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A Survey of Plastid Crystals and Microtubules in Flowering Plants  

Kim, In-Sun (Biology Department, College of Natural Sciences, Keimyung University)
Publication Information
Applied Microscopy / v.39, no.2, 2009 , pp. 73-80 More about this Journal
Abstract
The plastid inclusion has long been known to exist in leaves of numerous plant species, especially in those of flowering plants. Among the inclusions, crystalline bodies are the most frequently distinguished structures of the foliar plastids, however, microtubules and phytoferritins are also reported occasionally. The crystalline inclusions vary in shape, and are located either in the stroma or within intrathylakoidal spaces, whereas microtubules and phytoferritins are more uniform in shape and are formed in the stroma. In crystalline structures, the composing elements exhibit a lattice pattern and/or paralleled tubules that are either bounded by membranes or exist without membrane enclosing. Other types of inclusions have not been shown to be enclosed by any membranous structures. According to the current survey, the plastid inclusion, with the exception of phytoferritins, has been shown to exhibit a crystalline or tubular pattern, and has been reported in more than 56 species of various families. Their occurrence is not restricted to any photosynthetic pathway, but is found to be randomly distributed among C-3, C-4 and CAM species, without phylogenetic relationships. The progress in plastid inclusion research reveals more information about the function and complexity, but the need for characterizing the 3-D structure of the crystalline inclusions also has been acknowledged in previous studies. A 3-D characterization would utilize tilting and tomography of serial sections with appropriate image processing that would provide valuable information on the sub-structures of the crystalline inclusions. In fact, recent studies performed on 3-D reconstruction of the plastid inclusions revealed important information about their comprising elements. In this article, the crystals and microtubules that have been reported in various types of plastids have been reviewed, with special consideration given to their possible sub-cellular function within the plastids.
Keywords
Crystals; Flowering plants; Microtubules; Plastid inclusions;
Citations & Related Records
Times Cited By KSCI : 2  (Citation Analysis)
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1 Rickson FR: The ultrastructure of Acasia cornigera L. Beltian body tissue. Amer J Bot 62 : 913-922, 1975   DOI   ScienceOn
2 Rivera ER, Arnott HJ: Tubular structure in the plastids of Echinomastus intertextus Brit. & Rose. New Phytol 90 : 551-561, 1982   DOI   ScienceOn
3 Ryberg H, Ryberg M, Sundqvist C: Plastid ultrastructure and development. In: Sundqvist, C Ryberg M. eds, Pigment-Protein Complexes in Plastids: synthesis and Assembly, pp. 25-62, Academic Press, San Diego, 1993
4 Santos I, Salema R: Chloroplast microtubules in some CAM-plants. Bol Soc Brot Ser (2) 53 : 1115-1122, 1981
5 Santos I, Salema R: Stereological study of the variation of the chloroplast tubules and volume in the CAM plant Sedum telephium. Z Pflanzenphysiol Bd 113 : 29-37, 1983   DOI
6 Shojima S, Nishizawa NK, Mori S: Do intrathylakoidal inclusions really contain RUBPCase? Protoplasma 140 : 187-189, 1987   DOI
