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Etioplasts and Their Significance in Chloroplast Biogenesis

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Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 36))

Summary

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.

This chapter is dedicated to the late Professor Christer Sundqvist, a friend and major contributor to the etioplast-chloroplast transition art.

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Abbreviations

ALA –:

5-aminolevulinic acid;

Chl(s) –:

Chlorophyll(s);

Chlide –:

Chlorophyllide;

Coprogen III –:

Coproporphyrinogen III;

DGDG –:

Digalactosyl diacylglycerol;

DPOR –:

Dark-operative NADPH: Pchl­ide oxidoreductase;

GG – Geranylgeraniol; GGPP –:

Geranylgeraniol diphosphate;

GSA –:

Glutamate-1-semialdehyde;

IPP –:

Isopentenyl diphosphate;

LDC –:

Light–dark cycle;

LPOR –:

Light-dependent NADPH: Pchlide oxidoreductase;

LPOR-A, -B, -C –:

Isoforms of LPOR;

MGDG –:

Monogalactosyl diacylglycerol;

Pchlide –:

Protochlorophyllide;

PGB –:

Porphobilinogen;

PLB –:

Prolamellar body;

Protogen IX –:

Porphyrinogen III;

PSI –:

Photosystem I;

PSII –:

Photosystem II;

PT –:

Prothylakoid;

Urogen III –:

Uroporphyrinogen III

References

  • 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 150:269–274

    Article  CAS  Google Scholar 

  • Adamson H, Packer N, Gregory J (1985) Chloroplast development and the synthesis of chlorophyll and protochlorophyllide in Zostera transferred to darkness. Planta 165:469–476

    Article  CAS  Google Scholar 

  • 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 105:529–534

    PubMed  Google Scholar 

  • 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 121:377–390

    Article  CAS  Google Scholar 

  • 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 128:751–762

    Article  CAS  Google Scholar 

  • 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 120:89–93

    Article  PubMed  CAS  Google Scholar 

  • Aronsson H, Sohrt K, Soll J (2000) NADPH:proto­chloro­phyllide oxidoreductase uses the general import pathway. Biol Chem 381:1263–1267

    Article  PubMed  CAS  Google Scholar 

  • 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 502:11–15

    Article  PubMed  CAS  Google Scholar 

  • 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 111:239–244

    Article  CAS  Google Scholar 

  • Aronsson H, Sundqvist C, Dahlin C (2003a) POR hits the road: import and assembly of a plastid protein. Plant Mol Biol 51:1–7

    Article  PubMed  CAS  Google Scholar 

  • Aronsson H, Sundqvist C, Dahlin C (2003b) POR – import and membrane association of a key element in chloroplast development. Physiol Plant 118:1–9

    Article  PubMed  CAS  Google Scholar 

  • 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 148:580–592

    Article  PubMed  CAS  Google Scholar 

  • Bahl J (1977) Chlorophyll, carotenoid and lipid content in Triticum sativum L. plastid envelopes, prolamellar bodies, stroma lamellae, and grana. Planta 136:21–24

    Article  CAS  Google Scholar 

  • 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 129:193–201

    Article  Google Scholar 

  • Barry P, Young AJ, Britton G (1991) Accumulation of pigments during the greening of etiolated seedlings of Hordeum vulgare L. J Exp Bot 42:229–234

    Article  CAS  Google Scholar 

  • 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 64:63–76

    Article  PubMed  Google Scholar 

  • 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 892:118–129

    Article  CAS  Google Scholar 

  • Benz J, Wolf C, Rüdiger W (1980) Chlorophyll biosynthesis: hydrogenation of geranylgeraniol. Plant Sci Lett 19:225–230

    Article  CAS  Google Scholar 

  • 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:443–448

    Google Scholar 

  • Biswal UC, Biswal B, Raval MK (2003) Chloroplast biogenesis. From proplastid to gerontoplast. Kluwer, Dordrecht

    Book  Google Scholar 

  • 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 128:368–381

    Article  CAS  Google Scholar 

  • Blomqvist LA, Ryberg M, Sundqvist C (2008) Proteomic analysis of highly purified prolamellar bodies reveals their significance in chloroplast development. Photosynth Res 96:37–50

