Organization and regulation of the actin cytoskeleton in the pollen tube

Frontiers in Plant Science

Volumn 5, Issue JAN, 2015, Pages

  Qu, Xiaolu ^a   Jiang, Yuxiang ^b   Chang, Ming ^b   Liu, Xiaonan ^b   Zhang, Ruihui ^b   Huang, Shanjin ^b  

^a TSINGHUA UNIVERSITY   (China)

^b INSTITUTE OF BOTANY   (China)

Author keywords

Actin; Actin binding protein; ADF; Fimbrin; Formin; Pollen tube; Villin

Indexed keywords

EID: 84922258817     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00786     Document Type: Review

References (94)

1. Bao, C. C., Wang, J., Zhang, R. H., Zhang, B. C., Zhang, H., Zhou, Y. H., et al. (2012). Arabidopsis VILLIN2 and VILLIN3 act redundantly in scle-renchyma development via bundling of actin filaments. Plant J. 71, 962-975. doi: 10.1111/j.1365-313x.2012.05044.x
2. Bedinger, P. (1992). The remarkable biology of pollen. Plant Cell 4, 879-887. doi: 10.1105/tpc.4.8.879
3. Blanchoin, L., and Staiger, C. J. (2010). Plant formins: diverse isoforms and unique molecular mechanism. Biochim. Biophys. Acta 1803, 201-206. doi: 10.1016/j.bbamcr.2008.09.015
4. Brandizzi, F., Fricker, M., and Hawes, C. (2002). A greener world: the revolution in plant bioimaging. Na,t. Rev. Mol. Cell Biol. 3, 520-530. doi: 10.1038/n.rm861
5. Chaudhry, F., Guerin, C., Von Witsch, M., Blanchoin, L., and Staiger, C. J.. Identification of Arabidopsis cyclase-associated protein 1 as the first nucleotide exchange factor for plant actin. Mol. Biol. Cell 18, 3002-3014. doi: 10.1091/mbc.e06-11-1041
6. 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 actin-depolymerizing factor in elongating pollen tubes. Plant Cell 14, 2175-2190. doi: 10.1105/tpc.0.03038
7. Chen, N. Z., Qu, X. L., Wu, Y. J., and Huang, S. J. (2009). Regulation of actin dynamics in pollen tubes: control of actin polymer level. J. Integr. Plant Biol. 51, 740-750. doi: 10.1111/j.1744-7909.2009.00850.x
8. Chen, Q., and Pollard, T. D. (2011). Actin filament severing by cofilin is more importantfor assemblythan constriction of the cytokinetic contractilering. J. Cell Biol. 195,485-498. doi: 10.1083/jcb.201103067
9. Cheung, A. Y., Niroomand, S., Zou, Y. J., and Wu, H. M. (2010). A transmembrane formin nucleates subapical actin assembly and controls tip-focused growth in pollen tubes. Proc. Natl. Acad. Sci. U.S.A. 107, 16390-16395. doi: 10.1073/pnas.1008527107
10. Cheung, A. Y., and Wu, H. M. (2004). Overexpression of an Arabidopsis formin stimulates supernumeraryactin cable formation from pollen tube cell membrane. PlantCell 16,257-269. doi: 10.1105/tpc.016550
11. 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. doi: 10.1146/annurev.arplant.59.032607.092921
12. Daher, F. B., and Geitmann, A. (2011). Actin is involved in pollen tube tropism through redefining the spatial targeting of secretory vesicles. Traffic 12, 15371551. doi: 10.1111/j.1600-0854.2011.01256.x
13. Daher, F. B., Van Oostende, C., and Geitmann, A. (2011). Spatial and temporal expression of actin depolymerizing factors ADF7 and ADF10 during male game-tophyte development in Arabidopsis thaliana. Plant Cell Physiol. 52, 1177-1192. doi: 10.1093/pcp/pcr068
