Are kinesins required for organelle trafficking in plant cells?

Frontiers in Plant Science

Volumn 3, Issue JUL, 2012, Pages

  Cai, Giampiero ^a   Cresti, Mauro ^a  

^a UNIVERSITY OF SIENA   (Italy)

Author keywords

Chloroplast; Golgi; Kinesin; Microtubule; Mitochondria; Organelle movement

Indexed keywords

EID: 84885835097     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2012.00170     Document Type: Review

References (105)

1. Alexander, M., Andreas, H., and Eckhard, M. (2009). Structures of kinesin motor proteins. Cell Motil. Cytoskeleton66, 958-966.
2. Ambrose, J. C., Li, W., Marcus, A., Ma, H., and Cyr, R. (2005). A minus-end-directed kinesin with plus-end tracking protein activity is involved in spindle morphogenesis. Mol. Biol. Cell 16, 1584-1592.
3. Avisar, D., Abu-Abied, M., Belausov, E., Sadot, E., Hawes, C., and Sparkes, I. A. (2009). A Comparative study of the involvement of 17 Arabidopsis myosin family members on the motility of Golgi and other organelles. Plant Physiol.150, 700-709.
4. Avisar, D., Prokhnevsky, A. I., Makarova, K. S., Koonin, E. V., and Dolja, V. V. (2008). Myosin XI-K is required for rapid trafficking of Golgi stacks, peroxisomes, and mitochondria in leaf cells of Nicotiana benthamiana. Plant Physiol. 146, 1098-1108.
5. Bannigan, A., Scheible, W. R., Lukowitz, W., Fagerstrom, C., Wadsworth, P., Somerville, C., and Baskin, T. I. (2007). A conserved role for kinesin-5 in plant mitosis. J. Cell Sci. 120, 2819-2827.
6. Barroso, C., Chan, J., Allan, V., Doonan, J. H., Hussey, P. J., and Lloyd, C. W. (2000). Two kinesin-related proteins associated with the cold-stable cytoskeleton of carrot cells: characterization of a novel kinesin, DcKRP120-2. Plant J. 24, 859-868.
7. Boevink, P., Oparka, K., Santa, C. S., Martin, B., Betteridge, A., and Hawes, C. (1998). Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J. 15, 441-447.
8. Bowser, J., and Reddy, A. S. (1997). Localization of a kinesin-like calmodulin-binding protein in dividing cells ofArabidopsis and tobacco. Plant J. 12, 1429-1437.
9. Bradley, M. O. (1973). Microfilaments and cytoplasmic streaming: inhibition of streaming with cytochalasin. J. Cell Sci. 12, 327-343.
10. Cai, G., Bartalesi, A., Del Casino, C., Moscatelli, A., Tiezzi, A., and Cresti, M. (1993). The kinesin-immunoreactive homologue from Nicotiana tabacum pollen tube: biochemical properties and subcellular localization. Planta 191, 496-506.
11. Cai, G., and Cresti, M. (2009). Organelle motility in the pollen tube: a tale of 20 years. J. Exp. Bot. 60, 495-508.
12. Cai, G., Romagnoli, S., Moscatelli, A., Ovidi, E., Gambellini, G., Tiezzi, A., and Cresti, M. (2000). Identification and characterization of a novel microtubule-based motor associated with membranous organelles in tobacco pollen tubes. Plant Cell 12, 1719-1736.
13. Chan, J. (2012). Microtubule and cellulose microfibril orientation during plant cell and organ growth. J. Microsc.247, 23-32.
14. Condeelis, J. S. (1974). The identification of F-actin in the pollen tube and protoplast of Amaryllus belladonna. Exp. Cell Res. 88, 435-439.
15. Crowell, E. F., Bischoff, V., Desprez, T., Rolland, A., Stierhof, Y. D., Schumacher, K., Gonneau, M., Hofte, H., and Vernhettes, S. (2009). Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. Plant Cell 21, 1141-1154.