    Article  PubMed  CAS  Google Scholar 

  • Böddi B, Lindsten A, Ryberg M, Sundqvist C (1989) On the aggregational states of protochlorophyllide and its protein complexes in wheat etioplasts. Physiol Plant 76:135–143

    Article  Google Scholar 

  • Böddi B, Lindsten A, Ryberg M, Sundqvist C (1990) Phototransformation of aggregated forms of protochlorophyllide in isolated etioplast inner membranes. Photochem Photobiol 52:83–87

    Article  Google Scholar 

  • 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 12:389–401

    Article  Google Scholar 

  • Boffey SA, Sellden G, Leech RM (1980) Influence of cell age on chlorophyll formation in light-grown and etiolated wheat seedlings. Plant Physiol 65:680–684

    Article  PubMed  CAS  Google Scholar 

  • 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 2:1397–1409

    Article  PubMed  CAS  Google Scholar 

  • 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 107:5693

    Google Scholar 

  • 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 120:427–434

    Article  Google Scholar 

  • 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 1391:320–328

    Article  PubMed  CAS  Google Scholar 

  • 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 73:271–279

    Article  CAS  Google Scholar 

  • 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 73:263–270

    Article  CAS  Google Scholar 

  • 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 148:568–579

    Article  PubMed  CAS  Google Scholar 

  • 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 38:89–97

    Article  CAS  Google Scholar 

  • Casadoro G, Rascio N (1979) Patterns of thylakoid system formation. J Ultrastruct Res 69:307–315

    Article  PubMed  CAS  Google Scholar 

  • 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 61:824–829

    Article  PubMed  CAS  Google Scholar 

  • 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 12:243–254

    Article  CAS  Google Scholar 

  • 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 8:1613–1626

    PubMed  CAS  Google Scholar 

  • 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 109:298–303

    Article  CAS  Google Scholar 

  • 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 75:47–54

    Article  CAS  Google Scholar 

  • Dehesh K, Ryberg M (1985) The NADPH:protochloro­phyllide oxidoreductase is the major protein constituent of prolamellar bodies in wheat (Triticum aestivum L.). Planta 164:396–399

    Article  CAS  Google Scholar 

  • 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 169:162–171

    Article  CAS  Google Scholar 

  • 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 169:172–183

    Article  CAS  Google Scholar 

  • 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 1716:97–103

    Article  PubMed  CAS  Google Scholar 

  • Domanskii VP, Rüdiger W (2001) On the nature of the two pathways in chlorophyll formation from protochlorophyllide. Photosynth Res 68:131–139

    Article  PubMed  CAS  Google Scholar 

  • 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 216:475–483

    PubMed  CAS  Google Scholar 

  • 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 27:297–304

    Article  PubMed  CAS  Google Scholar 

  • 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 190:536–545

    Article  PubMed  CAS  Google Scholar 

  • 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 365–381

    Google Scholar 

  • Franck F, Inoue Y (1984) Light-driven reversible transformation of chlorophyllide P696,682 into chlorophyllide P688,678 in illuminated etiolated bean leaves. Photobioch Photobiop 8:85–96

    Google Scholar 

  • Franck F, Barthélemy X, Strzałka K (1993) Spectroscopic characterization of protochlorophyllide photoreduction in the greening leaf. Photosynthetica 29:185–194

    CAS  Google Scholar 

  • 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 51:107–118

    Article  CAS  Google Scholar 

  • Friedmann HC, Thauer RK, Gough SP, Kannangara CG (1987) Δ-aminolevulinic acid formation in the archaebacterium Methanobacterium thermoautotrophicum requires tRNA Glu. Carlsberg Res Commun 52:363–371

    Article  CAS  Google Scholar 

  • 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 109–156

    Google Scholar 

  • 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 1:463–471

    Article  CAS  Google Scholar 

  • Gunning BES (1965) The greening process in plastids. 1. The structure of the prolamellar body. Protoplasma 60:111–130

    Article  Google Scholar 

  • Gunning BES (2001) Membrane geometry of “open” prolamellar bodies. Protoplasma 215:4–15

    Article  PubMed  CAS  Google Scholar 

  • Gunning BES (2004) Plant cell biology on DVD. http://www.plantcellbiologyondvd.com. Accessed 15 Oct 2007

