New insights into dynamic actin-based chloroplast photorelocation movement

Molecular Plant

Volumn 4, Issue 5, 2011, Pages 771-781

  Kong, Sam Geun ^a   Wada, Masamitsu ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Actin filament(s); blue light; chloroplast movement; cytoskeleton dynamics; photoreceptor; phototropin

Indexed keywords

EID: 80053475882     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/ssr061     Document Type: Review

References (102)

1. Aihara, Y., Tabata, R., Suzuki, T., Shimazaki, K.-I., and Nagatani, A. (2008). Molecular basis of the functional specificities of phototropin 1 and 2. Plant J. 56, 364-375.
2. Anielska-Mazur, A., Bernaś, T., and Gabryś, H. (2009). In vivo reorganization of the actin cytoskeleton in leaves of Nicotiana tabacum L. transformed with plastin-GFP: Correlation with light-activated chloroplast responses. BMC Plant Biol. 9, 64.
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. (Pubitemid 352844128)
5. Babourina, O., Newman, I., and Shabala, S. (2002). Blue lightinduced kinetics of H+ and Ca2+ fluxes in etiolated wild-type and phototropin-mutant Arabidopsis seedlings. Proc. Natl Acad. Sci. U S A. 99, 2433-2438. (Pubitemid 34169078)
6. Baum, G., Long, J.C., Jenkins, G.I., and Trewavas, A.J. (1999). Stimulation of the blue light phototropic receptor NPH1 causes a transient increase in cytosolic Ca2+. Proc. Natl Acad. Sci. U S A. 96, 13554-13559.
7. Blanchoin, L., Boujemaa-Paterski, R., Henty, J.L., Khurana, P., and Staiger, C.J. (2010). Actin dynamics in plant cells: A team effort from multiple proteins orchestrates this very fast-paced game. Curr. Opin. Plant Biol. 13, 714-723.
8. Briggs, W.R., et al. (2001). The phototropin family of photoreceptors. Plant Cell. 13, 993-997. (Pubitemid 32497464)
9. Christie, J.M. (2007). Phototropin blue-light receptors. Annu. Rev. Plant Biol. 58, 21-45. (Pubitemid 46986316)
10. Christie, J.M., Swartz, T.E., Bogomolni, R.A., and Briggs, W.R. (2002). Phototropin LOV domains exhibit distinct roles in regulating photoreceptor function. Plant J. 32, 205-219. (Pubitemid 35249919)
11. DeBlasio, S.L., Luesse, D.L., and Hangarter, R.P. (2005). A plantspecific protein essential for blue-light-induced chloroplast movements. Plant Physiol. 139, 101-114. (Pubitemid 43951595)
12. DeBlasio, S.L., Mullen, J.L., Luesse, D.R., and Hangarter, R.P. (2003). Phytochrome modulation of blue light-induced chloroplast movements in Arabidopsis. Plant Physiol. 133, 1471-1479. (Pubitemid 38047279)
13. Dong, X.J., Ryu, J.H., Takagi, S., and Nagai, R. (1996). Dynamic changes in the organization of microfilaments associated with the photocontrolled motility of chloroplasts in epidermal cells of Vallisneria. Protoplasma. 195, 18-24. (Pubitemid 27028074)
14. Gabryś, H. (2004). Blue light-induced orientation movements of chloroplasts in higher plants: Recent progress in the study of their mechanisms. Acta Physiol. Plant. 26, 473-478. (Pubitemid 40024963)
15. Galván-Ampudia, C.S., and Offringa, R. (2007). Plant evolution: AGC kinases tell the auxin tale. Trends Plant Sci. 12, 541-547. (Pubitemid 350181562)
16. Harada, A., and Shimazaki, K.-I. (2009). Measurement of changes in cytosolic Ca2+ in Arabidopsis guard cells and mesophyll cells in response to blue light. Plant Cell Physiol. 50, 360-373.
17. Harada, A., Sakai, T., and Okada, K. (2003). Phot1 and phot2 mediate blue light-induced transient increases in cytosolic Ca2+ differently in Arabidopsis leaves. Proc. Natl Acad. Sci. U S A. 100, 8583-8588. (Pubitemid 36842587)
18. Huang, K., and Beck, C.F. (2003). Phototropin is the blue-light receptor that controls multiple steps in the sexual life cycle of the green alga Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. U S A. 100, 6269-6274. (Pubitemid 36576965)
19. 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. (Pubitemid 44061020)
20. Inoue, S.-I., et al. (2011). Functional analyses of the activation loop of phototropin2 in Arabidopsis. Plant Physiol. 156, 117-128.
