     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.110940     Document Type: Article

References (78)

1. Allwood, E.G., Anthony, R.G., Smertenko, A.P., Reichelt, S., Drobak, B.K., Doonan, J.H., Weeds, A.G., and Hussey, P.J. (2002). Regulation of the pollen-specific actin-depolymerizing factor LlADF1. Plant Cell 14: 2915-2927.
2. Augustine, R.C., Pattavina, K.A., Tüzel, E., Vidali, L., and Bezanilla, M. (2011). Actin interacting protein1 and actin depolymerizing factor drive rapid actin dynamics in Physcomitrella patens. Plant Cell 23: 3696-3710.
3. 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.
4. Bao, C., Wang, J., Zhang, R., Zhang, B., Zhang, H., Zhou, Y., and Huang, S. (2012). Arabidopsis VILLIN2 and VILLIN3 act redundantly in sclerenchyma development via bundling of actin filaments. Plant J. 71: 962-975.
5. Bedinger, P.A., Hardeman, K.J., and Loukides, C.A. (1994). Travelling in style: The cell biology of pollen. Trends Cell Biol. 4: 132-138.
6. Berepiki, A., Lichius, A., and Read, N.D. (2011). Actin organization and dynamics in filamentous fungi. Nat. Rev. Microbiol. 9: 876-887.
7. Cárdenas, 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.
8. Chaudhry, F., Guérin, C., vonWitsch, M., Blanchoin, L., and Staiger, C.J. (2007). Identification of Arabidopsis cyclase-associated protein 1 as the first nucleotide exchange factor for plant actin. Mol. Biol. Cell 18: 3002-3014.
9. Chen, C.Y., Wong, E.I., Vidali, L., Estavillo, A., Hepler, P.K., Wu, H.M., and Cheung, A.Y. (2002). The regulation of actin organization by actin-depolymerizing factor in elongating pollen tubes. Plant Cell 14: 2175-2190.
10. Chen, N., Qu, X., Wu, Y., and Huang, S. (2009). Regulation of actin dynamics in pollen tubes: Control of actin polymer level. J. Integr. Plant Biol. 51: 740-750.
11. Cheung, A.Y., Niroomand, S., Zou, Y., and Wu, H.M. (2010). A transmembrane formin nucleates subapical actin assembly and controls tip-focused growth in pollen tubes. Proc. Natl. Acad. Sci. USA 107: 16390-16395.
12. Cheung, A.Y., and Wu, H.M. (2004). Overexpression of an Arabidopsis formin stimulates supernumerary actin cable formation from pollen tube cell membrane. Plant Cell 16: 257-269.
13. Cheung, A.Y., and Wu, H.M. (2008). Structural and signaling networks for the polar cell growth machinery in pollen tubes. Annu. Rev. Plant Biol. 59: 547-572.
14. Clough, S.J., and Bent, A.F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
15. Cole, R.A., and Fowler, J.E. (2006). Polarized growth: Maintaining focus on the tip. Curr. Opin. Plant Biol. 9: 579-588.
16. Bou Daher, F., and Geitmann, A. (2011). Actin is involved in pollen tube tropism through redefining the spatial targeting of secretory vesicles. Traffic 12: 1537-1551.
17. Deeks, M.J., Rodrigues, C., Dimmock, S., Ketelaar, T., Maciver, S.K., Malhó, R., and Hussey, P.J. (2007). Arabidopsis CAP1-A key regulator of actin organisation and development. J. Cell Sci. 120: 2609-2618.
18. 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.
19. Furt, F., Liu, Y.C., Bibeau, J.P., Tüzel, E., and Vidali, L. (2013). Apical myosin XI anticipates F-actin during polarized growth of Physcomitrella patens cells. Plant J. 73: 417-428.
20. 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.
21. Gu, Y., Fu, Y., Dowd, P., Li, S., Vernoud, V., Gilroy, S., and Yang, Z. (2005). A Rho family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes. J. Cell Biol. 169: 127-138.
