Skip to main content
Log in

Photoactive pigment—enzyme complexes of chlorophyll precursor in plant leaves

  • Review
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

This review summarizes contemporary data on structure and function of photoactive pigment—enzyme complexes of the chlorophyll precursor that undergoes photochemical transformation to chlorophyllide. The properties and functions of the complex and its principal components are considered including the pigment (protochlorophyllide), the hydrogen donor (NADPH), and the photoenzyme protochlorophyllide oxidoreductase (POR) that catalyzes the photochemical production of chlorophyllide. Chemical variants of the chlorophyll precursor are described (protochlorophyllide, protochlorophyll, and their mono- and divinyl forms). The nature and photochemical activity of spectrally distinct native protochlorophyllide forms are discussed. Data are presented on structural organization of the photoenzyme POR, its substrate specificity, localization in etioplasts, and heterogeneity. The significance of different POR forms (PORA, PORB, and PORC) in adaptation of chlorophyll biosynthesis to various illumination conditions is considered. Attention is paid to structural and functional interactions of three main constituents of the photoactive complex and to possible existence of additional components associated with the pigment-enzyme complex. Historical aspects of the problem and the prospects of further investigations are outlined.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

Pchl:

protochlorophyll

Pchlide:

protochlorophyllide

PLB:

prolamellar bodies

POR:

protochlorophyllide oxidoreductase

PS1, PS2:

photosystems 1 and 2, respectively

References

  1. Fischer, H. (1940) Naturwissenschaften, 28, 401–405.

    CAS  Google Scholar 

  2. Ficher, H., and Oestreicher, A. (1940) Z. Physiol. Chem., 262, 243.

    Google Scholar 

  3. Ficher, H., Mittenzwei, H., and Oestreicher, A. (1939) Z. Physiol. Chem., 257, IV.

    Google Scholar 

  4. Belyaeva, O. B. (2003) Photosynth. Res., 76, 405–411.

    PubMed  CAS  Google Scholar 

  5. Lyubimenko, V. N. (1923) Izv. Ros. Akad. Nauk, Ser. 6, 17, 129.

    Google Scholar 

  6. Lyubimenko, V. N., and Gyubbenet, E. K. (1930) Izv. Estestv.-Nauch. Inst. Lesgafta, 16, 165.

    Google Scholar 

  7. Smith, J. H. C. (1948) Arch. Biochem., 19, 449–454.

    PubMed  CAS  Google Scholar 

  8. Smith, J. H. C. (1952) Year Book Carneg. Inst., 51, 151.

    Google Scholar 

  9. Krasnovsky, A. A., and Kosobutskaya, L. M. (1952) Dokl. Akad. Nauk SSSR, 85, 177–180.

    Google Scholar 

  10. Kosobutskaya, L. M., and Krasnovsky, A. A. (1954) Biokhimiya, 19, 37–44.

    CAS  Google Scholar 

  11. Smith, J. H. C., and Benitez, A. (1953) Carnegie Inst. Wash. Year Book, 52, 151–153.

    Google Scholar 

  12. Smith, J. H. C., and Benitez, A. (1954) Plant Physiol., 29, 135–143.

    PubMed  CAS  Google Scholar 

  13. Smith, J. H. C., and Kupke, D. W. (1956) Nature, 178, 751–752.

    CAS  Google Scholar 

  14. Smith, J. H. C., Kupke, D. W., and Giese, A. T. (1956) Carn. Inst. Wash. Yearly Book, 55, 243–245.

    Google Scholar 

  15. Smith, J. H. C. (1960) in Comparative Biochemistry of Photoreactive Systems (Allen, M. B., ed.) Academic Press, New York, pp. 257–277.

    Google Scholar 

  16. Smith, J. H. C. (1961) in Biological Structure and Function, Vol. 2 (Goodwin, T. W., and Linberg, O., eds.) Academic Press, London, pp. 325–338.

    Google Scholar 

  17. Boardman, N. K. (1962) Biochim. Biophys. Acta, 62, 63–79.

    PubMed  CAS  Google Scholar 

  18. Wolf, J. B., and Price, L. (1956) Plant Physiol., 31, 31.

    Google Scholar 

  19. Godnev, T. N., Shlyk, A. A., and Lyakhnovich, Ya. P. (1957) Fiziol. Rast., 4, 393–400.

    CAS  Google Scholar 

  20. Griffiths, W. T. (1974) FEBS Lett., 46, 301–304.

    PubMed  CAS  Google Scholar 

  21. Griffiths, W. T. (1975) Biochem. J., 152, 623–635.

    PubMed  CAS  Google Scholar 

  22. Griffiths, W. T., and Mapleston, R. E. (1978) in Chloroplast Development (Akoyunoglou, G., and Argyroudi-Akoyunoglou, J. H., eds.) Amsterdam, pp. 99–104.

