Photosynthetica, 2019 (vol. 57), issue 4

Photosynthetica 2019, 57(4):974-984 | DOI: 10.32615/ps.2019.116

Advances in the members and biosynthesis of chlorophyll family

N.W. QIU1,†, D.C. JIANG1,2,†, X.S. WANG1, B.S. WANG3, F. ZHOU5
1 College of Life Sciences, Qufu Normal University, Qufu, 273165 Shandong, China
2 Shanghai Institute of Nutrition and Health, Shanghai Institutes for Biological Sciences, University of Chinese Academy of Sciences, Chinese Academy of Sciences, 200031 Shanghai, China
3 Shandong Provincial Key Laboratory of Plant Stress, Shandong Normal University, 250014 Jinan, China
5 School of Food Science, Nanjing Xiaozhuang University, 211171 Nanjing, China

Chlorophylls are vital for photosynthesis, allowing plants to absorb energy from light for photosynthesis. More than one hundred species of chlorophyll have been identified. Among them, chlorophylls a, b, c (c1, c2, and c3), d, and f exist in oxygenic photosynthetic organisms (e.g., higher plants, algae, and cyanobacteria), whereas anoxygenic photosynthetic bacteria possess bacteriochlorophylls a, b, c, d, e, and g. These chlorophylls have different chemical structures and properties that enable photosynthetic organisms to perform photosynthesis in different environments. All of the chlorophylls are biosynthesized from 3,8-divinyl-protochlorophyllide a by a series of enzymes. The synthetic pathways of chlorophylls have now been basically clarified. This review succinctly summarizes the structures, properties, and synthetic pathways of the chlorophylls.

Keywords: absorption spectrum; chemical bond; porphyrin; side chain; synthetase.

Received: February 23, 2019; Accepted: July 22, 2019; Prepublished online: September 3, 2019; Published: November 1, 2019Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
QIU, N.W., JIANG, D.C., WANG, X.S., WANG, B.S., & ZHOU, F. (2019). Advances in the members and biosynthesis of chlorophyll family. Photosynthetica, 57(4), 974-984. doi: 10.32615/ps.2019.116.
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Addlesee H.A., Fiedor L., Hunter C.N.: Physical mapping of bchG, orf427, and orf177 in the photosynthesis gene cluster of Rhodobacter sphaeroides: Functional assignment of the bacteriochlorophyll synthetase gene. - J. Bacteriol. 182: 3175-3182, 2000. Go to original source...
    2. Allakhverdiev S.I., Kreslavski V.D., Zharmukhamedov S.K. et al.: Chlorophylls d and f and their role in primary photosynthetic processes of cyanobacteria. - Biochemistry-Moscow+ 81: 201-212, 2016. Go to original source...
    3. Allen M.B.: Distribution of chlorophylls. - In: Vernon L.P., Seely G.R. (ed.): The Chlorophylls. Pp.511-519. Academic Press, New York 1966. Go to original source...
    4. Beale S.I.: Biosynthesis of photosynthetic pigments. - In: Baker N.R., Barber J. (ed.): Chloroplast Biogenesis. Pp. 135-205. Elsevier, Amsterdam 1984.
    5. Beale S.I.: Green genes gleaned. - Trends Plant Sci. 10: 309-312, 2005. Go to original source...
    6. Beale S.I.: Biosynthesis of 5-aminolevulinic acid. - In: Grimm B., Porra R.J., Rüdiger W., Scheer H. (ed.): Chlorophylls and Bacteriochlorophylls. Advances in Photosynthesis and Respiration. Pp. 147-158. Springer, Dordrecht 2006. Go to original source...
    7. Bennett M.S., Triemer R.E.: Chloroplast genome evolution in the Euglenaceae. - J. Eukaryot. Microbiol. 62: 773-785, 2015. Go to original source...
    8. Björkman O.: Responses to different quantum flux densities. - In: Lange O.L., Nobel P.S., Osmond C.B., Ziegler H. (ed.): Physiological Plant Ecology I. Responses to the Physical Environment. Pp. 57-107. Springer-Verlag, New York 1981. Go to original source...
