Etioplasts and Their Significance in Chloroplast Biogenesis

  • Katalin Solymosi
  • Henrik AronssonEmail author
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 36)


Etioplasts are considered as convenient but not completely adequate laboratory models of proplastid-to-chloroplast development. These plastids are formed in light-deprived tissues of angiosperm plants that would become chlorenchyma in the light. Etioplasts have a unique inner membrane consisting of highly regular, paracrystalline prolamellar bodies (PLBs) and of lamellar prothylakoids (PTs). First, we recall different situations where etioplasts or PLBs do appear and play an important role during normal leaf ontogenesis and chloroplast biogenesis under natural light conditions. These structures appear almost exclusively in young tissues with not completely differentiated chloroplasts and photosynthetic apparatus, and under conditions where light is either temporally and/or spatially limited during development. PLBs can be formed in young leaves during the dark phase of the light–dark cycles (LDC); or in young seedlings developing in the soil from seeds; in water plants or inside special structures, where a decreasing light gradient is naturally formed, e.g. buds, enveloping sheaths of outer leaves. Having discussed the relevance of etioplasts in chloroplast biogenesis, we then outline the structure, organization and assembly of etioplast inner membranes in etiolated seedlings. Furthermore, the different factors important for PLB formation, and in parallel, the mole­cular composition of the PLBs are reviewed in details. A special lipid composition, a high lipid per protein ratio, the presence of oligomers of NADPH:protochlorophyllide (Pchlide) oxidoreductase (LPOR) proteins binding Pchlide, NADPH and carotenoids may all be important for the stabilization and formation of the special cubic membrane of the PLBs. Therefore, the biosynthesis of pigments in etioplasts is also discussed. The last part focuses on the etioplast-to-chloroplast transition during greening of etiolated seedlings, and summarizes the ultrastructural, molecular and physiological changes observed during this process. Finally, the significance of PLBs in plant development and leaf ontogeny is outlined.


Carotenoid Biosynthesis Spectral Form Fluorescence Emission Maximum Chloroplast Biogenesis Chloroplast Differentiation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



5-aminolevulinic acid;

Chl(s) –


Chlide –


Coprogen III –

Coproporphyrinogen III;


Digalactosyl diacylglycerol;


Dark-operative NADPH: Pchl­ide oxidoreductase;

GG – Geranylgeraniol; GGPP –

Geranylgeraniol diphosphate;




Isopentenyl diphosphate;


Light–dark cycle;


Light-dependent NADPH: Pchlide oxidoreductase;

LPOR-A, -B, -C –

Isoforms of LPOR;


Monogalactosyl diacylglycerol;

Pchlide –





Prolamellar body;

Protogen IX –

Porphyrinogen III;


Photosystem I;


Photosystem II;

PT –


Urogen III –

Uroporphyrinogen III



The authors are grateful to Csilla Jónás for skilful technical assistance, Dr Beata Mysliwa-Kurdziel for providing original pictures (Fig. 3.6), Prof. Benoit Schoefs for helpful discussion, and the Swedish Research Council VR for financial support (H.A). The electron microscopic examinations and fluorescence spectroscopy (Fig. 3.4) were done as in Solymosi et al. (2006a). Ultrathin sections were examined using Hitachi 7100 and JEOL JEM 1011 transmission electron microscopes. The project was supported by the European Union and co-financed by the European Social Fund (grant agreement no. TAMOP 4.2.1/B-09/1/KMR-2010-0003) (S.K.).


