Triterpenes from Cabralea canjerana as in Vitro Inhibitors to Light Reactions of Photosynthesis


Aims: Cabraleadiol (1), Ocotilone (2) and Odoratone (3) are three triterpenes isolated from Cabralea canjerana (Vell.) Mart. (Meliaceae). They were chemically characterized, and their effect was tested on the light reaction of photosynthesis. Study Design: Natural products were used as models to find new models for inhibitors of photosynthesis. Place and Duration of Study: Departmento de Química, Universidade Federal de São Carlos and Departmento de Bioquímica, Facultad de Química, Universidad Nacional Autonoma de México, between May 2013 and January 2014. Methodology: The natural products had their effect on the light reaction of photosynthesis studied by pollarography and Chlorophyll a (Chl a) fluorescence transients. Results: The compounds inhibited ATP synthesis and electron transport rate (basal, phosphorylating and uncoupled). Therefore, they act as Hill reactions inhibitors. Their inhibition site were located in the range of electron flow from OEC complex and between P680 to QA of PS II, and inhibited the photosystem II (PS II) by inducing the appearance of a K-band which is an indicative that the photochemical apparatus is failing at the donor side of PS II interacting at the OEC complex and by transforming active reaction centers to “heat sinks” or the formation of silent reaction centers unable to reduce QA. Conclusion: Furthermore, these triterpenes inhibit PS II and induce the appearance of small G band which is related with the decreased plastoquinone (PQ) pool reduction.

Share and Cite:

King-Díaz, B. , Soares, M. , G. F. da Silva, M. , Lotina-Hennsen, B. and Veiga, T. (2014) Triterpenes from Cabralea canjerana as in Vitro Inhibitors to Light Reactions of Photosynthesis. American Journal of Plant Sciences, 5, 2528-2540. doi: 10.4236/ajps.2014.516267.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] Diner, B.A. and Babcock, G.T. (1996) Oxygenic Photosynthesis: The Light Reactions. Kluwer Academic Publishers, Dordrecht, 213-247.
[2] Britt, R.D. (1996) Oxygenic Photosynthesis: The Light Reactions. Kluwer Academic Publishers, Dordrecht, 137-159.
[3] Nugent, J.H.A., Rich, A.M. and Evans, M.C.W. (2001) Photosynthetic Water Oxidation: Towards a Mechanism. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1503, 138-146.
[4] Tyystjarvi, E. (2008) Photoinhibition of Photosystem II and Photodamage of the Oxygen Evolving Manganese Cluster. Coordination Chemistry Reviews, 252, 361-376.
[5] Vass, I., Styring, S., Hundal, T., Koivuniemi, A., Aro, E.M. and Andersson, B. (1992) Reversible and Irreversable Intermediates during Photoinhibition of Photosystem II: Stable Reduced QA Species Promote Chlorophyll Triplet Formation. Proceedings of the National Academy of Sciences, 89, 1408-1412.
[6] Vass, I. and Styring, S. (1993) Characterization of Chlorophyll Triplet Promoting States in Photosystem II Sequentially Induced during Photoinhibition. Biochemistry, 32, 3334-3341.
[7] Good, N.E., Izawa, S. and Hind, G. (1981) Current Topics in Bioenergetics. Academic Press, New York, 75-112.
[8] Torres-Romero, D., King-Diaz, B., Jimenez, I.A., Lotina-Hennsen, B. And Bazzocchi, I.L. (2008) Sesquiterpenes from Celastrus Vulcanicola as Photosynthetic Inhibitors. Journal of Natural Products, 71, 1331-1335.
[9] Koodkaew, I., Sunohara, Y., Matsuyama, S. and Matsumoto, H. (2012) Isolation of Ambiguine D Isonitrile from Hapalosiphon sp. and characterization of Its Phytotoxic Activity. Plant Growth Regulation, 68, 141-150.
