THE GENETICS OF CHLOROPHYLL BIOSYNTHESIS: LIGHT-INDEPENDENT AND LIGHT-DEPENDENT PATHWAYS



Cite item

Full Text

Abstract

 The review summarizes contemporary genetical, molecular biological and biochemical data on the two protochlorophyllide oxidoreductases (POR), enzymes responsible of light-dependent (LPOR) and dark-operative (DPOR) protochlorophyllide reduction. Evolutionary aspects of origin and functioning of these enzymes are also discussed. The main focus of this review will be the genetics of archaic dark chlorophyll biosynthesis.

About the authors

Elena M Chekunova

Saint-Petersburg State University., Saint-Petersburg, RF

Email: elena_chekunova@mail.ru

References

  1. Александрова Н. Н., Крэла Л. П., Тугаринов В. В., 1979. Генетическая детерминация признаков хлоропласта у хла- мидомонады. Сообщ. I. Создание множественно-маркированных линий // Исследования по генетике. Вып. 8. С. 139-149.
  2. Беляева О. Б., 2009. Светозависимый биосинтез хлорофилла // Москва: Изд. «Бином. Лаборатория знаний»/ 232 с.
  3. Беляева О. Б., Литвин Ф. Ф., 2007. Фотоактивные пигмент-ферментные комплексы предшественника хлорофилла в листьях растений // Усп. биол. химии. Т. 47. С. 189-232.
  4. Красновский А. А., Кособуцкая Л. М., 1952. Спектральные исследования состояния хлорофилла при его образовании в растении и в коллоидных растворах вещества этиолированных листьев // ДАН СССР. Т. 85. С. 177-180.
  5. Пиневич А. В., Аверина С. Г., 2002. Оксигенная фототрофия // СПб: Изд. СПбГУ. 236 с.
  6. Чекунова Е. М., Квитко К. В., 1986. Генетическое изучение мутантов хламидомонады, накапливающих протопорфи- рин IX // Исследования по генетике. № 10. С. 104-112.
  7. Чекунова Е. М., Савельева Н. В., 2010. Ген LTS3 контролирует светонезависимый биосинтез хлорофилла у зеленой водоросли Chlamydomonas reinhardtii // Экологическая генетика. № 2. С. 35-44.
  8. Шалыго Н. В., 2004. Биосинтез хлорофилла и фотодинамические процессы в растениях // Минск: ИООО «Право и экономика». 156 с.
  9. Шалыго Н. В., Чекунова Е. М., Чунаев А. С., Аверина Н. Г., 1990. Анализ состава порфиринов в мутантах Chlamydomonas reinhardtii // Изв. АН БССР. Сер. Биол. наук. № 4. С. 53-57.
  10. Шестаков С. В. Молекулярная генетика фотосинтеза // СОЖ. 1998. № 9. С. 22-27.
  11. Adamson H., Griffiths T., Parker N., Sutherland M., 1985. Light independent accumulation of chlorophyll a and b and protochlorophyllide in green barley (Hordeum vulgare) // Plant Physiol. Vol. 64. P. 345-352.
  12. Apel K., Santel H. J., Redlinger T. E., Falk H., 1980. The protochlorophyllide holochrome of barley (Hordeum vulgare). Isolation and characterization of the NADPH: protochlorophyllide oxidoreductase // Eur. J. Biochem. Vol. 111. P. 251-258.
  13. Armstrong G. A., 1998. Greening in the dark: light independent chlorophyll biosynthesis from anoxygenic photosynthetic bacteria to gymnosperms // J. Photochem. Photobiol. Vol. 43. P. 87-100.
  14. Aronsson H., Sundqvist Ch., Dahlin C., 2003. POR hits the road: import and assembly of a plastid protein // Plant Mol. Biol. Vol. 51. P. 1-7.
  15. Batschauer A., Santel H. J., Apel K., 1982. The presence and synthesis of the NADPH-protochlorophyllide oxidoreductase in barley leaves with a high-temperature-induced deficiency of plastid ribosomes // Planta. Vol. 154. P. 459-464.
