Stromules and the dynamic nature of plastid morphology

Journal of Microscopy

Volumn 214, Issue 2, 2004, Pages 124-137

  Kwok, E Y ^a   Hanson, M R ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Actin; Chloroplast; Cytoskeleton; GFP; Microfilament; Microtubule; Morphology; Motility; Plastid; Protein trafficking; Stromule; Tubulin

Indexed keywords

FLUORESCENCE; PLANTS (BOTANY); PROTEINS;

ACTIN; CHLOROPLAST; CYTOSKELETONS; GREEN FLUORESCENT PROTEIN; MICROFILAMENTS; MICROTUBULES; MOTILITY; PLASTID; PROTEIN TRAFFICKING; STROMULE; TUBULIN;

PHOTOBLEACHING;

ARTEMIS; DNA; DYNAMIN; FTSZ PROTEIN; GREEN FLUORESCENT PROTEIN; PROTEIN; RNA; UNCLASSIFIED DRUG;

ARABIDOPSIS; BLEACHING; CELL MEMBRANE; CHLOROPLAST; CONFERENCE PAPER; CYTOLOGY; DYNAMICS; FLUORESCENCE; GENOME; GOLGI COMPLEX; MICROSCOPY; MICROTUBULE; MORPHOLOGY; NONHUMAN; PLANT CELL; PLANT GENETICS; PLANT LEAF; PLASTID; PRIORITY JOURNAL;

ARABIDOPSIS;

EID: 2142805911     PISSN: 00222720     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0022-2720.2004.01317.x     Document Type: Conference Paper

References (128)