[10] Menezes-de-Oliveira, D., Aguilar, M.I., King-Díaz, B., Vieira-Filho, A.S., Pains-Duarte, L., Silva, G.D.F. and Lotina-Hennsen, B. (2011) The Triterpenes 3β-Lup-20(29)-en-3-ol and 3β-Lup-20(29)-en-3-yl Acetate and the Carbohydrate 1,2,3,4,5,6-Hexa-O-acetyl-Dulcitol as Photosynthesis Light Reactions Inhibitors. Molecules, 16, 9939-9956.
[11] Macias, F.A., Simonet, A.M. and Esteban, M.D. (1994) Potential Allelopathic Lupane Triterpenes from Bioactive Fractions of Melilotus Messanensis. Phytochemistry, 36, 1369-1379.
[12] Silva, S.R.S., Silva, G.D.F., Barbosa, L.C.A., Duarte, L.P., King-Diaz, B., Archundia-Camacho, F. and Lotina-Hennsen, B. (2007) Uncoupling and Inhibition Properties of 3,4-Seco-Friedelan-3-Oic Acid Isolated from Maytenus Imbricata. Pesticide Biochemistry and Physiology, 87, 109-114.
[13] Torres-Romero, D., King-Diaz, B., Strasser, R.J., Jimenez, I.A., Lotina-Hennsen, B. and Bazzocchi, I.L. (2010) Friedelane Triterpenes from Celastrus vulcanicola as Photosynthetic Inhibitors. Journal of Agricultural and Food Chemistry, 58, 10847-10854.
[14] Achnine, L., Mata, R., Iglesias-Prieto, R. and Lotina-Hennsen, B. (1998) Impairment of Photosystem II Donor Side by the Natural Product Odoratol. Journal of Agricultural and Food Chemistry, 46, 5313-5317.
[15] Cascon, S.C. and Brown Jr., K.S. (1972) Biogenetically Significant Triterpenes in a Species of Meliaceae: Cabralea Polytricha A. Juss. Tetrahedron, 28, 315-323.
[16] Braga, P.A.C., Soares, M.S., Da Silva, M.F.G.F., Vieira, P.C., Fernandes, J.B. and Pinheiro, A.L. (2006) Dammarane Triterpenes from Cabralea canjerana (Vell.) Mart. (Meliaceae): Their Chemosystematic Significance. Biochemical Systematics and Ecology, 34, 282-290.
[17] Aalbersberg, W. and Singh, Y. (1991) Tirucallane Triterpenoids from Dysoxylum hainanense. Phytochemistry, 30, 921-926.
[18] Tanaka, O. and Yahara, S. (1978) Dammarane Saponins of Leaves of Panax pseudo-ginseng subsp. Himalaicus. Phytochemistry, 17, 1353-1358.
[19] Hisham, A., Bai, M.D.A., Fujimoto, Y., Hara, N. and Shimada, H. (1996) Complete 1H and 13C NMR Spectral Assignment of Cabraleadiol, a Dammarane Triterpene from Dysoxylum Malabaricum Bedd. Magnetic Resonance in Chemistry, 34, 146-150.<146::AID-OMR850>3.0.CO;2-U
[20] Mohamad, K., Sevenet, T., Dumontet, V., Pais, M., Tri, V.M., Hadi, H., Awang, K. and Martin, M. (1999) Dammarane Triterpenes and Pregnane Steroids from Aglaia lawii and A. tomentosa. Phytochemistry, 51, 1031-1037.
[21] Roux, D., Martin, M.T., Adeline, M.T., Sevenet, T., Hadi, H. and Pais, M. (1998) Foveolins A and B, Dammarane Triterpenes from Aglaia foveolata. Phytochemistry, 49, 1745-1748.
[22] Veiga, T.A.M., King-Díaz, B., Marques, A.S.F., Sampaio, O.M., Vieira, P.C., da Silva, M.F.G.F. and Lotina-Hennsen, B. (2013) Furoquinoline Alkaloids Isolated from Balfourodendron riedelianum as Photosynthetic Inhibitors in Spinach Chloroplasts. Journal of Photochemistry and Photobiology B: Biology, 120, 36-43.