16. Derksen, J. (1996). Pollen tubes: a model system for plant cell growth. Bot. Acta 109, 341-345.
17. Dillman, J. F. III, Dabney, L. P., Karki, S., Paschal, B. M., Holzbaur, E. L., and Pfister, K. K. (1996). Functional analysis of dynactin and cytoplasmic dynein in slow axonal transport. J. Neurosci. 16, 6742-6752.
18. Erickson, R. P., Jia, Z., Gross, S. P., and Yu, C. C. (2011). How molecular motors are arranged on a cargo is important for vesicular transport. PLoS Comput. Biol. 7, e1002032. doi: 10.1371/journal.pcbi.1002032
19. Foissner, I. (2004). Microfilaments and microtubules control the shape, motility, and subcellular distribution of cortical mitochondria in characean internodal cells. Protoplasma 224, 145-157.
20. Foissner, I., Menzel, D., and Wasteneys, G. O. (2009). Microtubule-dependent motility and orientation of the cortical endoplasmic reticulum in elongating characean internodal cells. Cell Motil. Cytoskeleton. 66, 142-155.
21. Frederick, R. L., and Shaw, J. M. (2007). Moving mitochondria: establishing distribution of an essential organelle. Traffic 8, 1668-1675.
22. Frey, N., Klotz, J., and Nick, P. (2009). Dynamic bridges-a calponin-domain kinesin from rice links actin filaments and microtubules in both cycling and non-cycling cells. Plant Cell Physiol. 50, 1493-1506.
23. Frey, N., Klotz, J., and Nick, P. (2010). A kinesin with calponin-homology domain is involved in premitotic nuclear migration. J. Exp. Bot. 61, 3423-3437.
24. Goode, B. L., Drubin, D. G., and Barnes, G. (2000). Functional cooperation between the microtubule and actin cytoskeletons. Curr. Opin. Cell Biol. 12, 63-71.
25. Goto, Y., and Asada, T. (2007). Excessive expression of the plant kinesin TBK5 converts cortical and perinuclear microtubules into a radial array emanating from a single focus. Plant Cell Physiol. 48, 753-761.
26. Gutierrez, R., Lindeboom, J. J., Paredez, A. R., Emons, A. M., and Ehrhardt, D. W. (2009). Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat. Cell Biol. 11, 797-806.
27. Hamada, T., Tominaga, M., Fukaya, T., Nakamura, M., Nakano, A., Watanabe, Y., Hashimoto, T., and Baskin, T. I. (2012). RNA processing bodies, peroxisomes, Golgi bodies, mitochondria, and endoplasmic reticulum tubule junctions frequently pause at cortical microtubules. Plant Cell Physiol. 53, 699-708.
28. Hanton, S. L., Bortolotti, L. E., Renna, L., Stefano, G., and Brandizzi, F. (2005). Crossing the divide-transport between the endoplasmic reticulum and Golgi apparatus in plants. Traffic 6, 267-277.
29. Higashi-Fujime, S., and Nakamura, A. (2009). Cell and molecular biology of the fastest myosins. Int. Rev. Cell Mol. Biol. 276, 301-347.
30. Hirokawa, N., Noda, Y., Tanaka, Y., and Niwa, S. (2009). Kinesin superfamily motor proteins and intracellular transport. Nat. Rev. Mol. Cell Biol. 10, 682-696.
31. Hodges, A. R., Bookwalter, C. S., Krementsova, E. B., and Trybus, K. M. (2009). A nonprocessive class V myosin drives cargo processively when a kinesin-related protein is a passenger. Curr. Biol. 19, 2121-2125.
32. Holweg, C., and Nick, P. (2004). Arabidopsis myosin XI mutant is defective in organelle movement and polar auxin transport. Proc. Natl. Acad. Sci. U.S.A. 101, 10488-10493.
33. Holweg, C., and Nick, P. (2008). Retraction for Holweg and Nick: Arabidopsis myosin XI mutant is defective in organelle movement and polar auxin transport. Proc. Natl. Acad. Sci. U.S.A. 105, 3658.