1. Addinall, S.G. & Holland, B. (2002) The tubulin ancestor, FtsZ, draughtsman, designer and driving force for bacterial cytokinesis. J. Mol. Biol. 318, 219-236.
2. Arimura, S., Hirai, A. & Tsutsumi, N. (2001) Numerous and highly developed tubular projections from plastids observed in Tobacco epidermal cells. Plant Sci. 160, 449-454.
3. Arimura, S. & Tsutsumi, N. (2002) A dynamin-like protein (ADL2b), rather than FtsZ, is involved in Arabidopsis mitochondrial division. Proc. Natl Acad. Sci. USA, 99, 5727-5731.
4. Bechtel, D.B. & Wilson, J.D. (2003) Amyloplast formation and starch granule development in hard red winter wheat. Cereal Chem. 80, 175-183.
5. Bi, E.F. & Lutkenhaus, J. (1991) FtsZ ring structure associated with division in Escherichia coli. Nature, 354, 161-164.
6. Birky, C.W. Jr (2001) The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models. Annu. Rev. Genet. 35, 125-148.
7. Blatt M.R., Wessells, N.K. & Briggs, W.R. (1980) Actin and cortical fiber reticulation in the siphonaceous alga Vaucheria sessilis. Planta, 147, 363-375.
8. Bourett, T.M., Czymmek, K.J. & Howard, R.J. (1999) Ultrastructure of chloroplast protuberances in rice leaves preserved by high-pressure freezing. Planta, 208, 472-479.
9. Britz, S.J. (1979) Chloroplast and nuclear migration. Encyclopedia of Plant Physiology, New Series, Vol. 7 (ed. by W. Haupt and M. E. Feinleib), pp. 170-205. Springer-Verlag, Berlin.
10. Buttrose, M.S. (1960) Submicroscopic development and structure of starch granules in cereal endosperms. J. Ultrastruct. Mol. Struct. Res. 4, 231-257.
11. Cai, G., Del Casino, C. & Cresti, M. (2000) Cytoskeletal basis of organelle trafficking in the angiosperm pollen tube. Ann. Bot.-London, 85, 69-77.
12. Chaly, N. & Possingham, J.V. (1981) Structure of constricted proplastids in meristematic plant tissues. Biol. Cell, 41, 203-210.
13. Chaly, N., Possingham, J. V. & Thomson, W.W. (1980) Chloroplast division in spinach leaves examined by scanning electron-microscopy and freeze-etching. J. Cell Sci. 46, 87-96.
14. Charon, J., Launay, J. & Carde, J.P. (1987) Spatial organization and volume density of leukoplastids in pine secretory cells. Protoplasma, 138, 45-53.
15. Clark, E., Schnabelrauch, L., Hanson, M.R. & Sink, K.C. (1986) Differential fate of plastid and mitochondrial genomes in petunia somatic hybrids. Theor. Appl. Genet. 72, 748-755.
16. Colletti, K.S., Tattersall, E.A., Pyke, K.A., Froelich, J.E., Stokes, K.D. & Osteryoung. K.W. (2000) A homologue of the bacterial cell division site-determining factor MinD mediates placement of the chloroplast division apparatus. Curr. Biol. 10, 507-516.
17. Collings, D.A., Zsuppan, G., Allen, N.S. & Blancaflor, E.B. (2001) Demonstration of prominent actin filaments in the root columella. Planta, 212, 392-403.
18. Crotty, W.J. & Ledbetter, M.C. (1973) Membrane continuities involving chloroplasts and other organelles in plant cells. Science, 182, 839-841.
19. Danino, D. & Hinshaw, J.E. (2001) Dynamin family of mechanoenzymes. Curr. Opin. Cell Biol. 13, 454-460.
20. Dinkins, R., Reddy, M.S., Leng, M. & Collins, G.B. (2001) Overexpression of the Arabidopsis thaliana MinD1 gene alters chloroplast size and number in transgenic tobacco plants. Planta, 214, 180-188.
21. Egelman, E.H. (2003) Actin's prokaryotic homologs. Curr. Opin. Struct Biol. 13, 244-248.
22. van den Ent, F., Amos, L.A. & Löwe, J. (2001) Prokaryotic origin of the actin cytoskeleton. Nature, 413, 39-44.