21. Inoue, S.-I., Kinoshita, T., Matsumoto, M., Nakayama, K.I., Doi, M., and Shimazaki, K.-I. (2008). Blue light-induced autophosphorylation of phototropin is a primary step for signaling. Proc. Natl Acad. Sci. U S A. 105, 5626-5631. (Pubitemid 351753913)
22. Inoue, S.-I., Takemiya, A., and Shimazaki, K.-I. (2010). Phototropin signaling and stomatal opening as a model case. Curr. Opin. Plant Biol. 13, 587-593.
23. Islam, M.S., Niwa, Y., and Takagi, S. (2009). Light-dependent intracellular positioning of mitochondria in Arabidopsis thaliana mesophyll cells. Plant Cell Physiol. 50, 1032-1040.
24. Iwabuchi, K., Minamino, R., and Takagi, S. (2010). Actin reorganization underlies phototropin-dependent positioning of nuclei in Arabidopsis leaf cells. Plant Physiol. 152, 1309-1319.
25. Iwabuchi, K., Sakai, T., and Takagi, S. (2007). Blue light-dependent nuclear positioning in Arabidopsis thaliana leaf cells. Plant Cell Physiol. 48, 1291-1298. (Pubitemid 47428914)
26. Izutani, Y., Takagi, S., and Nagai, R. (1990). Orientation movements of chloroplasts in Vallisneria epidermal-cells: Different effects of light at low-fluence and high-fluence rate. Photochem. Photobiol. 51, 105-111.
27. Jarillo, J.A., Gabryś, H., Capel, J., Alonso, J.M., Ecker, J.R., and Cashmore, A.R. (2001). Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature. 410, 952-954. (Pubitemid 32335843)
28. Jouhet, J., andGray, J.C. (2009). Interactionof actinandthe chloroplast protein import apparatus. J. Biol. Chem. 284, 19132-19141.
29. Kadota,A., andWada, M. (1989). Photoinduction of circular F-actin on chloroplast in a fern protonemal cell. Protoplasma. 151, 171-174.
30. Kadota, A., and Wada, M. (1992). Photoinduction of formation of circular structures by microfilaments on chloroplasts during intracellular orientation in protonemal cells of the fern Adiantum-Capillus-Veneris. Protoplasma. 167, 97-107.
31. Kadota, A., et al. (2009). Short actin-based mechanism for light-directed chloroplast movement in Arabidopsis. Proc. Natl Acad. Sci. U S A. 106, 13106-13111.
32. Kadota,A.,Sato,Y.,andWada,M.(2000). Intracellular chloroplastphotorelocation in the moss Physcomitrella patens ismediated by phytochrome as well as by a blue-light receptor. Planta. 210, 932-937. (Pubitemid 30334071)
33. Kagawa, T., and Wada, M. (2002). Blue light-induced chloroplast relocation. Plant Cell Physiol. 43, 367-371. (Pubitemid 34514225)
34. Kagawa, T., andWada, M. (2004). Velocity of chloroplast avoidance movement is fluence rate dependent. Photochem. Photobiol. Sci. 3, 592-595. (Pubitemid 38968073)
35. Kagawa, T., et al. (2001). Arabidopsis NPL1: A phototropin homolog controlling the chloroplast high-light avoidance response. Science. 291, 2138-2141. (Pubitemid 32224442)
36. Kagawa, T., Kasahara, M., Abe, T., Yoshida, S., andWada, M. (2004). Function analysis of phototropin2 using fern mutants deficient in blue light-induced chloroplast avoidance movement. Plant Cell Physiol. 45, 416-426. (Pubitemid 38592368)
37. Kagawa,T.,andWada,M.(1993). Light-dependent nuclear positioning in prothallial cells of Adiantum capillus-veneris. Protoplasma. 177, 82-85. (Pubitemid 2024061)
38. Kami, C., Lorrain, S., Hornitschek, P., and Fankhauser, C. (2010). Light-regulated plant growth and development. Curr. Top. Dev. Biol. 91, 29-66.
39. Kandasamy, M.K., and Meagher, R.B. (1999). Actin-organelle interaction: Association with chloroplast in arabidopsis leaf mesophyll cells. Cell Motil. Cytoskeleton. 44, 110-118. (Pubitemid 29480306)
40. Kasahara, M., Kagawa, T., Oikawa, K., Suetsugu, N., Miyao, M., and Wada, M. (2002). Chloroplast avoidance movement reduces photodamage in plants. Nature. 420, 829-832. (Pubitemid 36019632)
41. Kasahara, M., Kagawa, T., Sato, Y., Kiyosue, T., andWada,M. (2004). Phototropinsmediateblueandredlight-inducedchloroplastmovements in Physcomitrella patens. Plant Physiol. 135, 1388-1397.