14. Deeks, M. J., Hussey, P. J., and Davies, B. (2002). Formins: intermediates in signal-transduction cascades that affect cytoskeletal reorganization. Trends Plant Sci. 7, 492-498. doi: 10.1016/s1360-1385(02)02341-5
15. Deeks, M. J., Rodrigues, C., Dimmock, S., Ketelaar, T., Maciver, S. K., Malho, R., et al. (2007). Arabidopsis CAP1-a key regulator of actin organisation and development. J. Cell Sci. 120, 2609-2618. doi: 10.1242/jcs.007302
16. Derksen, J., Rutten, T., Vanamstel, T., Dewin, A., Doris, F., and Steer, M. (1995). Regulation ofpollentubegrowth. ActaBot. Neerl. 44,93-119. doi: 10.1111/j.1438-8677.1995.tb00773.x
17. Dong, H. J., Pei, W. K., and Ren, H. Y. (2012). Actin fringe is correlated with tip growth velocity of pollen tubes. Mol. Plant 5, 1160-1162. doi: 10.1093/mp/s.ss073
18. Fu, Y. (2010). The actin cytoskeleton and signaling network during pollen tube tip growth. J. Integr. PlantBiol. 52,131-137. doi: 10.1111/j.1744-7909.2010.00922.x
19. Fu, Y., Wu, G., and Yang, Z. B. (2001). Rop GTPase-dependent dynamics of tip-localized F-actin controls tip growth in pollen tubes. J. Cell Biol. 152, 1019-1032. doi: 10.1083/jcb.152.5.1019
20. Geitmann, A., Snowman, B. N., Emons, A. M. C., and Franklin-Tong, V. E. (2000). Alterations in the actin cytoskeleton of pollen tubes are induced by the self-incompatibility reaction in Papaver rhoeas. Plant Cell 12, 1239-1251. doi: 10.1105/tpc.12.7.1239
21. 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. doi: 10.2307/3870960
22. Gui, C. P., Dong, X., Liu, H. K., Huang, W. J., Zhang, D., Wang, S. J., et al. (2014). Overexpression of the tomato pollen receptor kinase LePRK1 rewires pollen tube growth to a blebbing mode. Plant Cell 26, 3538-3555. doi: 10.1105/tpc.114.127381
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. doi: 10.1146/annurev.cellbio.17.1.159
24. Hoffmann, C., Moes, D., Dieterle, M., Neumann, K., Moreau, F., Dumas, D., et al. (2014). Live cell imaging approaches reveal actin cytoskeleton-induced selfassociation of the actin-bundling protein WLIM1. J. Cell Sci. 127, 583-598. doi: 10.1242/jcs.134536
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. PlantCell 9,19992010.doi: 10.1105/tpc.9.11.1999
26. Huang, S., Qu, X., and Zhang, R. (2014). Plant villins: versatile actin regulatory proteins. J. Integr. PlantBiol. doi: 10.1111/jipb.12293 [Epub ahead of print].
27. 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. doi: 10.1146/annurev.arplant.57.032905.105206
28. 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 5385-5399. doi: 10.1091/mbc.E05-05-0409
29. Ingouff, M., Gerald, J. N. F., Guerin, C., Robert, H., Sorensen, M. B., Van Damme, D., et al. (2005). Plant formin AtFH5 is an evolutionarily conserved actin nucleator involved in cytokinesis. Nat. Cell Biol. 7, 374-380. doi: 10.1038/nc.b1238
30. Jia, H. L., Li, J. S., Zhu, J. G., Fan, T. T., Qian, D., Zhou, Y. L., et al. (2013). Arabidopsis CROLIN1, a novel plant actin-binding protein, functions in crosslinking and stabilizing actin filaments. J. Biol. Chem. 288, 32277-32288. doi: 10.1074/jbc.m113.483594
31. Ketelaar, T., Allwood, E. G., Anthony, R., Voigt, B., Menzel, D., and Hussey, P. J. (2004a). The actin-interacting protein AIP1 is essential for actin organization and plant development. Curr. Biol. 14, 145-149. doi: 10.1016/j.cub.2004.01.004