  23. Griffiths, W. T. (1978) Biochem. J., 174, 681–692.

    PubMed  CAS  Google Scholar 

  24. Suzuki, J. Y., and Bauer, C. E. (1995) Proc. Natl. Acad. Sci. USA, 92, 3749–3753.

    PubMed  CAS  Google Scholar 

  25. Fujita, Y. (1996) Plant. Cell. Physiol., 37, 411–421.

    PubMed  CAS  Google Scholar 

  26. Armstrong, G. A. (1998) J. Photochem. Photobiol. B, 43, 87–100.

    CAS  Google Scholar 

  27. Oliver, R. P., and Griffiths, W. T. (1980) Biochem. J., 191, 277–280.

    PubMed  CAS  Google Scholar 

  28. Apel, K., Santel, H. J., Redlinger, T. E., and Falk, H. (1980) Eur. J. Biochem., 111, 251–258.

    PubMed  CAS  Google Scholar 

  29. Oliver, R. P., and Griffiths, W. T. (1981) Biochem. J., 195, 93–101.

    PubMed  CAS  Google Scholar 

  30. Apel, K. (1981) Eur. J. Biochem., 120, 89–93.

    PubMed  CAS  Google Scholar 

  31. Teakle, R., and Griffiths, W. T. (1993) Biochem. J., 296, 225–230.

    PubMed  CAS  Google Scholar 

  32. Reinbothe, S., Reinbothe, C., Lebedev, N., and Apel, K. (1996) Plant Cell, 8, 763–769.

    PubMed  CAS  Google Scholar 

  33. Baker, M. E. (1994) Biochem. J., 300, 605–607.

    PubMed  CAS  Google Scholar 

  34. Wilks, H. M., and Timko, M. P. (1995) Proc. Natl. Acad. Sci. USA, 92, 724–728.

    PubMed  CAS  Google Scholar 

  35. Birve, S., Selstam, E., and Johansson, L. (1996) Biochem. J., 317, 549–555.

    PubMed  CAS  Google Scholar 

  36. Labesse, G., Vidal-Cros, A., Chomilie, J., Gaudry, M., and Morno, J. P. (1994) Biochem. J., 304, 95–99.

    PubMed  CAS  Google Scholar 

  37. Jornvall, H., Persson, B, Krook, M., Atrian, S., Gonzalez-Duarte, R., Jeffery, J., and Ghosh, D. (1995) Biochemistry, 34, 6003–6013.

    PubMed  CAS  Google Scholar 

  38. Tanaka, N., Nonaka, T., Tanabe, T., Yoshimoto, T., Tsuru, D., and Mitsui, Y. (1996) Biochemistry, 35, 7715–7730.

    PubMed  CAS  Google Scholar 

  39. Tanaka, N., Nonaka, T., Nakanishi, M., Deyashiki, Y., Hara, A., and Mitsui, Y. (1996) Structure, 4, 33–45.

    PubMed  CAS  Google Scholar 

  40. Townley, H. E., Sessions, R. B., Clarke, A. R., Dafforn, T. R., and Griffiths, W. T. (2001) Proteins, 44, 329–335.

    PubMed  CAS  Google Scholar 

  41. Schultz, R., Steinmuller, K., Klaas, M., Forreiter, C., Rasmussen, S., Hiller, C., and Apel, A. (1989) Genetics, 217, 355–361.

    Google Scholar 

  42. Oliver, R. P., and Griffiths, W. T. (1982) Plant Physiol., 70, 1019–1025.

    PubMed  CAS  Google Scholar 

  43. Griffiths, W. T. (1980) Biochem. J., 186, 267–278.

    PubMed  CAS  Google Scholar 

  44. Dahlin, C., Aronsson, H., Wilks, H. M., Lebedev, N., Sundqvist, C., and Timko, M. (1999) Plant Mol. Biol., 39, 309–323.

    PubMed  CAS  Google Scholar 

  45. Wiktorsson, B., Engdahl, S., Zhong, L. B., Boddi, B., Ryberg, M., and Sundqvist, C. (1993) Photosynthetica, 29, 205–218.

    CAS  Google Scholar 

  46. Martin, G. E. M., Timko, M. P., and Wilks, H. M. (1997) Biochem. J., 325, 139–145.

    PubMed  CAS  Google Scholar 

  47. Griffiths, W. T., McHugh, T., and Blankenship, R. E. (1996) FEBS Lett., 398, 235–238.

    PubMed  CAS  Google Scholar 

  48. Lebedev, N., and Timko, M. (1999) Proc. Natl. Acad. Sci. USA, 96, 17954–17959.

    Google Scholar 

  49. Klement, H., Helfrich, M., Oster, U., Schoch, S., and Rudiger, W. (1999) Eur. J. Biochem., 265, 862–874.

    PubMed  CAS  Google Scholar 

  50. Heyes, D. J., and Hunter, C. N. (2002) Biochem. Soc. Trans., 30, 601–604.

    PubMed  CAS  Google Scholar 

  51. Lebedev, N., Karginova, O., McIvor, W., and Timko, M. (2001) Biochemistry, 40, 12562–12574.

    PubMed  CAS  Google Scholar 

  52. Schoefs, B., and Franck, F. (2003) Photochem. Photobiol., 78, 543–557.

    PubMed  CAS  Google Scholar 

  53. Horton, P., and Leech, R. M. (1975) Plant Physiol., 56, 113–120.

    PubMed  CAS  Google Scholar 

  54. Schoch, S., Helfrich, M., Wiktorsson, B., Sundqvist, C., Rudiger, W., and Ryberg, M. (1995) Eur. J. Biochem., 229, 291–298.

