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Journal of Chemical Ecology

, Volume 20, Issue 6, pp 1281–1328 | Cite as

Metabolic costs of terpenoid accumulation in higher plants

  • Jonathan Gershenzon
Article

Abstract

The net value of any plant trait can be assessed by measuring the costs and benefits associated with that trait. While the other contributors to this issue examine the possible benefits of terpenoids to plants, this article explores the metabolic costs of terpenoid accumulation in plants in the light of recent advances in terpenoid biochemistry. Terpenoids are more expensive to manufacture per gram than most other primary and secondary metabolites due to their extensive chemical reduction. The enzyme costs of making terpenoids are also high since terpenoid biosynthetic enzymes are apparently not shared with other metabolic pathways. In fact, plant cells may even possess more than one set of enzymes for catalyzing the basic steps of terpenoid formation. Terpenoids are usually sequestered in complex, multicellular secretory structures, and so storage costs for these substances are also likely to be substantial. However, not all of the processes involved in terpenoid accumulation require large investments of resources. For instance, the maintenance of terpenoid pools is probably inexpensive because there is no evidence that substantial quantities of terpenes are lost as a result of metabolic turnover, volatilization, or leaching. Moreover, plants may reduce their net terpenoid costs by employing individual compounds in more than one role or by catabolizing substances that are no longer needed, although it is still unclear if such practices are widespread. These findings (and other facets of terpenoid biochemistry and physiology) are discussed in relation to the assumptions and predictions of several current theories of plant defense, including the carbonnutrient balance hypothesis, the growth-differentiation balance hypothesis, and the resource availability hypothesis.

Key Words

Terpenoid biosynthesis terpenoid storage secretory structures metabolic turnover volatilization catabolism carbon-nutrient balance hypothesis growth-differentiation balance hypothesis resource availability hypothesis 

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References

  1. Adams, R.P., andHagerman, A. 1977. Diurnal variation in the volatile terpenoids ofJuniperus scopulorum (Cupressaceae).Am. J. Bot. 64:278–285.Google Scholar
  2. Adzet, T., Ponz, R., Wolf, E., andSchulte, E. 1992. Genetic variability of the essential oil content ofMelissa officinalis.Planta Med. 58:558–561.Google Scholar
  3. Alonso, W.R., andCroteau, R. 1991. Purification and characterization of the monoterpene cyclaseγ-terpinene synthase fromThymus vulgaris.Arch. Biochem. Biophys. 286:511–517.PubMedGoogle Scholar
  4. Alonso, W.R., Rajaonarivony, J.I.M., Gershenzon, J., andCroteau, R. 1992. Purification of 4S-limonene synthase, a monoterpene cyclase from the glandular trichomes of peppermint (Mentha × piperita) and spearmint (Mentha spicata).J. Biol. Chem. 267:7582–7587.PubMedGoogle Scholar
  5. Amelunxen, F. 1965. Elektronenmikroskopische Untersuchungen an den Drüsenschuppen vonMentha piperita L.Planta Med. 13:457–473.Google Scholar
  6. Asakawa, Y., Dawson, G.W., Griffiths, D.C., Lallemand, J.-Y., Ley, S. V., Mori, K., Mudd, A., Pezechk-Leclaire, M., Pickett, J.A., Watanabe, H., Woodcock, C.M., andZhong-Ning, Z. 1988. Activity of drimane antifeedants and related compounds against aphids, and comparative biological effects and chemical reactivity of (-)- and (+)-polygodial.J. Chem. Ecol. 14:1845–1855.Google Scholar
  7. Bach, T.J. 1986. Hydroxymethylglutaryl-CoA reductase, a key enzyme in phytosterol synthesis?Lipids 21:82–88.PubMedGoogle Scholar
  8. Bach, T.J., Boronat, A., Caelles, C., Ferrer, A., Weber, T., andWettstein, A. 1991. Aspects related to mevalonate biosynthesis in plants.Lipids 26:637–648.PubMedGoogle Scholar