  1. Adamson HY, Hiller RG, Vesk M (1980) Chloroplast development and the synthesis of chlorophyll a and b and chlorophyll protein complexes I and II in the dark in Tradescantia albiflora (Kunth). Planta 150:269–274CrossRefGoogle Scholar
  2. Adamson H, Packer N, Gregory J (1985) Chloroplast development and the synthesis of chlorophyll and protochlorophyllide in Zostera transferred to darkness. Planta 165:469–476CrossRefGoogle Scholar
  3. Albrecht M, Sandmann G (1994) Light-stimulated carotenoid biosynthesis during transformation of maize etioplasts is regulated by increased activity of isopentenyl pyrophosphate isomerase. Plant Physiol 105:529–534PubMedGoogle Scholar
  4. Amirjani MR, Sundqvist C (2004) Regeneration of protochlorophyllide in green and greening leaves of plants with varying proportions of protochlorophyllide forms in darkness. Physiol Plant 121:377–390CrossRefGoogle Scholar
  5. Amirjani MR, Sundqvist K, Sundqvist C (2006) Protochlorophyllide and POR development in dark-grown plants with different proportions of short-wavelength and long-wavelength protochlorophyllide spectral forms. Physiol Plant 128:751–762CrossRefGoogle Scholar
  6. Apel K (1981) The protochlorophyllide holochrome of barley (Hordeum vulgare L.). Phytochrome-induced decrease of translatable mRNA coding for the NADPH:protochlorophyllide oxidoreductase. Eur J Biochem 120:89–93PubMedCrossRefGoogle Scholar
  7. Aronsson H, Sohrt K, Soll J (2000) NADPH:proto­chloro­phyllide oxidoreductase uses the general import pathway. Biol Chem 381:1263–1267PubMedCrossRefGoogle Scholar
  8. Aronsson H, Sundqvist C, Timko MP, Dahlin C (2001a) The importance of the C-terminal region and Cys residues for the membrane association of the NADPH: protochlorophyllide oxidoreductase in pea. FEBS Lett 502:11–15PubMedCrossRefGoogle Scholar
  9. Aronsson H, Sundqvist C, Timko MP, Dahlin C (2001b) Characterisation of the assembly pathway of the pea NADPH:protochlorophyllide (Pchlide) oxidoreductase (POR), with emphasis on the role of its substrate, Pchlide. Physiol Plant 111:239–244CrossRefGoogle Scholar
  10. Aronsson H, Sundqvist C, Dahlin C (2003a) POR hits the road: import and assembly of a plastid protein. Plant Mol Biol 51:1–7PubMedCrossRefGoogle Scholar
  11. Aronsson H, Sundqvist C, Dahlin C (2003b) POR – import and membrane association of a key element in chloroplast development. Physiol Plant 118:1–9PubMedCrossRefGoogle Scholar
  12. Aronsson H, Schüttler MA, Kelly AA, Sundqvist C, Dörmann P, Karim S, Jarvis J (2008) Monogalacto­syldiacylglycerol deficiency in Arabidopsis thaliana affects pigment composition in the prolamellar body and impairs thylakoid membrane energetization and photoprotection in leaves. Plant Physiol 148:580–592PubMedCrossRefGoogle Scholar
  13. Bahl J (1977) Chlorophyll, carotenoid and lipid content in Triticum sativum L. plastid envelopes, prolamellar bodies, stroma lamellae, and grana. Planta 136:21–24CrossRefGoogle Scholar
  14. Bahl J, Francke B, Monéger R (1976) Lipid composition of envelopes, prolamellar bodies and other plastid membranes in etiolated, green and greening wheat leaves. Planta 129:193–201CrossRefGoogle Scholar
  15. Barry P, Young AJ, Britton G (1991) Accumulation of pigments during the greening of etiolated seedlings of Hordeum vulgare L. J Exp Bot 42:229–234CrossRefGoogle Scholar
  16. Barthélemy X, Bouvier H, Radunz A, Docquier S, Schmid GH, Franck F (2000) Localization of NADPH-protochlorophyllide reductase in plastids of barley at different greening stages. Photosynth Res 64:63–76PubMedCrossRefGoogle Scholar
  17. Bennett J, Schwender JR, Shaw EK, Tempel N, Ledbetter M, Williams RS (1987) Failure of corn leaves to acclimate to low irradiance. Role of protochlorophyllide reductase in regulating levels of five chlorophyll-binding proteins. Biochim Biophys Acta 892:118–129CrossRefGoogle Scholar
  18. Benz J, Wolf C, Rüdiger W (1980) Chlorophyll biosynthesis: hydrogenation of geranylgeraniol. Plant Sci Lett 19:225–230CrossRefGoogle Scholar
  19. Bertrand M, Bereza B, Dujardin E (1988) Evidence for photoreduction of NADP + in a suspension of lysed plastids from etiolated bean leaves. Z Naturforsch 43e:443–448Google Scholar
  20. Biswal UC, Biswal B, Raval MK (2003) Chloroplast biogenesis. From proplastid to gerontoplast. Kluwer, DordrechtCrossRefGoogle Scholar
  21. Blomqvist LA, Ryberg M, Sundqvist C (2006) Proteomic analysis of the etioplast inner membranes of wheat (Triticum aestivum) by two-dimensional electrophoresis and mass spectrometry. Physiol Plant 128:368–381CrossRefGoogle Scholar
  22. Blomqvist LA, Ryberg M, Sundqvist C (2008) Proteomic analysis of highly purified prolamellar bodies reveals their significance in chloroplast development. Photosynth Res 96:37–50PubMedCrossRefGoogle Scholar
  23. Böddi B, Lindsten A, Ryberg M, Sundqvist C (1989) On the aggregational states of protochlorophyllide and its protein complexes in wheat etioplasts. Physiol Plant 76:135–143CrossRefGoogle Scholar
  24. Böddi B, Lindsten A, Ryberg M, Sundqvist C (1990) Phototransformation of aggregated forms of protochlorophyllide in isolated etioplast inner membranes. Photochem Photobiol 52:83–87CrossRefGoogle Scholar
  25. Böddi B, Ryberg M, Sundqvist C (1992) Identification of four universal protochlorophyllide forms in dark-grown leaves by analyses of the 77 K fluorescence emission spectra. J Photochem Photobiol B Biol 12:389–401CrossRefGoogle Scholar
  26. Boffey SA, Sellden G, Leech RM (1980) Influence of cell age on chlorophyll formation in light-grown and etiolated wheat seedlings. Plant Physiol 65:680–684PubMedCrossRefGoogle Scholar
  27. Boij P, Patel R, Garcia C, Jarvis P, Aronsson H (2009) In vivo studies on the roles of Tic55-related proteins in chloroplast protein import in Arabidopsis thaliana. Mol Plant 2:1397–1409PubMedCrossRefGoogle Scholar