    PubMed  CAS  Google Scholar 

  55. Griffiths, W. T. (1991) in Chlorophyll (Sheer, H., ed.) CRC Press, Boca Raton, FL, pp. 433–450.

    Google Scholar 

  56. Kotzabasis, K., Schuring, M. P., and Senger, H. (1989) Physiol. Plant., 75, 221–226.

    CAS  Google Scholar 

  57. Ignatov, N. V., and Litvin, F. F. (1995) Biochemistry (Moscow), 60, 1429–1438.

    Google Scholar 

  58. Ignatov, N. V., and Litvin, F. F. (1996) Photosynth. Res., 50, 271–283.

    CAS  Google Scholar 

  59. Bjorn, L. O. (1963) Physiol. Plant., 16, 142–150.

    CAS  Google Scholar 

  60. Bjorn, L. O. (1969) Physiol. Plant., 22, 1–17.

    CAS  Google Scholar 

  61. Rebeiz, C. A., Yaghi, M., Abou-Haidar, M., and Castelfranco, P. A. (1970) Plant Physiol., 46, 57–63.

    PubMed  CAS  Google Scholar 

  62. Lang, F., Vorobyeva, L. M., and Krasnovsky, A. A. (1971) Mol. Biol. (Moscow), 5, 366–374.

    CAS  Google Scholar 

  63. Cohen, C. E., and Schiff, J. A. (1976) Photochem. Photobiol., 24, 555–566.

    PubMed  CAS  Google Scholar 

  64. Belanger, F. C., and Rebeiz, C. A. (1980) J. Biol. Chem., 255, 1266–1272.

    PubMed  CAS  Google Scholar 

  65. Belanger, F. C., and Rebeiz, C. A. (1980) Biochemistry, 19, 4875–4883.

    PubMed  CAS  Google Scholar 

  66. Belanger, F. C., and Rebeiz, C. A. (1980) Plant Sci. Lett., 18, 343–350.

    CAS  Google Scholar 

  67. Chereskin, B. M., Wong, Y. S., and Castelfranco, P. A. (1982) Plant Physiol., 70, 987–993.

    PubMed  CAS  Google Scholar 

  68. Belanger, F. C., and Rebeiz, C. A. (1985) J. Biol. Chem., 255, 1266–1272.

    Google Scholar 

  69. Whyte, B. J., and Griffiths, W. T. (1993) Biochem. J., 291, 939–944.

    PubMed  CAS  Google Scholar 

  70. Adra, A. N., and Rebeiz, C. A. (1998) Photochem. Photobiol., 68, 852–856.

    CAS  Google Scholar 

  71. Bombart, P., and Dujardin, E. (1984) in Protochlorophyllide Reduction and Greening (Sironval, C., and Brouers, M., eds.) Martinus Nijhoff/Dr. Junk Publishers, The Hague, pp. 175–179.

    Google Scholar 

  72. Krasnovsky, A. A., Bistrova, M. I., and Safronova, I. A. (1984) in Protochlorophyllide Reduction and Greening (Sironval, C., and Brouers, M., eds.) Martinus Nijhoff/Dr. Junk Publishers, The Hague, pp. 331–339.

    Google Scholar 

  73. Helfrich, M., Schoch, S., Schafer, W., Ryberg, M., and Rudiger, W. (1996) J. Am. Chem. Soc., 118, 2606–2611.

    CAS  Google Scholar 

  74. Nakamura, A., and Watanabe, T. (1998) FEBS Lett., 426, 201–204.

    PubMed  CAS  Google Scholar 

  75. Ikeuchi, M., and Murakami, S. (1982) Plant Cell Physiol., 23, 575–583.

    CAS  Google Scholar 

  76. Ikeuchi, M., and Murakami, S. (1982) Plant Cell Physiol., 23, 1089–1099.

    CAS  Google Scholar 

  77. Ryberg, M., and Sundqvist, C. (1982) Physiol. Plant., 56, 125–132.

    CAS  Google Scholar 

  78. Selstam, E. A., Widell, A., and Johansson, L. B. (1987) Physiol. Plant., 70, 209–214.

    CAS  Google Scholar 

  79. Benli, M., Schulz, R., and Apel, K. (1991) Plant Mol. Biol., 16, 615–625.

    PubMed  CAS  Google Scholar 

  80. Dehesh, K., Klaas, M., Hauser, I., and Apel, K. (1986) Planta, 169, 162–171.

    CAS  Google Scholar 

  81. Armstrong, G., Runge, S., Frick, G., Sperling, U., and Apel, K. (1995) Plant Physiol., 108, 1505–1517.

    PubMed  CAS  Google Scholar 

  82. Holtorf, H., Reinbothe, S., Reinbothe, C., Bereza, B., and Apel, K. (1995) Proc. Natl. Acad. Sci. USA, 92, 3254–3258.

    PubMed  CAS  Google Scholar 

  83. Frick, G., Su, Q., Apel, K., and Armstrong, G. A. (2003) Plant J., 35, 141–153.

    PubMed  CAS  Google Scholar 

  84. Sperling, U., van Cleve, B., Frick, G., Apel, K., and Armstrong, G. A. (1997) Plant J., 12, 649–658.

    PubMed  CAS  Google Scholar 

  85. Sperling, U., Franck, F., van Cleve, B., Frick, G., Apel, K., and Armstrong, G. A. (1998) Plant Cell, 10, 283–296.

    PubMed  CAS  Google Scholar 

  86. Sperling, U., Frick, G., van Cleve, B., and Apel, K. (1999) in The Chloroplast: From Molecular Biology to Biotechnology (Argyroudi-Akoyunoglou, J. H., and Senger, H., eds.) Kluwer, Dordrecht, pp. 97–102.

    Google Scholar 

  87. Franck, F., Sperling, U., Frick, G., Pochert, B., van Cleve, B., Apel, K., and Armstrong, G. A. (2000) Plant Physiol., 124, 1678–1696.

    PubMed  CAS  Google Scholar 

  88. Santel, H.-J., and Apel, K. (1981) Eur. J. Biochem., 120, 95–103.

    PubMed  CAS  Google Scholar 

  89. Reinbothe, C., Apel, K., and Reinbothe, S. (1995) Mol. Cell. Biol., 15, 6206–6212.

    PubMed  CAS  Google Scholar 

  90. Reinbothe, S., Reinbothe, C., Apel, K., and Lebedev, N. (1996) Cell, 86, 703–705.

    PubMed  CAS  Google Scholar 

  91. Schunmann, P. H., and Ougham, H. J. (1996) Plant. Mol. Biol., 31, 529–537.

    PubMed  CAS  Google Scholar 

  92. Skinner, J. S., and Timko, M. P. (1998) Plant Cell Physiol., 39, 795–806.

    PubMed  CAS  Google Scholar 

  93. Kaneko, T., Sato, S., Kotani, H., Tanaka, A., Asamizu, E., Nakamura, Y., Miyajima, N., Hirosawa, M., Sugiura, M., Sasamoto, S., Kimura, T., Hosouchi, T., Matsuno, A., Muraki, A., Nakazaki, N., Naruo, K., Okamura, S., Shimpo, S., Takeuchi, C., Wada, T., Watanabe, A., Yamada, M., Ysaduda, M., and Tabata, S. (1996) DNA Res., 3, 109–136.