34. Horgan, C. P., and McCaffrey, M. W. (2011). Rab GTPases and microtubule motors. Biochem. Soc. Trans. 39, 1202-1206.
35. Itoh, R., Fujiwara, M., and Shigeo, Y. (2001). Kinesin-related proteins with a mitochondrial targeting signal. Plant Physiol. 127, 724-726.
36. Jiang, S., and Ramachandran, S. (2004). Identification and molecular characterization of myosin gene family inOryza sativa genome. Plant Cell Physiol. 45, 590-599.
37. Jürgens, G. (2005). Plant cytokinesis: fission by fusion. Trends Cell Biol. 15, 277-283.
38. Kashina, A. S., Semenova, I. V., Ivanov, P. A., Potekhina, E. S., Zaliapin, I., and Rodionov, V. I. (2004). Protein kinase A, which regulates intracellular transport, forms complexes with molecular motors on organelles. Curr. Biol.14, 1877-1881.
39. Klotz, J., and Nick, P. (2012). A novel actin-microtubule cross-linking kinesin, NtKCH, functions in cell expansion and division. New Phytol. 193, 576-589.
40. Kumar, J., Yu, H., and Sheetz, M. P. (1995). Kinectin, an essential anchor for kinesin-driven vesicles motility. Science 267, 1834-1837.
41. Lawrence, C. J., Dawe, R. K., Christie, K. R., Cleveland, D. W., Dawson, S. C., Endow, S. A., Goldstein, L. S., Goodson, H. V., Hirokawa, N., Howard, J., Malmberg, R. L., McIntosh, J. R., Miki, H., Mitchison, T. J., Okada, Y., Reddy, A. S., Saxton, W. M., Schliwa, M., Scholey, J. M., Vale, R. D., Walczak, C. E., and Wordeman, L. (2004). A standardized kinesin nomenclature. J. Cell Biol. 167, 19-22.
42. Ledbetter, M. C., and Porter, K. R. (1963). A "microtubule" in plant cell fine structure. J. Cell Biol. 19, 239-250.
43. Lee, Y. R. J., Giang, H. M., and Liu, B. (2001). A novel plant kinesin-related protein specifically associates with the phragmoplast organelles. Plant Cell 13, 2427-2439.
44. Lee, Y. R. J., Li, Y., and Liu, B. (2007). Two Arabidopsis phragmoplast-associated kinesins play a critical role in cytokinesis during male gametogenesis. Plant Cell 19, 2595-2605.
45. Lee, Y. R. J., and Liu, B. (2000). Identification of a phragmoplast-associated kinesin-related protein in higher plants. Curr. Biol. 10, 797-800.
46. Lee, Y. R. J., and Liu, B. (2004). Cytoskeletal motors in Arabidopsis. Sixty-one kinesins and seventeen myosins. Plant Physiol. 136, 3877-3883.
47. Levi, V., Serpinskaya, A. S., Gratton, E., and Gelfand, V. (2006). Organelle transport along microtubules in Xenopusmelanophores: evidence for cooperation between multiple motors. Biophys. J. 90, 318-327.
48. Li, J., Jiang, J., Qian, Q., Xu, Y., Zhang, C., Xiao, J., Du, C., Luo, W., Zou, G., Chen, M., Huang, Y., Feng, Y., Cheng, Z., Yuan, M., and Chong, K. (2011). Mutation of rice BC12/GDD1, which encodes a kinesin-like protein that binds to a GA biosynthesis gene promoter, leads to dwarfism with impaired cell elongation. Plant Cell 23, 628-640.
49. Li, J., Xu, Y., and Chong, K. (2012). The novel functions of kinesin motor proteins in plants. Protoplasma249(Suppl.), 95-100.
50. Li, S., Lei, L., Somerville, C. R., and Gu, Y. (2012). Cellulose synthase interactive protein 1 (CSI1) links microtubules and cellulose synthase complexes. Proc. Natl. Acad. Sci. U.S.A. 109, 185-190.
51. Liebe, S., and Menzel, D. (1995). Actomyosin-based motility of endoplasmic reticulum and chloroplasts in Vallisneria mesophyll cells. Biol. Cell 85, 207-222.