7 Sitte P: Plastid metamorphosis and chromoplasts in Chrysosplenium. Z Pflanzenphysiol 73 : 243-265, 1974
8 Sprey B: Membranassoziierte Tubuli Wahrend der Chloroplastengenese von Hordeum vulgare L. Protoplasma 84 : 197-203, 1975   DOI
9 Thompson A, Vogel J, Lee RE: Carbon dioxide uptake in relation to a plastid inclusion body in the succulent Kalancho pinnata Persoon. J Exp Bot 28 : 1037-1041, 1977   DOI
10 Thomson WW, Journett RD: Observations on bodies in subsidiary cells of Opuntia sp. J Ultrastruct Res 31 : 439-443, 1970   DOI   ScienceOn
11 Artus NN, Ryberg M, Sundqvist C: Plastid microtubule structures in wheat are insensitive to microtubule inhibitors. Physiol Plant 79 : 641-648, 1990   DOI   ScienceOn
12 Casadoro G, Rascio N, Pagiusco M, Ravagnan N: Flowers of Orontium aquaticum L.: membrane rearrangement in chloroplastchromoplast interconversions. J Ultrastruct Res 81 : 202-208, 1982   DOI   ScienceOn
13 Emter O, Falk H, Sitte P: Specific carotenoids and proteins as prerequisites for chromoplast tubule formation. Protoplasma 157 : 128-135, 1990   DOI
14 Gailhofer M, Kferbck T, Thaler I: Cytochemische Undersuchungen an Einschlssen in Plastiden der Bltter von Taraxacum officinale. Phyton 30 : 173-185, 1990
15 Vanderzee D, Kennedy RA: Plastid development in seedlings of Echinochloa crus-galli var. oryzicola under anoxic germination conditions. Planta 155 : 1-7, 1982   DOI   ScienceOn
16 Varkey PJ, Nadakavukaren MJ: Influence of leaf differentiation on the developmental pathway of Coleus chloroplasts. New Phytol 92 : 273-278, 1982   DOI   ScienceOn
17 Wrischer M: Kristalloide im Plastidenstroma I. Elektronenmikroskopisch-cytochemische untersuchungen. Planta 75 : 309-318, 1967   DOI   ScienceOn
18 Hohl HR: Plastids and tumorigenesis. Am J Bot 48 : 528, 1961
19 Gailhofer M, Thaler I: Eiweibkristalle in den Plastiden der Keimpflanzen einiger Palmen. Phyton 15 : 251-258, 1974
20 Hoefert LL, Esau K: Plastid inclusion in epidermal cells of Beta. Am J Bot 62 : 36-40, 1975   DOI   ScienceOn
21 Kim IS: Changes in the plastid ultrastructure during Sedum rotundifolium leaf development. J Plant Biol 49 : 376-383, 2006   과학기술학회마을   DOI   ScienceOn
22 Knoth R: Protein crystalloids in ribosome-deficient plastids of Aeonium domesticum cv. variegatum (Crassulaceae). Planta 156 : 528-535, 1982   DOI   ScienceOn
23 Larsson C, Collin C, Albertsson P: The fine structure of chloroplast stroma crystal. J Ultrastruct Res 45 : 50-58, 1973   DOI   ScienceOn
24 Lee KB: Ultrastructure of crystalline inclusion in the thylakoids of dodder (Cuscuta japonica) plastids. J Plant Biol 50 : 325-330, 2007b   DOI   ScienceOn
25 Lyshede OB: Electron microscopy of the filiform seedling axis of Cuscuta pedicellata. Bot Gaz 150 : 230-238, 1989   DOI   ScienceOn
26 Newcomb EH: Fine structure of protein-storing plastids in bean root tips. J Cell Biol 33 : 143-163, 1967   DOI
27 Price WC, Martinez AP, Warmke HE: Crystalline inclusions in chloroplasts of the coconut palm. J Ultrastruct Res 14 : 618-621, 1966   DOI   ScienceOn
28 Lee KB: Structure and development of the upper haustorium in the parasitic flowering plant Cuscuta japonica (Convolvulaceae). Amer J Bot 94 : 737-745, 2007   DOI   ScienceOn
29 Suzuki S: Crystalline inclusion in epidermal and vascular plastids of the mature Amaranthus leaf. J Electron Microsc 27 : 141-143, 1978