  • Gunning BES, Steer MW (1996) Plant cell biology: structure and function. Jones and Bartlett, Boston

    Google Scholar 

  • 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 106:537–546

    PubMed  CAS  Google Scholar 

  • 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 93:1121–1127

    Article  Google Scholar 

  • 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 5:757–793

    PubMed  CAS  Google Scholar 

  • Henningsen KW, Boynton JE (1974) Macromolecular physiology of plastids IX. Development of plastid membranes during greening of dark-grown barley seedlings. J Cell Sci 15:31–55

    PubMed  CAS  Google Scholar 

  • 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 42:1–349

    Google Scholar 

  • Hirschberg J (2001) Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol 4:210–218

    Article  PubMed  CAS  Google Scholar 

  • Horton P, Leech RM (1972) The effect of ATP on photoconversion of protochlorophyllide into chlorophyllide in isolated etioplasts. FEBS Lett 26:277–280

    Article  CAS  Google Scholar 

  • Hyde S, Andersson S, Larsson K, Blum Z, Landh T, Lidin S, Ninham BW (1997) The language of shape. Elsevier, Amsterdam

    Google Scholar 

  • Ikeda T (1970) Changes in fine structure of prolamellar body in relation to the formation of the chloroplast. Bot Mag Tokyo 83:1–9

    Google Scholar 

  • Ikeda T (1971) Prolamellar body formation under different light and temperature conditions. Bot Mag Tokyo 84:363–376

    Google Scholar 

  • Ikeuchi M, Murakami S (1983) Separation and characterization of prolamellar bodies and prothylakoids from squash etioplasts. Plant Cell Physiol 24:71–80

    CAS  Google Scholar 

  • 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 282:100–103

    Article  PubMed  CAS  Google Scholar 

  • 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 97:8175–8179

    Article  PubMed  CAS  Google Scholar 

  • 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 48:85–101

    Article  PubMed  CAS  Google Scholar 

  • 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 49:396–410

    Article  PubMed  CAS  Google Scholar 

  • Kesselmeier J, Schäfer B, Laudenbach U (1987) Changes of the galactolipid composition during illumination of isolated oat etioplasts. Plant Cell Physiol 28:123–130

    CAS  Google Scholar 

  • Kim C, Apel K (2004) Substrate-dependent and organ-specific chloroplast protein import in planta. Plant Cell 16:88–98

    Article  PubMed  CAS  Google Scholar 

  • 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 42:329–340

    Article  PubMed  CAS  Google Scholar 

  • Kirk JTO, Tilney-Bassett RAE (1967) The plastids. Their chemistry, structure, growth and inheritance. Freeman, London

    Google Scholar 

  • Kirk JTO, Tilney-Bassett R (1978) The Plastids. Freeman, San Francisco

    Google Scholar 

  • 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 60:87–98

    Article  CAS  Google Scholar 

  • 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 143:912–923

    Article  PubMed  CAS  Google Scholar 

  • 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 49:619–626

    Article  PubMed  CAS  Google Scholar 

  • 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 22:433–442

    Article  PubMed  CAS  Google Scholar 

  • Klement H, Helfrich M, Oster U, Schoch S, Rüdiger W (1999) Pigment-free NADPH:protochlorophyllide oxido­reduc­tase from Avena sativa L. Eur J Biochem 265:862–874

    Article  PubMed  CAS  Google Scholar 

  • Kohn S, Klein S (1976) Light-induced structural changes during incubation of isolated maize etioplasts. Planta 132:169–175

    Article  Google Scholar 

  • Kovacheva S, Ryberg M, Sundqvist C (2000) ADP/ATP and protein phosphorylation dependence of phototransformable protochlorophyllide in isolated etioplast membranes. Photosynth Res 64:127–136

    Article  PubMed  CAS  Google Scholar 

  • Kreuz K, Beyer P, Kleinig H (1982) The site of carotenogenic enzymes in chromoplasts from Narcissus pseudonarcissus L. Planta 154:66–69

    Article  CAS  Google Scholar 

  • Kutik J (1998) The development of chloroplast structure during leaf ontogeny. Photosynthetica 35:481–505

