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Postgenomic Chemical Ecology: From Genetic Code to Ecological Interactions

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Abstract

Environmental response genes are defined as those encoding proteins involved in interactions external to the organism, including interactions among organisms and between the organism and its abiotic environment. The general characteristics of environmental response genes include high diversity, proliferation by duplication events, rapid rates of evolution, and tissue-or temporal-specific expression. Thus, environmental response genes include those that encode proteins involved in the manufacture, binding, transport, and breakdown of semiochemicals. Postgenomic elucidation of the function of such genes requires an understanding of the chemical ecology of the organism and, in particular, of the “small molecules” that act as selective agents either by promoting survival or causing selective mortality. In this overview, the significance of several groups of environmental response genes is examined in the context of chemical ecology. Cytochrome P-450 monooxygenases provide a case in point; these enzymes are involved in the biosynthesis of furanocoumarins (furocoumarins), toxic allelochemicals, in plants, as well as in their detoxification by lepidopterans. Biochemical innovations in insects and plants have historically been broadly defined in a coevolutionary context. Considerable insight can be gained by defining with greater precision components of those broad traits that contribute to diversification. Molecular approaches now allow chemical ecologists to characterize specifically those biochemical innovations postulated to lead to adaptation and diversification in plant/insect interactions.

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REFERENCES

  • adams, M. D., Celniker, S. E., Holt, R. A., Evans, C. A., Gocayne, J. D., Amanatides, P.G., Scherer, S. E., Li, P. W., Hoskins, R. A., Galle, R. F., George, R. A., Lewis, S. E., Richards, S., Ashburner, M., Henderson, S. N., Sutton, G. G., Wortman, J. R., Yandell, M. D., Zhang, Q., Chen, L. X., Brandon, R. C., Rogers, Y. H. C., Blazej, R. G., Champe, M., Pfeiffer, B. D., et al. 2000. The genome sequence of Drosophila.Science 287:2185–2191.

    Google Scholar 

  • Akashi, T., Aoki, T., and Ayabe, S. 1999.Cloning and functional expression of a cytochrome P-450 cDNA encoding 2-hydroxyisoflavanone synthase involved in the biosynthesis of the isoflavonoid skeleton in licorice.Plant Physiol. 121:821–828.

    PubMed  Google Scholar 

  • Anonymous. 2000. Millenium bug captures media.ANIC News 16:13.

    Google Scholar 

  • Andersen, J. F., Walding, J. K., Evans, P. H., Bowers, W. S., and Feyereisen, R. 1997. Substrate specificity for the epoxidation of terpenoids and active site topology of house fly cytochrome P-450 6A1.Chem. Res. Toxicol.10:156–164.

    PubMed  Google Scholar 

  • Bak, S., Tax, F. E., Feldmann, K. A., Galbraith, D. W., and Feyereisen, R. 2001. CYP83B1, a cytochrome P-450 at the metabolic branch point in auxin and indole glucosinolate biosynthesis in Arabidopsis.Plant Cell 13:101–111.

    PubMed  Google Scholar 

  • Berenbaum, M. R.1983.Coumarins and caterpillars: A case for coevolution.Evolution37:63–179.

    Google Scholar 

  • Berenbaum, M. R. 1991.Coumarins, pp. 221–249 in G. Rosenthal and M. R. Berenbaum. (eds.). Herbivores: Their Interactions with Secondary Plant Metabolites, Vol. 1.Academic Press, New York.

    Google Scholar 

  • Berenbaum, M. R.1995a. Chemical defense: Theory and practice.Proc. Natl. Acad. Sci. USA 92:2.

    PubMed  Google Scholar 

  • Berenbaum, M. R.1995b. Phototoxicity of plant secondary metabolites: Insect and mammalian perspectives. Arch. Insect Biochem. Physiol. 29:119–134.

    PubMed  Google Scholar 

  • Berenbaum, M. 1999.Animal-plant warfare: molecular basis for cytochrome P-450-mediated natural adaptation, pp. 553–571 in A. Puga and K. B. Wallace (eds.). Molecular Biology of the Toxic Response. Taylor and Francis, New York.