  16. Beale S. I., 1999. Enzymes of chlorophyll biosynthesis // Photosynth. Res. Vol. 60. P. 43-73.
  17. Begley T. P., 1994. Photoenzymes: a novel class of biological catalysts // Acc. Chem. Res. Vol. 27. P. 394-401.
  18. Birve S. J., Selstam E, Johansson L. B. A., 1996. Secondary structure of NADH: protochlorophyllide oxidoreductase examined by circular dichroism and prediction methods // Biochemistry. Vol. 317. P. 549-555.
  19. Bogorad L., 1976. Chlorophyll biosynthesis // In: Chemistry and Biochemistry of Plant Pigments / ed. Goodwin T. W. New York: Acad. Press. P. 64-148.
  20. Burke D. H., Alberti M., Hearst J. E., 1993. bchFNBH bacteriochlorophyll synthesis genes of Rhodobacter capsulatus and identification of the third subunit of light-independent protochlorophyllide reductase in bacteria and plants // J. Bacteriol. Vol. 175. P. 2414-2422.
  21. Cahoon A. B., Timko M. P., 2000. Yellow-in-the-dark mutants of Chlamydomonas lack the CHLL subunit of light-independent protochlorophyllide reductase // Plant Cell. Vol. 12. P. 559-568.
  22. Choquet Y., Rahire M., Girard-Bascou J., Erickson J., Rochaix J.-D., 1992. A chloroplast gene is required for lightindependent accumulation of chlorophyll in Chlamydomonas reinhardtii // J. EMBO. Vol. 11. No. 5. P. 1697-1704.
  23. Choudhary M., Kaplan S., 2000. DNA sequence analysis of the photosynthesis region of Rhodobacter sphaeroides 2. 4. 1 // Nucl. Acids Res. Vol. 28. P. 862-867.
  24. Dahlin C., Aronsson H., Wilks H. M., Lebedev N., Sundqvist C., M. P. Timko M. P., 1999. The role of protein surface charge in catalytic activity and chloroplast membrane association of the pea NADPH:protochlorophyllide oxidoreductase (POR) as revealed by alanine mutagenesis // Plant Mol. Biol. Vol. 39. P. 309-323.
  25. Demko V., Pavlovic A., Valkova D., Slovakova L., Grimm B., Hudak J., 2009. A novel insight into the regulation of light-independent chlorophyll biosynthesis in Larix decidua and Picea abies seedlings // Planta. Vol. 230. P. 165-176.
  26. Drumm-Herrel H., Mohr H., 1994. Regulation by light of chlorophyll synthesis in the cotyledons of Scots pine (Pinus sylvestris) seedlings // Physiol. Plant. Vol. 91. P. 300-306.
  27. Fong A., Archibald J. M., 2008. Evolutionary dynamics of light-independent protochlorophyllide oxidoreductase genes in the secondary plastids of cryptophyte algae // Eukar. Cell. Vol. 7. P. 550-553.
  28. Ford C., Mitchell S., Wang W. Y., 1981. Protochlorophyllide photoconversion mutants of Chlamydomonas reinhardtii // Mol. Gen. Genet. Vol. 184. P. 460-464.
  29. Ford C., Mitchell S., Wang W. -Y., 1983. Characterization of NADPH:protochlorophyllide oxidoreductase in the y-7 and pc-1 y-7 mutants of Chlamydomonas reinhardtii // Mol. Gen. Genet. Vol. 192. P. 290-292.
  30. Ford C., Wang W-Y., 1980a. Three new yellow loci in Chlamydomonas reinhardtii // Mol. Gen. Genet. Vol. 179. P. 259-263.
  31. Ford C., Wang W-Y., 1980b. Temperature sensitive yellow mutants of Chlamydomonas reinhardtii // Mol. Gen. Genet. Vol. 180. P. 5-10.