  28. Bonneville J-M, Tichtinsky G (2010) Correction for Pollmann et al., A plant porphyria related to defects in plastid import of protochlorophyllide oxidoreductase A. Proc Natl Acad Sci USA 107:5693Google Scholar
  29. Bonzi LM, Bonatti PM, Marini C, Fornasiero RB, Paoletti C (1992) Ultrastructural studies on differentiating chloroplasts in the ‘forma fuscoviridis’ of Ceratozamia mexicana Brongn. New Phytol 120:427–434CrossRefGoogle Scholar
  30. Bouvier F, Keller Y, d’Harlingue A, Camara B (1998) Xanthophyll biosynthesis: molecular and functional charac­terization of carotenoid hydroxylases from pepper fruits (Capsicum annuum L). Biochim Biophys Acta 1391:320–328PubMedCrossRefGoogle Scholar
  31. Bradbeer JW, Gyldenholm AO, Ireland HMM, Smith JW, Rest J, Edge HJW (1974a) Plastid development in primary leaves of Phaseolus vulgaris VIII. The effect of the transfer of dark-grown plants to continuous illumination. New Phytol 73:271–279CrossRefGoogle Scholar
  32. Bradbeer JW, Ireland HMM, Smith JW, Rest J, Edge HJW (1974b) Plastid development in primary leaves of Phaseolus vulgaris VII. Development during growth in continuous darkness. New Phytol 73:263–270CrossRefGoogle Scholar
  33. Bräutigam A, Hoffmann-Benning S, Weber APM (2008) Comparative proteomics of chloroplast envelopes from C3 and C4 plants reveals specific adaptations of the plastid envelope to C4 photosynthesis and candidate proteins required for maintaining C4 metabolite fluxes. Plant Physiol 148:568–579PubMedCrossRefGoogle Scholar
  34. Canovas F, McLarney B, Silverthorne J (1993) Light-independent synthesis of LHC IIb polypeptides and assembly of the major pigmented complexes during the initial stages of Pinus palustris seedling development. Photosynth Res 38:89–97CrossRefGoogle Scholar
  35. Casadoro G, Rascio N (1979) Patterns of thylakoid system formation. J Ultrastruct Res 69:307–315PubMedCrossRefGoogle Scholar
  36. Cohen CE, Rebeiz CA (1978) Chloroplast biogenesis XXII. Contribution of short wavelength and long wavelength protochlorophyll species to the greening of higher plants. Plant Physiol 61:824–829PubMedCrossRefGoogle Scholar
  37. Covello PS, Webber AN, Danko JS, Markwell JP, Baker NR (1987) Phosphorylation of thylakoid proteins during chloroplast biogenesis in greening etiolated and light-grown wheat leaves. Photosynth Res 12:243–254CrossRefGoogle Scholar
  38. Cunningham FX, Pogson BJ, Sun Z, McDonald K, DellaPenna D, Gantt E (1996) Functional analysis of the beta and epsilon lycopene cyclase enzymes of Arabidopsis reveals a mechanism for control of cyclic carotenoid formation. Plant Cell 8:1613–1626PubMedGoogle Scholar
  39. Dahlin C, Aronsson H, Almkvist J, Sundqvist C (2000) Pchlide independent import of two NADPH:proto­chlorophyllide oxidoreductase proteins (PORA and PORB) from barley into isolated plastids. Physiol Plant 109:298–303CrossRefGoogle Scholar
  40. Davies TGE, Ougham HJ, Thomas H, Rogers LJ (1989) Leaf development in Lolium temulentum: plastid membrane polypeptides in relation to assembly of the photosynthetic apparatus and leaf growth. Physiol Plant 75:47–54CrossRefGoogle Scholar
  41. Dehesh K, Ryberg M (1985) The NADPH:protochloro­phyllide oxidoreductase is the major protein constituent of prolamellar bodies in wheat (Triticum aestivum L.). Planta 164:396–399CrossRefGoogle Scholar
  42. Dehesh K, Klaas M, Häuser I, Apel K (1986a) Light-induced changes in the distribution of the 36000-Mr polypeptide of NADPH-protochlorophyllide oxidoreductase within different cellular compartments of barley (Hordeum vulgare L.). I. Localization by immunoblotting in isolated plastids and total leaf extracts. Planta 169:162–171CrossRefGoogle Scholar
  43. Dehesh K, Cleve B, Ryberg M, Apel K (1986b) Light-induced changes in the distribution of the 36000-Mr polypeptide of NADPH-protochlorophyllide oxidoreductase within different cellular compartments of barley (Hordeum vulgare L.). II. The localization of the polypeptide as revealed by the method of by immunogold labelling in ultrathin sections of barley leaves. Planta 169:172–183CrossRefGoogle Scholar
  44. Denev ID, Yahubyan GT, Minkov IN, Sundqvist C (2005) Organization of protochlorophyllide oxidoreductase in prolamellar bodies isolated from etiolated carotenoid-deficient leaves as revealed by fluorescence probes. Biochim Biophys Acta 1716:97–103PubMedCrossRefGoogle Scholar
  45. Domanskii VP, Rüdiger W (2001) On the nature of the two pathways in chlorophyll formation from protochlorophyllide. Photosynth Res 68:131–139PubMedCrossRefGoogle Scholar
  46. Domanskii VP, Rassadina V, Gus-Mayer S, Wanner G, Schoch S, Rüdiger W (2003) Characterization of two phases of chlorophyll formation during greening of etiolated barley leaves. Planta 216:475–483PubMedGoogle Scholar
  47. Engdahl S, Aronsson H, Sundqvist C, Timko MP, Dahlin C (2001) Association of the NADPH:proto­chlorophyllide oxidoreductase (POR) with isolated etioplast inner membranes from wheat. Plant J 27:297–304PubMedCrossRefGoogle Scholar
  48. Forreiter C, Apel K (1993) Light-independent and light-dependent protochlorophyllide-reducing activities and two distinct NADPH-protochlorophyllide oxidoreductase polypeptides in mountain pine (Pinus mugo). Planta 190:536–545PubMedCrossRefGoogle Scholar
  49. Franck F (1993) Photosynthetic activities during early assembly of thylakoid membranes. In: Ryberg M, Sundqvist C (eds) Pigment protein complexes in plastids: synthesis and assembly. Academic Press, San Diego, pp 365–381Google Scholar
  50. Franck F, Inoue Y (1984) Light-driven reversible transformation of chlorophyllide P696,682 into chlorophyllide P688,678 in illuminated etiolated bean leaves. Photobioch Photobiop 8:85–96Google Scholar
  51. Franck F, Barthélemy X, Strzałka K (1993) Spectroscopic characterization of protochlorophyllide photoreduction in the greening leaf. Photosynthetica 29:185–194Google Scholar
  52. Franck F, Eullaffroy P, Popovic R (1997) Formation of long-wavelength chlorophyllide (Chlide695) is required for the assembly of photosystem II in etiolated barley leaves. Photosynth Res 51:107–118CrossRefGoogle Scholar