    Article  CAS  Google Scholar 

  • Laetsch WM, Price I (1969) Development of the dimorphic chloroplasts of sugar cane. Am J Bot 56:77–87

    Article  Google Scholar 

  • 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 40:205–214

    Article  PubMed  Google Scholar 

  • Laudi G, Manzini ML (1975) Chlorophyll content and plastid ultrastructure in leaflets of Metasequoia glyptostroboides. Protoplasma 84:185–190

    Article  CAS  Google Scholar 

  • 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 271–308

    Google Scholar 

  • Leech RM, Rumsby MG, Thomson WW (1973) Plastid differentiation, acyl lipid, and fatty acid changes in developing green maize leaves. Plant Physiol 52:240–245

    Article  PubMed  CAS  Google Scholar 

  • Lichtenthaler HK, Rohmer M, Schwender J (1997) Two independent biochemical pathways for isopentenyl diphosphate and isoprenoid biosynthesis in higher plants. Physiol Plant 101:643–652

    Article  CAS  Google Scholar 

  • Linden FI, Lucas M, de Felipe MR, Sandmann G (1993) Immunogold localization of phytoene desaturase in higher plant chloroplasts. Physiol Plant 88:229–236

    Article  CAS  Google Scholar 

  • 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 72:167–176

    Article  CAS  Google Scholar 

  • 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 80:277–285

    Article  CAS  Google Scholar 

  • 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 88:29–36

    Article  CAS  Google Scholar 

  • 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 170:121–129

    Article  Google Scholar 

  • Lütke-Brinkhaus F, Liedvogel B, Kreuz K, Kleinig H (1982) Phytoene synthase and phytoene dehydrogenase associated with envelope membranes from spinach chloroplasts. Planta 156:176–180

    Article  Google Scholar 

  • Lütz C (1981a) Development and ageing of etioplast structures in dark grown leaves of Avena sativa (L.). Protoplasma 108:83–98

    Article  Google Scholar 

  • Lütz C (1981b) On the significance of prolamellar bodies in membrane development of etioplasts. Protoplasma 108:99–115

    Article  Google Scholar 

  • Mackender RO (1978) Etioplast development in dark-grown leaves of Zea mays L. Plant Physiol 62:499–505

    Article  PubMed  CAS  Google Scholar 

  • Mariani Colombo P, Rascio N, Casadoro G (1983) Differentiation of the photosynthetic apparatus in Phyllitis scolopendrium (L.) Newman. New Phytol 93:457–465

    Article  Google Scholar 

  • Mascia PN, Robertson DS (1978) Studies of chloroplast development in four maize mutants defective in chlorophyll biosynthesis. Planta 143:207–211

    CAS  Google Scholar 

  • 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 44:963–974

    Article  PubMed  CAS  Google Scholar 

  • 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 30:389–398

    CAS  Google Scholar 

  • 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 122:123–132

    Article  CAS  Google Scholar 

  • Murakami S, Yamada N, Nagano M, Osumi M (1985) Three dimensional structure of the prolamellar body in squash etioplasts. Protoplasma 128:147–156

    Article  Google Scholar 

  • 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 107:230–239

    Article  Google Scholar 

  • 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 7:2139–2149

    PubMed  CAS  Google Scholar 

  • Ohnishi J, Yamada M (1980) Glycerolipid synthesis in Avena leaves during greening of etiolated seedlings I. Lipid changes in leaves. Plant Cell Physiol 21:1595–1606

    CAS  Google Scholar 

  • 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 21:305–310

    Article  PubMed  CAS  Google Scholar 

  • Ouazzani-Chahdi MA, Schoefs B, Franck F (1998) Isolation and characterisation of photoactive complexes of NADPH:protochlorophyllide oxidoreductase from wheat. Planta 206:673–680

    Article  Google Scholar 

  • 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 14:321–332

    Article  PubMed  CAS  Google Scholar 

  • Paulsen H (2001) Pigment assembly – transport and ligation. In: Aro EM, Anderson B (eds) Regulation of Photosynthesis, vol 11. Kluwer, Dordrecht, pp 219–233