  32. Frick G., Su Q., Apel K., Armstrong G. A., 2003. An Arabidopsis porB porC double mutant lacking light-dependent NADPH:protochlorophyllide oxidoreductases B and C is highly chlorophyll-deficient and developmentally arrested // Plant J. Vol. 35 (2). P. 141-53.
  33. Fujita, Y., Bauer C. E., 2000. Reconstitution of light-independent protochlorophyllide reductase from purified BchL and BchN-BchB subunits. In vitro confirmation of nitrogen-like features of a bacteriochlorophyll biosynthesis enzyme // J. Biol. Chem. Vol. 275. P. 23583-23588.
  34. Fujita, Y., Matsumoto H., Takahashi Y., Matsubara H., 1993. Identification of a nifDK-like gene (ORF467) involved in the biosynthesis of chlorophyll in the cyanobacterium Plectonema boryanum // Plant Cell Physiol. Vol. 34. P. 305-314.
  35. Fujita, Y., Takagi H., Hase T., 1996. Identification of a chlB gene product essential for light-independent chlorophyll biosynthesis in the cyanobacterium Plectonema boryanum // Plant Cell Physiol. Vol. 37. P. 313-323.
  36. Fujita Y., Takagi H., Hase T., 1998. Cloning of the gene encoding a protochlorophyllide reductase: the physiological significance of the co-existence of light-dependent and -independent protochlorophyllide reduction systems in the cyanobacterium Plectonema boryanum // Plant Cell Physiol. Vol. 39. P. 177-185.
  37. Fujita, Y., Takahashi Y., Chuganji M., Matsubara H., 1992. The nifH-like (frxC) gene is involved in the biosynthesis of chlorophyll in the filamentous cyanobacterium Plectonema boryanum // Plant Cell Physiol. Vol. 33. P. 81-92.
  38. Fujita Y., Takahashi, Y., Koschi., Ozeki H., Ohyama K., Matsubara H., 1989. Identification of a novel nifH-like (frxC) protein in chloroplasts of liverwort Marchantia polymorpha // Plant Mol. Biol. Vol. 13. P. 551-561.
  39. Fujita, Y., Takahashi Y., Koschi T., Ozeki H., Ohyama K., Matsubara H., 1991. Cloning, nucleotide sequences and differential expression of the nifH and nifH-like (frxC) genes from the filamentous nitrogen-fixing cyanobacterium Plectonema boryanum // Plant Cell. Physiol. Vol. 32. P. 1093-1106.
  40. Griffiths, W. T., 1991. Protochlorophyllide reduction // Chlorophylls / Ed. Scheer H. Boca Raton - CRC Press. P. 433-450.
  41. Griffiths W. T., McHugh T., Blankenship R. E., 1996. The light intensity dependence of protochlorophyllide photoconversion and its significance to the catalytic mechanism of protochlorophyllide reductase // FEBS Lett. Vol. 398. P. 235-238.
  42. Hearst J. E., Alberti R. F., Doolittle R. F., 1985. A putative nitrogenase reductase gene found in the nucleotide sequences from photosynthetic gene cluster of R. capsulata // Cell. Vol. 40. P. 219-220.
  43. Heyes D. J., Ruban A. V., Hunter C. N., 2003. Protophlorophyllide oxidoreductase: "dark" reactions of a light-driven enzyme // Biochemistry. Vol. 42. P. 523-538.
  44. Holtorf H., Reinbothe S., Reinbothe R., Bereza B., Apel K., 1995. Two routes of chlorophyllide synthesis that are differentially regulated by light in barley (Hordeum vulgare L.) // Proc. Natl. Acad. Sci. USA. Vol. 92. P. 3254- 3258.
  45. Huang C., Liu X-Q., 1992. Nucleotide sequence of the frxC, petB and trnL genes in the chloroplast genome of Chlamydomonas reinhardtii // Plant Mol. Biol. Vol. 18. P. 985-988.