  53. Friedmann HC, Thauer RK, Gough SP, Kannangara CG (1987) Δ-aminolevulinic acid formation in the archaebacterium Methanobacterium thermoautotrophicum requires tRNA Glu. Carlsberg Res Commun 52:363–371CrossRefGoogle Scholar
  54. Fujita Y, Bauer CE (2003) The light-independent protochlorophyllide reductase: a nitrogenase-like enzyme catalyzing a key reaction for greening in the dark. In: Kadish KM, Smith KM, Guilard R (eds) Chlorophylls and bilins: Biosynthesis, synthesis, and degradation. Academic Press, New York, pp 109–156Google Scholar
  55. Guillot-Salomon T, Douce R, Signol M (1973) Rapport entre l’évolution ultrastructurale des plastes de feuilles de plantules étiolées de maïs soumises à l’action de la lumière et la synthèse de nouvelles molécules de phosphatidylglycérol. Plant Sci Lett 1:463–471CrossRefGoogle Scholar
  56. Gunning BES (1965) The greening process in plastids. 1. The structure of the prolamellar body. Protoplasma 60:111–130CrossRefGoogle Scholar
  57. Gunning BES (2001) Membrane geometry of “open” prolamellar bodies. Protoplasma 215:4–15PubMedCrossRefGoogle Scholar
  58. Gunning BES (2004) Plant cell biology on DVD. Accessed 15 Oct 2007
  59. Gunning BES, Steer MW (1996) Plant cell biology: structure and function. Jones and Bartlett, BostonGoogle Scholar
  60. He Z-H, Li J, Sundqvist C, Timko MP (1994) Leaf developmental age controls expression of genes encoding enzymes of chlorophyll and heme biosynthesis in pea (Pisum sativum). Plant Physiol 106:537–546PubMedGoogle Scholar
  61. Heinze A, Görlach J, Leuschner C, Hoppe P, Hagelstein P, Schulze-Siebert D, Schultz G (1990) Plastidic isoprenoid synthesis during chloroplast development. Change for metabolic autonomy to a division-of-labor stage. Plant Physiol 93:1121–1127CrossRefGoogle Scholar
  62. Henningsen KW, Boynton JE (1969) Macromolecular physiology of plastids VII. The effect of brief illumination on plastids of dark-grown barley leaves. J Cell Sci 5:757–793PubMedGoogle Scholar
  63. Henningsen KW, Boynton JE (1974) Macromolecular physiology of plastids IX. Development of plastid membranes during greening of dark-grown barley seedlings. J Cell Sci 15:31–55PubMedGoogle Scholar
  64. Henningsen KW, Boynton JE, von Wettstein D (1993) Mutants at xantha and albina loci in relation to chloroplast biogenesis in barley (Hordeum vulgare L.). Biol Skr Copenhagen Munksgaard 42:1–349Google Scholar
  65. Hirschberg J (2001) Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol 4:210–218PubMedCrossRefGoogle Scholar
  66. Horton P, Leech RM (1972) The effect of ATP on photoconversion of protochlorophyllide into chlorophyllide in isolated etioplasts. FEBS Lett 26:277–280CrossRefGoogle Scholar
  67. Hyde S, Andersson S, Larsson K, Blum Z, Landh T, Lidin S, Ninham BW (1997) The language of shape. Elsevier, AmsterdamGoogle Scholar
  68. Ikeda T (1970) Changes in fine structure of prolamellar body in relation to the formation of the chloroplast. Bot Mag Tokyo 83:1–9Google Scholar
  69. Ikeda T (1971) Prolamellar body formation under different light and temperature conditions. Bot Mag Tokyo 84:363–376Google Scholar
  70. Ikeuchi M, Murakami S (1983) Separation and characterization of prolamellar bodies and prothylakoids from squash etioplasts. Plant Cell Physiol 24:71–80Google Scholar
  71. Jarvis P, Chen LJ, Li H, Peto CA, Fankhauser C, Chory J (1998) An Arabidopsis mutant defective in the plastid general protein import apparatus. Science 282:100–103PubMedCrossRefGoogle Scholar
  72. Jarvis P, Dörmann P, Peto CA, Lutes J, Benning C, Chory J (2000) Galactolipid deficiency and abnormal chloroplast development in the Arabidopsis MGD synthase 1 mutant. Proc Natl Acad Sci USA 97:8175–8179PubMedCrossRefGoogle Scholar
  73. Kahn A, Boardman NK, Thorne SW (1970) Energy transfer between protochlorophyllide molecules: evidence for multiple chromophores in the photoactive protochlorophyllide-protein complex in vivo and in vitro. J Mol Biol 48:85–101PubMedCrossRefGoogle Scholar
  74. Kanervo E, Singh M, Suorsa M, Paakkarinen V, Aro E, Battchikova N, Aro E-M (2008) Expression of protein complexes and individual proteins upon transition of etioplasts to chloroplasts in pea (Pisum sativum). Plant Cell Physiol 49:396–410PubMedCrossRefGoogle Scholar
  75. Kesselmeier J, Schäfer B, Laudenbach U (1987) Changes of the galactolipid composition during illumination of isolated oat etioplasts. Plant Cell Physiol 28:123–130Google Scholar
  76. Kim C, Apel K (2004) Substrate-dependent and organ-specific chloroplast protein import in planta. Plant Cell 16:88–98PubMedCrossRefGoogle Scholar
  77. Kim C, Ham H, Apel K (2005) Multiplicity of different cell- and organ-specific import routes for the NADPH-protochlorophyllide oxidoreductases A and B in plastids of Arabidopsis seedlings. Plant J 42:329–340PubMedCrossRefGoogle Scholar
  78. Kirk JTO, Tilney-Bassett RAE (1967) The plastids. Their chemistry, structure, growth and inheritance. Freeman, LondonGoogle Scholar
  79. Kirk JTO, Tilney-Bassett R (1978) The Plastids. Freeman, San FranciscoGoogle Scholar
  80. Kis-Petik K, Böddi B, Kaposi AD, Fidy J (1999) Protochlorophyllide forms and energy transfer in dark-grown wheat leaves. Studies by conventional and laser excited fluorescence spectroscopy between 10 K–100 K. Photosynth Res 60:87–98CrossRefGoogle Scholar
  81. Kleffmann T, von Zychlinski A, Russenberger D, Hirsch-Hoffmann M, Gehrig P, Gruissem W, Baginsky S (2007) Proteome dynamics during plastid differentiation in rice. Plant Physiol 143:912–923PubMedCrossRefGoogle Scholar
  82. Klein S, Schiff JK (1972) The correlated appearance of prolamellar bodies, protochlorophyllide species, and the Shibata shift during development of bean etioplasts in the dark. Plant Physiol 49:619–626PubMedCrossRefGoogle Scholar
  83. Klein S, Bryan G, Bogorad L (1964) Early stages in the development of plastid fine structure in red and far-red light. J Cell Biol 22:433–442PubMedCrossRefGoogle Scholar