    PubMed  CAS  Google Scholar 

  94. Heyes, D. J., Martin, G. E. M., Reid, R. T., Hunter, C. N., and Wilks, H. M. (2000) FEBS Lett., 483, 47–51.

    PubMed  CAS  Google Scholar 

  95. Li, J., and Timko, M. P. (1996) Plant Mol. Biol., 30, 15–37.

    PubMed  CAS  Google Scholar 

  96. Kuroda, H., Masuda, T., Fusada, N., Ohta, H., and Takamiya, K. (2000) Plant Cell Physiol., 41, 226–229.

    PubMed  CAS  Google Scholar 

  97. Spano, A. J., He, Z., Michel, H., Hunt, D. F., and Timko, M. P. (1992) Plant Mol. Biol., 18, 967–972.

    PubMed  CAS  Google Scholar 

  98. Oosawa, N., Masuda, T., Awai, K., Fusada, N., Shimada, H., Ohta, H., and Takamiya, K. (2000) FEBS Lett., 474, 133–136.

    PubMed  CAS  Google Scholar 

  99. Su, Q., Frick, G., Armstrong, G., and Apel, K. (2001) Plant Mol. Biol., 47, 805–813.

    PubMed  CAS  Google Scholar 

  100. Kuroda, H., Masuda, T., Fusada, N., Ohta, H., and Takamiya, K. (1995) Plant Cell Physiol., 41, 226–229.

    Google Scholar 

  101. Takio, S., Nakao, N., Suzuki, T., Tanaka, K., Yamamoto, I., and Satoh, T. (1998) Plant Cell Physiol., 39, 665–669.

    PubMed  CAS  Google Scholar 

  102. Masuda, T., Fusada, N., Oosawa, N., Takamatsu, K., Yamamoto, Y. Y., Ohta, M., Nakamura, K., Goto, K., Shibata, D., Shirano, Y., Hayashi, H., Kato, T., Tabata, S., Shimada, H., Ohta, H., and Takamiya, K. (2003) Plant Cell Physiol., 44, 963–974.

    PubMed  CAS  Google Scholar 

  103. He, Z. H., Li, J., Sundqvist, C., and Timko, M. P. (1994) Plant Physiol., 106, 537–546.

    PubMed  CAS  Google Scholar 

  104. Yoshida, K., Chen, R. M., Tanaka, A., Teramoto, H., Tanaka, R., Timko, M. P., and Tsuji, H. (1995) Plant Physiol., 109, 231–238.

    PubMed  CAS  Google Scholar 

  105. Boardman, N. K., and Anderson, J. M. (1964) Aust. J. Biol. Sci., 17, 86–92.

    CAS  Google Scholar 

  106. Leyon, H. (1953) Exp. Cell. Res., 5, 520–529.

    PubMed  CAS  Google Scholar 

  107. Von Wettstein, D. (1959) in Developmental Cytology (Rudnick, D., ed.) Ronald Press, New York, pp. 123–160.

    Google Scholar 

  108. Ryberg, M., and Sundqvist, C. (1982) Physiol. Plant., 56, 125–132.

    CAS  Google Scholar 

  109. Ryberg, M., and Sundqvist, C. (1982) Physiol. Plant., 56, 133–138.

    CAS  Google Scholar 

  110. Lindsten, A., Ryberg, M., and Sundqvist, C. (1988) Physiol. Plant., 72, 167–176.

    CAS  Google Scholar 

  111. Shaw, P. J., Henwood, J. A., Oliver, R. P., and Griffiths, W. T. (1985) Eur. J. Cell Biol., 39, 50–55.

    Google Scholar 

  112. Ryberg, M., and Dehesh, K. (1986) Physiol. Plant., 66, 616–624.

    CAS  Google Scholar 

  113. Klein, S., and Schiff, J. A. (1972) Plant Physiol., 49, 619–626.

    PubMed  CAS  Google Scholar 

  114. Rowe, J. D., and Griffiths, W. T. (1981) Biochem. J., 311, 417–424.

    Google Scholar 

  115. Schultz, R., Steinmuller, K., Klaas, M., Forreiter, C., Rasmussen, S., Hiller, C., and Apel, K. (1989) Mol. Gen. Genet., 217, 355–361.

    Google Scholar 

  116. Darrah, P. M., Kay, S. A., Teakle, G. R., and Griffiths, W. T. (1990) Biochem. J., 265, 789–798.

    PubMed  CAS  Google Scholar 

  117. Joyard, J., Block, M., Pineau, B., Albrieux, C., and Douce, R. (1990) J. Biol. Chem., 265, 21820–21827.

    PubMed  CAS  Google Scholar 

  118. Pineau, B., Gerard-Hirne, C., Douce, R., and Joyard, J. (1993) Plant Physiol., 102, 821–828.

    PubMed  CAS  Google Scholar 

  119. Dahlin, C., Sundqvist, C., and Timko, M. P. (1995) Plant Mol Biol., 29, 317–330.

    PubMed  CAS  Google Scholar 

  120. Masuda, T., and Takamiya, K. (2004) Photosynth. Res., 81, 1–29.

    PubMed  CAS  Google Scholar 

  121. Savchenko, G. E., Abramchik, L. M., Serdyuchenko, E. V., and Chaika, M. T. (1989) Dokl. Akad. Nauk Bel. SSR, 33, 660–663.