  46. Kim C., Apel K., 2004. Substrate-dependent and organ-specific chloroplast protein import in planta // Plant Cell. Vol. 16. P. 88-98.
  47. Laudi G., Manzini M. L., 1975. Chlorophyll content and plastid ultrastructure in leaflets of Metasequoia glyptostroboides // Protoplasma. Vol. 84. P. 185-190.
  48. Lebedev N., Timko M., 1998. Protochlorophyllide photoreduction // Photosynth. Res. Vol. 58. P. 5-23.
  49. Li J., Goldschmidt-Clermont M., Timko M. P., 1993. Chloroplast encoded chlB is required for light-independent protochlorophyllide reductase activity in Chlamydomonas reinhardtii // Plant Cell. Vol. 5. P. 1817-1829.
  50. Li J., Timko M. P., 1996. The pc-1 phenotype of Chlamydomonas reinhardtii results from a deletion mutation in the nuclear gene for NADPH protochlorophyllide oxidoreductase // Plant. Mol. Biol. Vol. 30. P. 15-37.
  51. Lindholm J., Gustafsson P., 1991. Homologues of the green algal gidA and the liverwort frxC gene are present on the chloroplast genomes of conifers // Plant Mol. Biol. Vol. 17. P. 787-798.
  52. McCoy S. R., Kuehl J. V., Boore J. L Raubeson L. A., 2008. The complete plastid genome sequence of Welwitschia mirabilis: an unusually compact plastome with accelerated divergence rates // Evol Biol. Vol. 8. P. 130.
  53. Mariani P., De Carli M. E., Rascio N., Baldan B., Casadoro G., Gennari G., Bodner M., Larcher W., 1990. Synthesis of chlorophyll and photobiosynthetic competence in etiolated and greening seedlings of Larix decidua as compared with Picea abies // J. Plant Physiol. Vol. 137. P. 5-14.
  54. Marrison J. L., Schunmann P. H. D., Oughan H. J., Leech R. M., 1996. Subcellular visualization of gene transcripts encoding key proteins of the chlorophyll accumulation process in developing chloroplasts // Plant Physiol. Vol. 110, P. 1089-1096.
  55. Masuda T., Takamiya K-I., 2005. Novel insights into the enzymology, regulation and physiological functions of light-dependent protochlorophyllide oxidoreductase in angiosperms // Photosynth. Res. Vol. 81. P. 1-29.
  56. Muraki N., Nomata J., Ebata K., Mizoguchi T., Shiba T., Tamiaki H., Kurisu G., FujitaY., 2010. X-ray crystal structure of the light-independent protochlorophyllide reductase // Nature Vol. 465. P. 110-114.
  57. Nomata J., Mizoguchi T., Tamiaki H., Fujita Y., 2006. A second nitrogenase-like enzyme for bacteriochlorophyll biosynthesis: reconstitution of chlorophyllide a reductase with purified X-protein (BchX) and YZ-protein (BchY-BchZ) from Rhodobacter capsulatus // J. Biol. Chem. Vol. 281. P. 15021-15028.
  58. Nomata J., Swem L. R., Bauer C. E., Fujita Y., 2005. Overexpression and characterization of dark-operative protochlorophyllide reductase from Rhodobacter capsulatus // Biochim. Biophys. Acta. Vol. 1708. P. 229-235.
  59. Ogura Y., Takemura M., Oda K., Yamatu K., Ohta E., Fukazawa H., Ohyama K., 1992. Cloning and nucleotide sequence of a frxC-ORF469 gene cluster of Synechocystis PCC6803 conservation with liverwort chloroplast frxCORF465 and nif operon // Biosci. Biotech. Biochem. Vol. 56. P. 788-793.
  60. Ohyama K., Fukazawa H., Kohchi T., Shirai H., Sano T., Sano S., Umesono K., Shiki Y., et al., 1986. Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha // Nature. Vol. 322. P. 572-574.
  61. Oliver R. P., Griffiths W. T., 1980. Identification of the polypeptides of NADPH: protochlorophyllide oxidoreductase // Biochem. J. Vol. 191. P. 277-280.