52. Liu, G. Q., Cai, G., Del Casino, C., Tiezzi, A., and Cresti, M. (1994). Kinesin-related polypeptide is associated with vesicles from Corylus avellana pollen. Cell Motil. Cytoskeleton 29, 155-166.
53. Lovy-Wheeler, A., Cardenas, L., Kunkel, J. G., and Hepler, P. K. (2007). Differential organelle movement on the actin cytoskeleton in lily pollen tubes. Cell Motil. Cytoskeleton 64, 217-232.
54. Lu, L., Lee, Y. R. J., Pan, R., Maloof, J. N., and Liu, B. (2005). An internal motor kinesin is associated with the Golgi apparatus and plays a role in trichome morphogenesis in Arabidopsis. Mol. Biol. Cell 16, 811-823.
55. Marcus, A. I., Ambrose, J. C., Blickley, L., Hancock, W. O., and Cyr, R. J. (2002). Arabidopsis thaliana protein, ATK1, is a minus-end directed kinesin that exhibits non-processive movement. Cell Motil. Cytoskeleton 52, 144-150.
56. Matsui, K., Collings, D., and Asada, T. (2001). Identification of a novel plant-specific kinesin-like protein that is highly expressed in interphase tobacco BY-2 cells. Protoplasma 215, 105-115.
57. Moscatelli, A., Del Casino, C., Lozzi, L., Cai, G., Scali, M., Tiezzi, A., and Cresti, M. (1995). High molecular weight polypeptides related to dynein heavy chains in Nicotiana tabacum pollen tubes. J. Cell Sci. 108, 1117-1125.
58. Mu, Z., Baocai, Z., Qian, Q., Yanchun, Y., Rui, L., Junwen, Z., Xiangling, L., Dali, Z., Jiayang, L., and Yihua, Z. (2010). Brittle Culm 12, a dual-targeting kinesin-4 protein, controls cell-cycle progression and wall properties in rice. Plant J. 63, 312-328.
59. Muller, S., Han, S., and Smith, L. G. (2006). Two kinesins are involved in the spatial control of cytokinesis inArabidopsis thaliana. Curr. Biol. 16, 888-894.
60. Muresan, V., and Muresan, Z. (2008). No conventional function for the conventional kinesin? Traffic 9, 1823-1827.
61. Muresan, V., and Muresan, Z. (2012). Unconventional functions of microtubule motors. Arch. Biochem. Biophys.520, 17-29.
62. Nebenführ, A., Gallagher, L. A., Dunahay, T. G., Frohlick, J. A., Mazurkiewicz, A. M., Meehl, J. B., and Staehelin, L. A. (1999). Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol.121, 1127-1142.
63. Nebenführ, A., and Staehelin, L. A. (2001). Mobile factories: Golgi dynamics in plant cells. Trends Plant Sci. 6, 160-167.
64. Ni, C. Z., Wang, H. Q., Xu, T., Qu, Z., and Liu, G. Q. (2005). AtKP1, a kinesin-like protein, mainly localizes to mitochondria in Arabidopsis thaliana. Cell Res. 15, 725-733.
65. Paredez, A. R., Somerville, C. R., and Ehrhardt, D. W. (2006). Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312, 1491-1495.
66. Pathak, D., Sepp, K. J., and Hollenbeck, P. J. (2010). Evidence that myosin activity opposes microtubule-based axonal transport of mitochondria. J. Neurosci. 30, 8984-8992.
67. 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.
68. Preuss, M. L., Delmer, D. P., and Liu, B. (2003). The cotton kinesin-like calmodulin-binding protein associates with cortical microtubules in cotton fibers. Plant Physiol. 132, 154-160.
69. Preuss, M. L., Kovar, D. R., Lee, Y.-R. J., Staiger, C. J., Delmer, D. P., and Liu, B. (2004). A plant-specific kinesin binds to actin microfilaments and interacts with cortical microtubules in cotton fibers. Plant Physiol. 136, 3945-3955.