  84. Klement H, Helfrich M, Oster U, Schoch S, Rüdiger W (1999) Pigment-free NADPH:protochlorophyllide oxido­reduc­tase from Avena sativa L. Eur J Biochem 265:862–874PubMedCrossRefGoogle Scholar
  85. Kohn S, Klein S (1976) Light-induced structural changes during incubation of isolated maize etioplasts. Planta 132:169–175CrossRefGoogle Scholar
  86. Kovacheva S, Ryberg M, Sundqvist C (2000) ADP/ATP and protein phosphorylation dependence of phototransformable protochlorophyllide in isolated etioplast membranes. Photosynth Res 64:127–136PubMedCrossRefGoogle Scholar
  87. Kreuz K, Beyer P, Kleinig H (1982) The site of carotenogenic enzymes in chromoplasts from Narcissus pseudonarcissus L. Planta 154:66–69CrossRefGoogle Scholar
  88. Kutik J (1998) The development of chloroplast structure during leaf ontogeny. Photosynthetica 35:481–505CrossRefGoogle Scholar
  89. Laetsch WM, Price I (1969) Development of the dimorphic chloroplasts of sugar cane. Am J Bot 56:77–87CrossRefGoogle Scholar
  90. Laflèche D, Bové JM, Duranton J (1972) Localization and translocation of the protochlorophyllide holochrome during the greening of etioplasts in Zea mays L. J Ultrastruct Res 40:205–214PubMedCrossRefGoogle Scholar
  91. Laudi G, Manzini ML (1975) Chlorophyll content and plastid ultrastructure in leaflets of Metasequoia glyptostroboides. Protoplasma 84:185–190CrossRefGoogle Scholar
  92. Leech RM, Baker NR (1983) The development of photosynthetic capacity in leaves. In: Dale JE, Milthorpe FL (eds) The growth and functioning of leaves: proceedings of a symposium. Cambridge Academic Press, Bath, pp 271–308Google Scholar
  93. Leech RM, Rumsby MG, Thomson WW (1973) Plastid differentiation, acyl lipid, and fatty acid changes in developing green maize leaves. Plant Physiol 52:240–245PubMedCrossRefGoogle Scholar
  94. Lichtenthaler HK, Rohmer M, Schwender J (1997) Two independent biochemical pathways for isopentenyl diphosphate and isoprenoid biosynthesis in higher plants. Physiol Plant 101:643–652CrossRefGoogle Scholar
  95. Linden FI, Lucas M, de Felipe MR, Sandmann G (1993) Immunogold localization of phytoene desaturase in higher plant chloroplasts. Physiol Plant 88:229–236CrossRefGoogle Scholar
  96. Lindsten A, Ryberg M, Sundqvist C (1988) The polypeptide composition of highly purified prolamellar bodies and prothylakoids from wheat (Triticum aestivum) as revealed by silver staining. Physiol Plant 72:167–176CrossRefGoogle Scholar
  97. Lindsten A, Welch CJ, Schoch S, Ryberg M, Rüdiger W, Sundqvist C (1990) Chlorophyll synthetase is latent in well preserved prolamellar bodies of etiolated wheat. Physiol Plant 80:277–285CrossRefGoogle Scholar
  98. Lindsten A, Wiktorsson B, Ryberg M, Sundqvist C (1993) Chlorophyll synthetase activity is relocated from transforming prolamellar bodies to developing thylakoids during irradiation of dark-grown wheat. Physiol Plant 88:29–36CrossRefGoogle Scholar
  99. Lütke-Brinkhaus F, Kleinig H (1987) Carotenoid and chlorophyll biosynthesis in isolated plastids from mustard seedling cotyledons (Sinapis alba L.) during etioplast-chloroplast conversion. Planta 170:121–129CrossRefGoogle Scholar
  100. Lütke-Brinkhaus F, Liedvogel B, Kreuz K, Kleinig H (1982) Phytoene synthase and phytoene dehydrogenase associated with envelope membranes from spinach chloroplasts. Planta 156:176–180CrossRefGoogle Scholar
  101. Lütz C (1981a) Development and ageing of etioplast structures in dark grown leaves of Avena sativa (L.). Protoplasma 108:83–98CrossRefGoogle Scholar
  102. Lütz C (1981b) On the significance of prolamellar bodies in membrane development of etioplasts. Protoplasma 108:99–115CrossRefGoogle Scholar
  103. Mackender RO (1978) Etioplast development in dark-grown leaves of Zea mays L. Plant Physiol 62:499–505PubMedCrossRefGoogle Scholar
  104. Mariani Colombo P, Rascio N, Casadoro G (1983) Differentiation of the photosynthetic apparatus in Phyllitis scolopendrium (L.) Newman. New Phytol 93:457–465CrossRefGoogle Scholar
  105. Mascia PN, Robertson DS (1978) Studies of chloroplast development in four maize mutants defective in chlorophyll biosynthesis. Planta 143:207–211Google Scholar
  106. Masuda T, Fusada N, Oosawa N, Takamatsu K, Yamamoto YY, Ohto M, Nakamura K, Goto K, Shibata D, Shirano Y, Hayashi H, Kato T, Tabata S, Shimada H, Ohta H, Takamiya K (2003) Functional analysis of isoforms of NADPH:protochlorophyllide oxidoreductase (POR), PORB and PORC, in Arabidopsis thaliana. Plant Cell Physiol 44:963–974PubMedCrossRefGoogle Scholar
  107. Mayer MP, Nievelstein V, Beyer P (1992) Purification and characterization of a NADPH dependent oxidoreductase from chromoplasts of Narcissus pseudonarcissus – a redox-mediator possibly involved in carotene desaturation. Plant Physiol Biochem 30:389–398Google Scholar
  108. Moro I, Dalla Vecchia F, La Rocca N, Navari-Izzo F, Quartacci MF, Di Baccio D, Rüdiger W, Rascio N (2004) Impaired carotenogenesis can affect organization and functionality of etioplast membranes. Physiol Plant 122:123–132CrossRefGoogle Scholar
  109. Murakami S, Yamada N, Nagano M, Osumi M (1985) Three dimensional structure of the prolamellar body in squash etioplasts. Protoplasma 128:147–156CrossRefGoogle Scholar
  110. Myśliwa-Kurdziel B, Franck F, Ouazzani-Chahdi MA, Strzałka K (1999) Changes in endothermic transitions associated with light-induced chlorophyllide formation, as investigated by differential scanning calorimetry. Physiol Plant 107:230–239CrossRefGoogle Scholar
  111. Norris SR, Barrette TR, DellaPenna D (1995) Genetic dissection of carotenoid synthesis in Arabidopsis defines plastoquinone as an essential component of phytoene desaturation. Plant Cell 7:2139–2149PubMedGoogle Scholar
  112. Ohnishi J, Yamada M (1980) Glycerolipid synthesis in Avena leaves during greening of etiolated seedlings I. Lipid changes in leaves. Plant Cell Physiol 21:1595–1606Google Scholar