  62. Oosawa N., Masuda T., Awai K., Fusada N., Shimada H., Ohta H., Takamiya K., 2000. Identification and light-induced expression of a novel gene of NADPH: protochlorophyllide oxidoreductase isoform in Arabidopsis thaliana // FEBS Lett. Vol. 474. P. 133-136.
  63. Ou K., Adamson H., 1995. Chlorophyll accumulation in cotyledons, hypocotyls and primary needles of Pinus pinea seedlings in light and dark // Physiol. Plant. Vol. 93. P. 719-724.
  64. Popov K., Dilova S., 1969. On the dark sinthesis and stabilization of chlorophyll // In: Progress in Photosynthesis Research / ed. Metzner H. Inst. Union Biol. Sci.,Tubingen Vol. 2. P. 606-609.
  65. Raskin V. I., Schwartz A., 2003. Experimental approach to elucidating the mechanism of light-independent chlorophyll biosynthesis in green barley // Plant Physiol. Vol. 133. P. 25-28.
  66. Raymond J., Siefert J. L., Staples Ch. R., Blankenship R. E., 2004. The natural history of nitrogen fixation // Mol. Biol. Evol. Vol. 21. P. 541-554.
  67. Reinbothe S., Pollmann S., Springer A., James R. J., Tichtinsky. G., Reinbothe C., 2005. A role of Toc33 in the protochlorophyllide- dependent plastid import pathway of NADPH: protochlorophyllide oxidoreductase (POR) A // Planta. Vol. 42. P. 1-12.
  68. Reinbothe S., Quigley F., Gray J., Schemenewitz A., Reinbothe C., 2004. Identification of plastid envelope proteins required for import of protochlorophyllide oxidoreductase A into the chloroplast of barley // Proc. Natl. Acad. Sci. USA. Vol. 97. P. 9795-9800.
  69. Reinbothe S., Reinbothe C., 1996. The regulation of enzymes involved in chlorophyll biosynthesis // Eur. J. Biochem. Vol. 237. P. 323-343.
  70. Reinbothe S., Runge S., Reinbothe C., van Cleve B., Apel K., 1995. Substrate-dependent transport of the NADPH: protochlorophyllide oxidoreductase into isolated plastids // Plant Cell. Vol. 7. P. 161-172.
  71. Richard M., Tremblay C., Bellemare G., 1994. Chloroplastic genomes of Ginkgo biloba and Chlamydomonas moewusii contain a chlB gene encoding one subunit of a light-independent protochlorophyllide reductase // Curr. Genet. Vol. 26. P. 159-156.
  72. Roitgrund C., Mets L. J., 1990. Localization of two novel chloroplast genome functions: trans-splicing of RNA and protochlorophyllide reduction // Curr. Genet. Vol. 17. P. 147-153.
  73. Rubio L. M., Ludden P. W., 2005. Maturation of nitrogenase: a biochemical puzzle // J. Bacteriol. Vol. 187. P. 405-414.
  74. Sager R., 1955. Inheritance in the green alga Chlamydomonas reinhardtii // Genetics. Vol. 40. P. 476-489.
  75. Schemenewitz A., Pollmann S., Reinbothe C., Reinbothe S., 2007. A substrate-independent, 14:3:3 protein-mediated plastid import pathway of NADPH:protochlorophyllide oxidoreductase A // Proc. Natl. Acad. Sci. USA. Vol. 104. P. 8538-8543.
  76. Schoefs B., Franck F., 2003. Protochlorophyllide reduction: mechanisms and evolution // Photochem. Photobiol. Vol. 78. P. 543-557.
  77. Schulz R., Steinmuller K., Klaas M., Forreiter C., Rasmussen S., Hiller C., Apel K., 1989. Nucleotide sequence of cDNA coding for the NADPH-protochlorophyllide oxidoreductase (POR) of barley (Hordeum vulgare L.) and its expression in Escherichia coli // Mol. Gen. Genet. Vol. 217. P. 355-361.
