Tetrapyrroles pp 263-273 | Cite as

Regulation of the Late Steps of Chlorophyll Biosynthesis

  • Wolfhart Rüdiger
Part of the Molecular Biology Intelligence Unit book series (MBIU)


The regulatory network that controls formation of the various components of the photosynthetic machinery becomes evident when late steps of chlorophyll biosynthesis are investigated by deregulation. A major regulatory point is revealed by a dark-to-light shift revealing the interplay between the light dependent reduction of protochlorophyllide a to chlorophyllide a with phase transitions of plastid membranes and stable accumulation of chlorophyll a-binding proteins. The second part deals with chlorophyll b formation, details of which are controversially disputed in the literature. This is connected with the formation of nuclear-encoded proteins of light-harvesting complexes; expression of their genes, in turn, responds to plastid signals one of which is a chlorophyll precursor. Finally, a hypothetical role for carotenoids to maintain a well-regulated tetrapyrrole pathway will be discussed.


Chlorophyll Biosynthesis Prolamellar Body Protochlorophyllide Oxidoreductase Lhcb Gene Chlorophyll Precursor 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Domanskii V, Rüdiger W. On the nature of the two pathways in chlorophyll formation from protochlorophyllide//Photosynthesis Research. Photosynth Res 2001; 68:131–139.CrossRefPubMedGoogle Scholar
  2. 2.
    Domanskii V, Rassadina V, Gus-Mayer S et al. Characterization of two phases of chlorophyll formation during greening of etiolated barley leaves. Planta 2003; 216:475–483.PubMedGoogle Scholar
  3. 3.
    Schmid HC, Rassadina V, Oster U et al. Preloading of chlorophyll synthase with tetraprenyl diphosphate is an obligatory step in chlorophyll biosynthesis. Biol Chem 2002; 383:1769–1776.CrossRefPubMedGoogle Scholar
  4. 4.
    Oliver RP, Griffiths T. Pigment-protein complexes of illuminated etiolated leaves. Plant Physiol 1982; 70:1019–1025.CrossRefPubMedGoogle Scholar
  5. 5.
    Keller Y, Bouvier FD, Harlingue A. Metabolic compartmentation of plastid prenyllipid biosynthesis-Evidence for the involvement of a multifunctional geranylgeranyl reductase. Eur J Biochem 1998; 251:413–417.CrossRefPubMedGoogle Scholar
  6. 6.
    Schmid HC, Oster U, Kögel J et al. Cloning and characterisation of chlorophyll synthase from Avena sativa. Biol Chem 2001; 382:903–911.CrossRefPubMedGoogle Scholar
  7. 7.
    Benz J, Fischer I, Rüdiger W. Determination of phythyl diphosphate and geranylgeranyldiphosphate in etiolated oat seedlings. Phytochemistry 1983; 22:2801–2804.CrossRefGoogle Scholar
  8. 8.
    Schoefs B, Bertrand M. The formation of chlorophyll from chlorophyllide in leaves containing proplastids is a four-step process. FEBS Lett 2000; 486:243–246.CrossRefPubMedGoogle Scholar
  9. 9.
    Tanaka, R, Oster U, Kruse E et al. Reduced activity of geranylgeranyl reductase leads to loss of chlorophyll and tocopherol and to partially geranylgeranylated Chlorophyll in transgenic tobacco plants expressing antisense RNA for geranylgeranyl reductase. Plant Physiol 1999; 120:695–704.CrossRefPubMedGoogle Scholar
  10. 10.
    Benz J, Haser A, Rüdiger W. Changes in the endogenous pools of tetraprenyl diphosphates in etiolated oat seedlings after irradiation. Z Pflanzenphysiol 1983; 111:349–356.Google Scholar
  11. 11.