    CAS  Google Scholar 

  122. Pineau, B., Dubertret, G., Joyard, J., and Douce, R. (1986) J. Biol. Chem., 261, 9210–9215.

    PubMed  CAS  Google Scholar 

  123. Aronsson, H., Sundqvist, C., Timko, M. P., and Dahlin, C. (2001) FEBS Lett., 502, 11–15.

    PubMed  CAS  Google Scholar 

  124. Aronsson, H., Sundqvist, C., and Dahlin, C. (2003) Plant Mol. Biol., 51, 1–7.

    PubMed  CAS  Google Scholar 

  125. Dahlin, C., Aronsson, H., Wilks, H. M., Lebedev, N., Sundqvist, C., and Timko, M. (1999) Plant Mol. Biol., 39, 309–323.

    PubMed  CAS  Google Scholar 

  126. Godnev, T. N., Galaktionov, S. G., and Raskin, V. I. (1968) Dokl. Akad. Nauk SSSR, 181, 237–240.

    PubMed  CAS  Google Scholar 

  127. Bjorn, L. O. (1963) Physiol. Plant., 16, 142–150.

    CAS  Google Scholar 

  128. Boardman, N. K. (1966) in The Chlorophylls (Vernon, L. P., and Seely, G. R., eds.) Academic Press, New York, pp. 437–479.

    Google Scholar 

  129. Lang, F., Vorobyeva, L. M., and Krasnovsky, A. A. (1971) Mol. Biol. (Moscow), 5, 366–374.

    CAS  Google Scholar 

  130. Rebeiz, C. A., and Castelfranco, P. A. (1973) Ann. Rev. Plant Physiol., 24, 129–172.

    CAS  Google Scholar 

  131. Rebeiz, C. A., Smith, B. B., Mattheis, J. R., Cohen, C. E., and McCarthy, S. A. (1978) in Chloroplast Development (Akoyounoglou, G., and Argyroudi-Akoyounoglou, J. H., eds.) Amsterdam, pp. 59–76.

  132. Boddi, B., Lindsten, A., Ryberg, M., and Sundqvist, C. (1989) Physiol. Plant., 76, 135–143.

    Google Scholar 

  133. Ellsworth, R. K., and Nowak, C. (1974) Ann. Biochem., 57, 534–546.

    CAS  Google Scholar 

  134. Liljenberg, C. L. (1974) Physiol. Plant., 32, 208–213.

    CAS  Google Scholar 

  135. Liljenberg, C. L. (1977) in Lipids and Lipid Polymers in Higher Plants (Tevini, M., and Lichtentaler, H. K., eds.) Berlin, pp. 259–270.

  136. Shioi, Y., and Sasa, T. (1982) Plant Cell Physiol., 23, 1315–1321.

    CAS  Google Scholar 

  137. Shioi, Y., and Sasa, T. (1983) Plant Cell Physiol., 24, 835–840.

    CAS  Google Scholar 

  138. Aronoff, S., and Ellsworth, R. K. (1968) Photosynthetica, 2, 288–297.

    CAS  Google Scholar 

  139. Jones, O. T. G. (1979) in The Porphyrins (Dolphyn, D., ed.) Vol. 6, New York, pp. 179–232.

  140. Belanger, F. C., and Rebeiz, C. A. (1979) Biochem. Biophys. Res. Commun., 88, 365–372.

    PubMed  CAS  Google Scholar 

  141. Belanger, F. C., Duggan, J. X., and Rebeiz, C. A. (1982) J. Biol. Chem., 257, 4849–4858.

    PubMed  CAS  Google Scholar 

  142. Wu, S. M., Mayasich, M., and Rebeiz, C. A. (1989) Analyt. Biochem., 178, 294–300.

    PubMed  CAS  Google Scholar 

  143. Carey, E. E., and Rebeiz, C. A. (1985) Plant Physiol., 79, 1–6.

    PubMed  CAS  Google Scholar 

  144. Carey, E. E., Tripathy, B. C., and Rebeiz, C. A. (1985) Plant Physiol., 79, 1059–1063.

    PubMed  CAS  Google Scholar 

  145. Granick, S., and Gassman, M. L. (1970) Plant Physiol., 45, 201–205.

    PubMed  CAS  Google Scholar 

  146. Rebeiz, C. A., Belanger, F. C., McCarthy, S. A., Fressinet, G., Duggan, J. X., Wu, S. M., and Mattheis, J. R. (1981) Proc. 5th Int. Congr. Photosynth. (Akoyunoglou, G., ed.) Vol. 5, Int. Sci. Services, Jerusalem, pp. 197–212.