42. Kawai, H., et al. (2003). Responses of ferns to red light are mediated by an unconventional photoreceptor. Nature. 421, 287-290. (Pubitemid 36139135)
43. 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.
44. Kodama, Y., Suetsugu, N., Kong, S.-G., and Wada, M. (2010). Two interacting coiled-coil proteins, WEB1 and PMI2, maintain the chloroplast photorelocation movement velocity in Arabidopsis. Proc. Natl Acad. Sci. U S A. 107, 19591-19596.
45. Kong, S.-G., Kinoshita, T., Shimazaki, K.-I., Mochizuki, N., Suzuki, T., and Nagatani, A. (2007). The C-terminal kinase fragment of Arabidopsis phototropin 2 triggers constitutive phototropin responses. Plant J. 51, 862-873. (Pubitemid 47301660)
46. Kong, S.-G., Suzuki, T., Tamura, K., Mochizuki, N., Hara-Nishimura, I., and Nagatani, A. (2006). Blue light-induced association of phototropin 2 with the Golgi apparatus. Plant J. 45, 994-1005. (Pubitemid 43344760)
47. Krzeszowiec, W., and Gabryś, H. (2007). Phototropin mediated relocation of myosins in Arabidopsis thaliana. Plant Signal. Behav. 2, 333-336. (Pubitemid 350124651)
48. Krzeszowiec,W., Rajwa, B., Dobrucki, J., and Gabryś, H. (2007). Actin cytoskeleton in Arabidopsis thaliana under blue and red light. Biol. Cell. 99, 251-260. (Pubitemid 46746117)
49. Kumatani, T., et al. (2006). Possible association of actin filaments with chloroplasts of spinach mesophyll cells in vivo and in vitro. Protoplasma. 229, 45-52. (Pubitemid 44825286)
50. Luesse, D.R., DeBlasio, S.L., and Hangarter, R.P. (2006). Plastid movement impaired 2, a new gene involved in normal bluelight- induced chloroplast movements in Arabidopsis. Plant Physiol. 141, 1328-1337. (Pubitemid 44223285)
51. Luesse, D.R., DeBlasio, S.L., and Hangarter, R.P. (2010). Integration of Phot1, Phot2, and PhyB signalling in light-induced chloroplast movements. J. Exp. Bot. 61, 4387-4397.
52. Malec, P., Rinaldi, R.A., and Gabryś, H. (1996). Light-induced chloroplast movements in Lemna trisulca: Identification of the motile system. Plant Sci. 120, 127-137. (Pubitemid 27073825)
53. Matsuoka, D., and Tokutomi, S. (2005). Blue light-regulated molecular switch of Ser/Thr kinase in phototropin. Proc. Natl Acad. Sci. U S A. 102, 13337-13342. (Pubitemid 41325024)
54. Mittmann, F., et al. (2004). Targeted knockout in Physcomitrella reveals direct actions of phytochrome in the cytoplasm. Proc. Natl Acad. Sci. U S A. 101, 13939-13944. (Pubitemid 39298511)
55. Nozue, K., et al. (1998). A phytochrome from the fern Adiantum with features of the putative photoreceptor NPH1. Proc. Natl Acad. Sci. U S A. 95, 15826-15830. (Pubitemid 29018785)
56. Odeh, H., et al. (2010). Mutations in Grxcr1 are the basis for inner ear dysfunction in the pirouette mouse. Am. J. Hum. Genet. 86, 148-160.
57. Oikawa, K., et al. (2003). Chloroplast unusual positioning1 is essential for proper chloroplast positioning. Plant Cell. 15, 2805-2815. (Pubitemid 37546252)
58. Oikawa, K., et al. (2008). Chloroplast outer envelope protein CHUP1 is essential for chloroplast anchorage to the plasma membrane and chloroplast movement. Plant Physiol. 148, 829-842. (Pubitemid 352847542)
59. Onodera, A., et al. (2005). Phototropin from Chlamydomonas reinhardtii is functional in Arabidopsis thaliana. Plant Cell Physiol. 46, 367-374. (Pubitemid 40413240)
60. Paves, H., and Truve, E. (2007). Myosin inhibitors block accumulation movement of chloroplasts in Arabidopsis thaliana leaf cells. Protoplasma. 230, 165-169. (Pubitemid 46673991)
61. 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.