  113. Oster U, Tanaka R, Tanaka A, Rüdiger W (2000) Cloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis CAO from Arabidopsis thaliana. Plant J 21:305–310PubMedCrossRefGoogle Scholar
  114. Ouazzani-Chahdi MA, Schoefs B, Franck F (1998) Isolation and characterisation of photoactive complexes of NADPH:protochlorophyllide oxidoreductase from wheat. Planta 206:673–680CrossRefGoogle Scholar
  115. Park H, Kreunen SS, Cuttriss AJ, Della Penna D, Pogson BJ (2002) Identification of the carotenoid isomerase provides insight into carotenoid biosynthesis, prolamellar body formation and photomorphogenesis. Plant Cell 14:321–332PubMedCrossRefGoogle Scholar
  116. Paulsen H (2001) Pigment assembly – transport and ligation. In: Aro EM, Anderson B (eds) Regulation of Photosynthesis, vol 11. Kluwer, Dordrecht, pp 219–233CrossRefGoogle Scholar
  117. Paulsen H, Rümler U, Rüdiger W (1990) Reconstitution of pigment-containing complexes from light-harvesting chlorophyll a/b-binding protein overexpressed in Escherichia coli. Planta 181:204–211CrossRefGoogle Scholar
  118. Perner ES (1956) Die ontogenetische Entwicklung der Chloroplasten von Chlorophytum comosum. II. Das Verhalten der Proplastiden bei der Entwicklung zu Jungchloroplasten. Z Naturforsch 11b:567–573Google Scholar
  119. Philippar K, Geis T, Ilkavets I, Oster U, Schwenkert S, Meurer J, Soll J (2007) Chloroplast biogenesis: the use of mutants to study the etioplast-chloroplast transition. Proc Natl Acad Sci USA 104:678–683PubMedCrossRefGoogle Scholar
  120. Platt-Aloia KW, Thomson WW (1977) Chloroplast development in young sesame plants. New Phytol 78:599–605CrossRefGoogle Scholar
  121. Pogson B, McDonald K, Truong M, Britton G, DellaPenna D (1996) Arabidopsis carotenoid mutants demonstrate that lutein is not essential for photosynthesis in higher plants. Plant Cell 8:1627–1639PubMedGoogle Scholar
  122. Polettini G, Dalla Vecchia F, Rascio N, Mariani P (1986) Ontogenesis of spinach chloroplasts in different periods of a seasonal cycle. G Bot Ital 120:116–118Google Scholar
  123. Protoschill-Krebs G, Kesselmeier J (1988) Prolamellar bodies of oat, wheat, and rye: structure, lipid composition, and adsorption of saponins. Protoplasma 146:1–9CrossRefGoogle Scholar
  124. Pudelski B, Soll J, Philippar K (2009) A search for factors influencing etioplast–chloroplast transition. Proc Natl Acad Sci USA 106:12201–12206PubMedCrossRefGoogle Scholar
  125. Pyke KA (2007) Plastid biogenesis and differentiation. In: Bock R (ed) Cell and molecular biology of plastids. Topics in current genetics 19. Springer, Heidelberg, pp 1–28CrossRefGoogle Scholar
  126. Rascio N, Orsenigo M, Arboit D (1976) Prolamellar body transformation with increasing cell age in the maize leaf. Protoplasma 90:253–263CrossRefGoogle Scholar
  127. Rascio N, Mariani P, Casadoro G (1984a) Etioplast-chloroplast transformation in maize leaves: effects of tissue age and light intensity. Protoplasma 119:110–120CrossRefGoogle Scholar
  128. Rascio N, Mariani P, Orsenigo M (1984b) Photosynthetic apparatus differentiation in Ginkgo biloba L. In: Sybesma C (ed) Advances in photosynthesis research, vol IV. Martinus Nijhoff/Dr. W. Junk, The Hague/Boston/Lancaster, pp 661–664Google Scholar
  129. Rascio N, Mariani Colombo P, Dalla Vecchia F, Chitano P (1985) Intrathylakoidal crystal appearance during the vital cycle of spinach chloroplasts. Protoplasma 126:153–157CrossRefGoogle Scholar
  130. Rascio N, Mariani P, Chitano P, Dalla Vecchia F (1986) An ultrastructural study of maize leaf etioplasts throughout their entire life-cycle. Protoplasma 130:98–107CrossRefGoogle Scholar
  131. Rascio N, Mariani P, Dalla Vecchia F, Chitano P (1988) Development and aging of leaf etioplasts in maize cultured with and without sucrose. J Ultrastruct Mol Struct Res 99:226–233CrossRefGoogle Scholar
  132. Rassadina V, Domanskii VP, Averina NG, Schoch S, Rüdiger W (2004) Correlation between chlorophyllide esterification, Shibata shift and regeneration of protochlorophyllide650 in flash-irradiated etiolated barley leaves. Physiol Plant 121:556–567CrossRefGoogle Scholar
  133. Rebeiz CC, Rebeiz CA (1986) Chloroplast biogenesis 53: Ultrastructural study of chloroplast development during photoperiodic greening. In: Akoyunoglou G, Senger H (eds) Regulation of chloroplast differentiation. Alan R Liss, New York, pp 389–396Google Scholar
  134. Reinbothe C, Pollmann S, Desvignes C, Weigele M, Beck E, Reinbothe S (2004a) LHPP, the light-harvesting NADPH:protochlorophyllide (Pchlide) oxidoreductase: Pchlide complex of etiolated plants, is developmentally expressed across the barley leaf gradient. Plant Sci 167:1027–1041CrossRefGoogle Scholar
  135. Reinbothe S, Quigley F, Gray J, Schemenewitz A, Reinbothe C (2004b) Identification of plastid envelope proteins required for import of protochlorophyllide oxidoreductase A into the chloroplast of barley. Proc Natl Acad Sci USA 7:2197–2202CrossRefGoogle Scholar
  136. Rissler H, Pogson BJ (2001) Antisense inhibition of the beta-carotene and nonphotochemical quenching in Arabidopsis. Photosynth Res 67:127–137PubMedCrossRefGoogle Scholar
  137. Robertson D, Laetsch WM (1974) Structure and function of developing barley plastids. Plant Physiol 54:148–159PubMedCrossRefGoogle Scholar
  138. Rüdiger W, Benz J, Guthoff C (1980) Detection and partial characterization of activity of chlorophyll synthetase in etioplast membranes. Eur J Biochem 190:193–200CrossRefGoogle Scholar
  139. Ryberg M, Dehesh K (1986) Localization of NADPH:proto­chlorophyllide oxidoreductase in dark-grown wheat (Triticum aestivum) by immuno-electron microscopy before and after transformation of the prolamellar bodies. Physiol Plant 66:616–624CrossRefGoogle Scholar
  140. Ryberg M, Sundqvist C (1982) Spectral forms of proto­chlorophyllide in prolamellar bodies and prothylakoids fractionated from wheat etioplasts. Physiol Plant 56:133–138CrossRefGoogle Scholar