    Google Scholar 

  147. Duggan, J. X., and Rebeiz, C. A. (1982) Plant Sci. Lett., 24, 27–37.

    CAS  Google Scholar 

  148. Duggan, J. X., and Rebeiz, C. A. (1982) Plant Sci. Lett., 27, 137–145.

    CAS  Google Scholar 

  149. Rebeiz, C. A., and Lascelles, J. (1982) in Photosynthesis (Govindjee, ed.) New York, pp. 699–780.

  150. Rebeiz, C. A., Wu, S. M., Kuhadja, M., Daniell, H., and Perkins, E. J. (1983) Mol. Cell. Biochem., 57, 97–125.

    PubMed  CAS  Google Scholar 

  151. Koski, V. M., and Smith, J. H. C. (1948) J. Amer. Chem. Soc., 70, 3558–3562.

    CAS  Google Scholar 

  152. Krasnovsky, A. A., and Voinovskaya, K. K. (1949) Dokl. Akad. Nauk SSSR, 66, 663–666.

    Google Scholar 

  153. Monteverde, N. A., and Lubimenko, W. N. (1911) Biologisches Centralblat, 31, 481–498.

    Google Scholar 

  154. Koski, V. M., French, C. S., and Smith, J. H. C. (1951) Arch. Biochem. Biophys., 31, 1–17.

    CAS  Google Scholar 

  155. Shibata, K. (1956) Carn. Inst. Wash. Yearly Book, 1956, 55, 248–250.

    Google Scholar 

  156. Shibata, K. (1957) J. Biochem. (Tokyo), 44, 147–173.

    CAS  Google Scholar 

  157. Litvin, F. F., and Krasnovsky, A. A. (1957) Dokl. Akad. Nauk SSSR, 117, 106–109.

    CAS  Google Scholar 

  158. Litvin, F. F., and Krasnovsky, A. A. (1958) Dokl. Akad. Nauk SSSR, 120, 764–767.

    Google Scholar 

  159. Litvin, F. F., and Krasnovsky, A. A. (1959) Izv. Akad. Nauk SSSR, 120, 764–767.

    Google Scholar 

  160. Lang, F., Vorobyeva, L. M., and Krasnovsky, A. A. (1968) Dokl. Akad. Nauk SSSR, 183, 711–714.

    CAS  Google Scholar 

  161. Lang, F., Vorobyeva, L. M., and Krasnovsky, A. A. (1969) Biokhimiya, 34, 257–265.

    CAS  Google Scholar 

  162. Lang, F., Vorobyeva, L. M., and Krasnovsky, A. A. (1969) Biofizika, 14, 245–255.

    PubMed  CAS  Google Scholar 

  163. Lang, F., Vorobyeva, L. M., and Krasnovsky, A. A. (1971) Mol. Biol. (Moscow), 5, 366–374.

    CAS  Google Scholar 

  164. Sironval, C., Brouers, M., Michel, J. M., and Kuyper, Y. (1968) Photosynthetica, 2, 268–287.

    CAS  Google Scholar 

  165. Kahn, A., Boardman, N. K., and Thorne, S. W. (1970) J. Mol. Biol., 48, 85–101.

    PubMed  CAS  Google Scholar 

  166. Litvin, F. F., and Stadnichuk, I. N. (1980) Fiziol. Rast., 27, 1024–1032.

    CAS  Google Scholar 

  167. Boddi, B., Ryberg, M., and Sundqvist, C. (1992) J. Photochem. Photobiol., 12, 389–401.

    CAS  Google Scholar 

  168. Boddi, B., and Franck, F. (1997) J. Photochem. Photobiol. B: Biol., 41, 73–82.

    CAS  Google Scholar 

  169. Schoefs, B., Bertrand, M., and Franck, F. (2000) Photochem. Photobiol., 72, 85–93.

    PubMed  CAS  Google Scholar 

  170. Stadnichuk, I. N., Amirjani, M. R., and Sundqvist, C. (2005) Photochem. Photobiol. Sci., 4, 230–238.

    PubMed  CAS  Google Scholar 

  171. Bovey, F., Ogawa, T., and Shibata, K. (1974) Plant Cell Physiol., 15, 1133–1137.

    CAS  Google Scholar 

  172. Cohen, C. E., and Rebeiz, C. A. (1981) Plant Physiol., 67, 98–103.

    PubMed  CAS  Google Scholar 

  173. Shioi, Y., and Sasa, T. (1984) Plant Cell Physiol., 25, 131–137.

    CAS  Google Scholar 

  174. Franck, F., and Strazlka, K. (1992) FEBS Lett., 309, 73–77.

    PubMed  CAS  Google Scholar 

  175. Virgin, H. I. (1993) Physiol. Plant., 89, 761–766.

    CAS  Google Scholar 

  176. Valter, G., Belyaeva, O. B., Ignatov, N. V., Krasnovsky, A. A., and Litvin, F. F. (1982) Biol. Nauki, No. 9, 35–39.

  177. Sundqvist, C., and Dahlin, C. (1997) Physiol. Plant., 100, 748–759.

    CAS  Google Scholar 

  178. Litvin, F. F., Belyaeva, O. B., and Ignatov, N. V. (2000) Usp. Biol. Khim., 40, 3–42.

    CAS  Google Scholar 

  179. Akulovich, N. K. (1983) Formation and State of Photoactive Protochlorophyllous Pigment [in Russian], Nauka i Tekhnika, Minsk.

    Google Scholar 

  180. Mysliwa-Kurdziel, B., Amirjani, M. R., Strzalka, K., and Sundqvist, C. (2003) Photochem. Photobiol., 78, 205–212.

    PubMed  CAS  Google Scholar 

  181. Litvin, F. F., Efimtsev, E. I., and Ignatov, N. V. (1976) Biofizika, 21, 307–312.

    PubMed  CAS  Google Scholar 

  182. Ignatov, N. V. (1977) Investigation of Photochemical Stage of Chlorophyll Biosynthesis: Author’s abstract of Candidate’s dissertation [in Russian], Moscow.

  183. Ignatov, N. V., and Litvin, F. F. (1981) Biofizika, 26, 664–668.

    PubMed  CAS  Google Scholar 

  184. Akulovich, N. K., and Raskin, V. I. (1971) in Topics in Chlorophyll Biosynthesis [in Russian], Nauka i Tekhnika, Minsk, pp. 5–52.