  9. Bakker, M.E., andBaas, P. 1993. Cell walls in oil and mucilage cells.Acta Bot. Neerl. 42:133–139.Google Scholar
  10. Bakker, M.E., Gerritsen, A.G., andVan Der Schaff, P.J. (1991). Development of oil and mucilage cells inCinnamomum burmanni. An ultrastructural study.Acta Bot. Neerl. 40:339–356.Google Scholar
  11. Baldwin, I.T., Sims, C.L., andKean, S.E. 1990. The reproductive consequences associated with inducible alkaloidal responses in wild tobacco.Ecology 71:252–262.Google Scholar
  12. Balliano, G., Caputo, O., Viola, F., Delprino, L., andCattel, L. 1983. The transformation of 10α-cucurbita-5,24-dien-3β-ol into cucurbitacin C by seedlings ofCucumis sativus.Phytochemistry 22:909–913.Google Scholar
  13. Banthorpe, D.V., andEkundayo, O. 1976. Biosynthesis of (+)-car-3-ene inPinus species.Phytochemistry 15:109–112.Google Scholar
  14. Banthorpe, D.V., Doonan, H.J., andWirz-Justice, A. 1972. Terpene biosynthesis. Part V. Interconversions of some monoterpenes in higher plants and their possible role as precursors of carotenoids.J. Chem. Soc. Perkin Trans. I, 1972:1764–1769.Google Scholar
  15. Belingheri, L., Pauly, G., Gleizes, M., andMarpeau, A. 1988. Isolation by aqueous two-polymer phase system and identification of endomembranes fromCitrofortunella mitis fruits for sesquiterpene hydrocarbon synthesis.J. Plant Physiol. 132:80–85.Google Scholar
  16. Berger., R.G., Akkan, Z., andDrawert, R. 1990. Catabolism of geraniol by cell suspension cultures ofCitrus limon.Biochim. Biophys. Acta 1055:234–239.PubMedGoogle Scholar
  17. Bernard-Dagan, C. 1988. Biosynthesis of lower terpenoids: Genetic and physiological controls in woody plants, pp. 329–351,in J.W. Hanover and D.E. Keathley (eds.). Genetic Manipulation of Woody Plants. Plenum Press, New York.Google Scholar
  18. Bernard-Dagan, C., Pauly, G., Marpeau, A., Gleizes, M., Carde, J.-P., andBaradat, P. 1982. Control and compartmentation of terpene biosynthesis in leaves ofPinus pinaster.Physiol. Veg. 20:775–795.Google Scholar
  19. Bhatt, J.R. 1987. Development and structure of primary secretory ducts in the stem ofCommiphora wightii (Burseraceae).Ann. Bot. 60:405–416.Google Scholar
  20. Bjorkman, C., Larsson, S., andGref, R. 1991. Effects of nitrogen fertilization on pine needle chemistry and sawfly performance.Oecologica 86:202–209.Google Scholar
  21. Breccia, A., andBadiello, R. 1967. The role of general metabolites in the biosynthesis of natural products. I. The terpene marrubiin.Z. Naturforsch. 22b:44–49.Google Scholar
  22. Briggs, M.A., andSchultz, J.C. 1990. Chemical defense production inLotus corniculatus L. II. Trade-offs among growth, reproduction and defense.Oecologia 83:32–37.Google Scholar
  23. Brown, D.G. 1988. The cost of plant defense: An experimental analysis with inducible proteinase inhibitors in tomato.Oecologia 76:467–470.Google Scholar
  24. Bryant, J.P., Chapin, F.S., III, andKlein, D.R. 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory.Oikos 40:357–368.Google Scholar
  25. Bryant, J.P., Reichardt, P.B., Clausen, T.P., Provenza, F.D., andKuropat, P.J. 1992. Woody plant-mammal interactions, pp. 343–370,in G.A. Rosenthal and M.R. Berenbaum (eds.). Herbivores: Their Interactions with Secondary Plant Metabolites, Vol. 2, 2nd ed. Academic Press, San Diego.Google Scholar
  26. Burbott, A.J., andLoomis, W.D. 1969. Evidence for metabolic turnover of monoterpenes in peppermint.Plant Physiol. 44:173–179.Google Scholar
  27. Caelles, C., Ferrer, A., Balcells, L., Hegardt, F.G., andBoronat, A. 1989. Isolation and structural characterization of a cDNA encodingArabidopsis thaliana 3-hydroxy-3-methylglutaryl coenzyme A reductase.Plant Mol. Biol. 13:627–638.PubMedGoogle Scholar
  28. Cane, D.E. 1990. Enzymatic formation of sesquiterpenes.Chem. Rev. 90:1089–1103.Google Scholar