    9. Björn L.O., Papageorgiou G.C., Blankenship R.E., Govindjee: A viewpoint: Why chlorophyll a? - Photosynth. Res. 99: 85-98, 2009. Go to original source...
    10. Bogorad L.: Chlorophyll biosynthesis. - In: Goodwin T.W. (ed.): Chemistry and Biochemistry of Plant Pigments. Pp. 64-148. Academic Press Inc., London 1976.
    11. Bollivar D.W., Suzuki J.Y., Beatty J.T., Dobrowolski J.M., Bauer C.E.: Directed mutational analysis of bacteriochlorophyll a biosynthesis in Rhodobacter capsulatus. - J. Mol. Biol. 237: 622-640, 1994. Go to original source...
    12. Bollivar D.W.: Recent advances in chlorophyll biosynthesis. - Photosynth. Res. 90: 173-194, 2006.
    13. Brestič M., Živčák M., Kunderlíková K., Allakhverdiev S.I.: High temperature specifically affects the photoprotective responses of chlorophyll b deficient wheat mutant lines. - Photosyn. Res. 130: 251-266, 2016. Go to original source...
    14. Canniffe D.P., Chidgey J.W., Hunter C.N.: Elucidation of the preferred routes of C8-vinyl reduction in chlorophyll and bacteriochlorophyll biosynthesis. - Biochem. J. 462: 433-440, 2014. Go to original source...
    15. Chen M., Blankenship R.E.: Expanding the solar spectrum used by photosynthesis. - Trends Plant Sci. 16: 427-431, 2011. Go to original source...
    16. Chen M., Schliep M., Willows R.D. et al.: A red-shifted chlorophyll. - Science 329: 1318-1319, 2010. Go to original source...
    17. Chen M.: Chlorophyll modifications and their spectral extension in oxygenic photosynthesis. - Annu. Rev. Biochem. 83: 317-340, 2014. Go to original source...
    18. Chew A.G.M., Bryant D.A.: Chlorophyll biosynthesis in bacteria: The origins of structural and functional diversity. - Annu. Rev. Microbiol. 61: 113-129, 2007. Go to original source...
    19. Chew A.G.M., Frigaard N.U., Bryant D.A.: Bacteriochlorophyllide c C-82 and C-121 methyltransferases are essential for adaptation to low light in Chlorobaculum tepidum. - J. Bacteriol. 189: 6176-6184, 2007. Go to original source...
    20. Croce R., van Amerongen H.: Natural strategies for photosynthetic light harvesting. - Nat. Chem. Biol. 10: 492-501, 2014. Go to original source...
    21. Eisen J.A., Nelson K.E., Paulsen I.T. et al.: The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium. - P. Natl. Acad. Sci. USA 99: 9509-9514, 2002. Go to original source...
    22. Esteban R., Barrutia O., Artetxe U. et al.: Internal and external factors affecting photosynthetic pigment composition in plants: a meta-analytical approach. - New Phytol. 206: 268-280, 2015. Go to original source...
    23. Fawley M.W.: A new form of chlorophyll c involved in light-harvesting. - Plant Physiol. 91: 727-732, 1989. Go to original source...
    24. Fookes C.J.R., Jeffrey S.W.: The structure of chlorophyll c3, a novel marine photosynthetic pigment. - J. Chem. Soc. Chem. Comm. 23: 1827-1828, 1989.
    25. Frigaard N.U., Chew A.G.M., Li H. et al.: Chlorobium tepidum: Insights into the structure, physiology, and metabolism of a green sulfur bacterium derived from the complete genome sequence. - Photosynth. Res. 78: 93-117, 2003. Go to original source...
    26. Frigaard N.U., Chew A.G.M., Maresca J.A., Bryant D.A.: Bacteriochlorophyll biosynthesis in green bacteria. - In: Grimm B., Porra R.J., Rüdiger W., Scheer H. (ed.): Chlorophylls and Bacteriochlorophylls. Advances in Photosynthesis and Respiration. Pp. 201-221. Springer, Dordrecht 2006. Go to original source...