    Benz J, Hampp R, Rüdiger W. Chlorophyll biosynthesis by Mesophyll protoplasts and plastids from etiolated oat (Avena sativa L.) leaves. Planta 1981; 152:54–58.CrossRefGoogle Scholar
  12. 12.
    Eichacker LA, Soll J, Lauterbach P et al. In vitro synthesis of Chlorophyll a in the dark triggers accumulation of Chlorophyll a apoproteins in barley etioplasts. J Biol Chem 1990; 265:13566–13571PubMedGoogle Scholar
  13. 13.
    Kim J, Eichacker LA, Rüdiger W et al. Chlorophyll regulates accumulation of the plastid-encoded chlorophyll proteins P700 and Dl by increasing apoprotein stability. Plant Physiol 1994; 104:907–916.CrossRefPubMedGoogle Scholar
  14. 14.
    Eichacker LA, Helfrich M, Rüdiger W et al. Stabilization of chlorophyll a-binding apoproteins P700, CP47, CP43, D2, and Dl by chlorophyll a or Zn-pheophytin a. J Biol Chem 1996; 271:32174–32179.CrossRefPubMedGoogle Scholar
  15. 15.
    Böddi B, Lindsten A, Ryberg M et al. On the aggregational states of protochlorophyllide and its protein complexes in wheat etioplasts. Physiol. Plant 1989; 76:135–143.CrossRefGoogle Scholar
  16. 16.
    Böddi B, Lindsten A, Ryberg M et al. Phototransformation of aggregated forms of protochlorophyllide in isolated etioplast inner membranes. Photochem Photobiol 1990; 52:83–87.CrossRefGoogle Scholar
  17. 17.
    Ryberg M, Dehesh K. 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 1986; 66:616–624.CrossRefGoogle Scholar
  18. 18.
    Zhong LB, Wiktorsson B, Ryberg M et al. The Shibata shift: Effects of in vitro conditions on the spectral blue shift of chlorophyllide in irradiated isolated prolamellar bodies. J Photochem Photobiol B Biol 1996; 36:263–270.CrossRefGoogle Scholar
  19. 19.
    Selstam E, Widell Wigge A. Chloroplast lipids and the assembly of membranes. In: Sundqvist C, Ryberg M, eds. Pigment-protein complexes in plastids, synthesis and assembly. San Diego: Academic Press, 1993:241–277.Google Scholar
  20. 20.
    Lindsten A, Welch CJ, Schoch S et al. Chlorophyll synthetase is latent in well preserved prolamellar bodies of etiolated wheat. Physiol Plant 1990; 80:277–285.CrossRefGoogle Scholar
  21. 21.
    Reinbothe C, Lebedev N, Reinbothe S. A protochlorophyllide light-harvesting complex involved in detiolation of higher plants. Nature 1999; 397:80–84.CrossRefGoogle Scholar
  22. 22.
    Reinbothe S, Pollmann S, Reinbothe C. In situ conversion of protochlorophyllide b to protochlorophyllide a in barley. J Biol Chem 2003; 278:800–806.CrossRefPubMedGoogle Scholar
  23. 23.
    Tanaka A, Ito H, Tanaka R et al. Chlorophyll a oxygenase (CAO) is involved on chlorophyll b formation from chlorophyll a. Proc. Natl Acad Sci USA 1998; 95:12719–12723.CrossRefPubMedGoogle Scholar
  24. 24.
    Espineda CE, Linford AS, Devine D et al. The AtCAO gene, encoding chlorophyll a oxygenase, is required for chlorophyll b synthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 1999; 96:10507–10511.CrossRefPubMedGoogle Scholar
  25. 25.
    Oster U, Tanaka R, Tanaka A et al. Cloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis (CAO) from Arabidopsis thaliana. Plant J 2000; 21:305–310.CrossRefPubMedGoogle Scholar
  26. 26.
    Rüdiger W. Biosynthesis of chlorophyll b and the chlorophyll cycle. Photosynth. Res 2002; 74:187–193.CrossRefPubMedGoogle Scholar
  27. 27.