62. Reddy, A.S., and Day, I.S. (2001). Analysis of the myosins encoded in the recently completed Arabidopsis thaliana genome sequence. Genome Biol. 2, RESEARCH0024.
63. Reiland, S., et al. (2009). Large-scale Arabidopsis phosphoproteome profiling reveals novel chloroplast kinase substrates and phosphorylation networks. Plant Physiol. 150, 889-903.
64. Reisen,D.,andHanson,M.R.(2007).AssociationofsixYFP-myosinXItail fusions with mobile plant cell organelles.BMC Plant Biol. 7, 6.
65. Sakai, T., et al. (2001). Arabidopsis nph1 and npl1: Blue light receptors that mediate both phototropism and chloroplast relocation. Proc. Natl Acad. Sci. U S A. 98, 6969-6974. (Pubitemid 32538326)
66. Sakurai, N., Domoto, K., and Takagi, S. (2005). Blue-light-induced reorganization of the actin cytoskeleton and the avoidance response of chloroplasts in epidermal cells of Vallisneria gigantea. Planta. 221, 66-74. (Pubitemid 40600011)
67. Sato, Y., Wada, M., and Kadota, A. (2001). Choice of tracks, microtubules and/or actin filaments for chloroplast photo-movement is differentially controlled by phytochrome and a blue light receptor. J. Cell Sci. 114, 269-279. (Pubitemid 32149571)
68. Sattarzadeh, A., Krahmer, J., Germain, A.D., and Hanson, M.R. (2009). A myosin XI tail domain homologous to the yeast myosin vacuole-binding domain interacts with plastids and stromules in Nicotiana benthamiana. Mol. Plant. 2, 1351-1358.
69. Schmidt von Braun, S., and Schleiff, E. (2008). The chloroplast outer membrane protein CHUP1 interacts with actin and profilin. Planta. 227, 1151-1159.
70. Senn, G. (1908). Die Gestalts- und Lageveränderung der Pflanzen- Chromatophoren (Leipzig: Wilhelm-Engelmann).
71. Shimmen, T. (2007). The sliding theory of cytoplasmic streaming: Fifty years of progress. J. Plant Res. 120, 31-43.
72. Shimmen, T., and Yokota, E. (2004). Cytoplasmic streaming in plants. Curr. Opin. Cell Biol. 16, 68-72. (Pubitemid 38368154)
73. 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.
74. Stoelzle, S., Kagawa, T., Wada, M., Hedrich, R., and Dietrich, P. (2003). Blue light activates calcium-permeable channels in Arabidopsis mesophyll cells via the phototropin signaling pathway. Proc. Natl Acad. Sci. U S A. 100, 1456-1461. (Pubitemid 36184023)
75. Suetsugu, N., and Wada, M. (2007a). Chloroplast photorelocation movement mediated by phototropin family proteins in green plants. Biol. Chem. 388, 927-935. (Pubitemid 47258540)
76. Suetsugu, N., andWada, M. (2007b). Phytochrome-dependent photomovement responses mediated by phototropin family proteins in cryptogam plants. Photochem. Photobiol. 83, 87-93. (Pubitemid 46697227)
77. Suetsugu, N., and Wada, M. (2009). Chloroplast photorelocation movement. In The Chloroplast: Interactions with the Environment, Sandelius A.S., Aronsson,H., eds (Berlin Heidelberg: Springer), pp. 235-266.
78. Suetsugu, N., Dolja, V.V., and Wada, M. (2010a). Why have chloroplasts developed a unique motility system? Plant Signal. Behav. 5, 1190-1196.
79. Suetsugu, N., et al. (2010b). Two kinesin-like proteins mediate actin- based chloroplast movement in Arabidopsis thaliana. Proc. Natl Acad. Sci. U S A. 107, 8860-8865.
80. Suetsugu, N., Kagawa, T., and Wada, M. (2005a). An auxilin-like Jdomain protein, JAC1, regulates phototropin-mediated chloroplast movement in Arabidopsis. Plant Physiol. 139, 151-162. (Pubitemid 43951599)
81. Suetsugu, N., Mittmann, F., Wagner, G., Hughes, J., and Wada, M. (2005b). A chimeric photoreceptor gene, NEOCHROME, has arisen twice during plant evolution. Proc. Natl Acad. Sci. U S A. 102, 13705-13709. (Pubitemid 41420912)
82. Sugiyama, Y., andKadota, A. (2011). Photosynthesis-dependent but neochrome1- independent light positioning of chloroplasts and nuclei in the fern Adiantum capillus-veneris. Plant Physiol. 155, 1205-1213.