23. van den Ent, F., Meller-Jensen, J., Amos, L.A., Gerdes, K. & Löwe, J. (2002) F-actin-like filaments formed by plasmid segregation protein ParM. EMBO J. 21, 6935-6943.
24. Erickson, H.P., Taylor, D.W., Taylor, K.A. & Bramhill, D. (1996) Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers. Proc. Natl Acad. Sci. USA. 93, 519-523.
25. Esau, K. (1944) Anatomical and cytological studies on beet mosaic. J. Agr. Res. 69, 95-117.
26. Faguy, D.M. & Doolittle, W.F. (1998) Cytoskeletal proteins: the evolution of cell division. Curr. Biol. 8, R338-R341.
27. Fester, T., Strack, D. & Hause, B. (2001) Reorganization of tobacco root plastids during arbuscule development. Planta. 213, 864-868.
28. Freeman, T.P. & Duysen, M.E. (1975) Effect of imposed water stress on development and ultrastructure of wheat chloroplasts. Protoplasma. 83, 131-145.
29. Fulgosi, H., Gerdes, L., Westphal, S., Glockmann, C. & Soll, J. (2002) Cell and chloroplast division requires ARTEMIS. Proc. Natl Acad. Sci. USA. 99, 11501-11506.
30. Gao, H.B., Kadirjan-Kalbach, D., Froehlich, J.E. & Osteryoung, K.W. (2003) ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery. Proc. Natl Acad. Sci. USA. 100, 4328-4333.
31. Gardner, I.C., Abbas, H. & Scott, A. (1989) The occurrence of ameboid plastids in the actinorhizal root-nodules of Alnus glutinosa (L.) Gaertn, Plant Cell Environ. 12, 205-211.
32. Gillham, N.W. (1994) Organelle Genes and Genomes. Oxford University Press, New York.
33. Gray, J.C., Hibberd, J.M., Linley, P.J. & Uijtewaal, B. (1999) GFP movement between chloroplasts. Nat. Biotechnol. 17, 1146.
34. Gray, J.C., Sullivan, J.A., Hibberd, J.M. & Hansen, M.R. (2001) Stromules: mobile protrusions and interconnections between plastids. Plant Biol. 3, 223-233.
35. Gunning, B.E.S. (2003) Plant Cell Biology on CD. Details available at http://www.plantcellbiologycd.com
36. Hanson, M.R., O'Connell, M.A. & Vidair, C. (1987) Regeneration of calli and plants following protoplast fusion in Lycopersicon. Iowa State J. Res. 61, 445-458.
37. Haupt, W. & Scheuerlein, R. (1990) Chloroplast movement. Plant Cell Environ. 13, 595-614.
38. He, S.Y. & Jin, Q.L. (2003) The Hrp pilus: learning from flagella. Curr. Opin. Microbiol. 6, 15-19.
39. Hejnowicz, Z., Rusin, A. & Rusin, T. (2000) Tensile tissue stress affects the orientation of cortical microtubules in the epidermis of sunflower hypocotyl. J. Plant Growth Reg. 19, 31-44.
40. Hibberd, J.M., Linley, P.J., Khan, M.S. & Gray, J.C. (1998) Transient expression of green fluorescent protein in various plastid types following microprojectile bombardment. Plant J. 16, 627-632.
41. Huang, C.X. & van Steveninck, R.F.M. (1990) Salinity induced structural changes in meristematic cells of barley roots. New Phytol. 115, 17-22.
42. Itoh, R., Fujiwara, M., Nagata, N. & Yoshida, S. (2001) A chloroplast protein homologous to the eubacterial topological specificity factor MinE plays a role in chloroplast division. Plant Physiol. 127, 1644-1655.
43. Jasik, J. & Hudak, J. (1987) Plastid polymorphism in grapevine (Vitis labrusca X, V-Riparia) tissue-culture. Photosynthetica. 21, 179-181.
44. Jeong, W.J., Jeong, S.K., Min, S.R., Yoo, O.J. & Liu, J.R. (2002) Growth retardation of plants transformed by overexpression of NtFtsZ1-2 in tobacco. J. Plant Biol. 45, 107-111.
45. Jin, J.B., Kim, Y.A., Kim, S.J., Lee, S.H., Kim, D.H., Cheong, G.W. & Hwang, I. (2001) A new dynamin-like protein, ADL6, is involved in trafficking from the trans-Golgi network to the central vacuole in Arabidopsis. Plant Cell. 13, 1511-1525.