    27. Frigaard N.U., Voigt G.D., Bryant D.A.: Chlorobium tepidum mutant lacking bacteriochlorophyll c made by inactivation of the bchK gene, encoding bacteriochlorophyll c synthase. - J. Bacteriol. 184: 3368-3376, 2002. Go to original source...
    28. Gan F., Zhang S., Rockwell N.C. et al.: Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. - Science 345: 1312-1317, 2014. Go to original source...
    29. Garcia-Gil L.J., Gich F.B., Fuentes-Garcia X.: A comparative study of bchG from green photosynthetic bacteria. - Arch. Microbiol. 179: 108-115, 2003. Go to original source...
    30. Garg H., Loughlin P.C., Willows R.D., Chen M.: The C21-formyl group in chlorophyll f originates from molecular oxygen. - J. Biol. Chem. 292: 19279-19289, 2017. Go to original source...
    31. Glaeser J., Bañeras L., Rütters H., Overmann J.: Novel bacteriochlorophyll e structures and species-specific varia-bility of pigment composition in green sulfur bacteria. - Arch. Microbiol. 177: 475-485, 2002. Go to original source...
    32. Gloe A., Pfennig N., Brockmann Jr. H., Trowitzsch W.: A new bacteriochlorophyll from brown-colored Chlorobiaceae. - Arch. Microbiol. 102: 103-109, 1975. Go to original source...
    33. Granick S.: The structural and functional relationships between heme and chlorophyll. - Harvey Lect. 44: 220-245, 1948.
    34. Green B., Anderson J., Parson W.W.: Photosynthetic membranes and their light-harvesting antennas. - In: Green B., Parson W. (ed.): Light-Harvesting Antennas in Photosynthesis. Pp. 1-28. Kluwer Academic Publishers, Dordrecht 2003. Go to original source...
    35. Harada J., Mizoguchi T., Tsukatani Y. et al.: Chlorophyllide a oxidoreductase works as one of the divinyl reductases specifically involved in bacteriochlorophyll a biosynthesis. - J. Biol. Chem. 289: 12716-12726, 2014. Go to original source...
    36. Harada J., Saga Y., Yaeda Y. et al.: In vitro activity of C-20 methyltransferase, BchU, involved in bacteriochlorophyll c biosynthetic pathway in green sulfur bacteria. - FEBS Lett. 579: 1983-1987, 2005. Go to original source...
    37. Harada J., Teramura M., Mizoguchi T. et al.: Stereochemical conversion of C3-vinyl group to 1-hydroxyethyl group in bacteriochlorophyll c by the hydratases BchF and BchV: adaptation of green sulfur bacteria to limited-light environments. - Mol. Microbiol. 98: 1184-1198, 2015. Go to original source...
    38. Hastings G., Durrant J.R., Barber J. et al.: Observation of pheophytin reduction in photosystem two reaction centers using femtosecond transient absorption spectroscopy. - Biochemistry 31: 7638-7647, 1992. Go to original source...
    39. Helfrich M., Bommer B., Oster U. et al.: Chlorophylls of the c family: Absolute configuration and inhibition of NADPH:protochlorophyllide oxidoreductase. - BBA-Bioenergetics 1605: 97-103, 2003. Go to original source...
    40. Heyes D.J., Heathcote P., Rigby S.E.J. et al.: The first catalytic step of the light-driven enzyme protochlorophyllide oxidoreductase proceeds via a charge transfer complex. - J. Biol. Chem. 281: 26847-26853, 2006. Go to original source...
    41. Ho M.Y., Shen G., Canniffe D.P. et al.: Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II. - Science 353: aaf9178, 2016.
    42. Huster M.S., Smith K.M.: Biosynthetic studies of substituent homologation in bacteriochlorophylls c and d. - Biochemistry 29: 4348-4355, 1990. Go to original source...
    43. Ishikita H., Saenger W., Biesiadka J. et al.: How photosynthetic reaction centers control oxidation power in chlorophyll pairs P680, P700, and P870. - P. Natl. Acad. Sci. USA 103: 9855-9860, 2006. Go to original source...