30 Dustin P: Microtubules. Springer-Verlag, Berlin, pp. 94-126, 1984
31 Esau K: Crystalline inclusion in thylakoids of spinach chloroplasts. J Utrastruct Res 53 : 235-243, 1975   DOI   ScienceOn
32 Nisius A: The stromacentre in Avena plastids: An aggregation of $\beta$-glucosidase responsible for the activation of oat-leaf saponins. Planta 173 : 474-481, 1988   DOI   ScienceOn
33 Sherman TD, Pettigrew WT, Vaughn KC: Structural and immunological characterization of the Cuscuta pentagona L. chloroplast. Plant Cell Physiol 40 : 592-603, 1999   DOI
34 Gailhofer M, Thaler I: 'Stromazentrum' in Leukoplasten der Epidermis von Asphodelus microcarpus. Phyton 19 : 97-102, 1978
35 Lee RE, Thompson A: The stromacentre of plastids of Kalancho Pinnata Persoon. J Ultrastruct Res 42 : 451-456, 1973   DOI   ScienceOn
36 Pettifrew, WT, Vaughn KC: Physiological, structural, and immunological characterization of leaf and chloroplast development in cotton. Protoplasma 202 : 23-37, 1998   DOI   ScienceOn
37 Brinkley W: Microtubules: a brief historical perspective. J Struct Biol 118 : 84-86, 1997   DOI   ScienceOn
38 Wrischer M: Protein crystalloids in the stroma of bean plastids. Protoplasma 77 : 141-150, 1973   DOI
39 Willison JHM, Davey MR: Fraction 1 protein crystals in chloroplasts of isolated tobacco leaf protoplasts: a thin-section and freeze-etch morphological study. J Ultrastruct Res 55 : 303-311, 1976   DOI   ScienceOn
40 Lawrence ME, Possingham JV: Observations of microtubule structures within spinach plastids. Biol Cell 53 : 77-82, 1984
41 Laudi G, Medeghini Bonatti P, Fricano G: Ultrastructure of plastids of parasitic higher plants. V. Influence of light on Cuscuta plastids. Isr J Bot 23 : 145-150, 1974
42 Dey PM, Brownleader MD, Harborne JB: The plant cell and its molecular components, In: Dey PM, Harborne JB, ed, Plant Biochemistry, pp. 1-48, Academic Press, 1997
43 Dodge JD, Lawes GB: Plastid ultrastructure in some parasitic and semi-parasitic plants. Cytobilogie 9 : 1-9, 1974
44 Platt-Aloia KA, Thomson WW: Membrane bound inclusions in epidermal plastids of developing sesame leaves and cotyledons. New Pytol 83 : 793-799, 1979   DOI   ScienceOn
45 Vaughn KC, Coyle PC, Wilson KG: Modifications of plastid ultrastructure in an efficient yellow mutant of spinach. Photosynthetica 15 : 201-204, 1981
46 Nick P: Plant Microtubules: Potential for Biotechnology. Springer, Berlin, pp.1-50, 83-136, 2000
47 Kim IS, Pak JH, Seo SB, Song SD: Foliar ultrastructure of Korean Orostachys species. Korean J Electron Microscopy 25 : 457-463, 1995
48 Kuhn H: Chemismus, Struktur und Entstehung der Carotinkristllchen in der Nebenkrone von Narcissus poeticus L. var. 'La Riante'. J Ultrastruct Res 33 : 332-355, 1970   DOI   ScienceOn
49 Rascio N, Colombo PM, Vicca FD, Chitano P: Intrathylakoidal crystal appearance during the vital cycle of spinach chloroplasts. Protoplasma 126 : 153-157, 1985   DOI
50 Gunning BES, Steer MW: Plant Cell Biology: Structure and Function. Jones and Bartlett Publishers, Boston, pp. 1-60, 1996
51 Miller KR, Bloodgood RA, Staehelin LAL: Crystals within thylakoids: a structural analysis. J Ultrastruct Res 54 : 29-36, 1976   DOI   ScienceOn
52 Newcomb W: Plastid structure and development. In: Dennis DT, Turpin DH, Lefebvre DD, Layzell DB, eds, Plant Metabolism, pp. 255-259, Longman, Harlow, 1997