    Tanaka R, Koshino Y, Sawa S et al. Overexpression of chlorophyllide a oxygenase (CAO) enlarges the antenna size of photosystem II in Arabidopsis thaliana. Plant J 2001; 26:365–373.CrossRefPubMedGoogle Scholar
  28. 28.
    Satoh S, Ikeuchi M, Mimuro M et al. Chlorophyll b expressed in cyanobacteria functions as a light-harvesting antenna in photosystem I through flexibility of the proteins. J Biol Chem 2001; 276:4293–4297.CrossRefPubMedGoogle Scholar
  29. 29.
    Xu H, Vavilin D, Vermaas W. Chlorophyll b can serve as the major pigment in functional photo-system II complexes of cyanobacteria. Proc Natl Acad Sci USA 2001; 98:14168–14173.CrossRefPubMedGoogle Scholar
  30. 30.
    Xu H, Vavilin D, Vermaas W. The presence of chlorophyllb in Synechocystis sp. PCC. J Biol Chem 2002; 277:42726–42732.CrossRefPubMedGoogle Scholar
  31. 31.
    Rodermel S. Pathways of plastid-to-nucleus signalling. Trends Plant Sci 2001; 6:471–478.CrossRefPubMedGoogle Scholar
  32. 32.
    Strand A, Asami T, Alonso J et al. Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 2003; 421:79–83.CrossRefPubMedGoogle Scholar
  33. 33.
    Kittsteiner U, Brunner H, Rüdiger W. The greening process in cress seedlings. II. Complexing agents and 5-aminolevulinate inhibit accumulation of cab-mRNA coding for the light-harvesting chlorophyll a/b protein. Physiol Plant 1991; 81:190–196.CrossRefGoogle Scholar
  34. 34.
    La Rocca N, Rascio N, Oster U et al. Amitrole treatment of etiolated barley seedlings leads to deregulation of tetrapyrrole synthesis and to reduced expression of Lhc and RbcS genes. Planta 2001; 213:101–108.CrossRefPubMedGoogle Scholar
  35. 35.
    Kropat J, Oster U, Rüdiger W et al. Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heat-shock genes. Proc Natl Acad Sci USA 1997; 94:14168–14172.CrossRefPubMedGoogle Scholar
  36. 36.
    Kropat J, Oster U, Rüdiger W et al. Chloroplast signalling in the light induction of nuclear HSP70 genes requires the accumulation of chlorophyll precursors and their accessibility to cytoplasm/nucleus. Plant J 2000; 24:523–531.CrossRefPubMedGoogle Scholar
  37. 37.
    Schroda M, Kropat J, Oster U et al. Possible role for molecular chaperones in assembly and repair of photosystem IL Biochem. Soc Trans 2001; 29:413–418.Google Scholar
  38. 38.
    Pöpperl G, Oster U, Rüdiger W. Light-dependent increase in chlorophyll precursors during the day-night cycle in tobacco and barley seedlings. J Plant Physiol 1998; 153:40–45.Google Scholar
  39. 39.
    Sullivan JA, Gray JC. Plastid translation is required for the expression of nuclear photosynthesis genes in the dark and in roots of the pea lip 1 mutant. Plant Cell 1999; 11:901–910.CrossRefPubMedGoogle Scholar
  40. 40.
    Maxwell DP, Laudenbach DE, Huner NPA. Redox regulation of light-harvesting complex II and cab mRNA abundance in Dunaliella salina. Plant Physiol 1995; 109:787–795.PubMedGoogle Scholar
  41. 41.
    Escoubas JM, Lomas M, La Roche J et al. Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proc Natl Acad Sci USA 1995; 92:10237–10241.CrossRefPubMedGoogle Scholar
  42. 42.
    Streatfield SJ, Weber A, Konsman EA et al. The phosphoenolpyruvate/phosphate translocator is required for phenolic metabolism, palisade cell development and plastid-dependent nuclear gene expression. Plant Cell 1999; 11:1609–1622.CrossRefPubMedGoogle Scholar
  43. 43.
    Karpinski S, Reynolds H, Karpinska B et al. Systemic signalling and acclimation in response to excess excitation energy in Arabidopsis. Science 1999; 284:654–657.CrossRefPubMedGoogle Scholar