32. Ketelaar, T., Anthony, R. G., and Hussey, P. J. (2004b). Green fluorescent protein-mTalin causes defects in actin organization and cell expansion in Arabidopsis and inhibits actin depolymerizing factor’s actin depolymerizingactivityin vitro. Plant Physiol. 136,3990-3998. doi: 10.1104/pp.104.050799
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. PlantJ. 16,393-401. doi: 10.1046/j.1365-313x.1998.00304.x
34. Lancelle, S. A., and Hepler, P. K. (1992). Ultrastructure of freeze-substituted pollen tubes of Lilium longiflorum. Protoplasma 167,215-230. doi: 10.1007/bf01403385
35. Lee, Y. J., Szumlanski, A., Nielsen, E., and Yang, Z. B. (2008). Rho-GTPase-dependent filamentous actin dynamics coordinate vesicle targeting and exo-cytosis during tip growth. J. Cell Biol. 181, 1155-1168. doi: 10.1083/jcb.2008 01086
36. Li, J. J., Wang, X. L., Qin, T., Zhang, Y., Liu, X. M., Sun, J. B., et al. (2011). MDP25, a novel calcium regulatory protein, mediates hypocotyl cell elongation by destabilizing cortical microtubules in Arabidopsis. PlantCell 23, 4411-4427. doi: 10.1105/tpc.111.092684
37. Li, Y., Zee, S. Y., Liu, Y. M., Huang, B. Q., and Yen, L. F. (2001). Circular F-actin bundlesandaG-actin gradientinpollenandpollen tubes of Lilium davidii. Planta 213, 722-730. doi: 10.1007/s004250100543
38. Liao, F. L., Wang, L., Yang, L. B., Peng, X. B., and Sun, M. X. (2010). NtGNL1 plays an essential role in pollen tube tip growth and orientation likelyvia regulation of post-golgi trafficking. PLoS ONE 5:e13401. doi: 10.1371/journal.pone.00.13401
39. Lord, E. M., and Russell, S. D. (2002). The mechanisms of pollination and fertilization in plants. Annu. Rev. Cell Dev. Biol. 18, 81-105. doi: 10.1146/annurev.cellbio.18.012502.083438
40. Lovy-Wheeler, A., Kunkel, J. G., Allwood, E. G., Hussey, P. J., and Hepler, P. K.. Oscillatory increases in alkalinity anticipate growth and may regulate actin dynamics in pollen tubes of lily. Plant Cell 18, 2182-2193. doi: 10.1105/tpc.106.044867
41. 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 ofthepollen tube. Planta 221, 95-104. doi: 10.1007/s00425-004-1423-2
42. Mathur, J., and Hulskamp, M. (2001). Cell growth: howto growandwhere to grow. Curr. Biol. 11, R402-R404. doi: 10.1016/s0960-9822(01)00219-6
43. McCormick, S. (2013). Pollen. Curr. Biol. 23, R988-R990. doi: 10.1016/j.cub.2013.08.016
44. 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. doi: 10.1006/dbio.2000.9709
45. Miller, D. D., Lancelle, S. A., and Hepler, P. K. (1996). Actin microfilaments do not form a dense meshwork in Lilium longiflorum pollen tube tips. Protoplasma 195, 123-132. doi: 10.1007/bf01279191
46. 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. doi: 10.1006/bbrc.1998.9088
47. Papuga, J., Hoffmann, C., Dieterle, M., Moes, D., Moreau, F., Tholl, S., et al.. Arabidopsis LIM proteins: a family of actin bundlers with distinct expression patterns and modes of regulation. Plant Cell 22, 3034-3052. doi: 10.1105/tpc.110.075960
48. Picton, J. M., and Steer, M. W. (1982). A model for the mechanism of tip extension in pollen tubes. J. Theor. Biol. 98, 15-20. doi: 10.1016/0022-5193(82)90054-6