22. Henty, J.L., Bledsoe, S.W., Khurana, P., Meagher, R.B., Day, B., Blanchoin, L., and Staiger, C.J. (2011). Arabidopsis actin depolymerizing factor4 modulates the stochastic dynamic behavior of actin filaments in the cortical array of epidermal cells. Plant Cell 23: 3711-3726.
23. Hepler, P.K., Vidali, L., and Cheung, A.Y. (2001). Polarized cell growth in higher plants. Annu. Rev. Cell Dev. Biol. 17: 159-187.
24. Higaki, T., Kutsuna, N., Sano, T., Kondo, N., and Hasezawa, S. (2010). 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. Plant J. 61: 156-165.
25. Holdaway-Clarke, 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. Holdaway-Clarke, T.L., Weddle, N.M., Kim, S., Robi, A., Parris, C., Kunkel, J.G., and Hepler, P.K. (2003). Effect of extracellular calcium, pH and borate on growth oscillations in Lilium formosanum pollen tubes. J. Exp. Bot. 54: 65-72.
27. Honys, D., and Twell, D. (2003). Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol. 132: 640-652.
28. Huang, S., Blanchoin, L., Chaudhry, F., Franklin-Tong, V.E., and Staiger, C.J. (2004). A gelsolin-like protein from Papaver rhoeas pollen (PrABP80) stimulates calcium-regulated severing and depolymerization of actin filaments. J. Biol. Chem. 279: 23364-23375.
29. Huang, S., Blanchoin, L., Kovar, D.R., and Staiger, C.J. (2003). Arabidopsis capping protein (AtCP) is a heterodimer that regulates assembly at the barbed ends of actin filaments. J. Biol. Chem. 278: 44832-44842.
30. Hwang, J.U., Vernoud, V., Szumlanski, A., Nielsen, E., and Yang, Z. (2008). A tip-localized RhoGAP controls cell polarity by globally inhibiting Rho GTPase at the cell apex. Curr. Biol. 18: 1907-1916.
31. Ketelaar, T., Allwood, E.G., Anthony, R., Voigt, B., Menzel, D., and Hussey, P.J. (2004). The actin-interacting protein AIP1 is essential for actin organization and plant development. Curr. Biol. 14: 145-149.
32. Khurana, P., Henty, J.L., Huang, S., Staiger, A.M., Blanchoin, L., and Staiger, C.J. (2010). Arabidopsis VILLIN1 and VILLIN3 have overlapping and distinct activities in actin bundle formation and turnover. Plant Cell 22: 2727-2748.
33. Kost, B., Spielhofer, P., and Chua, N.H. (1998). A GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes. Plant J. 16: 393-401.
34. Kovar, D.R., Drøbak, B.K., and Staiger, C.J. (2000). Maize profilin isoforms are functionally distinct. Plant Cell 12: 583-598.
35. Kroeger, J.H., Daher, F.B., Grant, M., and Geitmann, A. (2009). Microfilament orientation constrains vesicle flow and spatial distribution in growing pollen tubes. Biophys. J. 97: 1822-1831.
36. Lee, Y.J., Szumlanski, A., Nielsen, E., and Yang, Z. (2008). Rho-GTPase-dependent filamentous actin dynamics coordinate vesicle targeting and exocytosis during tip growth. J. Cell Biol. 181: 1155-1168.
37. Lenartowska, M., and Michalska, A. (2008). Actin filament organization and polarity in pollen tubes revealed by myosin II subfragment 1 decoration. Planta 228: 891-896.
38. Li, J., Henty-Ridilla, J.L., Huang, S., Wang, X., Blanchoin, L., and Staiger, C.J. (2012). Capping protein modulates the dynamic behavior of actin filaments in response to phosphatidic acid in Arabidopsis. Plant Cell 24: 3742-3754.
39. Lovy-Wheeler, A., Kunkel, J.G., Allwood, E.G., Hussey, P.J., and Hepler, P.K. (2006). Oscillatory increases in alkalinity anticipate growth and may regulate actin dynamics in pollen tubes of lily. Plant Cell 18: 2182-2193.