    Google Scholar 

  185. El Hamouri, B., and Sironval, C. (1979) FEBS Lett., 103, 345–347.

    PubMed  Google Scholar 

  186. Houssier, C., and Sauer, K. (1970) J. Amer. Chem. Soc., 92, 779–791.

    CAS  Google Scholar 

  187. Schultz, A., and Sauer, K. (1972) Biochim. Biophys. Acta, 267, 320–340.

    PubMed  CAS  Google Scholar 

  188. Vaugan, G. D., and Sauer, K. (1974) Biochim. Biophys. Acta, 347, 383–394.

    Google Scholar 

  189. El Hamouri, B., and Sironval, C. (1980) Photobiochem. Photobiophys., 1, 219–223.

    Google Scholar 

  190. El Hamouri, B., Brouers, M., and Sironval, C. (1981) Plant Sci. Lett., 21, 375–379.

    Google Scholar 

  191. Franck, F., Bereza, B., and Boddi, B. (1999) Photosynth. Res., 59, 53–61.

    CAS  Google Scholar 

  192. Belyaeva, O. B., and Litvin, F. F. (1980) Biofizika, 25, 617–623.

    CAS  Google Scholar 

  193. Belyaeva, O. B., and Litvin, F. F. (1981) Photosynthetica, 15, 210–215.

    CAS  Google Scholar 

  194. Ignatov, N. V., and Litvin, F. F. (2001) Biochemistry (Moscow), 66, 195–204.

    CAS  Google Scholar 

  195. Ignatov, N. V., and Litvin, F. F. (2002) Photosynth. Res., 71, 195–207.

    PubMed  CAS  Google Scholar 

  196. Franck, F., Berthelemy, X., and Strazlka, K. (1993) Photosynthetica, 29, 185–194.

    CAS  Google Scholar 

  197. Litvin, F. F., Rikhireva, G. T., and Krasnovskii, A. A. (1962) Biofizika, 7, 578–591.

    CAS  Google Scholar 

  198. Ignatov, N. V., and Litvin, F. F. (2002) Biochemistry (Moscow), 67, 949–955.

    CAS  Google Scholar 

  199. Schoefs, B., and Franck, F. (1998) Plant Physiol., 118, 1159–1168.

    PubMed  CAS  Google Scholar 

  200. Kasha, M. (1963) Radiat. Res., 20, 55–70.

    PubMed  CAS  Google Scholar 

  201. Litvin, F. F., and Sineshchekov, V. A. (1965) in Molecular Biophysics [in Russian], Nauka, Moscow, pp. 191–203.

    Google Scholar 

  202. Krasnovsky, A. A., Bystrova, M. I., and Sorokina, A. V. (1961) Dokl. Akad Nauk SSSR, 136, 1227–1230.

    Google Scholar 

  203. Vorobyeva, L. M., and Krasnovsky, A. A. (1966) Biokhimiya, 31, 578–584.

    Google Scholar 

  204. Butler, W. L., and Briggs, W. R. (1966) Biochim. Biophys. Acta, 112, 45–53.

    PubMed  CAS  Google Scholar 

  205. Dujardin, E., and Sironval, C. (1970) Photosynthetica, 4, 129–138.

    CAS  Google Scholar 

  206. Seliskar, C., and Ke, B. (1968) Biochim. Biophys. Acta, 153, 685–691.

    PubMed  CAS  Google Scholar 

  207. Brouers, M. (1972) Photosynthetica, 6, 415–423.

    CAS  Google Scholar 

  208. Brouers, M. (1979) Photosynthetica, 13, 9–14.

    CAS  Google Scholar 

  209. Losev, A. P., and Gurinovich, G. P. (1969) Biofizika, 14, 110–118.

    PubMed  CAS  Google Scholar 

  210. Zenkevich, E. I., and Losev, A. P. (1976) Mol. Biol. (Moscow), 10, 294–304.

    CAS  Google Scholar 

  211. Zenkevich, E. I., Kochubeev, G. A., Losev, A. P., and Gurinovich, G. P. (1978) Mol. Biol. (Moscow), 12, 1002–1011.

    CAS  Google Scholar 

  212. Shlyk, A. A., Fradkin, L. I., and Kalinina, L. M. (1973) in Topics in Biophotochemistry [in Russian], Nauka, Moscow, pp. 122–132.

    Google Scholar 

  213. Kotzabasis, K., Senge, M., Seyfried, B., and Senger, H. (1990) Photochem. Photobiol., 52, 95–101.

    CAS  Google Scholar 

  214. Bystrova, M. I., and Krasnovsky, A. A. (1967) Mol. Biol. (Moscow), 1, 362–272.

    CAS  Google Scholar 

  215. Bystrova, M. I., Lang, F., and Krasnovsky, A. A. (1972) Mol. Biol. (Moscow), 6, 77–86.

    CAS  Google Scholar 

  216. Bystrova, M. I., Safronova, I. A., and Krasnovsky, A. A. (1982) Mol. Biol. (Moscow), 16, 291–301.

    CAS  Google Scholar 

  217. Bystrova, M. I., Safronova, I. A., and Krasnovsky, A. A. (1985) Mol. Biol. (Moscow), 19, 915–925.

    CAS  Google Scholar 

  218. Krasnovsky, A. A., and Bystrova, M. I. (1974) in Chlorophyll (Shlyk, A. A., ed.) [in Russian], Nauka i Tekhnika, Minsk, pp. 139–153.