  29. Carlton, R.R., Waterman, P.G., andGray, A.I. 1992. Variation of leaf gland volatile oil within a population of sweet gale (Myrica gale) (Myricaceae).Chemoecology 3:45–54.Google Scholar
  30. Chapin, F.S., III. 1980. The mineral nutrition of wild plants.Annu. Rev. Ecol. Syst. 11:233–260.Google Scholar
  31. Chapin, F.S., III. 1989. The cost of tundra plant structures: Evaluation of some concepts and currencies.Am. Nat. 133:1–19.Google Scholar
  32. Chappell, J., Vonlanken, C., andVogeli, U. 1991. Elicitor-inducible 3-hydroxy-3-methylglutaryl coenzyme A reductase activity is required for sesquiterpene accumulation in tobacco cell suspension cultures.Plant Physiol. 97:693–698.Google Scholar
  33. Charon, J., Launay, J., andVindt-Balguerie, E. 1986. Ontogenèse des canaux sécréteurs d'origine primaire dans le bourgeon de Pin maritime.Can. J. Bot. 64:2955–2964.Google Scholar
  34. Chew, F.S., andRodman, J.E. 1979. Plant resources for chemical defense, pp. 271–307,in G.A. Rosenthal and D.H. Janzen (eds.). Herbivores: Their Interaction with Secondary Plant Metabolites, 1st ed. Academic Press, New York.Google Scholar
  35. Chiariello, N.R., Mooney, H.A., andWilliams, K. 1989. Growth, carbon allocation and cost of plant tissues, pp. 327–365,in R.W. Pearcy, J.R. Ehleringer, H.A. Mooney, and P.W. Rundel (eds.). Plant Physiological Ecology: Field Methods and Instrumentation. Chapman and Hall, London.Google Scholar
  36. Chye, M.-L., Tan, C.-T., andChua, N.-H. 1992. Three genes encode 3-hydroxy-3-methylglutaryl-coenzyme A reductase inHevea brasiliensis: hmg1 andhmg3 are differentially expressed.Plant Mol. Biol. 19:473–484.PubMedGoogle Scholar
  37. Coley, P.D., Bryant, J.P., andChapin, F.S., III. 1985. Resource availability and plant antiherbivore defense.Science 230:895–899.Google Scholar
  38. Cornish, K. 1992. Natural rubber biosynthesis, a branch of the isoprenoid pathway in plants, pp. 18–26,in W.D. Nes, E.J. Parish, and J.M. Trzaskos (eds.). Regulation of Isopentenoid Metabolism, ACS Symposium Series No. 497. American Chemical Society, Washington, D.C.Google Scholar
  39. Cotton, C.M., Evans, L.V., andGramshaw, J.W. 1991. The accumulation of volatile oils in whole plants and cell cultures of tarragon (Artemisia dracunculus).J. Exp. Bot. 42:365–375.Google Scholar
  40. Croteau, R. 1987. Biosynthesis and catabolism of monoterpenoids.Chem. Rev. 87:929–954.Google Scholar
  41. Croteau, R. 1988. Catabolism of monoterpenes in essential oil plants, pp. 65–84,in B.D. Mookherjee and B.J. Willis (eds.). Flavors and Fragrances: A World Perspective. Elsevier, Amsterdam.Google Scholar
  42. Croteau, R., andGershenzon, J. 1994. Genetic control of monoterpene biosynthesis in mints (Mentha: Lamiaceae),in H. Stafford (ed.). Recent Advances in Phytochemistry, Vol. 28. Plenum Press, New York.Google Scholar
  43. Croteau, R., andLoomis, W.D. 1972. Biosynthesis of mono- and sesquiterpenes in peppermint from mevalonate-2-14C.Phytochemistry 11:1055–1066.Google Scholar
  44. Croteau, R., andLoomis, W.D. 1973. Biosynthesis of squalene and other triterpenes inMentha piperita from mevalonate-2-14C.Phytochemistry 12:1957–1965.Google Scholar
  45. Croteau, R., andShaskus, J. 1985. Biosynthesis of monoterpenes: Demonstration of a geranyl pyrophosphate: (-)-bornyl pyrophosphate cyclase in soluble enzyme preparations from tansy (Tanacetum vulgare).Arch. Biochem. Biophys. 236:535–543.PubMedGoogle Scholar
  46. Croteau, R., andSood, V.K. 1985. Metabolism of monoterpenes: Evidence for the function of monoterpene catabolism in peppermint (Mentha piperita) rhizomes.Plant Physiol. 77:801–806.Google Scholar
  47. Croteau, R., andVenkatachalam, K.V. 1986. Metabolism of monoterpenes: Demonstration that (+)-cis-isopulegone, not piperitenone, is the key intermediate in the conversion of (-)-isopiperitenone to (+)-pulegone in peppermint (Mentha piperita).Arch. Biochem. Biophys. 249:306–315.PubMedGoogle Scholar