46. Kadota, A. & Wada, M. (1992a) 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.
47. Kadota, A. & Wada, M. (1992b) Photoorientation of chloroplasts in protonemal cells of the fern Adiantum as analyzed by use of video-tracking system. Bot. Mag. Tokyo. 105, 265-279.
48. Kamiya, N. & Kuroda, K. (1956) Velocity distribution of the cytoplasmic streaming in Nitella cells. Bot. Mag. 69, 544-554.
49. Kanamaru, K., Fujiwara, M., Kim, M., Nagashima, A., Nakazato, E., Tanaka, K. & Takahashi, H. (2000) Chloroplast targeting, distribution and transcriptional fluctuation of AtMinD1, a Eubacteria-type factor critical for chloroplast division. Plant Cell Physiol. 41, 1119-1128.
50. Kandasamy, M.K. & Meagher, R.B. (1999) Actin-organelle interaction: association with chloroplast in Arabidopsis leaf mesophyll cells. Cell Motil. Cytoskeleton. 44, 110-118.
51. Kang, B.H., Busse, J.S., Dickey, C., Rancour, D.M. & Bednarek, S.Y. (2001) The Arabidopsis cell plate-associated dynamin-like protein, ADL1Ap, is required for multiple stages of plant growth and development. Plant Physiol. 126, 47-68.
52. Kiessling, J., Kruse, S., Rensing, S.A., Harter, K., Decker, E.L. & Reski, R. (2000) Visualization of a cytoskeleton-like FtsZ network in chloroplasts. J. Cell Biol. 151, 945-950.
53. Kim, Y.W., Park, D.S., Park, S.C., Kim, S.H., Cheong, G.W. & Hwang, I. (2001) Arabidopsis dynamin-like 2 that binds specifically to phosphatidylinositol 4-phosphate assembles into a high-molecular weight complex in vivo and in vitro. Plant Physiol. 127, 1243-1255.
54. Kirk, J.T.O. & Tilney-Bassett, R.A.E. (1978) The Plastids. Elsevier/North-Holland Biomedical Press, New York.
55. Klonis, N., Rug, M., Harper, I., Wickham, M., Cowman, A. & Tilley, L. (2002) Fluorescence photobleaching analysis for the study of cellular dynamics. Eur. Biophys. J. 31, 36-51.
56. Knoblauch, M., Hibberd, J.M., Gray, J.C. & van Bel, A.J. (1999) A galinstan expansion femtosyringe for microinjection of eukaryotic organelles and prokaryotes. Nat. Biotechnol. 17, 906-909.
57. Knudson, L. (1940) Permanent changes of chloroplasts induced by X rays in the gametophyte of Polypodium aureum. Bot. Gaz. 101, 721-758.
58. Kobayashi, T., Takahara, M., Miyagishima, S.Y., Kuroiwa, H., Sasaki, N., Ohta, N., Matsuzaki, M. & Kuroiwa, T. (2002) Detection and localization of a chloroplast-encoded HU-like protein that organizes chloroplast nucleoids. Plant Cell. 14, 1579-1589.
59. Köhler, R.H., Cao, J., Zipfel, W.R., Webb, W.W. & Hanson, M.R. (1997) Exchange of protein molecules through connections between higher plant plastids. Science, 276, 2039-2042.
60. Köhler, R.H. & Hanson, M.R. (2000) Plastid tubules of higher plants are tissue-specific and developmentally regulated. J. Cell Sci. 113, 81-89.
61. Kuroiwa, T. (1991) The replication, differentiation, and inheritance of plastids with emphasis on the concept of organelle nuclei. Int. Rev. Cytol. 128, 1-62.
62. Kuroiwa, T., Kuroiwa, H., Sakai, A., Takahashi, H., Toda, K. & Itoh, R. (1998) The division apparatus of plastids and mitochondria. Int. Rev. Cytol. 181, 1-41.
63. Kuroiwa, T., Suzuki, T., Ogawa, K. & Kawano, S. (1981) The chloroplast nucleus - distribution, number, size, and shape, and a model for the multiplication of the chloroplast genome during chloroplast development. Plant Cell Physiol. 22, 381-396.