40. Lovy-Wheeler, A., Wilsen, K.L., Baskin, T.I., and Hepler, P.K. (2005). Enhanced fixation reveals the apical cortical fringe of actin filaments as a consistent feature of the pollen tube. Planta 221: 95-104.
41. Lowery, L.A., and Van Vactor, D. (2009). The trip of the tip: Understanding the growth cone machinery. Nat. Rev. Mol. Cell Biol. 10: 332-343.
42. Marga, F., Grandbois, M., Cosgrove, D.J., and Baskin, T.I. (2005). Cell wall extension results in the coordinate separation of parallel microfibrils: Evidence from scanning electron microscopy and atomic force microscopy. Plant J. 43: 181-190.
43. Mathur, J., and Hülskamp, M. (2001). Cell growth: How to grow and where to grow. Curr. Biol. 11: R402-R404.
44. 2+ during pollen tube growth. Dev. Biol. 222: 84-98.
45. Nakayasu, T., Yokota, E., and Shimmen, T. (1998). Purification of an actin-binding protein composed of 115-kDa polypeptide from pollen tubes of lily. Biochem. Biophys. Res. Commun. 249: 61-65.
46. 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.
47. 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.
48. Pierson, E.S., Miller, D.D., Callaham, D.A., Shipley, A.M., Rivers, B.A., Cresti, M., and Hepler, P.K. (1994). Pollen tube growth is coupled to the extracellular calcium ion flux and the intracellular calcium gradient: Effect of BAPTA-type buffers and hypertonic media. Plant Cell 6: 1815-1828.
49. Pina, C., Pinto, F., Feijó, J.A., and Becker, J.D. (2005). Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol. 138: 744-756.
50. Pollard, T.D. (2007). Regulation of actin filament assembly by Arp2/3 complex and formins. Annu. Rev. Biophys. Biomol. Struct. 36: 451-477.
51. Preuss, M.L., Serna, J., Falbel, T.G., Bednarek, S.Y., and Nielsen, E. (2004). The Arabidopsis Rab GTPase RabA4b localizes to the tips of growing root hair cells. Plant Cell 16: 1589-1603.
52. Qin, Y., and Yang, Z. (2011). Rapid tip growth: Insights from pollen tubes. Semin. Cell Dev. Biol. 22: 816-824.
53. Rounds, C.M., and Bezanilla, M. (2013). Growth mechanisms in tipgrowing plant cells. Annu. Rev. Plant Biol. 64: 243-265.
54. Shi, M., Xie, Y., Zheng, Y., Wang, J., Su, Y., Yang, Q., and Huang, S. (2013). Oryza sativa actin-interacting protein 1 is required for rice growth by promoting actin turnover. Plant J. 73: 747-760.
55. Snowman, B.N., Kovar, D.R., Shevchenko, G., Franklin-Tong, V.E., and Staiger, C.J. (2002). Signal-mediated depolymerization of actin in pollen during the self-incompatibility response. Plant Cell 14: 2613-2626.
56. Staiger, C.J., Poulter, N.S., Henty, J.L., Franklin-Tong, V.E., and Blanchoin, L. (2010). Regulation of actin dynamics by actin-binding proteins in pollen. J. Exp. Bot. 61: 1969-1986.
57. Staiger, C.J., Sheahan, M.B., Khurana, P., Wang, X., McCurdy, D.W., and Blanchoin, L. (2009). Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array. J. Cell Biol. 184: 269-280.
58. Su, H., Zhu, J., Cai, C., Pei, W., Wang, J., Dong, H., and Ren, H. (2012). FIMBRIN1 is involved in lily pollen tube growth by stabilizing the actin fringe. Plant Cell 24: 4539-4554.
59. van der Honing, H.S., Kieft, H., Emons, A.M., and Ketelaar, T. (2012). Arabidopsis VILLIN2 and VILLIN3 are required for the generation of thick actin filament bundles and for directional organ growth. Plant Physiol. 158: 1426-1438.