  48. Croteau, R., andWinters, J.N. 1982. Demonstration of the intercellular compartmentation ofl-menthone metabolism in peppermint (Mentha piperita) leaves.Plant Physiol. 69:975–977.Google Scholar
  49. Croteau, R., Burbott, A.J., andLoomis, W.D. 1972a. Biosynthesis of mono- and sesqui-terpenes in peppermint from glucose-14C and14CO2.Phytochemistry 11:2459–2467.Google Scholar
  50. Croteau, R., Burbott, A.J., andLoomis, W.D. 1972b. Apparent energy deficiency in mono- and sesqui-terpene biosynthesis in peppermint.Phytochemistry 11:2937–2948.Google Scholar
  51. Croteau, R., Felton, M., Karp, F., andKjonaas, R. 1981. Relationship of camphor biosynthesis to leaf development in sage (Salvia officinalis).Plant Physiol. 67:820–824.Google Scholar
  52. Croteau, R., Sood, V.K., Renstrom, B., andBhusan, R. 1984a. Metabolism of monoterpenes: Early steps in the metabolism ofd-neomenthyl-β-d-glucoside in peppermint (Mentha piperita) rhizomes.Plant Physiol. 76:647–653.Google Scholar
  53. Croteau, R., El-Bialy, H., andEl-Hindawi, S. 1984b. Metabolism of monoterpenes: Lactonization of (+)-camphor and conversion of the corresponding hydroxy acid to the glucosideglucose ester in sage (Salvia officinalis).Arch. Biochem. Biophys. 228:667–680.PubMedGoogle Scholar
  54. Croteau, R., Munck, S.L., Akoh, C.C., Fisk, H.J., andSatterwhite, D.M. 1987a. Biosynthesis of the sesquiterpene patchoulol from farnesyl pyrophosphate in leaf extracts ofPogostemon cablin (patchouli): Mechanistic considerations.Arch. Biochem. Biophys. 256:56–68.PubMedGoogle Scholar
  55. Croteau, R., Gurkewitz, S., Johnson, M.A., andFisk, H.J. 1987b. Biochemistry of oleoresinosis: Monoterpene and diterpene biosynthesis in lodgepole pine saplings infected withCeratocystis clavigera or treated with carbohydrate elicitors.Plant Physiol. 85:1123–1128.Google Scholar
  56. Croteau, R.B., Wheeler, C.J., Cane, D.E., Ebert, R., andHa, H.-J. 1987c. Isotopically sensitive branching in the formation of cyclic monoterpenes: Proof that (-)-α-pinene and (-)-β-pinene are synthesized by the same monoterpene cyclase via deprotonation of a common intermediate.Biochemistry 26:5383–5389.PubMedGoogle Scholar
  57. Croteau, R., El-Bialy, H., andDehal, S.S. 1987d. Metabolism of monoterpenes: Metabolic fate of (+)-camphor in sage (Salvia officinalis).Plant Physiol. 84:649–653.Google Scholar
  58. Damtoft, S., Jensen, S.R., andJessen, C.U. 1993a. Intermediates between 8-epi-deoxyloganic acid and 6,10-dideoxyaucubin in the biosynthesis of antirrhinoside.Phytochemistry 33:1087–1088.Google Scholar
  59. Damtoft, S., Jensen, S.R., Jessen, C.U., andKnudsen, T.B. 1993b. Late stages in the biosynthesis of aucubin inScrophularia.Phytochemistry 33:1089–1093.Google Scholar
  60. DeFaÿ, E. andJacob, J.-L. 1989. Anatomical organization of the laticiferous system in the bark, pp. 3–14,in J. d'Auzac, J.-L. Jacob, and H. Chrestin (eds.). Physiology of Rubber Tree Latex, The Laticiferous Cell and Latex—A Model of Cytoplasm. CRC Press, Boca Raton, Florida.Google Scholar
  61. Dehal, S.S., andCroteau, R. 1987. Metabolism of monoterpenes: Specificity of the dehydrogenases responsible for the biosynthesis of camphor, 3-thujone, and 3-isothujone.Arch. Biochem. Biophys. 258:287–291.PubMedGoogle Scholar
  62. Dehal, S.S., andCroteau, R. 1988. Partial purification and characterization of two sesquiterpene cyclases from sage (Salvia officinalis) which catalyze the respective conversion of farnesyl pyrophosphate to humulene and caryophyllene.Arch. Biochem. Biophys. 261:346–356.PubMedGoogle Scholar
  63. Deighton, N., Glidewell, S.M., Deans, S.G., andGoodman, B.A. 1993. Identification by EPR spectroscopy of carvacrol and thymol as the major sources of free radicals in the oxidation of plant essential oils.J. Sci. Food Agric. 63:221–225.Google Scholar
  64. Dell, B., andMcComb, A.J. 1975. Glandular hairs, resin production, and habitat ofNewcastelia viscida E. Pritzel (Dicrastylidaceae).Aust. J. Bot. 23:373–390.Google Scholar