83. Takagi, S. (2003). Actin-based photo-orientation movement of chloroplasts in plant cells. J. Exp. Biol. 206, 1963-1969. (Pubitemid 36761798)
84. Takagi, S., Islam, M.S., and Iwabuchi, K. (2011). Dynamic behavior of double-membrane-bounded organelles in plant cells. Int. Rev. Cell Mol. Biol. 286, 181-222.
85. Takagi, S., Takamatsu, H., and Sakurai-Ozato, N. (2009). Chloroplast anchoring: Its implications for the regulation of intracellular chloroplast distribution. J. Exp. Bot. 60, 3301-3310.
86. Takano, A., Suetsugu, N., Wada, M., and Kohda, D. (2010). Crystallographic and functional analyses of J-domain of JAC1 essential for chloroplast photorelocation movement in Arabidopsis thaliana. Plant Cell Physiol. 51, 1372-1376.
87. Tlalka, M., and Gabryś, H. (1993). Influence of calcium on blue-lightinduced chloroplast movement in Lemna-trisulca L. Planta. 189, 491-498.
88. Tominaga,M., et al. (2003). Higher plantmyosin XI moves processively on actin with 35 nm steps at high velocity. EMBO J. 22, 1263-1272. (Pubitemid 36362690)
89. Tsuboi, H., and Wada, M. (2010). Speed of signal transfer in the chloroplast accumulation response. J. Plant Res. 123, 381-390.
90. Tsuboi, H., and Wada, M. (2011). Chloroplasts can move in any direction to avoid strong light. J. Plant Res. 124, 201-210.
91. Tsuboi, H., Suetsugu, N., Kawai-Toyooka, H., and Wada, M. (2007). Phototropins and neochrome1 mediate nuclear movement in the fern Adiantum capillus-veneris. Plant Cell Physiol. 48, 892-896. (Pubitemid 47356093)
92. Tsuboi, H., Yamashita, H., andWada, M. (2009). Chloroplasts do not have a polarity for light-induced accumulation movement. J. Plant Res. 122, 131-140.
93. Ueda, H., et al. (2010). Myosin-dependent endoplasmic reticulum motility and F-actin organization in plant cells. Proc. Natl Acad. Sci. U S A. 107, 6894-6899.
94. Wada, M., and Kong, S.-G. (in press). Analysis of chloroplast movement and relocation in Arabidopsis. In Chloroplast Research in Arabidopsis: Methods and Protocols, Jarvis, R.P., ed. (Totowa, NJ: Humana).
95. Wada, M., and Suetsugu, N. (2004). Plant organelle positioning. Curr. Opin. Plant Biol. 7, 626-631. (Pubitemid 39379505)
96. Wada, M., Kagawa, T., and Sato, Y. (2003). Chloroplast movement. Annu. Rev. Plant Biol. 54, 455-468. (Pubitemid 37400002)
97. Wagner, G., Haupt,W., and Laux, A. (1972). Reversible inhibition of chloroplast movement by cytochalasin B in the green alga mougeofia. Science. 176, 808-809.
98. Wen, F., Xing, D., and Zhang, L.R. (2008). Hydrogen peroxide is involved in high blue light-induced chloroplast avoidance movements in Arabidopsis. J. Exp. Bot. 59, 2891-2901. (Pubitemid 351957506)
99. Whippo, C.W., et al. (2011). THRUMIN1 is a light-regulated actinbundling protein involved in chloroplast motility. Curr. Biol. 21, 59-64.
100. Wojtaszek, P., Anielska-Mazur, A., Gabryś, H., Baluska, F., and Volkmann,D. (2005).Recruitment ofmyosinVIIItowardsplastid surfaces is root-cap specific and provides the evidence for actomyosin involvement inrootosmosensing.FunctionalPlantBiol.32,721-736. (Pubitemid 41290865)
101. Yamashita, H., Sato, Y., Kanegae, T., Kagawa, T., Wada, M., and Kadota, A. (2011). Chloroplast actin filaments organize meshwork on the photorelocated chloroplasts in the moss Physcomitrella patens. Planta. 233, 357-368.
102. Yokota, E., et al. (2005). Plant villin, lily P-135-ABP, possesses G-actin binding activity and accelerates the polymerization and depolymerization of actin in a Ca2+-sensitive manner. Plant Cell Physiol. 46, 1690-1703. (Pubitemid 41619487)