    44. Klimov V.V.: Discovery of pheophytin function in the photo-synthetic energy conversion as the primary electron acceptor of Photosystem II. - Photosynth. Res. 76: 247-253, 2003. Go to original source...
    45. Kobayashi M., Akiyama M., Kise H., Watanabe T.: Unusual tetrapyrrole pigments of photosynthetic antenna and reaction centers: specially-tailored chlorophylls. - In: Grimm B., Porra R.J., Rüdiger W., Scheer H. (ed.): Chlorophylls and Bacteriochlorophylls. Advances in Photosynthesis and Respiration. Pp. 56-63. Springer, Dordrecht 2006. Go to original source...
    46. Kühl M., Chen M., Larkum A.W.D.: Algae and cyanobacteria in extreme environments. - In: Seckbach J. (ed.): Cellular Origin, Life in Extreme Habitats and Astrobiology. Pp. 101-123. Springer, Dordrecht 2007.
    47. Lange C., Kiesel S., Peters S. et al.: Broadened substrate specificity of 3-hydroxyethyl bacteriochlorophyllide a dehydrogenase (BchC) indicates a new route for the biosynthesis of bacteriochlorophyll a. - J. Biol. Chem. 290: 19697-19709, 2015. Go to original source...
    48. Larkum A.W.D., Kühl M.: Chlorophyll d: the puzzle resolved. - Trends Plant Sci. 10: 355-357, 2005. Go to original source...
    49. Larkum A.W.D., Ritchie R.J., Raven J.A.: Living off the Sun: chlorophylls, bacteriochlorophylls and rhodopsins. - Photosynthetica 56: 11-43, 2018. Go to original source...
    50. Li B., Bridwell-Rabb J.: Aerobic enzymes and their radical SAM enzyme counterparts in tetrapyrrole pathways. - Biochemistry 58: 85-93, 2019. Go to original source...
    51. Liu Z.F., Bryant D.A.: Identification of a gene essential for the first committed step in the biosynthesis of bacterio- chlorophyll c. - J. Biol. Chem. 286: 22393-22402, 2011. Go to original source...
    52. Manning W.M., Strain H.H.: Chlorophyll d, a green pigment of red algae. - J. Biol. Chem. 151: 1-19, 1943.
    53. Maresca J.A., Chew A.G.M., Ponsatí M.R. et al.: The bchU gene of Chlorobium tepidum encodes the bacteriochlorophyll C-20 methyltransferase. - J. Bacteriol. 186: 2558-2566, 2004. Go to original source...
    54. Melkozernov A.N., Blankenship R.E.: Photosynthetic functions of chlorophylls. - In: Grimm B., Porra R.J., Rüdiger W., Scheer H. (ed.): Chlorophylls and Bacteriochlorophylls. Advances in Photosynthesis and Respiration. Pp. 397-410. Springer, Dordrecht 2006. Go to original source...
    55. Miyashita H., Adachi K., Kurano N. et al.: Pigment composition of a novel oxygenic photosynthetic prokaryote containing chlorophyll d as the major chlorophyll. - Plant Cell Physiol. 38: 274-281, 1997. Go to original source...
    56. Moss G.P.: Nomenclature of tetrapyrroles. IUPAC-IUB Joint Commission on Biochemical Nomenclature (JCBN). Recommendations 1986. - Eur. J. Biochem. 178: 277-328, 1988. Go to original source...
    57. Niedzwiedzki D.M., Blankenship R.E.: Singlet and triplet excited state properties of natural chlorophylls and bacteriochlorophylls. - Photosynth. Res. 106: 227-238, 2010. Go to original source...
    58. Nomata J., Mizoguchi T., Tamiaki H., Fujita Y.: 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. 281: 15021-15028, 2006. Go to original source...
    59. Oh J.I., Eraso J.M., Kaplan S.: Interacting regulatory circuits involved in orderly control of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. - J. Bacteriol. 182: 3081-3087, 2000. Go to original source...