  65. Dell, B., andMcComb, A.J. 1977. Glandular hair formation and resin secretion inEremophila fraseri F. Meull (Myoporaceae).Protoplasma 92:71–86.Google Scholar
  66. Dell, B., andMcComb, A.J. 1978a. Plant resins—their formation, secretion and possible functions, pp. 277–316,in H.W. Woolhouse (ed.). Advances in Botanical Research, Vol. 6. Academic Press, London.Google Scholar
  67. Dell, B., andMcComb, A.J. 1978b. Biosynthesis of resin terpenes in leaves and glandular hairs ofNewcastelia viscida.J. Exp. Bot. 29:89–95.Google Scholar
  68. Dolman, D.M., Knight, D.W., Salan, U., andToplis, D. 1992. A quantitative method for the estimation of parthenolide and other sesquiterpene lactones containing α-methylenebutyrolactone functions present in feverfew,Tanacetum parthenium.Phytochem. Anal. 3:26–31.Google Scholar
  69. Dudai, N., Putievsky, E., Ravid, U., Palevitch, D., andHalevy, A.H. 1992. Monoterpene content inOriganum syriacum as affected by environmental conditions and flowering.Physiol. Plant. 84:453–459.Google Scholar
  70. Dudley, M.W., Dueber, M.T., andWest, C.A. 1986. Biosynthesis of the macrocyclic diterpene casbene in castor bean (Ricinus communis L.) seedlings: Changes in enzymes levels induced by fungal infection and intracellular localization of the pathway.Plant Physiol. 81:335–342.Google Scholar
  71. Dueber, M.T., Adolf, W., andWest, C.A. 1978. Biosynthesis of the diterpene phytoalexin casbene: Partial purification and characterization of casbene synthetase fromRicinus communis.Plant Physiol. 62:598–603.Google Scholar
  72. Dussourd, D.E., andDenno, R.F. 1991. Deactivation of plant defense: Correspondence between insect behavior and secretory canal architecture.Ecology 72:1383–1396.Google Scholar
  73. Emongor, V.E., andChweya, J.A. 1992. Effect of nitrogen and variety on essential-oil yield and composition from chamomile flowers.Trop. Agric. 60:290–292.Google Scholar
  74. Evans, F.J., andSoper, C.J. 1978. The tigliane, daphnane and ingenane diterpenes, their chemistry, distribution and biological activities. A reviewLloydia 41:193–233.Google Scholar
  75. Fagerstrom, T. 1989. Anti-herbivory chemical defense in plants: A note on the concept of cost.Am. Nat. 133:281–287.Google Scholar
  76. Fahn, A. 1979. Secretory Tissues in Plants. Academic Press, London, 302 pp.Google Scholar
  77. Fajer, E.D., 1989. The effects of enriched CO2 atmospheres on plant-insect herbivore interactions: Growth responses of larvae of the specialist butterfly,Junonia coenia (Lepidoptera: Nymphalidae).Oecologia 81:514–520.Google Scholar
  78. Fajer, E.D., Bowers, M.D., andBazzaz, F.A. 1989. The effects of enriched carbon dioxide atmospheres on plant-insect herbivore interactions.Science 243:1198–1200.Google Scholar
  79. Fajer, E.D., Bowers, M.D., andBazzaz, F.A. 1992. The effect of nutrients and enriched CO2 environments on production of carbon-based allelochemicals inPlantago: A test of the carbon/nutrient balance hypothesis.Am. Nat. 140:707–723.Google Scholar
  80. Feeny, P. 1976. Plant apparency and chemical defense, pp. 1–40,in J.W. Wallace and R.L. Mansell (eds.). Biochemical Interactions between Plants and Insects, Recent Advances in Phytochemistry, Vol. 10. Plenum Press, New York.Google Scholar
  81. Fischer, N.H. 1986. The function of mono and sesquiterpenes as plant germination and growth regulators, pp. 203–218,in A.R. Putnam and C.-S. Tang (eds.). The Science of Allelopathy. John Wiley & Sons, New York.Google Scholar
  82. Fischer, N.H. 1991. Plant terpenoids as allelopathic agents, pp. 377–398,in J.B. Harborne and F.A. Tomas-Barberan (eds.). Ecological Chemistry and Biochemistry of Plant Terpenoids, Annual Proceedings of the Phytochemical Society of Europe, Vol. 31. Clarendon Press, Oxford.Google Scholar