  44. 44.
    Hörtensteiner S, Vicentini F, Matile P. Chlorophyll breakdown in senescent cotyledons of rape, Brassica napus L: Enzymatic cleavage of phaeophorbide a in vitro. New Phytol 1995; 129:237–246.CrossRefGoogle Scholar
  45. 45.
    Kräutler B, Matile P. Solving the riddle of chlorophyll breakdown. Acc Chem Res 1999; 32:35–43.CrossRefGoogle Scholar
  46. 46.
    Gossauer A, Engel N. New trends in photobiology: Chlorophyll catabolism—structures, mechanisms, conversions. J Photochem Photobiol B 1996; 32:141–151.CrossRefGoogle Scholar
  47. 47.
    Scheumann V, Klement H, Helfrich M et al. Protochlorophyllide b does not occur in barley etioplasts. FEBS Lett 1999; 445:445–448.CrossRefPubMedGoogle Scholar
  48. 48.
    Armstrong GA, Apel K, Rüdiger W. Does a light-harvesting protochlorophyllide a/b-binding protein complex exist? Trends Plant Sci 2000; 5:40–44.CrossRefPubMedGoogle Scholar
  49. 49.
    Reinbothe C, Buhr F, Pollmann S et al. In vitro reconstitution of light-harvesting POR-protochlorophyllide complex with protochlorophyllides a and b. J Biol Chem 2003; 278:807–815.CrossRefPubMedGoogle Scholar
  50. 50.
    Schoch S, Helfrich M, Wiktorsson B et al. Photoreduction of Zinc-protopheophorbide b with NADPH-protochlorophyllide oxidoreductase from etiolated wheat (Triticum aestivum L.). Eur J Biochem 1995; 229:291–298.CrossRefPubMedGoogle Scholar
  51. 51.
    Helfrich M, Schoch S, Schäfer W et al. Absolute configuration of protochlorophyllide alpha and substrate specificity of NADPH-protochlorophyllide oxidoreductase. J Am Chem Soc 1996; 118:2606–2611.CrossRefGoogle Scholar
  52. 52.
    Kolossov VL, Rebeiz CA. Chloroplast biogenesis 88. Protochlorophyllide b occurs in green but not in etiolated plants. J Biol Chem 2003; 278:49675–49678.CrossRefPubMedGoogle Scholar
  53. 53.
    Paulsen H, Schmid VHR. Analysis and reconstitution of chlorophyll proteins. In: Witty M, Smith AG, eds. Analytical Methods in Heme, Chlorophyll, and Related Molecules. Natick: Eaton Publishing, 2001:235–254.Google Scholar
  54. 54.
    Böger P. Mode of action of herbicides affecting carotenogenesis. J Pesticide Sci 1996; 21:473–478.Google Scholar
  55. 55.
    Rassadina V, Domanskii V, Averina NG et al. Correlation between chlorophyllide esterification, Shibata shift and regeneration of protochlorophyllide650 in flash-irradiated etiolated barley leaves. Physiol Plant 2004; 121:556–567.CrossRefGoogle Scholar
  56. 56.
    Rocca NL, Rascio N, Oster U et al. Inhibition of lycopene cylase results in accumulation of chlorophyll precursors. Planta 2007; 225:1019–1029.CrossRefPubMedGoogle Scholar
  57. 57.
    Moulin M, McCormac AC, Terry MJ et al. Tetrapyrrole profiling in Arabidopsis seedlings reveals that retrograde plastid nuclear signaling is not due to Mg-protoporphyrin IX accumulation. Proc Natl Acad Sci USA 2008; 105:15178–15183.CrossRefPubMedGoogle Scholar
  58. 58.
    Mochizuki N, Tanaka R, Tanaka A et al. The steady-state level of Mg-protoporphyrin IX is not a determinant of plastid-to-nucleus signaling in Arabidopsis. Proc Natl Acad Sci USA 2008; 105:15184–15189.CrossRefPubMedGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2009

Authors and Affiliations

  1. 1.Department Biologie I, BotanikUniversität MünchenMünchenGermany

Personalised recommendations