  141. Ryberg M, Sundqvist C (1988) The regular ultrastructure of isolated prolamellar bodies depends on the presence of membrane-bound NADPH-protochlorophyllide oxidoreductase. Physiol Plant 73:218–226CrossRefGoogle Scholar
  142. Ryberg M, Sandelius AS, Selstam E (1983) Lipid composition of prolamellar bodies and prothylakoids of wheat etioplasts. Physiol Plant 57:555–560CrossRefGoogle Scholar
  143. Schnepf E (1964) Über Zusammenhänge zwischen Heitz-Leyon-Kristallen und Thylakoiden. Planta 61:371–373CrossRefGoogle Scholar
  144. Schoch S, Lempert U, Rüdiger W (1977) Über die letzten Stufen der Chlorophyll-Biosynthese Zwischenprodukte zwischen Chlorophyllid und phytolhaltigem Chlorophyll. Z Pflanzenphysiol 83:419–426Google Scholar
  145. Schoefs B (1999) The light-dependent and light-independent reduction of protochlorophyllide a to chlorophyllide a. Photosynthetica 36:481–496CrossRefGoogle Scholar
  146. Schoefs B (2001) The protochlorophyllide-chlorophyllide cycle. Photosynth Res 70:257–271PubMedCrossRefGoogle Scholar
  147. Schoefs B (2005) Protochlorophyllide reduction – what is new in 2005? Photosynthetica 43:329–343CrossRefGoogle Scholar
  148. Schoefs B, Bertrand M (2000) The formation of chlorophyll from chlorophyllide in leaves containing proplastids is a four-step process. FEBS Lett 486:243–246PubMedCrossRefGoogle Scholar
  149. Schoefs B, Franck F (1991) Photosystem II assembly in 2-day-old bean leaves during the first 16 h of greening. C R Acad Sci 313:441–445Google Scholar
  150. Schoefs B, Franck F (1993) Photoreduction of protochlorophyllide to chlorophyllide in 2-d-old dark-grown bean (Phaseolus vulgaris cv. Commodore) leaves. Comparison with 10-d-old dark-grown (etiolated) leaves. J Exp Bot 44:1053–1057CrossRefGoogle Scholar
  151. Schoefs B, Franck F (1998) Chlorophyll synthesis in dark-grown pine primary needles. Plant Physiol 118:1159–1168PubMedCrossRefGoogle Scholar
  152. Schoefs B, Franck F (2003) Protochlorophyllide reduction: mechanisms and evolution. Photochem Photobiol 78:543–557PubMedCrossRefGoogle Scholar
  153. Schoefs B, Franck F (2008) The photoenzymatic cycle of NADPH:protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) during the first days of photoperiodic growth. Photosynth Res 96:15–26PubMedCrossRefGoogle Scholar
  154. Schoefs B, Bertrand M, Lemoine Y (1998) Changes in the photosynthetic pigments in bean leaves during the first photoperiod of greening and the subsequent dark-phase. Comparison between old (10-d-old) leaves and young (2-d-old) leaves. Photosynth Res 57:203–213CrossRefGoogle Scholar
  155. Schoefs B, Bertrand M, Franck F (2000) Spectroscopic properties of protochlorophyllide analyzed in situ in the course of etiolation and in illuminated leaves. Photochem Photobiol 72:85–93PubMedCrossRefGoogle Scholar
  156. Selldén G, Selstam E (1976) Changes in chloroplast lipids during the development of photosynthetic activity in barley etio-chloroplasts. Physiol Plant 37:35–41CrossRefGoogle Scholar
  157. Selstam E (1998) Development of thylakoid membranes with respect to lipids. In: Siegenthaler P-A, Murata N (eds) Advances in photosynthesis 6. Lipids in photosynthesis: structure, function and genetics. Kluwer, Dordrecht/Boston/London, pp 209–224Google Scholar
  158. Selstam E, Sandelius AS (1984) A comparison between prolamellar bodies and prothylakoid membranes of etioplasts of dark-grown wheat concerning lipid and polypeptide composition. Plant Physiol 76:1036–1040PubMedCrossRefGoogle Scholar
  159. Selstam E, Widell A (1986) Characterization of prolamellar bodies, from dark-grown seedlings of Scots pine, containing light- and NADPH-dependent protochlorophyllide oxidoreductase. Physiol Plant 67:345–352CrossRefGoogle Scholar
  160. Selstam E, Widell A, Johansson LB-A (1987) A comparison of prolamellar bodies from wheat, Scots pine and Jeffrey pine. Pigment spectra and properties of protochlorophyllide oxidoreductase. Physiol Plant 70:209–214CrossRefGoogle Scholar
  161. Shibata K (1957) Spectroscopic studies on chlorophyll formation in intact leaves. J Biochem 44:147–173Google Scholar
  162. Smith H (ed) (1978) The molecular biology of plant cells. Botanical monographs. University of California Press, BerkeleyGoogle Scholar
  163. Smith H (1982) Light quality photoreception and plant strategy. Annu Rev Plant Physiol 33:481–518CrossRefGoogle Scholar
  164. Smith H (1994) Sensing the light environment: the functions of the phytochrome family. In: Kendrick RE, Kronenberg GHM (eds) Photomorphogenesis in plants, 2nd edn. Kluwer, Dordrecht, pp 377–416CrossRefGoogle Scholar
  165. Solymosi K, Böddi B (2006) Optical properties of bud scales and protochlorophyll(ide) forms in leaf primordia of closed and opened buds. Tree Physiol 26:1075–1085PubMedCrossRefGoogle Scholar
  166. Solymosi K, Schoefs B (2008) Prolamellar body: a unique plastid compartment, which does not only occur in dark-grown leaves. In: Schoefs B (ed) Plant cell organelles – selected topics. Research Signpost, Trivandrum, pp 151–202Google Scholar
  167. Solymosi K, Schoefs B (2010) Etioplast and etio-chloroplast formation under natural conditions: the dark side of chlorophyll biosynthesis in angiosperms. Photosynth Res 105:143–166PubMedCrossRefGoogle Scholar
  168. Solymosi K, Martinez K, Kristóf Z, Sundqvist C, Böddi B (2004) Plastid differentiation and chlorophyll biosynthesis in different leaf layers of white cabbage (Brassica oleracea cv. capitata). Physiol Plant 121:520–529CrossRefGoogle Scholar
  169. Solymosi K, Bóka K, Böddi B (2006a) Transient etiolation: protochlorophyll(ide) and chlorophyll forms in differentiating plastids of closed and breaking leaf buds of horse chestnut (Aesculus hippocastanum). Tree Physiol 26:1087–1096PubMedCrossRefGoogle Scholar
  170. Solymosi K, Myśliwa-Kurdziel B, Bóka K, Strzałka K, Böddi B (2006b) Disintegration of the prolamellar body structure at high concentrations of Hg2+. Plant Biol 8:627–635PubMedCrossRefGoogle Scholar