  83. Flesch, V., Jacques, M., Cosson, L., Teng, B.P., Petiard, V., andBalz, J.P. 1992. Relative importance of growth and light level on terpene content ofGinkgo biloba.Phytochemistry 31:1941–1945.Google Scholar
  84. Fox, L.R. 1981. Defense and dynamics in plant-herbivore systems.Am. Zool. 21:853–864.Google Scholar
  85. Francis, M.J.O., andO'Connell, M. 1969. The incorporation of mevalonic acid into rose petal monoterpenes.Phytochemistry 8:1705–1708.Google Scholar
  86. Funk, C., andCroteau, R. 1994. Diterpenoid resin acid biosynthesis in conifers: Characterization of two cytochrome P450-dependent monooxygenases and an aldehyde dehydrogenase involved in abietic acid biosynthesis.Arch. Biochem. Biophys. 308:258–266.PubMedGoogle Scholar
  87. Funk, C., Koepp, A.E., andCroteau, R. 1992. Catabolism of camphor in tissue cultures and leaf disks of common sage (Salvia officinalis).Arch. Biochem. Biophys. 294:306–313.PubMedGoogle Scholar
  88. Gambliel, H., andCroteau, R. 1984. Pinene cyclases I and II: Two enzymes from sage (Salvia officinalis) which catalyze stereospecific cyclizations of geranyl pyrophosphate to monoterpene olefins of opposite configuration.J. Biol. Chem. 259:740–748.PubMedGoogle Scholar
  89. Gershenzon, J. 1984. Changes in the level of plant secondary metabolite production under water and nutrient stress, pp. 273–320,in B.N. Timmermann, C. Steelink, and F.A. Loewus (eds.). Phytochemical Adaptations to Stress, Recent Advances in Phytochemistry, Vol. 18. Plenum Press, New York.Google Scholar
  90. Gershenzon, J. 1994. The cost of plant chemical defense against herbivory: A biochemical perspective, pp. 105–173,in E.A. Bernays (ed.). Insect-Plant Interactions, Vol. V. CRC Press, Boca Raton, Florida.Google Scholar
  91. Gershenzon, J. andCroteau, R. 1990. Regulation of monoterpene biosynthesis in higher plants, pp. 99–160,in G.H.N. Towers and H.A. Stafford (eds.). Biochemistry of the Mevalonic Acid Pathway to Terpenoids, Recent Advances in Phytochemistry, Vol. 24. Plenum Press, New York.Google Scholar
  92. Gershenzon, J., andCroteau, R. 1991. Terpenoids, pp. 165–219,in G.A. Rosenthal and M.R. Berenbaum (eds.). Herbivores: Their Interactions with Secondary Plant Metabolites, Vol. 1, 2nd ed. Academic Press, San Diego.Google Scholar
  93. Gershenzon, J., andCroteau, R. 1993. Terpenoid biosynthesis: The basic pathway and formation of monoterpenes, sesquiterpenes, and diterpenes, pp. 333–388,in T.S. Moore, Jr. (ed.). Lipid Metabolism In Plants. CRC Press, Boca Raton, Florida.Google Scholar
  94. Gershenzon, J., Maffei, M., andCroteau, R. 1989. Biochemical and histochemical localization of monoterpene biosynthesis in the glandular trichomes of spearmint (Mentha spicata).Plant Physiol. 89:1351–1357.Google Scholar
  95. Gershenzon, J., Murtagh, G.J., andCroteau, R. 1993. Absence of rapid terpene turnover in several diverse species of terpene-accumulating plants.Oecologia 96:583–592.Google Scholar
  96. Gijzen, M., Lewinsohn, E., andCroteau, R. 1992. Antigenic cross-reactivity among monoterpene cyclases from grand fir and induction of these enzymes upon stem wounding.Arch. Biochem. Biophys. 294:670–674.PubMedGoogle Scholar
  97. Gleizes, M., Pauly, G., Carde, J.-P., Marpeau, A., andBernard-Dagan, C. 1983. Monoterpene hydrocarbon biosynthesis by isolated leucoplasts ofCitrofortunella mitis.Planta 159:373–381.Google Scholar
  98. Goodwin, T.W., andMercer, E.I. 1983. Introduction to Plant Biochemistry, 2nd ed. Pergamon Press, Oxford, 677 pp.Google Scholar
  99. Graebe, J.E. 1987. Gibberellin biosynthesis and control.Annu. Rev. Plant Physiol. 38:419–465.Google Scholar
  100. Gray, J.C. 1987. Control of isoprenoid biosynthesis in higher plants.Adv. Bot. Res. 14:25–91.Google Scholar
  101. Grebenok, R.J., andAdler, J.H. 1991. Ecdysteroid distribution during development of spinach.Phytochemistry 30:2905–2910.Google Scholar