64. Kwok, E.Y. & Hanson, M.R. (2003) Microfilaments and microtubules control the morphology and movement of non-green plastids and stromules in Nicotiana tabacum. Plant J. 35, 16-26.
65. Laetsch, W.M. & Prince, I. (1969) Development of the dimorphic chloroplasts of sugar cane. Am. J. Bot. 56, 77-87.
66. Langeveld, S.M.J., van Wijk, R., Stuurman, N., Kijne, J.W. & de Pater, S. (2000) B-type granule containing protrusions and interconnections between amyloplasts in developing wheat endosperm revealed by transmission electron microscopy and GFP expression. J. Exp. Bot. 51, 1357-1361.
67. Lauber, M.H., Waizenegger, I., Steinmann, T., Schwarz, H., Mayer, U., Hwang, I., Lukowitz, W. & Jèurgens, G. (1997) The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J. Cell Biol. 139, 1485-1493.
68. Lu, C., Reedy, M. & Erickson, H.P. (2000) Straight and curved conformations of FtsZ are regulated by GTP hydrolysis. J. Bacteriol. 182, 164-170.
69. Lutkenhaus, J.F., Wolf-Watz, H. & Donachie, W.D. (1980) Organization of genes in the ftsA-envA region of the Escherichia coli genetic map and identification of a new fts locus (ftsZ). J. Bacteriol. 142, 615-620.
70. Lütz, C. & Moser, W. (1977) Beiträge zur Cytologie hochalpiner Pflanzen I. Untersuchungen zur Ultrastruktur von Ranunculus glacialis L. Flora. 166, 21-34.
71. Maple, J., Chua, N.H. & Moller, S.G. (2002) The topological specificity factor AtMinE1 is essential for correct plastid division site placement in Arabidopsis. Plant J. 31, 269-277.
72. McAndrew, R.S., Froehlich, J.E., Vitha, S., Stokes, K.D. & Osteryoung, K.W. (2001) Colocalization of plastid division proteins in the chloroplast stromal compartment establishes a new functional relationship between FtsZ1 and FtsZ2 in higher plants. Plant Physiol. 127, 1656-1666.
73. Medgyesy, P., Fejes, E. & Maliga, P. (1985) Interspecific chloroplast recombination in a Nicotiana somatic hybrid. Proc. Natl Acad. Sci. USA, 82, 6960-6964.
74. Menzel, D. (1994) An interconnected plastidom in Acetabularia - implications for the mechanism of chloroplast motility. Protoplasma, 179, 166-171.
75. Miyagishima, S.Y. Nishida, K., Mori, T., Matsuzaki, M., Higashiyama, T., Kuroiwa, H. & Kuroiwa, T. (2003) A plant-specific dynamin-related protein forms a ring at the chloroplast division site. Plant Cell. 15, 655-665.
76. Miyagishima, S.Y., Takahara, R. & Kuroiwa, T. (2001) Novel filaments 5 nm in diameter constitute the cytosolic ring of the plastid division apparatus. Plant Cell. 13, 707-721.
77. Mizukami, M. & Wada, S. (1981) Action spectrum for light-induced chloroplast accumulation in a marine coenocytic green-alga, Bryopsls plumosa. Plant Cell Physiol. 22, 1245-1255.
78. Nebenführ, A., Gallagher, L.A., Dunahay, T.G., Frohlick, J.A., Mazurkiewicz, A.M., Meehl, J.B. & Staehelin, L.A. (1999) Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol. 121, 1127-1141.
79. Newcomb, E.H. (1967) Fine structure of protein-storing plastids in bean root tips. J. Cell Biol. 33, 143-163.
80. Nothnagel, E.A. & Webb, W.W. (1982) Hydrodynamic models of viscous coupling between motile myosin and endoplasm in characean algae. J. Cell Biol. 94, 444-454.
81. O'Brien, J.A.J. (1951) Plastid development in the scutellum of Triticum aestivum and Secale cereale. Am. J. Bot. 38, 684-696.
82. Osteryoung, K.W. & McAndrew, R.S. (2001) The plastid division machine. Annu. Rev. Plant Phys. 52, 315-333.
83. Osteryoung, K.W., Stokes, K.D., Rutherford, S.M., Percival, A.L. & Lee, W.Y. (1998) Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial ftsZ. Plant Cell, 10, 1991-2004.