    60. Pinta V., Picaud M., Reiss-Husson F., Astier C.: Rubrivivax gelatinosus acsF (previously orf358) codes for a conserved, putative binuclear-iron-cluster-containing protein involved in aerobic oxidative cyclization of Mg-protoporphyrin IX monomethylester. - J. Bacteriol. 184: 746-753, 2002. Go to original source...
    61. Porra R.J., Schäfer W., Gad'on N. et al.: Origin of the two carbonyl oxygens of bacteriochlorophyll a: Demonstration of two different pathways for the formation of ring E in Rhodobacter sphaeroides and Roseobacter denitrificans, and a common hydratase mechanism for 3-acetyl group formation. - Eur. J. Biochem. 239: 85-92, 1996. Go to original source...
    62. Porra R.J.: Recent progress in porphyrin and chlorophyll biosynthesis. - Photochem. Photobiol. 65: 492-516, 1997. Go to original source...
    63. Raven P.H., Evert R.F., Eichhorn S.E.: Photosynthesis, light, and life. - In: Biology of Plants (7th Edition). Pp. 119-127. W.H. Freeman and Company Publishers, New York 2005.
    64. Reid J.D., Hunter C.N.: Magnesium-dependent ATPase activity and cooperativity of magnesium chelatase from Synechocystis sp. PCC6803. - J. Biol. Chem. 279: 26893-26899, 2004. Go to original source...
    65. Saunders A.H., Golbeck J.H., Bryant D.A.: Characterization of BciB: A ferredoxin-dependent 8-vinyl-protochlorophyllide reductase from the green sulfur bacterium Chloroherpeton thalassium. - Biochemistry 52: 8442-8451, 2013. Go to original source...
    66. Scheer H.: An overview of chlorophylls and bacteriochlorophylls: Biochemistry, biophysics, functions and applications. - In: Grimm B., Porra R.J., Rüdiger W., Scheer H. (ed.): Chlorophylls and Bacteriochlorophylls. Advances in Photo-synthesis and Respiration. Pp. 1-19. Springer, Dordrecht 2006. Go to original source...
    67. Schliep M., Crossett B., Willows R.D., Chen M.: 18O labeling of chlorophyll d in Acaryochloris marina reveals that chloro-phyll a and molecular oxygen are precursors. - J. Biol. Chem. 285: 28450-28456, 2010. Go to original source...
    68. Suzuki J.Y., Bauer C.E.: A prokaryotic origin for light-dependent chlorophyll biosynthesis of plants. - P. Natl. Acad. Sci. USA 92: 3749-3753, 1995. Go to original source...
    69. Suzuki J.Y., Bollivar D.W., Bauer C.E.: Genetic analysis of chlorophyll biosynthesis. - Annu. Rev. Genet. 31: 61-89, 1997. Go to original source...
    70. Tamiaki H., Komada J., Kunieda M. et al.: In vitro synthesis and characterization of bacteriochlorophyll-f and its absence in bacteriochlorophyll-e producing organisms. - Photosynth. Res. 107: 133-138, 2011. Go to original source...
    71. Tamiaki H., Teramura M., Tsukatani Y.: Reduction processes in biosynthesis of chlorophyll molecules: chemical implication of enzymatically regio- and stereoselective hydrogenations in the late stages of their biosynthetic pathway. - B. Chem. Soc. Jpn. 89: 161-173, 2016. Go to original source...
    72. Tanaka A., Ito H., Tanaka R. et al.: Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. - P. Natl. Acad. Sci. USA 95: 12719-12723, 1998. Go to original source...
    73. Tanaka R., Tanaka A.: Chlorophyll cycle regulates the construction and destruction of the light-harvesting complexes. - BBA-Bioenergetics 1807: 968-976, 2011.
    74. Taniguchi M., Lindsey J.S.: Synthetic chlorins, possible surrogates for chlorophylls, prepared by derivatization of porphyrins. - Chem. Rev. 117: 344-535, 2017. Go to original source...
    75. Teramura M., Harada J., Mizoguchi T. et al.: In vitro assays of BciC showing C132-demethoxycarbonylase activity requisite for biosynthesis of chlorosomal chlorophyll pigments. - Plant Cell Physiol. 57: 1048-1057, 2016a. Go to original source...