  78. Shiba, T. and Shimada K., 1997. Photosynthetic aspects of aerobic photosynthetic bacteria // Handbook of Photosynthesis / Ed. M. Pessarakli, Marcel Dekker, New York. P. 505-512.
  79. Skinner J. S., Timko M. P., 1999. Differential expression of genes encoding the light-dependent and light-independent enzymes for protochlorophyllide reduction during development in lobolly pine // Plant Mol. Biol. Vol. 39. P. 577-592.
  80. Shinohara K., Murakami A., Fujita Y., 1992. Biochemical characteristics of thylakoid membranes in chloroplasts of dark-grown pine cotyledons // Plant Physiol. Vol. 98. P. 39-43.
  81. Smith J. H. C., Benitez A., 1953. The protochlorophyllchlorophyll transformation: the nature of protochlorophyll in leaves // Carnegie Inst. Year Book. Washington, DC. 52, P. 151-153.
  82. Smith, J. H. C., French C. S., 1958. Quantum yield for the protochlorophyll conversion // Carnegie Inst. Yeare Book. Washington. Vol. 57. P. 290-293.
  83. Suzuki, J. Y., Bauer C. E., 1992. Light-independent chlorophyll biosynthesis: involvement of the chloroplast gene chlL (frxC) // Plant Cell. Vol. 4. P. 929-940. 84. Suzuki, J. Y, Bauer C. E., 1995. A procaryotic origin for lightdependent chlorophyll biosynthesis of plants // Proc. Natl. Acad. Scie. USA. Vol. 92. P. 3749-3753.
  84. Takio S., Satoh T., 1995. Expression patterns of chloroplast genes involved in light-independent chlorophyll synthesis in liverwort cells // In: Photosynthesis:from Light to Biosphere / ed: Mathi P. Dordrecht. Kluwer Acad. Publ. Vol. III. P. 941-944.
  85. Yamamoto H., Kurumiya S,, Ohashi., Fujita Y., 2009. Oxygen sensitivity of a nitrogenase-like protochlorophyllide reductase from the cyanobacterium Leptolyngbya boryana // Plant Cell Physiol. Vol. 50. P. 1663-1673.
  86. Yamazaki S, Nomata J, Fujita Y., 2006. Differential operation of dual protochlorophyllide reductases for chlorophyll biosynthesis in response to environmental oxygen levels in the cyanobacterium Leptolyngbya boryana // Plant Physiol. Vol. 142. P. 911-922.
  87. Yang J., Chen Q., 2004. Origin and evolution of the light-dependent protochlorophyllide oxidoreductase (LPOR) genes // Plant Biol. Vol. 6. P. 537-544.
  88. Xiong J., Fischer W. M., Inoue K., Nakahara M., Bauer C. E., 2000. Molecular evidence for the early evolution of photosynthesis // Science. Vol. 289. P. 1724-1730.
  89. Wang W. -Y., Wang W. L., Boynton J. E., Gillham N. E. 1974. Genetic control of chlorophyll biosynthesis in Chlamydomonas. Analysis of mutants at two loci mediating the conversion of protoporthyrin-IX to magnesium-protoporphyrin // J. Cell Biol. Vol. 63. P. 806-823.
  90. Wu Q., Vermaas W. F., 1995. Light-dependent chlorophyll a biosynthesis upon chlL deletion in wild type and Photosystem I-less strains of the cyanobacterium Synechocystis sp PCC 6803 // Plant Mol. Biol. Vol. 29. P. 933-945.
  91. Zsebo K. M., Hearst J. E., 1984. Genetic physical mapping of a photosynthetic gene cluster from R. capsulate // Cell. Vol. 37. P. 937-947.
  92. von Wettstein D., Gouth S., Kannangara C. G., 1995. Chlorophyll biosynthesis // Plant Cell. Vol. 7. P. 1039-1057.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2010 Chekunova E.M.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 65617 от 04.05.2016.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies