Abstract
Abstract
The long-lasting discussion, why plants produce secondary metabolites, which are pharmacologically and toxicologically active towards mammals traces back to the eminent role of medicinal plants in the millennia-old history of manhood. In recent years, the concept of an animal plant warfare emerged, which focused on the co-evolution between plants and herbivores. As a reaction to herbivory, plants developed mechanical defenses such as thorns and hard shells, which paved the way for adapted animal physiques. Plants evolved further defense systems by producing chemicals that exert toxic effects on the animals that ingest them. As a result of this selective pressure, animals developed special enzymes, e.g. cytochrome P450 monooxigenases (CYP450) that metabolize xenobiotic phytochemicals. As a next step in the evolutionary competition between plants and animals, plants evolved to produce non-toxic pro-drugs, which become toxic only after ingestion by animals through metabolization by enzymes such as CYP450. Because these sequestered evolutionary developments call to mind an arms race, the term animal plant warfare has been coined. The evolutionary competition between plants and animals may help to better understand the modes of action of medicinal plants and to foster the efficient and safe use of phytotherapy nowadays.
Graphical abstract
Article PDF
Similar content being viewed by others
References
Berenbaum, M. R. Proc. Natl. Acad. Sci. USA1995, 92, 2–8.
Gould, S. J.; Lewontin, R. C. Proc. R. Soc. Lond. B1979, 205, 581–598.
Valladares, G. R.; Zapata, A.; Zygadlo, J.; Banchio, E. J. Agric. Food Chem.2002, 50, 4059–4061.
Iason, G. R.; Villalba, J. J. J. Chem. Ecol.2006, 32, 1115–1132.
Vokou, D.; Kokkinit, S.; Bessiere, J. M. Biochem. Syst. Ecol.1993, 21, 287–295.
Maffei, M.; Mucciarelli, M.; Scannerini, S. Biochem. Syst. Ecol.1993, 21, 765–784.
McLean, S.; Duncan, A. J. J. Chem. Ecol.2006, 32, 1213–1228.
Bryant, J. P.; Clausen, T. P.; Swihart, R. K.; Landhäusser, S. M.; Stevens, M. T.; Hawkins, C. D.; Carrière, S.; Kirilenko, A. P.; Veitch, A. M.; Popko, R. A.; Cleland, D. T.; Williams, J. H.; Jakubas, W. J.; Carlson, M. R.; Bodony, K. L.; Cebrian, M.; Paragi, T. F.; Picone, P. M.; Moore, J. E.; Packee, E. C.; Malone, T. Am. Nat.2009, 174,13-23.
Mitchell, J. R.; Potter, W. Z.; Hinson, J. A.; Snodgrass, W. R.; Timbrell, J. A.; Gillette, J. R. Toxic drug reactions. Pages 383–419 in Gillete, J. R.; Mitchell J. R. eds. Handbook of Experimental Pharmacology vol. 28, part 3. Springer, 1975.
Swihart, R. K.; DeAngelis, D. L.; Feng, Z.; Bryant, J. P. BMC Ecol.2009, 9, 5.
Marsh, K. J.; Wallis, I. R.; Andrew, R. L.; Foley, W. J. J. Chem. Ecol.2006, 32, 1247–1266.
Sorensen, J. S.; Dearing, M. D. Oecologia2003, 134, 88–94.
DeGabriel, J. L.; Moore, B. D.; Foley, W. J.; Johnson, C. N. Ecology2009, 90, 711–719.
Zangerl, A. R.; Berenbaum, M. R. J. Chem. Ecol.2004, 30, 1985–2002.
Marsh, K. J.; Foley, W. J.; Cowling, A.; Wallis, I. R. J. Comp. Physiol. B2003, 173, 69–78.
DeGabriel, J. L.; Moore, B. D.; Shipley, L. A.; Krockenberger, A. K.; Wallis, I. R.; Johnson, C. N.; Foley, W. J. Oecologia2009, 161, 539–48.
Haley, S. L.; Lamb, J. G.; Franklin, M. R.; Constance, J. E.; Dearing, M. D. Physiol. Biochem. Zool.2008, 81, 584–93.
Magnanou, E.; Malenke, J. R.; Dearing, M. D. Mol. Ecol.2009, 18, 2401–2414.
Wiggins, N. L.; McArthur, C.; McLean, S.; Boyle, R. J. Chem. Ecol.2003, 29, 147–1464.
Marsh, K. J.; Wallis, I. R.; Foley, W. J. Nature2002, 419, 712–715.
Li, W.; Schuler, M. A.; Berenbaum, M. R. Proc. Natl. Acad. Sci. USA2003, 100, 14593–14598.
Li, W.; Zangerl, A. R.; Schuler, M. A.; Berenbaum, M. R. Insect Mol. Biol.2004, 13, 603–613.
Kohl, K. D.; Dearing, M. D. J. Exp. Biol.2011, 214, 4133–4140.
Marsh, K. J.; Wallis, I. R.; McLean, S.; Sorensen, J. S.; Foley, W. J. Ecology2006, 87, 2103–2112.
Wiggins, N. L.; McArthur, C.; Davies, N. W. Oecologia2006, 147, 650–657.
Wiggins, N. L.; McArthur, C.; Davies, N. W.; McLean, S. J. Chem. Ecol.2006, 32, 1133–1147.
Shipley, L. A.; Forbey, J. S.; Moore, B. D. Integr. Comp. Biol.2009, 49, 274–290.
Skopec, M. M.; Haley, S.; Dearing, M. D. Comp. Biochem. Physiol. Part D Genomics Proteomics2007, 2, 34–43.
Skopec, M. M.; Haley, S.; Torregrossa, A. M.; Dearing, M. D. Physiol. Biochem. Zool.2008, 81, 426–433.
Torregrossa, A. M.; Azzara, A. V.; Dearing, M. D. Oecologia2012, 168, 711–718.
Piccaglia, R.; Marottil, M.; Giovanellil, E.; Deans, S. G.; Eaglesham, E. Ind. Crops Prod.1993, 2, 47–50.
Zahorik, D. M.; Houpt, K. A.; Swartzmanadert, J. Appl. Animal Behav. Sci.1990, 26, 27–39.
Müller-Schwarze, D.; Thoss, V. J. Chem. Ecol.2008, 34, 1377–1381.
Mucciarelli, M.; Camusso, W.; Bertea, C. M.; Bossi, S.; Maffei, M. Phytochemistry2001, 57, 91–98.
Umezu, T.; Sakata, A.; Ito, H. Pharmacol. Biochem. Behav.2001, 69, 383–390.
Moorthy, B.; Madyastha, P.; Madyastha, K. M. Indian J. Chem. Section B1991, 30, 138–146.
McClanahan, R. H.; Thomasse, N. D.; Slattery, J. T.; Nelson, S. D. Chem. Res. Toxicol.1989, 2, 349–355.
European Agency for the Evaluation of Medicinal Products (EMEA). 2005, http://www.ema.europa.eu/docs/en_GB/document_library/Scientific_guideline/2010/04/WC500089958.pdf.
Maffei, M.; Camusso, W.; Sacco, S. Phytochemistry2001, 58, 703–707.
Gershenzon, J. J. Chem. Ecol.1994, 20, 1281–1328.
Gershenzon, J.; McConkey, E.; Croteau, R. B. Plant Physiol.2000, 122, 205–214.
Turner, G. W.; Croteau, R. Plant Physiol.2004, 136, 4215–4227.
De Feo, V.; Ricciardi, A. I.; Biscardi, D.; Senatore, F. J. Essential Oil Res.1998, 10, 61–65.
McConkey, M. E.; Gershenzon, J.; Croteau, R. B. Plant Physiol.2000, 122, 215–224.
Latta, R. G.; Linhart, Y. B.; Snyder, M. A.; Lundquist, L. Biochem. Syst. Ecol.2003, 31, 451–465.
Thoss, V.; O’Reilly-Wapstra, J.; Iason, G. R. J. Chem. Ecol.2007, 33, 477–491.
McAuslane, H. J.; Alborn, H. T.; Toth, J. P. J. Chem. Ecol.1997, 23, 2861–2879.
Baldwin, I. T. Chemical changes rapidly induced by folivory. Pages 1–23. In Bernays E, ed. Insect-Plant Interaction. CRC Press, 1994.
Barnola, L. F.; Hasegawa, M.; Cedno, A. Biochem. Syst. Ecol.1994, 22, 437–45.
Zygadlo, J.; Maestri, D. M.; Lamarque, A. L.; Guzman, C. A.; Velasco-Negueruela, A.; Perez Alonso, M. J.; Garcia-Vallejos, M. C.; Grosso, N. R. Biochem. Syst. Ecol.1994, 24, 319–323.
Alkire, B. H.; Tucker, A. O.; Maciarello, M. J. Econ. Bot.1994, 48, 60–64.
De Moraes, C. M.; Lewis, D. J.; Pare, P. W.; Alborn, H. T.; Tumlinson, J. H. Nature1998, 393, 570–573.
Halpern, M.; Raats, D.; Lev-Yadun, S. Environm. Microbiol.2007, 9, 584–592.
Stermitz, F. R.; Lorenz, P.; Tawara, J. N.; Zenewicz, L. A.; Lewis, K. Proc. Natl. Acad. Sci. USA2000, 97, 1433–1437.
Efferth T. Curr. Mol. Med.2001, 1, 45–65.
Gillet, J. P.; Efferth, T.; Remacle, J. Biochim. Biophys. Acta2007, 1775, 237–262.
Eichhorn, T.; Efferth, T. J. Ethnopharmacol.2012, 141, 557–570.
Efferth, T. Planta Med.2012, 78, 935–942.
Sorensen, J. S.; Dearing, M. D. J. Chem. Ecol.2006, 32, 1181–1196.
Sorensen, J. S.; Turnbull, C. A.; Dearing, M. D. Physiol. Biochem. Zool.2004, 77, 139–148.
Pass, G. J.; McLean, S.; Stupans, I.; Davies, N. Xenobiotica2001, 31, 205–221.
Madabushi, R.; Frank, B.; Drewelow, B.; Derendorf, H.; Butterweck, V. Europ. J. Clin. Pharmacol.2006, 62, 225–233.
Fahey, J. W.; Stephenson, K. K.; Dinkova-Kostova, A. T.; Egner, P. A.; Kensler, T. W.; Talalay, P. Carcinogenesis2005, 26, 1247–1255.
Fau, D.; Lekehal, M.; Farrell, G.; Moreau, A.; Moulis, C.; Feldmann, G.; Haouzi, D.; Pessayre, D. Gastroenterology1997, 113, 1334–1346.
Danielson, P. B. Curr. Drug Metabol.2002, 3, 561–597.
Gonzalez, F. J.; Nebert, D. W. Trends Genet.1990, 6, 182–186.
Conney, A. H. Pharmacol. Rev.1967, 19, 317–366.
Efferth, T. Molekulare Pharmakologie und Toxikologie. Springer, 2006.
Khani, S. C.; Zaphiropoulos, P. G.; Fujita, V. S.; Porter, T. D.; Koop, D. R.; Coon, M. J. Proc. Natl. Acad. Sci. USA1987, 84, 638–642.
Nebert, D. W.; Nelson, D. R.; Feyereisen, R. Xenobiotica1989, 19, 1149–1160.
Lewis, D. F.; Watson, E.; Lake, B. G. Mutat. Res.1998, 410, 245–270.
Cloud, P. Paleobiology1976, 2, 351–387.
Dover, G. A.; Tautz, D. Philos. Trans. R. Soc. Lond. B Biol. Sci.1986, 312, 275–289.
Dover, D. A. J. Mol. Evol.1987, 26, 47–58.
Strachan, T.; Read, A. Human molecular genetics. Wiley-Liss, 4th ed. 2010.
Heim, M. H.; Meyer, U. A. Genomics1992, 14, 49–58.
Kaplowitz, N. Gastroenterology1997, 113, 1408–1412.
Author information
Authors and Affiliations
Corresponding author
Additional information
This article is published with open access at Springerlink.com
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 2.0 International License (https://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
About this article
Cite this article
Wöll, S., Kim, S.H., Greten, H.J. et al. Animal plant warfare and secondary metabolite evolution. Nat. Prod. Bioprospect. 3, 1–7 (2013). https://doi.org/10.1007/s13659-013-0004-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13659-013-0004-0