    Google Scholar 

  • Berenbaum, M. R., and Zangerl, A. R.1999. Coping with life as a menu option: Inducible defenses of the wild parsnip, pp. 10–32, in R. Tollrian and C. D. Harvell (eds.). The Ecology and Evolution of Inducible Defenses.Princeton University Press, Princeton, New Jersey.

    Google Scholar 

  • Berenbaum, M. R., Favret, C., and Schuler, M. A., 1996. On defining “key innovations” in an adaptive radiation: Cytochrome P-450s and Papilionidae.Am. Nat.148:S139–S155.

    Google Scholar 

  • Chen, J.-S., Berenbaum, M. R., and Schuler, M. A.2002.Role of aromatic-aromatic interactions in the active site of cytochrome P-450 monooxygenase CYP6B1v1.Insect Biochem. Mol. Biol. (in press).

  • Clyne, P. S., Warr, C. G., and Carlson, J. R.2000.Candidate taste receptors in Drosophila. Science 287:1830–1834.

    PubMed  Google Scholar 

  • Cohen, M. B., Schuler, M. A., and Berenbaum, M. R. 1992.A host-inducible cytochrome P-450 from a host-specific caterpillar: Molecular cloning and evolution.Proc. Natl. Acad. Sci. USA 89:10920–10924.

    PubMed  Google Scholar 

  • Danielson, P. B., Foster, J. L. M., McMahill, N. M., Smith, M. K., and Fogleman, J. C.1998.Induction by alkaloids and phenobarbital of Family 4 cytochrome P450s in Drosophila: Evidence for involvement in host plant utilization.Mol. Gen. Genet.259:54–59.

    PubMed  Google Scholar 

  • Dunipace, L., Meister, S., McNealy, C., and Amrein, H.2001.Spatially restricted expression of candidate taste-receptors in the Drosophila gustatory system. Curr. Biol. (in press).

  • Dunkov, B. C., Guzov, V. M., Mocelin, G., Shotkoski, F., and Brun A., Amichot, M., Ffrenchconstant, R. H., and Feyereisen, R. 1997.The Drosophila cytochrome P-450 gene Cyp6a2: structure, localization, heterologous expression, and induction by phenobarbital. DNA Cell Biol. 16:1345–1356.

    PubMed  Google Scholar 

  • Ehrlich, P. R. and Raven, P. R., 1964.Butterflies and plants: A study in coevolution.Evolution 18:586–608.

    Google Scholar 

  • Feyereisen, R. 1999.Insect P-450 enzymes.Annu. Rev. Entomol.44:507–533.

    PubMed  Google Scholar 

  • Frey, M., Stettner, C., Pare, P. W., Schmelz, E. A., Tumlinson, J. H., and Gierl, A. 2000.An herbivore elicitor activates the gene for indole emission in maize.Proc. Natl. Acad. Sci. USA97:14801–14806.

    PubMed  Google Scholar 

  • Gonzalez, F. J. and Gelboin, H. V. 1989. The molecular biology of cytochrome P-450s. Pharmacol. Rev. 40:243–288.

    Google Scholar 

  • Gonzalez, F. J. and Nebert, D. W.1990. Evolution of the P450 gene superfamily: Animal-plant “warfare,” molecular drive, and human genetic differences in drug oxidation.Trends Genet.6:182–186.

    PubMed  Google Scholar 

  • Gotoh, O. 1992. Substrate recognition sites in cytochrome P-450 family 2 (CYP2) proteins inferred from comparative analyses of amino acid and coding nucleotide sequences.J. Biol. Chem.267:83–90.

    PubMed  Google Scholar 

  • Gotoh, O. 1998. Divergent structure of Caenorhabditis elegans cytochrome P-450 genes suggest the frequent loss and gain of introns during the evolution of nematodes.Mol. Biol. Evol.15:1447–1459. POSTGENOMIC CHEMICAL ECOLOGY 893

    PubMed  Google Scholar 

  • Guengerich, F. P.1998.The environmental genome project: Functional analysis of polymorphisms. Environ. Health Perspect. 106:365–368.

    PubMed  Google Scholar 

  • Hagen, R. H.1990.Population structure and host use in hybridizing subspecies of Papilio glaucus (Lepidoptera: Papilionidae).Evolution44:1914–1930.

    Google Scholar 

  • Hagen, R. H. and Scriber, J. M.1991. Systematics of the Papilio glaucus and Papilio troilus species groups (Lepidoptera: Papilionidae): Inferences from allozymes.Ann. Entomol. Soc. Am.84:380–395.

    Google Scholar 

  • Hagen, R. H. and Scriber, J.M.1995.Sex chromosomes and speciation in tiger swallowtail, pp. 211–227, in M. J. Scriber, Y. Tsubaki, and R. C. Lederhouse (eds.). Swallowtail Butterflies: Their Ecology and Evolutionary Biology.Scientific Publications, Gainesville, Florida.

    Google Scholar 

  • Hansen, C. H., Wittstock, U., Olsen, C. E., Hick, A. J., Pickett, J. A., and Halkier, B. A. 2001.Cytochrome P-450 CYP79F1 from Arabidopsis catalyzes the conversion of dihomomethionine and trihomomethionine to the corresponding aldoximes in the biosynthesis of aliphatic glucosinolates.J. Biol. Chem. 276:11078–11085.

    PubMed  Google Scholar 

  • Harrison, T., A. R. Zangerl, M.A. Schuler, and M. R. Berenbaum, 2001. Developmental variation in cytochrome P-450 expression in Papilio polyxenes.Arch. Insect Biochem. Physiol. 48:179–189.

    PubMed  Google Scholar 

  • Hung, C.-F., Harrison, T. L., Berenbaum, M. R., and Schuler., M. A. 1995. CYP6B3: A second furanocoumarin-inducible cytochrome P-450 expressed in Papilio polyxenes.Insect Mol. Biol. 4:149–160.

    PubMed  Google Scholar 

  • Hung, C.-F., Holzmacher, R., Connolly, E., Berenbaum, M. R., and Schuler, M. A.1996.Conserved promoter elements in theCYP6Bgene family suggestcommonancestry for cytochrome P-450 monooxygenases mediating furanocoumarin detoxification.Proc. Natl. Acad. Sci. USA 93:12200–12205.

    PubMed  Google Scholar 

  • Hung, C.-F., Berenbaum, M. R., and Schuler, M.A. 1997.Isolation and characterization of CYP6B4,a furanocoumarin-inducible cytochrome P-450 from a polyphagous caterpillar (Lepidoptera: Papilionidae).Insect Biochem. Mol. Biol. 27:377–385.

    PubMed  Google Scholar 

  • Irmler, S., Schroder, G., St-Pierre, B., Crouch, N. P., Hotze, M., Schmidt, J., Strack, D., Matern, U., and Schroder, J.2000.Indole alkaloid biosynthesis in Catharanthus roseus: New enzyme activities and identification of cytochrome P-450 CYP72A1 as a secologanin synthase.Plant J. 24:797–804.

    PubMed  Google Scholar 

  • Kimura, S., Umeno, M., Skoda, R. C., Meyer, U. A., and Gonzalez, F. J. 1989. The human debrisoquine 4-hydroxylase (CYP2D) locus: Sequence and identification of the polymorphic CYP2D6 gene, a related gene, and a pseudogene.Am. J. Hum. Genet.45:889–904.

    PubMed  Google Scholar 

  • Latunde-Dada, A. O., Cabello-Hurtado, F., Czittrich, N., Didierjean, L., Schopfer, C., Hertkorn, N., Werck-Reichhart, D., and Ebel, J. 2001. Flavonoid 6-hydroxylase from soybean(Glycine max L.), a novel plant P-450 monooxygenase.J. Biol. Chem.276:1688–1695.

    PubMed  Google Scholar 

  • Li, W., Berenbaum, M. R., and Schuler, M. A. 2001.Molecular analysis of multiple CYP6B genes from polyphagous Papilio species.Insect Biochem. Mol. Biol.31:999–1011.

    PubMed  Google Scholar 

  • Li, X., Berenbaum, M. R., and Schuler, M. A.2000.Molecular cloning and expression of CYP6B8:A xanthotoxin-inducible cytochrome P-450 cDNA from Helicoverpa zea.Insect Biochem. Mol. Biol.30:75–84.

    PubMed  Google Scholar 

  • Li, X., Berenbaum, M. R., and Schuler, M. A.2002.Cytochrome P-450 and actin genes expressed in Helicoverpa zea and Helicoverpa armigera: paralogy/orthology identification, gene conversion, and evolution.Insect Biochem. Mol. Biol. (in press).

  • Ma, R., Cohen, M. B., Berenbaum, M. R., and Schuler, M. A.1994.Black swallowtail (Papiliopolyxenes) alleles encode cytochrome P-450s that selectively metabolize linear furanocoumarins. Arch. Biochem. Biophys.310:332–340.

    PubMed  Google Scholar 

  • Mansuy, D. 1998.The great diversity of reactions catalyzed by cytochromes P-450.Comp. Biochem. Physiol. C.121:5–14.

    PubMed  Google Scholar 

  • Martens, S. and Forkmann, G. 1999.Cloning and expression of flavone synthase II from Gerbera hybrids.Plant J. 20:611–618.

    PubMed  Google Scholar 

  • Matern, U., Luer, P., and Kreusch, D.1999. Biosynthesis of coumarins, pp. 623–637, in U. Sankawa,(ed.). Comprehensive Natural Products Chemistry, Vol. 1: Polyketides and Other Secondary Metabolites Including Fatty Acids and their Derivatives. Pergamon, Oxford.

    Google Scholar 

  • Mikkelson, M. D., Hansen, C. H., Wittstock, U., and Halkier, B. A.2000. Cytochrome P-450 CYP79B2 from Arabidopsis catalyses the conversion of trytophan to indole-3-acetaldoxime, a precursor of indole glucosinolates and indole-3-acetic acid.J. Biol. Chem. 275:33712–33717.

    PubMed  Google Scholar 

  • Murray, R. D. H., Mendez, J., and Brown, S. A. 1982.The Natural Coumarins: Occurrence, Chemistry, and Biochemistry.John Wiley & Sons, Bristol, United Kingdom, 702 pp.

    Google Scholar 

  • Nebert, D. W.1997.Polymorphisms in drug-metabolizing enzymes: What is their clinical relevance and why do they exist?Am. J. Hum. Genet.60:265–271.

    PubMed  Google Scholar 

  • Negishi, M., Uno, T., Darden, T. A., Sueyoshi, T., and Pedersen, L. G. 1996.Structural flexibility and functional versatility of mammalian P-450 enzymes.FASEB J. 10:683–689.

    PubMed  Google Scholar 

  • Paquette, S. M., Bak, A., and Feyereisen, R.2000. Intron-exon organization and phylogeny in a large superfamily, the paralogous cytochrome P-450 genes of Arabidopsis thaliana.DNA Cell Biol.19:307–317.

    PubMed  Google Scholar 

  • Petersen, R. A., Zangerl, A. R., Berenbaum, M. R., and Schuler, M. A.2001. Expression of CYP6B1 and CYP6B3 cytochrome P450 monooxygenases and furanocoumarin metabolism in different tissues of Papilio polyxenes (Lepidoptera: Papilionidae).Insect Biochem. Mol. Biol. 31:679–690.

    PubMed  Google Scholar 

  • Prapaipong, H. 1995. Transcriptional regulation of CYP6B1v3, a furanocoumarin-inducible P450 gene from black swallowtail (Papilio polyxenes).PhDdissertation. University of Illinois at Urbana-Champaign.

    Google Scholar 

  • Prapaipong, H., Berenbaum, M. R., and Schuler., M. A., 1994. Transcriptional regulation of the Papilio polyxenes CYP6B1 gene.Nucleic Acids Res.22:3210–3217.

    PubMed  Google Scholar 

  • Robertson, H.M. 1998.Two large families of chemoreceptor genes in the nematodes Caenorhabditis elegans and Caenorhabditis briggsae reveal extensive gene duplication, diversification, movement, and intron loss.Genome Res.8:449–463.

    PubMed  Google Scholar 

  • Robertson, H. M. 2000.The large srh family of chemoreceptor genes in Caenorhabditis nematodes reveals processes of genome evolution involving large duplications and deletions and intron gains and losses.Genome Res.10:192–203.

    PubMed  Google Scholar 

  • Robertson, H.M.2001. Gustatory receptors: Independent origins of chemoreception coding systems? Curr. Biol. (in press).

  • Robertson, H. M., Martos, R, Sears, C. R., Todres, E. Z., Walden, K. K. O., and Nardi, J. B.1999.Diversity of odourant binding proteins revealed by an expressed sequence tag project on male Manduca sexta moth antennae.Insect Mol. Biol.8:501–518.

    PubMed  Google Scholar 

  • Roussel, F., Khan, K. K., and Halpert, J. R.2000.The importance of SRS-1 residues in catalytic specificity of human cytochrome P-450 3A4.Arch. Biochem. Biophys.374:269–278.

    PubMed  Google Scholar 

  • Rubin, G. M., Yandell, M. D., Wortman, J. R., Gabormiklos, G. L., Nelson, C. R., Hariharan, I. K., Fortini, M. E., Li, P. W., Apweiler, R., Fleischmann, W., et al.2000. Comparative genomics of the eukaryotes.Science 287:2204–2215.

    PubMed  Google Scholar 

  • Saner, C., Weibel, B., Wurgler, F. E., and Senstag, C. 1996.Metabolism of promutagens catalyzed by Drosophila melanogaster CYP6A2 enzyme in Saccharomyces cerevisiae.Environ. Mol. Mutagen.27:46–58.

    PubMed  Google Scholar 

  • Schroeder, F. C., Farmer, J. J., Smedley, S. R., Attygalle, A. B., Eisner, T., and Meinwald, J.2000.A combinatorial library of macrocyclic polyamines produced by a ladybird beetle.J. Am Chem. Soc.122:3628–3634.

    Google Scholar 

  • Scott, J. G.,1999.Cytochrome P450 and insecticide resistance.Insect Biochem. Mol. Biol. 29:757–777.

    PubMed  Google Scholar 

  • Scott, J. G., Liu, N., and Wen, Z. 1998.Insect cytochromes P450: diversity, insecticide resistance,and tolerance to plant toxins.Comp. Biochem. Physiol.C121:147–155.

    Google Scholar 

  • Scott, K., Brady, R., Jr., Cravchik, A., Morozov, P., Rzhetsky, A., Zuker, C., and Axel, R. 2001.A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila.Cell104:661–673.

    PubMed  Google Scholar 

  • Scriber, J. M.1988. Tale of the tiger: Beringial biogeography, binomial classification, and breakfast choices in thePapilio glaucus complex of butterflies, pp. 241–301, in K. C. Spencer (ed.). Chemical Mediation of Coevolution.Academic Press, New York.

    Google Scholar 

  • Scriber, J. M.1995.Overview of swallowtail butterflies: Taxonomic and distributional latitude, pp.3–8, in J. M. Scriber, Y. Tsubaki, and R. C. Lederhouse, (eds.). Swallowtail Butterflies: Their Ecology and Evolutionary Biology.Scientific Publications, Gainesville, Florida.

    Google Scholar 

  • Scriber, J. M., Lederhouse, R., and Hagen, R.1991.Foodplant and evolution within P. glaucus and P. troilus species groups (Lepidoptera: Papilionidae), pp. 341–373, inP. W. Price, T. M. Lewinsohn, G.W. Fernandes, and W.W. Benson (eds.). Plant–Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions. Wiley, New York.

    Google Scholar 

  • Sondheimer, E. and Simeone, J. B.1970. Chemical Ecology.Academic Press, New York.

    Google Scholar 

  • Stanjek, V., Herhaus, C., Ritgen, U., Boland, W., and Staedler, E. 1997.Changes in the leaf surface chemistry of Apium graveolens (Apiaceae) stimulated by jasmonic acid and perceived by a specialist insect.Helv. Chmi. Acta 80:1408–1420.