    Chapter  Google Scholar 

  • 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 181:204–211

    Article  CAS  Google Scholar 

  • Perner ES (1956) Die ontogenetische Entwicklung der Chloroplasten von Chlorophytum comosum. II. Das Verhalten der Proplastiden bei der Entwicklung zu Jungchloroplasten. Z Naturforsch 11b:567–573

    Google Scholar 

  • 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 104:678–683

    Article  PubMed  CAS  Google Scholar 

  • Platt-Aloia KW, Thomson WW (1977) Chloroplast development in young sesame plants. New Phytol 78:599–605

    Article  Google Scholar 

  • 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 8:1627–1639

    PubMed  CAS  Google Scholar 

  • Polettini G, Dalla Vecchia F, Rascio N, Mariani P (1986) Ontogenesis of spinach chloroplasts in different periods of a seasonal cycle. G Bot Ital 120:116–118

    Google Scholar 

  • Protoschill-Krebs G, Kesselmeier J (1988) Prolamellar bodies of oat, wheat, and rye: structure, lipid composition, and adsorption of saponins. Protoplasma 146:1–9

    Article  Google Scholar 

  • Pudelski B, Soll J, Philippar K (2009) A search for factors influencing etioplast–chloroplast transition. Proc Natl Acad Sci USA 106:12201–12206

    Article  PubMed  CAS  Google Scholar 

  • 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 1–28

    Chapter  Google Scholar 

  • Rascio N, Orsenigo M, Arboit D (1976) Prolamellar body transformation with increasing cell age in the maize leaf. Protoplasma 90:253–263

    Article  Google Scholar 

  • Rascio N, Mariani P, Casadoro G (1984a) Etioplast-chloroplast transformation in maize leaves: effects of tissue age and light intensity. Protoplasma 119:110–120

    Article  Google Scholar 

  • 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 661–664

    Google Scholar 

  • Rascio N, Mariani Colombo P, Dalla Vecchia F, Chitano P (1985) Intrathylakoidal crystal appearance during the vital cycle of spinach chloroplasts. Protoplasma 126:153–157

    Article  CAS  Google Scholar 

  • Rascio N, Mariani P, Chitano P, Dalla Vecchia F (1986) An ultrastructural study of maize leaf etioplasts throughout their entire life-cycle. Protoplasma 130:98–107

    Article  Google Scholar 

  • 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 99:226–233

    Article  Google Scholar 

  • 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 121:556–567

    Article  CAS  Google Scholar 

  • 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 389–396

    Google Scholar 

  • 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 167:1027–1041

    Article  CAS  Google Scholar 

  • 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 7:2197–2202

    Article  CAS  Google Scholar 

  • Rissler H, Pogson BJ (2001) Antisense inhibition of the beta-carotene and nonphotochemical quenching in Arabidopsis. Photosynth Res 67:127–137

    Article  PubMed  CAS  Google Scholar 

  • Robertson D, Laetsch WM (1974) Structure and function of developing barley plastids. Plant Physiol 54:148–159

    Article  PubMed  CAS  Google Scholar 

  • Rüdiger W, Benz J, Guthoff C (1980) Detection and partial characterization of activity of chlorophyll synthetase in etioplast membranes. Eur J Biochem 190:193–200

    Article  Google Scholar 

  • 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 66:616–624

    Article  CAS  Google Scholar 

  • Ryberg M, Sundqvist C (1982) Spectral forms of proto­chlorophyllide in prolamellar bodies and prothylakoids fractionated from wheat etioplasts. Physiol Plant 56:133–138

    Article  CAS  Google Scholar 

  • Ryberg M, Sundqvist C (1988) The regular ultrastructure of isolated prolamellar bodies depends on the presence of membrane-bound NADPH-protochlorophyllide oxidoreductase. Physiol Plant 73:218–226

    Article  CAS  Google Scholar 

  • Ryberg M, Sandelius AS, Selstam E (1983) Lipid composition of prolamellar bodies and prothylakoids of wheat etioplasts. Physiol Plant 57:555–560

    Article  CAS  Google Scholar 

  • Schnepf E (1964) Über Zusammenhänge zwischen Heitz-Leyon-Kristallen und Thylakoiden. Planta 61:371–373