  171. Sperling U, van Cleve B, Frick G, Apel K, Armstrong GA (1997) Overexpression of light-dependent PORA or PORB in plants depleted of endogenous POR by far-red light enhances seedling survival in white light and protects against photooxidative damage. Plant J 12:649–658PubMedCrossRefGoogle Scholar
  172. Sperling U, Franck F, van Cleve B, Frick G, Apel K, Armstrong GA (1998) Etioplast differentiation in Arabidopsis: both PORA and PORB restore the prolamellar body and photoactive protochlorophyllide-F655 to the cop1 photomorphogenic mutant. Plant Cell 10:283–296PubMedGoogle Scholar
  173. Stetler DA, Laetsch WM (1969) Chloroplast development in Nicotiana tabacum ‘Maryland Mammoth’. Am J Bot 56:260–270CrossRefGoogle Scholar
  174. Sundqvist C, Dahlin C (1997) With chlorophyll pigments from prolamellar bodies to light-harvesting complexes. Physiol Plant 100:748–759CrossRefGoogle Scholar
  175. Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58:321–346PubMedCrossRefGoogle Scholar
  176. Thelander M, Narita JO, Gruissem W (1986) Plastid differentiation and pigment biosynthesis during tomato fruit ripening. Curr Top Plant Biochem Physiol 5:128–141Google Scholar
  177. Treffry T (1970) Phytilation of chlorophyll(ide) and prolamellar body transformation in etiolated peas. Planta 91:279–284CrossRefGoogle Scholar
  178. Verbelen JP, De Greef JA (1979a) Leaf development of Phaseolus vulgaris L. in light and in darkness. Am J Bot 66:970–976CrossRefGoogle Scholar
  179. Verbelen JP, De Greef JA (1979b) De chloroplast-ontwikkeling bij Phaseolus vulgaris. Biologisch Jaarboek Dodonaea 47:123–129Google Scholar
  180. Vogelmann TC (1989) Penetration of light into plants. Photochem Photobiol 50:895–902CrossRefGoogle Scholar
  181. von Lintig J, Welsch R, Bonk M, Giuliano G, Batschauer A, Kleinig H (1997) Light-dependent regulation of carotenoid biosynthesis occurs at the level of phytoene synthase expression and is mediated by phytochrome in Sinapis alba and Arabidopsis thaliana seedlings. Plant J 12:625–634CrossRefGoogle Scholar
  182. von Wettstein D (1959) The formation of plastid structures. J Ultrastruct Res 3:234–240CrossRefGoogle Scholar
  183. von Wettstein D, Gough S, Kannangara CG (1995) Chlorophyll biosynthesis. Plant Cell 7:1039–1057Google Scholar
  184. von Zychlinski A, Kleffman T, Krishnamurthy N, Sjölander K, Baginsky S, Gruissem W (2005) Proteome analysis of the rice etioplast: metabolic and regulatory networks and novel protein functions. Mol Cell Proteomics 4:1072–1084CrossRefGoogle Scholar
  185. Walles B, Hudák J (1975) A comparative study of chloroplast morphogenesis in seedlings of some conifers (Larix decidua, Pinus sylvestris and Picea abies). Stud Forest Suec 127:2–22Google Scholar
  186. Waters M (2004) Plastid tubules in higher plants: an analysis of form and function. Ph.D. thesis, University of Nottingham, NottinghamGoogle Scholar
  187. Waters M, Pyke K (2004) Plastid development and differentiation. In: Moller SG (ed) Plastids, annual plant reviews. Blackwell/CRC Press, Oxford, pp 30–59Google Scholar
  188. Weier TE, Brown DL (1970) Formation of the prola­mellar body in 8-day, dark-grown seedlings. Am J Bot 57:267–275CrossRefGoogle Scholar
  189. Wellburn AR (1977) Distribution of chloroplast coupling factor (CF1) particles on plastid membranes during development. Planta 135:191–198CrossRefGoogle Scholar
  190. Wellburn AR (1982) Bioenergetic and ultrastructural changes associated with chloroplast development. Int Rev Cytol 80:133–191CrossRefGoogle Scholar
  191. Wellburn AR, Robinson DC, Wellburn FAM (1982) Chloroplast development in low-light grown barley seedlings. Planta 154:259–265CrossRefGoogle Scholar
  192. Welsch R, Beyer P, Hugueney P, Kleinig H, von Lintig J (2000) Regulation and activation of phytoene synthase, a key enzyme in carotenoid biosynthesis, during photomorphogenesis. Planta 211:846–854PubMedCrossRefGoogle Scholar
  193. Whatley JM (1974) Chloroplast development in primary leaves of Phaseolus vulgaris. New Phytol 73:1097–1110CrossRefGoogle Scholar
  194. Whatley JM (1977a) The effect of cotyledons on chloroplast development in primary leaves of Phaseolus vulgaris. New Phytol 79:55–60CrossRefGoogle Scholar
  195. Whatley JM (1977b) Variations in the basic pathway of chloroplast development. New Phytol 78:407–420CrossRefGoogle Scholar
  196. Whatley JM (1992) Plastid development in distinctively coloured juvenile leaves. New Phytol 120:417–426CrossRefGoogle Scholar
  197. Wiktorsson B, Engdahl S, Zhong LB, Böddi B, Ryberg M, Sundqvist C (1993) The effect of cross-linking of the subunits of NADPH:protochloro­phyllide oxidoreductase on the aggregational state of protochlorophyllide. Photosynthetica 29:205–218Google Scholar
  198. Wiktorsson B, Ryberg M, Sundqvist C (1996) Aggregation of NADPH-protochlorophyllide oxidoreductase pigment complexes is favoured by protein phosphorylation. Plant Physiol Biochem 34:23–34Google Scholar
  199. Wise RR (2006) The diversity of plastid form and function. In: Wise RR, Hoober KJ (eds) Advances in photosynthesis and respiration. The structure and function of plastids, vol 23. Springer, Dordrecht, pp 3–26CrossRefGoogle Scholar
  200. Wrischer M (1966) Neubildung von Prolamellar­körpern in Chloroplasten. Z Pflanzenphysiol 55:296–299Google Scholar
  201. Wrischer M (1967) The effects of inhibitors of protein synthesis on the differentiation of plastids in etiolated bean seedlings. Planta 73:324–327CrossRefGoogle Scholar
  202. Younis S, Ryberg M, Sundqvist C (1995) Plastid development in germinating wheat (Triticum aestivum) is enhanced by gibberellic acid and delayed by gabaculine. Physiol Plant 95:336–346CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Department of Plant AnatomyEötvös UniversityBudapestHungary
  2. 2.Department of Biological and Environmental SciencesUniversity of GothenburgGothenburgSweden

Personalised recommendations