    76. Teramura M., Harada J., Tamiaki H.: In vitro stereospecific hydration activities of the 3-vinyl group of chlorophyll derivatives by BchF and BchV enzymes involved in bacteriochlorophyll c biosynthesis of green sulfur bacteria. - Photosynth. Res. 130: 33-45, 2016b. Go to original source...
    77. Thweatt J.L., Ferlez B.H., Golbeck J.H., Bryant D.A.: BciD is a radical S-adenosyl-l-methionine (SAM) enzyme that completes bacteriochlorophyllide e biosynthesis by oxidizing a methyl group into a formyl group at C-7. - J. Biol. Chem. 292: 1361-1373, 2017. Go to original source...
    78. Tsuchiya T., Mizoguchi T., Akimoto S. et al.: Metabolic engineering of the Chl d-dominated cyanobacterium Acaryochloris marina: Production of a novel Chl species by the introduction of the chlorophyllide a oxygenase gene. - Plant Cell Physiol. 53: 518-527, 2012. Go to original source...
    79. Tsukatani Y., Harada J., Nomata J. et al.: Rhodobacter sphaeroides mutants overexpressing chlorophyllide a oxidoreductase of Blastochloris viridis elucidate functions of enzymes in late bacteriochlorophyll biosynthetic pathways. - Sci. Rep. 5: 9741, 2015. Go to original source...
    80. Tsukatani Y., Yamamoto H., Harada J. et al.: An unexpectedly branched biosynthetic pathway for bacteriochlorophyll b capable of absorbing near-infrared light. - Sci Rep. 3: 1217, 2013a. Go to original source...
    81. Tsukatani Y., Yamamoto H., Mizoguchi T. et al.: Completion of biosynthetic pathways for bacteriochlorophyll g in Heliobacterium modesticaldum: The C8-ethylidene group formation. - BBA-Bioenergetics 1827: 1200-1204, 2013b.
    82. Van Gorkom H.J.: Identification of the reduced primary electron acceptor of Photosystem II as a bound semiquinone anion. - BBA-Bioenergetics 347: 439-442, 1974. Go to original source...
    83. Vogl K., Tank M., Orf G.S. et al.: Bacteriochlorophyll f: properties of chlorosomes containing the "forbidden chlorophyll". - Front. Microbiol. 3: 298, 2012. Go to original source...
    84. Walker C.J., Willows R.D.: Mechanism and regulation of Mg-chelatase. - Biochem. J. 327: 321-333, 1997. Go to original source...
    85. Wang P.R., Gao J.X., Wan C.M. et al.: Divinyl chlorophyll(ide) a can be converted to monovinyl chlorophyll(ide) a by a divinyl reductase in rice. - Plant Physiol. 153: 994-1003, 2010. Go to original source...
    86. Willows R.D.: Biosynthesis of chlorophylls from proto- porphyrin IX. - Nat. Prod. Rep. 20: 327-341, 2003. Go to original source...
    87. Willows R.D., Li Y., Scheer H., Chen M.: Structure of chloro-phyll f. - Org. Lett. 15: 1588-1590, 2013. Go to original source...
    88. Xu M., Kinoshita Y., Matsubara S., Tamiaki H.: Synthesis of chlorophyll-c derivatives by modifying natural chlorophyll-a. -Photosynth. Res. 127: 335-345, 2016. Go to original source...
    89. Yamazaki S., Nomata J., Fujita Y.: Differential operation of dual protochlorophyllide reductases for chlorophyll biosynthesis in response to environmental oxygen levels in the cyanobacterium Leptolyngbya boryana. - Plant Physiol. 142: 911-922, 2006. Go to original source...
    90. Zapata M., Garrido J.L., Jeffrey S.W.: Chlorophyll c pigments: Current status. - In: Grimm B., Porra R.J., Rüdiger W., Scheer H. (ed.): Chlorophylls and Bacteriochlorophylls. Advances in Photosynthesis and Respiration. Pp. 40-50. Springer, Dordrecht 2006. Go to original source...

    Return to the content