70. Reddy, A. S. N., and Day, I. S. (2001). Kinesins in the Arabidopsis genome: a comparative analysis among eukaryotes. BMC Genomics 2, 2. doi: 10.1186/1471-2164-2-2
71. Reddy, A. S. N., and Day, I. S. (2011). "Microtubule motor proteins in the Eukaryotic green lineage: functions and regulation" in The Plant Cytoskeleton, ed. B. Liu (New York: Springer), 119-141.
72. Richardson, D. N., Simmons, M. P., and Reddy, A. S. (2006). Comprehensive comparative analysis of kinesins in photosynthetic eukaryotes. BMC Genomics 7, 18. doi: 10.1186/1471-2164-7-18
73. Romagnoli, S., Cai, G., and Cresti, M. (2003). In vitro assays demonstrate that pollen tube organelles use kinesin-related motor proteins to move along microtubules. Plant Cell 15, 251-269.
74. Romagnoli, S., Cai, G., Faleri, C., Yokota, E., Shimmen, T., and Cresti, M. (2007). Microtubule-and actin filament-dependent motors are distributed on pollen tube mitochondria and contribute differently to their movement. Plant Cell Physiol. 48, 345-361.
75. Schuchardt, I., Assmann, D., Thines, E., Schuberth, C., and Steinberg, G. (2005). Myosin-V, Kinesin-1, and Kinesin-3 cooperate in hyphal growth of the fungus Ustilago maydis. Mol. Biol. Cell 16, 5191-5201.
76. Schuster, M., Treitschke, S., Kilaru, S., Molloy, J., Harmer, N. J., and Steinberg, G. (2012). Myosin-5, kinesin-1 and myosin-17 cooperate in secretion of fungal chitin synthase. EMBO J. 31, 214-227.
77. Seabra, M. C., and Coudrier, E. (2004). Rab GTPases and myosin motors in organelle motility. Traffic 5, 393-399.
78. Shanina, N. A., Lazareva, E. M., Skorova, E. Y., Chentsov, Y. S., and Smirnova, E. A. (2009). A high molecular weight polypeptide cross-reacting with the antibodies to the dynein heavy chain localizes to the subset of Golgi complex in higher plant cells. Cell Biol. Int. 33, 290-300.
79. Shimmen, T. (2007). The sliding theory of cytoplasmic streaming: fifty years of progress. J. Plant Res. 120, 31-43.
80. Shimmen, T., Ridge, R. W., Lambiris, I., Plazinski, J., Yokota, E., and Williamson, R. E. (2000). Plant myosins. Protoplasma 214, 1-10.
81. Steinberg, G. (2011). Motors in fungal morphogenesis: cooperation versus competition. Curr. Opin. Microbiol. 14, 660-667.
82. Suetsugu, N., Yamada, N., Kagawa, T., Yonekura, H., Uyeda, T. Q., Kadota, A., and Wada, M. (2010). Two kinesin-like proteins mediate actin-based chloroplast movement in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 107, 8860-8865.
83. Suetsugu, N., Dolja, V. V., and Wada, M. (2010). Why have chloroplasts developed a unique motility system? Plant Sign. Behav. 5, 1190-1196.
84. Tiezzi, A., Moscatelli, A., Cai, G., Bartalesi, A., and Cresti, M. (1992). An immunoreactive homolog of mammalian kinesin in Nicotiana tabacum pollen tubes. Cell Motil. Cytoskeleton 21, 132-137.
85. 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. U.S.A. 107, 6894-6899.
86. Umezu, N., Umeki, N., Mitsui, T., Kondo, K., and Maruta, S. (2011). Characterization of a novel rice kinesin O12 with a calponin homology domain. J. Biochem. 149, 91-101.
87. Vale, R. D. (2003). The molecular motor toolbox for intracellular transport. Cell 112, 467-480.
88. Vale, R. D., Reese, T. S., and Sheetz, M. P. (1985). Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42, 39-50.
89. Van Gestel, K., Kohler, R. H., and Verbelen, J. P. (2002). Plant mitochondria move on F-actin, but their positioning in the cortical cytoplasm depends on both F-actin and microtubules. J. Exp. Bot. 53, 659-667.