    Article  Google Scholar 

  • Schoch S, Lempert U, Rüdiger W (1977) Über die letzten Stufen der Chlorophyll-Biosynthese Zwischenprodukte zwischen Chlorophyllid und phytolhaltigem Chlorophyll. Z Pflanzenphysiol 83:419–426

    Google Scholar 

  • Schoefs B (1999) The light-dependent and light-independent reduction of protochlorophyllide a to chlorophyllide a. Photosynthetica 36:481–496

    Article  CAS  Google Scholar 

  • Schoefs B (2001) The protochlorophyllide-chlorophyllide cycle. Photosynth Res 70:257–271

    Article  PubMed  CAS  Google Scholar 

  • Schoefs B (2005) Protochlorophyllide reduction – what is new in 2005? Photosynthetica 43:329–343

    Article  CAS  Google Scholar 

  • Schoefs B, Bertrand M (2000) The formation of chlorophyll from chlorophyllide in leaves containing proplastids is a four-step process. FEBS Lett 486:243–246

    Article  PubMed  CAS  Google Scholar 

  • 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 313:441–445

    CAS  Google Scholar 

  • 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 44:1053–1057

    Article  CAS  Google Scholar 

  • Schoefs B, Franck F (1998) Chlorophyll synthesis in dark-grown pine primary needles. Plant Physiol 118:1159–1168

    Article  PubMed  CAS  Google Scholar 

  • Schoefs B, Franck F (2003) Protochlorophyllide reduction: mechanisms and evolution. Photochem Photobiol 78:543–557

    Article  PubMed  CAS  Google Scholar 

  • 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 96:15–26

    Article  PubMed  CAS  Google Scholar 

  • 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 57:203–213

    Article  Google Scholar 

  • 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 72:85–93

    Article  PubMed  CAS  Google Scholar 

  • Selldén G, Selstam E (1976) Changes in chloroplast lipids during the development of photosynthetic activity in barley etio-chloroplasts. Physiol Plant 37:35–41

    Article  Google Scholar 

  • 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 209–224

    Google Scholar 

  • 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 76:1036–1040

    Article  PubMed  CAS  Google Scholar 

  • 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 67:345–352

    Article  CAS  Google Scholar 

  • 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 70:209–214

    Article  CAS  Google Scholar 

  • Shibata K (1957) Spectroscopic studies on chlorophyll formation in intact leaves. J Biochem 44:147–173

    CAS  Google Scholar 

  • Smith H (ed) (1978) The molecular biology of plant cells. Botanical monographs. University of California Press, Berkeley

    Google Scholar 

  • Smith H (1982) Light quality photoreception and plant strategy. Annu Rev Plant Physiol 33:481–518

    Article  CAS  Google Scholar 

  • 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 377–416

    Chapter  Google Scholar 

  • Solymosi K, Böddi B (2006) Optical properties of bud scales and protochlorophyll(ide) forms in leaf primordia of closed and opened buds. Tree Physiol 26:1075–1085

    Article  PubMed  CAS  Google Scholar 

  • 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 151–202

    Google Scholar 

  • Solymosi K, Schoefs B (2010) Etioplast and etio-chloroplast formation under natural conditions: the dark side of chlorophyll biosynthesis in angiosperms. Photosynth Res 105:143–166

    Article  PubMed  CAS  Google Scholar 

  • 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 121:520–529

    Article  CAS  Google Scholar 

  • 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 26:1087–1096

    Article  PubMed  CAS  Google Scholar 

  • 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 8:627–635

    Article  PubMed  CAS  Google Scholar 

  • 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 12:649–658

    Article  PubMed  CAS  Google Scholar 

  • 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 10:283–296

    PubMed  CAS  Google Scholar 

  • Stetler DA, Laetsch WM (1969) Chloroplast development in Nicotiana tabacum ‘Maryland Mammoth’. Am J Bot 56:260–270

    Article  Google Scholar 

  • Sundqvist C, Dahlin C (1997) With chlorophyll pigments from prolamellar bodies to light-harvesting complexes. Physiol Plant 100:748–759

    Article  CAS  Google Scholar 

  • Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58:321–346

    Article  PubMed  CAS  Google Scholar 

  • Thelander M, Narita JO, Gruissem W (1986) Plastid differentiation and pigment biosynthesis during tomato fruit ripening. Curr Top Plant Biochem Physiol 5:128–141