    Google Scholar 

  • Stanjek, V., Miksch, M., Lueer, P., Matern, U., and Boland, W. 1999. Biosynthesis of psoralen:Mechanism of a cytochrome P-450 catalyzed oxidative bond cleavage. Angew. Chem. Int. Ed. 38:400–402.

    Google Scholar 

  • Stevens, J. L., Snyder, M. J., Koerner, J. F., and Feyereisen, R.2000.Inducible P-450s of the CYP9 family from larval Manduca sexta midgut.Insect Biochem. Mol. Biol.30:559–568.

    PubMed  Google Scholar 

  • Straub, P., Lloyd, M., Johnson, E. F., and Kemper, B. 1994. Differential effects of mutations in substrate recognition site 1 of cytochrome P-450 2C2 on lauric acid and progesterone hydroxylation. Biochemistry 33:8029–8034.

    PubMed  Google Scholar 

  • Tijet, N., Helvig, C., and Feyereisen, R. 2001a. The cytochrome P-450 gene superfamily in Drosophila melanogaster: Annotation, intron–exon organization and phylogeny.Gene262:89–198.

    PubMed  Google Scholar 

  • Tijet, N., Schneider, C., Muller, B. L., and Brash, A. R.2001b.Biogenesis of volatile aldehydes from fatty acid hydroperoxides: Molecular cloning of a hydroperoxide lyase (CYP74C) wth specificity for both the 9-and 13-hydroperoxides of linoleic and linolenic acids.Arch. Biochem. Biophys.386:281–289.

    PubMed  Google Scholar 

  • Vinogradov, A. E.1997. Fine structure of gene frequency landscapes in domestic cat: The Old and New Worlds compared.Hereditas126:95–102.

    PubMed  Google Scholar 

  • vonWachenfeldt, C. and Johnson, E. F.1995.Structures of eukaryotic cytochrome P450 enzymes,pp.183–223, in P. R. Ortiz de Montellano (ed.). Cytochrome P-450: Structure, Mechanism, and Biochemistry,2nd ed. Plenum Press, New York.

    Google Scholar 

  • Werck-Reichhart, D., Hehn, A., and Didierjean, L. 2000. Cytochromes P450 for engineering herbicide tolerance.Trends Plant Sci.5:116–123.

    PubMed  Google Scholar 

  • Willett, C. S. 2000.Evidence for directional selection acting on pheromone-binding proteins in the genus Choristoneura.Mol. Biol. Evol. 17:553–562.

    PubMed  Google Scholar 

  • Wittstock, U. and Halkier, B. A.2000. Cytochrome P450 CYP79A from Arabidopsis thaliana L. catalyzes the conversion of L-phenylalanine to phenylacetaldoxime in the biosynthesis of benzylglucosinolate.J. Biol. Chem.275:14659–14666.

    PubMed  Google Scholar 

  • Wust, M., Little, D. B., Schalk, M., and Croteau, R.2001.Hydroxylation of limonene enantiomers and analogs by recombinant (—)-limonene-3-and 6-hydroxylases from mint (Mentha) species: Evidence for catalysis within sterically constrained active sites.Arch. Biochem. Biophys.387:125–136.

    PubMed  Google Scholar 

  • Yang, X.-L. and Wang, A. H. J.1999.Structural studies of atom-specific anticancer drugs acting on DNA.Pharmacol. Ther.83:181–215.

    PubMed  Google Scholar 

  • Zangerl, A. R. and Berenbaum, M. R., 1990.Furanocoumarin induction in wild parsnip: Evidence for an induced defense against herbivores.Ecology 71:1926–1932.

    Google Scholar 

  • Zangerl, A. R. and Berenbaum, M. R.1998.Damage inducibility of primary and secondary metabolites in Pastinaca sativa.Chemoecology 8:187–193.

    Google Scholar 

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    May R. Berenbaum

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Berenbaum, M.R. Postgenomic Chemical Ecology: From Genetic Code to Ecological Interactions. J Chem Ecol 28, 873–896 (2002). https://doi.org/10.1023/A:1015260931034

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