  102. Groeneveld, H.W., Elings, J.C., andKoops, A.J. 1987. Mobilisation of reserves and the earliest synthesis of sterols and latex triterpenes during germination and early seedling growth ofEuphorbia lathyris.Physiol. Plant. 71:296–301.Google Scholar
  103. Gulmon, S.L., andMooney, H.A. 1986. Costs of defense and their effects on plant productivity, pp. 681–698,in T.J. Givnish (ed.). On the Economy of Plant Form and Function. Cambridge University Press, Cambridge, U.K.Google Scholar
  104. Hallahan, T.W., andCroteau, R. 1988. Monoterpene biosynthesis: Demonstration of a geranyl pyrophosphate: sabinene hydrate cyclase in soluble enzyme preparations from sweet marjoram (Majorana hortensis).Arch. Biochem. Biophys. 264:618–631.PubMedGoogle Scholar
  105. Hanover, J.W. 1966. Genetics of terpenes. I. Gene control of monoterpene levels inPinus monticola Dougl.Heredity 21:73–84.Google Scholar
  106. Hasegawa, S., Herman, Z., Orme, E., andOu, P. 1986. Biosynthesis of limonoids inCitrus: Site and translocation.Phytochemistry 25:2783–2785.Google Scholar
  107. Hawkins, A.J.S. 1991. Protein turnover: A functional appraisal.Funct. Ecol. 5:222–233.Google Scholar
  108. Hefendehl, F.W., Underhill, E.W., andVon Rudloff, E. 1967. The biosynthesis of the oxygenated monoterpenes in mint.Phytochemistry 6:823–835.Google Scholar
  109. Heldt, H.W., andFlugge, U.I. 1987. Subcellular transport of metabolites in plant cells, pp. 49–85,in D.D. Davies (ed.). The Biochemistry of Plants, A Comprehensive Treatise, Vol. 12, Physiology of Metabolism. Academic Press, San Diego.Google Scholar
  110. Henry, M., Rochd, M., andBennini, B. 1991. Biosynthesis and accumulation of saponins inGypsophila paniculata.Phytochemistry 30:1819–1821.Google Scholar
  111. Herms, D.A., andMattson, W.J. 1992. The dilemma of plants: To grow or defend.Q. Rev. Biol. 67:283–335.Google Scholar
  112. Hopfinger, J.A., Kumamoto, J., andScora, R.W. 1979. Diurnal variation in the essential oils of Valencia orange leaves.Am. J. Bot. 66:111–115.Google Scholar
  113. Janson, R.W. 1993. Monoterpene emissions from Scots pine and Norwegian spruce.J. Geophys. Res. 98:2839–2850.Google Scholar
  114. Janzen, D.H. 1975. Behavior ofHymenaea courbaril when its predispersal seed predator is absent.Science 189:145–147.Google Scholar
  115. Jensen, S.R. 1991. Plant iridoids, their biosynthesis and distribution in angiosperms, pp. 133–158,in J.B. Harborne and F.A. Tomas-Barberan (eds.). Ecological Chemistry and Biochemistry of Plant Terpenoids, Annual Proceedings of the Phytochemical Society of Europe, Vol. 31. Clarendon Press, Oxford.Google Scholar
  116. Johnson, R.H., andLincoln, D.E. 1990. Sagebrush and grasshopper responses to atmospheric carbon dioxide concentration.Oecologia 84:103–110.Google Scholar
  117. Johnson, R.H., andLincoln, D.E. 1991. Sagebrush carbon allocation patterns and grasshopper nutrition: The influence of CO2 enrichment and soil mineral limitation.Oecologia 87:127–134.Google Scholar
  118. Kalinowska, M., andWojciechowski, Z.A. 1988. Substrate specificity of partially purified UDP-glucose: nuatigenin glucosyltransferase from oat leaves.Plant Sci. 55:239–245.Google Scholar
  119. Karp, F., Harris, J.L., andCroteau, R. 1987. Metabolism of monoterpenes: Demonstration of the hydroxylation of (+)-sabinene to (+)-cis-sabinol by an enzyme preparation from sage (Salvia officinalis) leaves.Arch. Biochem. Biophys. 256:179–193.PubMedGoogle Scholar
  120. Karp, F., Mihaliak, C.A., Harris, J.L., andCroteau, R. 1990. Monoterpene biosynthesis: Specificity of the hydroxylation of (−)-limonene by enzyme preparations from peppermint (Mentha piperita), spearmint (Mentha spicata) and perilla (Perilla frutescens) leaves.Arch. Biochem. Biophys. 276:219–226.PubMedGoogle Scholar
  121. Keene, C.K., andWagner, G.J. 1985. Direct demonstration of duvatrienediol biosynthesis in glandular heads of tobacco trichomes.Plant Physiol. 79:1026–1032.Google Scholar