    Google Scholar 

  219. Krasnovsky, A. A., Bystrova, M. I., and Lang, F. (1971) Dokl. Akad. Nauk SSSR, 201, 1485–1488.

    Google Scholar 

  220. Canaani, O. D., and Sauer, K. (1977) Plant Physiol., 60, 422–429.

    PubMed  CAS  Google Scholar 

  221. Sironval, C. (1972) Photosynthetica, 6, 375–380.

    CAS  Google Scholar 

  222. Fradkin, L. I., and Shlyk, A. A. (1978) Zh. Prikl. Spektrosk., 29, 1029–1039.

    CAS  Google Scholar 

  223. Henningsen, K. W., Thorne, S. W., and Bordman, N. K. (1974) Plant Physiol., 53, 419–425.

    PubMed  CAS  Google Scholar 

  224. Brouers, M., and Sironval, C. (1974) Plant Sci. Lett., 2, 67–72.

    CAS  Google Scholar 

  225. Brouers, M. (1975) Photosynthetica, 9, 304–310.

    CAS  Google Scholar 

  226. Martin, G. E. M., Timko, M. P., and Wilks, H. M. (1997) Biochem. J., 325, 139–145.

    PubMed  CAS  Google Scholar 

  227. Belyaeva, O. B., and Litvin, F. F. (1989) Photobiosynthesis of Chlorophyll [in Russian], MGU Publishers, Moscow.

    Google Scholar 

  228. Boddi, B., Lindsten, A., Ryberg, M., and Sundqvist, C. (1989) Physiol. Plant., 76, 135–143.

    Google Scholar 

  229. Boddi, B., Lindsten, A., Ryberg, M., and Sundqvist, C. (1990) Photochem. Photobiol., 52, 83–87.

    CAS  Google Scholar 

  230. Wiktorsson, B., Ryberg, M., Gough, S., and Sundqvist, C. (1992) Physiol. Plant., 85, 659–669.

    CAS  Google Scholar 

  231. Chahdi, M. A., Schoefs, B., and Franck, F. (1998) Planta, 206, 673–680.

    CAS  Google Scholar 

  232. Wiktorsson, B., Engdahl, S., Zhong, L. B., Boddi, B., Ryberg, M., and Sundqvist, C. (1993) Photosynthetica, 29, 205–218.

    CAS  Google Scholar 

  233. Boddi, B., Soos, J., and Lang, F. (1980) Biochim. Biophys. Acta, 593, 158–165.

    PubMed  CAS  Google Scholar 

  234. Boddi, B., Kovacs, K., and Lang, F. (1983) Biochim. Biophys. Acta, 722, 320–326.

    CAS  Google Scholar 

  235. Inada, Y., and Shibata, K. (1960) Plant Cell Physiol., 1, 311–316.

    CAS  Google Scholar 

  236. Sundqvist, C., and Ryberg, H. (1979) Physiol. Plant., 47, 124–128.

    CAS  Google Scholar 

  237. Sundqvist, C., Ryberg, H., Boddi, B., and Lang, F. (1980) Physiol. Plant., 48, 297–301.

    CAS  Google Scholar 

  238. Ignatov, N. V., Belyaeva, O. B., Timofeev, K. N., and Litvin, F. F. (1988) Biofizika, 33, 500–505.

    CAS  Google Scholar 

  239. Ignatov, N. V., Belyaeva, O. B., and Litvin, F. F. (1993) Photosynthetica, 29, 235–241.

    CAS  Google Scholar 

  240. Walker, C. J., and Griffiths, W. T. (1988) FEBS Lett., 239, 259–262.

    CAS  Google Scholar 

  241. Nayar, P., Brun, A., Harriman, A., and Begley, T. P. (1992) J. Chem. Soc. Chem. Commun., 395–397.

  242. Townley, H. E., Griffiths, W. T., and Nugent, J. P. (1998) FEBS Lett., 422, 19–22.

    PubMed  CAS  Google Scholar 

  243. Reinbothe, C., Lebedev, N., and Reinbothe, S. (1999) Nature (London), 397, 80–84.

    CAS  Google Scholar 

  244. Klement, H., Oster, U., and Rudiger, W. (2000) FEBS Lett., 480, 306–310.

    PubMed  CAS  Google Scholar 

  245. Selstam, E., and Widell-Wigge, A. (1993) in Pigment-Protein Complexes in Plastids: Synthesis and Assembly (Sundqvist, C., and Ryberg, M., eds.) Academic Press, San Diego, pp. 241–277.

    Google Scholar 

  246. Redlinger, T. E., and Apel, K. (1980) Arch. Biochem. Biophys., 200, 253–260.

    PubMed  CAS  Google Scholar 

  247. Mullet, J. E., Klein, P. G., and Klein, R. R. (1990) Proc. Natl. Acad. Sci. USA, 87, 4038–4042.

    PubMed  CAS  Google Scholar 

  248. Klein, R. R., Camble, P. E., and Mullet, J. E. (1988) Plant Physiol., 88, 1246–1256.

    PubMed  CAS  Google Scholar 

  249. Eichacker, L. F., Paulsen, H., and Rudiger, W. (1992) Eur. J. Biochem., 205, 17–24.

    PubMed  CAS  Google Scholar 

  250. Eichacker, L. F., Muller, B., and Helfrich, M. (1996) FEBS Lett., 395, 251–256.

    PubMed  CAS  Google Scholar 

  251. Kim, J., Klein, P., and Mullet, J. (1994) J. Biol. Chem., 269, 17918–17923.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to O. B. Belyaeva.

Additional information

Original Russian Text © O. B. Belyaeva, F. F. Litvin, 2007, published in Uspekhi Biologicheskoi Khimii, 2007, Vol. 47, pp. 189–232.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Belyaeva, O.B., Litvin, F.F. Photoactive pigment—enzyme complexes of chlorophyll precursor in plant leaves. Biochemistry Moscow 72, 1458–1477 (2007). https://doi.org/10.1134/S0006297907130044

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297907130044

Key words

Navigation