[23] Morales-Flores, F., Aguilar, M.I., King-Díaz, B. and Lotina-Hennsen, B. (2013) Derivatives of Diterpen Labdane-8α,15-diol as Photosynthetic Inhibitors in Spinach Chloroplasts and Growth Plant Inhibitors. Journal of Photochemistry and Photobiology B: Biology, 125, 42-50.
[24] Mills, J.D., Mitchell, P. and Schurmann, P. (1980) Modulation of Coupling Factor ATPase Activity in Intact Chloroplasts. FEBS Letters, 191, 144-148.
[25] Strain, H.H., Cope, T. and Svec, M.A. (1971) Analytical Procedures for the Isolation, Identification, Estimation and Investigation of the Chlorophylls. Methods in Enzymology, 23, 452-476.
[26] Allen, J.F. and Holmes, N.G. (1986) Photosynthesis: Energy Transduction: A Practical Approach. IRL Press, Oxford, 103-141.
[27] Dilley, R.A. (1972) Ion Transport (H+, K+, Mg2+ Exchange Phenomena). Methods in Enzymology, 24, 68-74.
[28] Strasser, R.J., Srivastava, A. and Govindjee (1995) Polyphasic Chlorophyll a Fluorescence Transient in Plants and Cyanobacteria. Photochemistry and Photobiology, 66, 32-42.
[29] Saha, S., Ouitrakul, R. and Izawa, S. (1971) Electron Transport and Photophosphorylation in Chloroplasts as a Function of the Electron Acceptor. Journal of Biological Chemistry, 246, 3204-3209.
[30] Vernon, L.P. (1969) Photoreduction of 2,6-Dichlorophenolindophenol by Diphenylcarbazide: A Photosystem 2 Reaction Catalyzed by Tris-Washed Chloroplasts and Subchloroplast Fragments. Plant Physiology, 44, 1645-1649.
[31] Rickert, K.W., Sears, J., Beck, W.F. and Brudvig, G.W. (1991) Mechanism of Irreversible Inhibition of O2 Evolution in Thotosystem II by Tris(hydroxymethyl) Aminomethane. Biochemistry, 30, 7888-7896.
[32] Strasser, R.J. (1997) Donor Site Capacity of Photosystem II Probed by Chlorophyll a Transients. Photosynthesis Research, 52, 147-155.
[33] Lazár, D., Pospísil, P. and Naus, J. (1999) Decrease of Fluorescence Intensity after the K Step in Chlorophyll a Fluorescence Induction Is Suppressed by Electron Acceptors and Donors to Photosystem 2. Photosynthetica, 37, 255-265.
[34] Strasser, R.J., Tsimilli-Michael, M. and Srivastava, A. (2004) Chlorophyll Fluorescence: A Signature of Photosynthesis. Kluwer Academic Publishers, Dordrecht, Chapter 12, 321.
[35] Veiga, T.A.M., Silva, S.C., Archundia-Camacho, F., Rodrigues Filho, E., Vieira, P.C., Fernandes, J.B., da Silva, M.F.G.F., Muller, M.W. and Lotina-Hennsen, B. (2007) Inhibition of Photophosphorylation and Electron Transport Chain in Thylakoids by Lasiodiplodin, a Natural Product from Botryosphaeria rhodina. Journal of Agricultural and Food Chemistry, 55, 4217-4221.
[36] Veiga, T.A.M., González-Vásquez, R., Oiano Neto, J., da Silva, M.F.G.F., King-Díaz, B. and Lotina-Hennsen, B. (2007) Siderin from Toona ciliata (Meliaceae) as Photosystem II Inhibitor on Spinach Thylakoids. Archives of Biochemistry and Biophysics, 465, 38-43.

Copyright © 2022 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.