84. Osteryoung, K.W. & Vierling, E. (1995) Conserved cell and organelle division. Nature, 376, 473-474.
85. Paleviz, B.A. & Hepler, P.K. (1975) Identification of actin in situ at the ectoplasm-endoplasm Interface of Nitella. Microfilament-chloroplast association. J. Cell Biol. 65, 29-38.
86. Parker, M.L. (1985) The relationship between A-type and B-type starch granules in the developing endosperm of wheat. J. Cereal Sci. 3, 271-278.
87. Possingham, J.V., Mercer, F.V. & Vesk, M. (1964) Fine structure of leaf cells of manganese-deficient spinach. J. Ultrastruct. Mol. Struct. Res. 11, 68-83.
88. Pyke, K.A. & Howells, C.A. (2002) Plastid and stromule morphogenesis in tomato. Ann. Bot.-London, 90, 559-566.
89. Pyke, K.A. & Leech, R.M. (1992) Chloroplast division and expansion is radically altered by nuclear mutations in Arabidopsis thaliana. Plant Physiol. 99, 1005-1008.
90. Pyke, K.A. & Leech, R.M. (1994) A genetic analysis of chloroplast division and expansion in Arabidopsis thaliana. Plant Physiol. 104, 201-207.
91. Pyke, K.A., Rutherford, S.M., Robertson, E.J. & Leech, R.M. (1994) arc6, a fertile Arabidopsis mutant with only two mesophyll cell chloroplasts. Plant Physiol. 106, 1169-1177.
92. Reddy, M.S., Dinkins, R. & Collins, G.B. (2002) Overexpression of the Arabidopsis thaliana MinE1 bacterial division inhibitor homologue gene alters chloroplast size and morphology in transgenic Arabidopsis and tobacco plants. Planta, 215, 167-176.
93. Robertson, E.J., Pyke, K.A. & Leech, R.M. (1995) arc6, an extreme chloroplast division mutant of Arabidopsis also alters proplastid proliferation and morphology in shoot and root apices. J. Cell Sci. 108, 2937-2944.
94. Robertson, E.J., Rutherford, S.M. & Leech, R.M. (1996) Characterization of chloroplast division using the Arabidopsis mutant arc5. Plant Physiol. 112, 149-159.
95. Sakoda, M., Hasegawa, K. & Ishizuka, K. (1992) Mode of action of natural growth inhibitors in radish hypocotyl elongation - influence of raphanusanin on auxin-mediated microtubule orientation. Physiol. Plantarum, 84, 509-513.
96. Sarafls, V. (1998) Chloroplasts: a structural approach. J. Plant Physiol. 152, 248-264.
97. Sato, Y., Wada, M. & 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.
98. Senn, G. (1908) Die Gestalts- und Lageverānderung der Pflanzen-Chromatophoren. Engelmann, Leipzig.
99. Serlin, B.S. & Ferrell, S. (1989) The involvement of microtubules in chloroplast rotation in the alga Mougeotia. Plant Sci. 60, 1-8.
100. Shalla, T.A. (1964) Assembly and aggregation of tobacco mosaic virus in tomato leaflets. J. Cell Biol. 21, 253-264.
101. Shiina, T., Hayashi, K., Ishii, N., Morikawa, K. & Toyoshima, Y. (2000) Chloroplast tubules visualized in transplastomic plants expressing green fluorescent protein. Plant Cell Physiol. 41, 367-371.
102. Shimmen, T. & Tazawa, M. (1982) Reconstitution of cytoplasmic streaming in characeae. Protoplasma, 113, 127-131.
103. Shimmen, T. & Yokota, E. (1994) Physiological and biochemical aspects of cytoplasmic streaming. Int. Rev. Cytol. 155, 97-139.
104. Spencer, D. & Unt, H. (1965) Biochemical and structural correlations in isolated spinach chloroplasts under isotonic and hypotonic conditions. Aust. J. Biol. Sci. 18, 197-210.
105. Steffen, K. (1964) Chromoplastenstudlen. 1. Der Amobolde Chromoplastentyp. Planta, 60, 506-522.