49. Pierson, E. S., and Cresti, M. (1992). Cytoskeleton and cytoplasmic organization of pollen and pollen tubes. Int. Rev. Cytol. 140, 73-125. doi: 10.1016/S0074-7696(08)61094-3
50. Pierson, E. S., Miller, D. D., Callaham, D. A., Shipley, A. M., Rivers, B. A., Cresti, M., et al. (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. doi: 10.1105/tpc.6.12.1815
51. Qin, T., Liu, X. M., Li, J. J., Sun, J. B., Song, L. N., and Mao, T. L. (2014). Arabidopsis microtubule-destabilizing protein 25 functions in pollen tube growth by severing actin filaments. Plant Cell 26, 325-339. doi: 10.1105/tpc.113.119768
52. Qu, X. L., Zhang, H., Xie, Y. R., Wang, J., Chen, N. Z., and Huang, S. J.. Arabidopsis villins promote actin turnover at pollen tube tips and facilitate the construction of actin collars. Plant Cell 25, 1803-1817. doi: 10.1105/tpc.113.110940
53. Raudaskoski, M., Astrom, H., and Laitiainen, E. (2001). Pollen tube cytoskele-ton: structure and function. J. Plant Growth Regul. 20, 113-130. doi: 10.1007/s003440010015
54. Ren, H. Y., and Xiang, Y. (2007). The function of actin-binding proteins in pollen tube growth. Protoplasma 230, 171-182. doi: 10.1007/s00709-006-0231-x
55. Riedl, J., Crevenna, A. H., Kessenbrock, K., Yu, J. H., Neukirchen, D., Bista, M., et al.. Lifeact: a versatile marker to visualize F-actin. Nat. Methods 5, 605-607. doi: 10.1038/nmeth.1220
56. Rounds, C. M., and Bezanilla, M. (2013). Growth mechanisms in tip-growing plant cells. Annu. Rev. Plant Biol. 64, 243-265. doi: 10.1146/annurev-arplant-050312-120150
57. Rounds, C. M., Hepler, P. K., and Winship, L. J. (2014). The apical actin fringe contributes to localized cell wall deposition and polarized growth in the lilypollen tube. PlantPhysiol. 166, 139-151. doi: 10.1104/pp.114.242974
58. Rutten, T. L. M., and Derksen, J. (1990). Organization of actin filaments in regenerating and outgrowing subprotoplasts from pollen tubes of Nicotiana tabacum L. Planta 180, 471-479. doi: 10.1007/bf02411443
59. Shi, M., Xie, Y. R., Zheng, Y. Y., Wang, J. M., Su, Y., Yang, Q. Y., et al. (2013). Oryza sativa actin-interacting protein1 is required for rice growth by promoting actin turnover. PlantJ. 73, 747-760. doi: 10.1111/tpj.12065
60. Shimmen, T., andYokota, E. (2004). Cytoplasmic streaming in plants. Curr. Opin. CellBiol. 16, 68-72. doi: 10.1016/j.ceb.2003.11.009
61. Smertenko, A. P., Allwood, E. G., Khan, S., Jiang, C. J., Maciver, S. K., Weeds, A. G., et al. (2001). Interaction of pollen-specific actin-depolymerizing factor withactin. PlantJ. 25,203-212.doi: 10.1046/j.1365-313x.2001.00954.x
62. Smertenko, A. P., Deeks, M. J., and Hussey, P. J. (2010). Strategies of actin reorganisation in plant cells. J. Cell Sci. 123, 3019-3029. doi: 10.1242/jcs.0.79749
63. Smith, L. G., and Oppenheimer, D. G. (2005). Spatial control of cell expansion by the plant cytoskeleton. Annu. Rev. Cell Dev. Biol. 21, 271-295. doi: 10.1146/annurev.cellbio.21.122303.114901
64. Snowman, B. N., Kovar, D. R., Shevchenko, G., Franklin-Tong, V. E., and Staiger, J. (2002). Signal-mediated depolymerization of actin in pollen during the self-incompatibility response. Plant Cell 14, 2613-2626. doi: 10.1105/tpc.0 02998