90. Vanstraelen, M., Inze, D., and Geelen, D. (2006). Mitosis-specific kinesins in Arabidopsis. Trends Plant Sci. 11, 167-175.
91. Verchot-Lubicz, J., and Goldstein, R. (2010). Cytoplasmic streaming enables the distribution of molecules and vesicles in large plant cells. Protoplasma 240, 99-107.
92. Wang, Z., and Pesacreta, T. C. (2004). A subclass of myosin XI is associated with mitochondria, plastids, and the molecular chaperone subunit TCP-1alpha in maize. Cell Motil. Cytoskeleton 57, 218-232.
93. Wei, L., Liu, B., and Li, Y. (2005). Distribution of a kinesin-related protein on Golgi apparatus of tobacco pollen tubes. Chi. Sci. Bull. 50, 2175-2181.
94. Wei, L., Zhang, W., Liu, Z., and Li, Y. (2009). AtKinesin-13A is located on Golgi-associated vesicle and involved in vesicle formation/budding in Arabidopsis root-cap peripheral cells. BMC Plant Biol. 9, 138. doi: 10.1186/1471-2229-9-138
95. Wickstead, B., and Gull, K. (2007). Dyneins across eukaryotes: a comparative genomic analysis. Traffic 8, 1708-1721.
96. Williamson, R. E. (1979). Actin in motile and other processes in plant cells. Can. J. Bot. 58, 766-771.
97. Xu, T., Qu, Z., Yang, X., Qin, X., Xiong, J., Wang, Y., Ren, D., and Liu, G. (2009). A cotton kinesin GhKCH2 interacts with both microtubules and microfilaments. Biochem. J. 421, 171-180.
98. Yang, X. Y., Chen, Z. W., Xu, T., Qu, Z., Pan, X. D., Qin, X. H., Ren, D. T., and Liu, G. Q. (2011). Arabidopsis kinesin KP1 specifically interacts with VDAC3, a mitochondrial protein, and regulates respiration during seed germination at low temperature. Plant Cell 23, 1093-1106.
99. Yokota, E., McDonald, A. R., Liu, B., Shimmen, T., and Palevitz, B. A. (1995). Localization of a 170 kDa myosin heavy chain in plant cells. Protoplasma 185, 178-187.
100. Yokota, E., Ueda, H., Hashimoto, K., Orii, H., Shimada, T., Hara-Nishimura, I., and Shimmen, T. (2011). Myosin XI-dependent formation of tubular structures from endoplasmic reticulum isolated from tobacco cultured BY-2 cells. Plant Physiol. 156, 129-143.
101. Yoneda, A., Ito, T., Higaki, T., Kutsuna, N., Saito, T., Ishimizu, T., Osada, H., Hasezawa, S., Matsui, M., and Demura, T. (2010). Cobtorin target analysis reveals that pectin functions in deposition of cellulose microfibrils parallel to cortical microtubules in a manner dependent on the methylesterification ratio of pectin and its distribution. Plant J. 64, 657-667.
102. Zheng, M., Wang, Q., Teng, Y., Wang, X., Wang, F., Chen, T., Samaj, J., Lin, J., and Logan, D. C. (2010). The speed of mitochondrial movement is regulated by the cytoskeleton and myosin in Picea wilsonii pollen tubes. Planta 231, 779-791.
103. Zhong, R., Burk, D. H., Morrison, W. H. III, and Ye, Z. H. (2002). A kinesin-Like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength. Plant Cell 14, 3101-3117.
104. Zhu, C., and Dixit, R. (2011a). Functions of the Arabidopsis kinesin superfamily of microtubule-based motor proteins. Protoplasma. doi: 10.1007/s00709-011-0343-9 [Epub ahead print].
105. Zhu, C., and Dixit, R. (2011b). Single molecule analysis of the Arabidopsis FRA1 kinesin shows that it is a functional motor protein with unusually high processivity. Mol. Plant 4, 879-885.