106. Stokes, K.D., McAndrew, R.S., Flgueroa, R., Vitha, S. & Osteryoung, K.W. (2000) Chloroplast division and morphology are differentially affected by overexpression of FtsZ1 and FtsZ2 genes in Arabidopsis. Plant Physiol. 124, 1668-1677.
107. Strepp, R., Scholz, S., Kruse, S., Speth, V. & Reski, R. (1998) Plant nuclear gene knockout reveals a role in plastid division for the homolog of the bacterial cell division protein FtsZ, an ancestral tubulin. Proc. Natl Acad. Sci. USA, 95, 4368-4373.
108. Svab, Z. & Maliga, P. (1993) High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene. Proc. Natl Acad. Sci. USA, 90, 913-917.
109. Thomson, W.W. & Whatley, J.M. (1980) Development of non-green plastids. Annu. Rev. Plant Phys. 31, 375-394.
110. Tirlapur, U.K., Dahse, I., Reiss, B., Meurer, J. & Oelmuller, R. (1999) Characterization of the activity of a plastid-targeted green fluorescent protein in Arabidopsis. Eur. J. Cell Biol. 78, 233-240.
111. Tlalka, M. & Gabrys, H. (1993) Influence of calcium on blue-light-induced chloroplast movement in Lemna trisulca L. Planta, 189, 491-498.
112. Ueda, K., Matsuyama, T. & Hashimoto, T. (1999) Visualization of microtubles in living cells of transgenic Arabidopsis thaliana. Protoplasma, 206, 201-206.
113. Vesk, M., Mercer, F.V. & Possingham, J.V. (1965) Observations on the origin of chloroplasts and mitochondria in the leaf cells of higher plants. Aust. J. Bot. 13, 161-169.
114. Vitha, S., Froehlich, J.E., Koksharova, O., Pyke, K.A., van Erp, H. & Osteryoung, K.W. (2003) ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell, 15, 1918-1933.
115. Vitha, S., McAndrew, R.S. & Osteryoung, K.W. (2001) FtsZ ring formation at the chloroplast division site in plants. J. Cell Biol. 153, 111-120.
116. Wada, M., Kagawa, T. & Sato, Y. (2003) Chloroplast movement. Ann. Rev. Plant Biol. 54, 455-468.
117. Wagner, G., Haupt, W. & Laux, A. (1972) Reversible inhibition of chloroplast movement by Cytochalasin B in the green-alga Mougeotia. Science, 176, 808-809.
118. Weier, T.E. & Thomson, W.W. (1962) Membranes of mesophyll cells of Nicotiana rustica and Phaseolus vulgaris with particular reference to the chloroplast. Am. J. Bot. 49, 807-820.
119. Whatley, J.M. (1974) Chloroplast development in primary leaves of Phaseolus vulgaris. New Phytol. 73, 1097-1110.
120. Whatley, J.M. (1977) Variations in the basic pathway of chloroplast development. New Phytol. 78, 407-420.
121. Whatley, J.M. (1983a) Plastids in the roots of Phaseolus vulgaris. New Phytol. 94, 381-391.
122. Whatley, J.M. (1983b) The ultrastructure of plastids in roots. Int. Rev. Cytol. 85, 175-220.
123. Whatley, J.M., Mclean, B. & Juniper, B.E. (1991) Continuity of chloroplast and endoplasmic-reticulum membranes in Phaseolus vulgaris. New Phytol. 117, 209-217.
124. Whatley, J.M. & Whatley, F.R. (1987) When is a chromoplast. New Phytol. 106, 667-678.
125. Wildman, S.G. (1967) The organization of grana-containing chloroplasts in relation to location of some enzymatic systems concerned with photosynthesis, protein synthesis, and ribonucleic acid synthesis. Biochemistry of Chloroplasts, Vol. II (ed. by T. W. Goodwin), pp. 295-319. Academic Press, New York.
126. Wildman, S.G., Hongladarom, T. & Honda, S.I. (1962) Chloroplasts and mitochondria in living plant cells: cinephotomicrographic studies. Science, 138, 434-436.
127. Williamson, R.E. (1993) Organelle movements. Annu. Rev. Plant Phys. 44, 181-202.
128. Yan, X.X. (1995) NaCl-induced amoeboid plastids and mitochondria in meristematic cells of barley roots. Biol. Plant. 37, 363-369.