60. 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.
61. Vidali, L., Burkart, G.M., Augustine, R.C., Kerdavid, E., Tüzel, E., and Bezanilla, M. (2010). Myosin XI is essential for tip growth in Physcomitrella patens. Plant Cell 22: 1868-1882.
62. Vidali, L., and Hepler, P.K. (1997). Characterization and localization of profilin in pollen grains and tubes of Lilium longiflorum. CellMotil. Cytoskeleton 36: 323-338.
63. Vidali, L., and Hepler, P.K. (2001). Actin and pollen tube growth. Protoplasma 215: 64-76.
64. Vidali, L., McKenna, S.T., and Hepler, P.K. (2001). Actin polymerization is essential for pollen tube growth. Mol. Biol. Cell 12: 2534-2545.
65. Vidali, L., Rounds, C.M., Hepler, P.K., and Bezanilla, M. (2009). Lifeact-mEGFP reveals a dynamic apical F-actin network in tip growing plant cells. PLoS ONE 4: e5744.
66. Wang, T., Xiang, Y., Hou, J., and Ren, H. (2008). ABP41 is involved in the pollen tube development via fragmenting actin filaments. Mol. Plant 1: 1048-1055.
67. Wu, Y., Yan, J., Zhang, R., Qu, X., Ren, S., Chen, N., and Huang, S. (2010). Arabidopsis FIMBRIN5, an actin bundling factor, is required for pollen germination and pollen tube growth. Plant Cell 22: 3745-3763.
68. Xiang, Y., Huang, X., Wang, T., Zhang, Y., Liu, Q., Hussey, P.J., and Ren, H. (2007). ACTIN BINDING PROTEIN 29 from Lilium pollen plays an important role in dynamic actin remodeling. Plant Cell 19: 1930-1946.
69. Yang, Z. (1998). Signaling tip growth in plants. Curr. Opin. Plant Biol. 1: 525-530.
70. Yang, Z. (2008). Cell polarity signaling in Arabidopsis. Annu. Rev. Cell Dev. Biol. 24: 551-575.
71. Ye, J., Zheng, Y., Yan, A., Chen, N., Wang, Z., Huang, S., and Yang, Z. (2009). Arabidopsis formin3 directs the formation of actin cables and polarized growth in pollen tubes. Plant Cell 21: 3868-3884.
72. Yokota, E., Takahara, K.-I., andShimmen, T. (1998). Actin-bundling protein isolated from pollen tubes of lily. Biochemical and immunocytochemical characterization. Plant Physiol. 116: 1421-1429.
73. 2+-sensitive manner. Plant Cell Physiol. 46: 1690-1703.
74. Yokota, E., Vidali, L., Tominaga, M., Tahara, H., Orii, H., Morizane, Y., Hepler, P.K., and Shimmen, T. (2003). Plant 115-kDa actinfilament bundling protein, P-115-ABP, is a homologue of plant villin and is widely distributed in cells. Plant Cell Physiol. 44: 1088-1099.
75. Zhang, H., Qu, X., Bao, C., Khurana, P., Wang, Q., Xie, Y., Zheng, Y., Chen, N., Blanchoin, L., Staiger, C.J., and Huang, S. (2010a). Arabidopsis VILLIN5, an actin filament bundling and severing protein, is necessary for normal pollen tube growth. Plant Cell 22: 2749-2767.
76. Zhang, Y., He, J., Lee, D., and McCormick, S. (2010b). Interdependence of endomembrane trafficking and actin dynamics during polarized growth of Arabidopsis pollen tubes. Plant Physiol. 152: 2200-2210.
77. 2+-dependent manner. New Phytol. 190: 667-682.
78. Zhu, L., Zhang, Y., Kang, E., Xu, Q., Wang, M., Rui, Y., Liu, B., Yuan, M., and Fu, Y. (2013). MAP18 regulates the direction of pollen tube growth in Arabidopsis by modulating F-actin organization. Plant Cell 25: 851-867.