65. Staiger, C. J., and Blanchoin, L. (2006). Actin dynamics: old friends with newstories. Curr. Opin. PlantBiol. 9, 554-562. doi: 10.1016/j.pbi.2006.09.013
66. Staiger, C. J., Poulter, N. S., Henty, J. L., Franklin-Tong, V. E., and Blanchoin, L.. Regulation of actin dynamics byactin-binding proteins in pollen. J. Exp. Bot. 61, 1969-1986. doi: 10.1093/jxb/erq012
67. Staiger, C. J., Sheahan, M. B., Khurana, P., Wang, X., Mccurdy, D. W., and Blan-choin, L. (2009). Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array. J. Cell Biol. 184, 269-280. doi: 10.1083/jcb.200806185
68. Steer, M. W., and Steer, J. M. (1989). Tansley review No. 16 pollen tube tip growth. NewPhytol. 111, 323-358. doi: 10.1111/j.1469-8137.1989.tb00697.x
69. Stringham, E. G., Marcus-Gueret, N., Ramsay, L., and Schmidt, K. L. (2012). Live cell imaging of the cytoskeleton. MethodsEnzymol. 505,203-217. doi: 10.1016/b978-0-12-388448-0.00019-x
70. Su, H., Zhu, J. S., Cai, C., Pei, W. K., Wang, J. J., Dong, H. J., et al. (2012). FIMBRIN1 is involved in lilypollen tube growth bystabilizing the actin fringe. Plant Cell 24, 4539-4554. doi: 10.1105/tpc.112.099358
71. Tang, X. J., Lancelle, S. A., and Hepler, P. K. (1989). Fluorescence microscopic localization of actin in pollen tubes: comparison of actin antibody and phal-loidin staining. Cell Motil. Cytoskeleton 12, 216-224. doi: 10.1002/cm.9701.20404
72. Taylor, L. P., and Hepler, P. K. (1997). Pollen germination and tube growth. Annu. Rev. PlantPhys. 48,461-491. doi: 10.1146/annurev.arplant.48.1.461
73. Tiwari, S. C., and Polito, V. S. (1988). Organization of the cytoskeleton in pollen tubes of Pyrus communis: astudyemploying conventional and freeze-substitution electron microscopy, immunofluorescence, and rhodamine-phalloidin. Protoplasma 147, 100-112. doi: 10.1007/bf01403337
74. Vidali, L., and Hepler, P. K. (1997). Characterization and localization of profilin in pollen grains and tubes of Lilium longiflorum. Cell Motil. Cytoskeleton 36, 323-338. doi: 10.1002/(SICI)1097-0169(1997)36.43.0.CO.2-6
75. Vidali, L., and Hepler, P. K. (2001). Actin and pollen tube growth. Protoplasma215, 64-76. doi: 10.1007/bf01280304
76. Vidali, L., Mckenna, S. T., and Hepler, P. K. (2001). Actin polymerization is essential for pollen tube growth. Mol. Biol. Cell 12, 2534-2545. doi: 10.1091/mbc.12.8.2534
77. 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. doi: 10.1371/journal.pone.0005744
78. Wang, H. J., Wan, A. R and Jauh, G. Y. (2008a). An actin-binding protein, LlLIM1, mediates calcium and hydrogen regulation of actin dynamics in pollen tubes. PlantPhysiol. 147, 1619-1636. doi: 10.1104/pp.108.118604
79. Wang, T., Xiang, Y., Hou, J., and Ren, H.Y. (2008b). ABP41 is involved in the pollen tube development via fragmenting actin filaments. Mol. Plant 1, 1048-1055. doi: 10.1093/mp/ssn073
80. Wang, H., Zhuang, X. H., Cai, Y., Cheung, A. Y., and Jiang, L. W. (2013). Apical F-actin-regulated exocytic targeting of NtPPME1 is essential for construction and rigidity of the pollen tube cell wall. PlantJ. 76, 367-379. doi: 10.1111/tpj.12300
81. Wang, X., Zhu, L., Liu, B. Q., Wang, C., Jin, L. F., Zhao, Q., et al. (2007). Ara-bidopsis MICROTUBULE-ASSOCIATED PROTEIN18 functions in directional cell growth by destabilizing cortical microtubules. Plant Cell 19, 877-889. doi: 10.1105/tpc.106.048579