53 Sprey B: Intrathylakoid occurrence of ribulose 1,5-diphosphate carboxylase in spinach chloroplasts. Z Pflanzenphysiol 78 : 85-89, 1976   DOI
54 Galatis B, Apostolakos P: Microtubule organization and morphogenesis of stomata in caffeine-affected seedlings of Zea mays. Protoplasma 165 : 11-26, 1991   DOI
55 Oross JW, Possingham JV: Tubular structures in developing plastids of three dicotyledonous species. Can J Bot 69 : 136-139, 1991   DOI
56 Shumway LK, Weier TE, Stocking CR: Crystalline structures in Vicia faba chloroplasts. Planta 76 : 182-189, 1967   DOI   ScienceOn
57 Ames IH, Pivorun JP: A cytochemical investigation of a chloroplast inclusion. Amer J Bot 61 : 794-797, 1974   DOI   ScienceOn
58 McDonald MS: Photobiology of Higher Plants. John Wiley & Sons Ltd., San Fransisco, pp. 33-73, 149-198, 2003
59 Gailhofer M: Die Feinstruktur der Plastideneinschlsse von Ranunculus bulbosus. Phyton 23 : 197-210, 1983
60 Ljubesic N: Chromoplasts in the petals of Liriodendron tulipifera L. Z Pflanzenphysiol 91 : 49-52, 1979   DOI
61 Kim IS, Park SC, Han SS, Kim ES: Three-dimensional analysis of the mesophyll plastids using ultra high voltage electron micro-scopy. Korean J Electron Microscopy 36 : 217-226, 2006
62 Ames IH: The fine structure of genetic tumor cells. Amer J Bot 59 : 341-345, 1972   DOI   ScienceOn
63 Spurr AR, Harris WM: Ultrastructure of chloroplasts and chromoplasts in Capsicum annumI. Thylakoid membrane changes during fruit ripening. Amer J Bot 55 : 1210-1224, 1968   DOI   ScienceOn
64 Vaughn KC, Wilson KG: Improved visualization of plastid fine structure: plastid microtubules. Protoplasma 108 : 21-27, 1981   DOI
65 Williams E: Fine structure of vascular and epidermal plastids of the mature maize leaf. Protoplasma 79 : 395-400, 1974   DOI
66 Lee KB: Ultrastructure and development of seedling of the parasitic weed Cuscuta japonica. J Plant Biol 50 : 213-219, 2007a   DOI   ScienceOn
67 Brandao I, Salema R: Microtubules in chloroplasts of a higher plant (Sedum sp.). J Submicr Cytol 6 : 381-390, 1974
68 Diaz-Ruiz JR: A Highly ordered protein from Pelargonium: structure and cellular localization. J Utrastruct Res 53 : 227-234, 1975   DOI   ScienceOn
69 Kim IS: Chloroplast microtubules in young leaves of Sedum rotundifolium. J Plant Biol 40 : 115-119, 1997   DOI   ScienceOn
70 Kim IS, Pak JH, Seo SB, Song SD: Ultrastructure of leaves in C$_{4}$ Cyperus iria and C$_{3}$ Carex siderosticta. J Plant Biol 42 : 213-221, 1999   DOI   ScienceOn
71 Mikulska E, Damsz B, Zolnierowicz H: Structural and functional polymorphism of plastids in leaves of Clivia miniata Rgl. I. Ontogenesis of plastids in epidermis and guard cells. Acta Soc Bot Pol 50 : 381-389, 1981
72 Kim IS, Fisher DG: Structure aspects of the leaves of seven species of Portulaca growing in Hawaii. Can J Bot 68 : 1803-1811, 1990   DOI
73 Salema R, Brandao I: Development of microtubules in chloroplasts of two halophytes forced to follow Crassulacean acid metabolism. J Ultrastruct Res 62 : 132-136, 1978   DOI   ScienceOn
74 Vapaavuori EM, Korpilahti E, Nurmi AH: Photosynthetic rate in willow leaves during water stress and changes in the chloroplast ultrastructure with special reference to crystal inclusions. J Exp Bot 35 : 306-321, 1984   DOI
75 Finer JJ, Smith RH: Structure and development of plastids in epidermal cells of African violet (Saintpaulia ionantha Wendl.) in culture. Ann Bot 51 : 691-695, 1983   DOI