    Google Scholar 

  • Treffry T (1970) Phytilation of chlorophyll(ide) and prolamellar body transformation in etiolated peas. Planta 91:279–284

    Article  CAS  Google Scholar 

  • Verbelen JP, De Greef JA (1979a) Leaf development of Phaseolus vulgaris L. in light and in darkness. Am J Bot 66:970–976

    Article  Google Scholar 

  • Verbelen JP, De Greef JA (1979b) De chloroplast-ontwikkeling bij Phaseolus vulgaris. Biologisch Jaarboek Dodonaea 47:123–129

    Google Scholar 

  • Vogelmann TC (1989) Penetration of light into plants. Photochem Photobiol 50:895–902

    Article  Google Scholar 

  • 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 12:625–634

    Article  Google Scholar 

  • von Wettstein D (1959) The formation of plastid structures. J Ultrastruct Res 3:234–240

    Article  Google Scholar 

  • von Wettstein D, Gough S, Kannangara CG (1995) Chlorophyll biosynthesis. Plant Cell 7:1039–1057

    Google Scholar 

  • 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 4:1072–1084

    Article  CAS  Google Scholar 

  • 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 127:2–22

    Google Scholar 

  • Waters M (2004) Plastid tubules in higher plants: an analysis of form and function. Ph.D. thesis, University of Nottingham, Nottingham

    Google Scholar 

  • Waters M, Pyke K (2004) Plastid development and differentiation. In: Moller SG (ed) Plastids, annual plant reviews. Blackwell/CRC Press, Oxford, pp 30–59

    Google Scholar 

  • Weier TE, Brown DL (1970) Formation of the prola­mellar body in 8-day, dark-grown seedlings. Am J Bot 57:267–275

    Article  Google Scholar 

  • Wellburn AR (1977) Distribution of chloroplast coupling factor (CF1) particles on plastid membranes during development. Planta 135:191–198

    Article  CAS  Google Scholar 

  • Wellburn AR (1982) Bioenergetic and ultrastructural changes associated with chloroplast development. Int Rev Cytol 80:133–191

    Article  CAS  Google Scholar 

  • Wellburn AR, Robinson DC, Wellburn FAM (1982) Chloroplast development in low-light grown barley seedlings. Planta 154:259–265

    Article  CAS  Google Scholar 

  • 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 211:846–854

    Article  PubMed  CAS  Google Scholar 

  • Whatley JM (1974) Chloroplast development in primary leaves of Phaseolus vulgaris. New Phytol 73:1097–1110

    Article  Google Scholar 

  • Whatley JM (1977a) The effect of cotyledons on chloroplast development in primary leaves of Phaseolus vulgaris. New Phytol 79:55–60

    Article  Google Scholar 

  • Whatley JM (1977b) Variations in the basic pathway of chloroplast development. New Phytol 78:407–420

    Article  Google Scholar 

  • Whatley JM (1992) Plastid development in distinctively coloured juvenile leaves. New Phytol 120:417–426

    Article  Google Scholar 

  • 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 29:205–218

    CAS  Google Scholar 

  • Wiktorsson B, Ryberg M, Sundqvist C (1996) Aggregation of NADPH-protochlorophyllide oxidoreductase pigment complexes is favoured by protein phosphorylation. Plant Physiol Biochem 34:23–34

    CAS  Google Scholar 

  • 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 3–26

    Chapter  Google Scholar 

  • Wrischer M (1966) Neubildung von Prolamellar­körpern in Chloroplasten. Z Pflanzenphysiol 55:296–299

    Google Scholar 

  • Wrischer M (1967) The effects of inhibitors of protein synthesis on the differentiation of plastids in etiolated bean seedlings. Planta 73:324–327

    Article  CAS  Google Scholar 

  • 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 95:336–346

    Article  CAS  Google Scholar 

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Acknowledgments

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.).

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Solymosi, K., Aronsson, H. (2013). Etioplasts and Their Significance in Chloroplast Biogenesis. In: Biswal, B., Krupinska, K., Biswal, U. (eds) Plastid Development in Leaves during Growth and Senescence. Advances in Photosynthesis and Respiration, vol 36. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5724-0_3

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