82. Wilsen, K. L., Lovy-Wheeler, A., Voigt, B., Menzel, D., Kunkel, J. G., and Hepler, P. K. (2006). Imaging the actin cytoskeleton in growing pollen tubes. Sex. Plant Reprod. 19, 51-62. doi: 10.1007/s00497-006-0021-9
83. Wu, Y. J., Yan, J., Zhang, R. H., Qu, X. L., Ren, S. L., Chen, N. Z., et al. (2010). Ara-bidopsis FIMBRIN5, an actin bundling factor, is required for pollen germination and pollen tube growth. PlantCell 22, 3745-3763. doi: 10.1105/tpc.110.080283
84. Xiang, Y., Huang, X., Wang, T., Zhang, Y., Liu, Q. W., Hussey, P. J., et al. (2007). ACTIN BINDING PROTEIN29 from Lilium pollen plays an important role in dynamicactinremodeling. PlantCell 19,1930-1946. doi: 10.1105/tpc.106.048413
85. Yanagisawa, M., Zhang, C. H., and Szymanski, D. B. (2013). ARP2/3-dependent growth in the plant kingdom: SCARs for life. Front. Plant Sci. 4:166. doi: 10.3389/fpls.2013.00166
86. Ye, J. R., Zheng, Y. Y., Yan, A., Chen, N. Z., Wang, Z. K., Huang, S. J., et al. (2009). Arabidopsis Formin3 directs the formation of actin cables and polarized growth in pollen tubes. PlantCell 21,3868-3884. doi: 10.1105/tpc.109.068700
87. Yokota, E., Takahara, K., and Shimmen, T. (1998). Actin-bundling protein isolated from pollen tubes of lily-Biochemical and immunocytochemical characterization. PlantPhysiol. 116, 1421-1429. doi: 10.1104/pp.116.4.1421
88. Yokota, E., Tominaga, M., Mabuchi, I., Tsuji, Y., Staiger, C. J., Oiwa, K., et al. (2005). Plant villin, lilyP-135-ABP, possesses G-actin binding activityand accelerates the polymerization and depolymerization of actin inaCa2+-sensitive manner. Plant CellPhysiol. 46, 1690-1703. doi: 10.1093/pcp/pci185
89. Zhang, H., Qu, X. L., Bao, C. C., Khurana, P., Wang, Q. N., Xie, Y. R., et al. (2010a). Arabidopsis VILLIN5, an actin filament bundling and severing protein, is necessary for normal pollen tube growth. PlantCell 22, 2749-2767. doi: 10.1105/tpc.110.076257
90. Zhang, Y., He, J. M., Lee, D., and Mccormick, S. (2010b). Interdependence of endomembrane trafficking and actin dynamics during polarized growth of Arabidopsis pollen tubes. PlantPhysiol. 152, 2200-2210.doi: 10.1104/pp.109.142349
91. Zhang, Y., He, J. M., and Mccormick, S. (2009). Two Arabidopsis AGC kinases are critical for the polarized growth of pollen tubes. Plant J. 58, 474-484. doi: 10.1111/j.1365-313X.2009.03792.x
92. Zheng, Y. Y., Xie, Y. R., Jiang, Y. X., Qu, X. L., and Huang, S. J. (2013). Arabidopsis ACTIN-DEPOLYMERIZING FACTOR7 severs actin filaments and regulates actin cable turnover to promote normal pollen tube growth. Plant Cell 25, 3405-3423. doi: 10.1105/tpc.113.117820
93. Zheng, Y. Y., Xin, H. B., Lin, J. X., Liu, C. M., and Huang, S. J. (2012). An Arabidopsis class II formin, AtFH19, nucleates actin assembly, binds to the barbed end of actin filaments, and antagonizes the effect of AtFH1 on actin dynamics. J. Integr. PlantBiol. 54, 800-813. doi: 10.1111/j.1744-7909.2012.0.1160.x
94. Zhu, L., Zhang, Y., Kang, E., Xu, Q., Wang, M., Rui, Y., et al. (2013). MAP18 regulates the direction of pollen tube growth in Arabidopsis by modulating F-actin organization. Plant Cell 25, 851-867. doi: 10.1105/tpc.113.1.10528