  122. Kelsey, R.G., andVance, N.C. 1992. Taxol and cephalomannine concentrations in the foliage and bark of shade-grown and sun-exposedTaxus brevifolia trees.J. Nat. Prod. 55:912–917.Google Scholar
  123. Kelsey, R.G., Reynolds, G.W., andRodriguez, E. 1984. The chemistry of biologically active constituents secreted and stored in plant glandular trichomes, pp. 187–241,in E. Rodriguez, P.L. Healey, and I. Mehta (eds.). Biology and Chemistry of Plant Trichomes. Plenum Press, New York.Google Scholar
  124. Kjonaas, R., andCroteau, R. 1983. Demonstration that limonene is the first cyclic intermediate in the biosynthesis of oxygenatedp-menthane monoterpenes inMentha piperita and otherMentha species.Arch. Biochem. Biophys. 220:79–89.PubMedGoogle Scholar
  125. Kjonaas, R., Martinkus-Taylor, C., andCroteau, R. 1982. Metabolism of monoterpenes: Conversion ofl-menthone tol-menthol andd-neomenthol by stereospecific dehydrogenases from pepperment (Mentha piperita) leaves.Plant Physiol. 69:1013–1017.Google Scholar
  126. Kjonaas, R.B., Venkatachalam, K.V., andCroteau, R. 1985. Metabolism of monoterpenes: Oxidation of isopiperitenol to isopiperitenone, and subsequent isomerization to piperitenone by soluble enzyme preparations from peppermint (Mentha piperita) leaves.Arch. Biochem. Biophys. 238:49–60.PubMedGoogle Scholar
  127. Kleinig, H. 1989. The role of plastids in isoprenoid biosynthesis.Annu. Rev. Plant Physiol. Plant Mol. Biol. 40:39–59.Google Scholar
  128. Koops, A.J., andGroeneveld, H.W. 1991. Triterpenoid biosynthesis in the etiolated seedling ofEuphorbia lathyris L. Developmental changes and the regulation of local triterpenoid production.J. Plant Physiol. 138:142–149.Google Scholar
  129. Krischik, V.A., andDenno, R.F. 1983. Individual, population, and geographic patterns in plant defense, pp. 463–512, in R.F. Denno and M.S. McClure (eds.). Variable Plants and Herbivores in Natural and Managed Systems. Academic Press, New York.Google Scholar
  130. Lamb, B., Guenther, A., Gay, D., andWestberg, H. 1987. A national inventory of biogenic hydrocarbon emissions.Atmos. Environ. 21:1695–1705.Google Scholar
  131. Lambers, H., andRychter, A.M. 1989. The biochemical background of variation in respiration rate: Respiratory pathways and chemical composition, pp. 199–225,in H. Lambers (ed.). Causes and Consequences of Variation in Growth Rate and Productivity of Higher Plants. SPB Academic Publishers, The Hague.Google Scholar
  132. Langenheim, J.H., Stubblebine, W.H., Lincoln, D.E., andFoster, C.E. 1978. Implications of variation in resin composition among organs, tissues and populations in the tropical legumeHymenaea.Biochem. Syst. Ecol. 6:299–313.Google Scholar
  133. Langenheim, J.H., Lincoln, D.E., Stubblebine, W.H., andGabrielli, A.C. 1982. Evolutionary implications of leaf resin pocket patterns in the tropical treeHymenaea (Caesalpinioideae: Leguminosae).Am. J. Bot. 69:595–607.Google Scholar
  134. Lapinjoki, S.P., Elo, H.A., andTaipale, H.T. 1991. Development and structure of resin glands on tissues ofBetula pendula Roth. during growth.New Phytol. 117:219–223.Google Scholar
  135. Lawrence, B.M. 1992. Chemical components of Labiatae oils and their exploitation, pp. 399–436,in R.M. Harley and T. Reynolds (eds.). Advances in Labiate Science. Royal Botanic Gardens, Kew, U.K.Google Scholar
  136. Lerdau, M. 1993. Formal equivalence among resource allocation models: What is the appropriate currency?Funct. Ecol. 7:507–508.Google Scholar
  137. Lerdau, M. Litvak, M., andMonson, R. 1994. Plant chemical defense: Monoterpenes and the growth-differentiation balance hypothesis.Trends Ecol. Evol. 9:58–61.Google Scholar
  138. Lewinsohn, E., Gijzen, M., andCroteau, R. 1992. Wound-inducible pinene cyclase from grand fir: Purification, characterization and renaturation after SDS-PAGE.Arch. Biochem. Biophys. 293:167–173.PubMedGoogle Scholar
  139. Lincoln, D.E., andCouvet, D. 1989. The effect of carbon supply on allocation to allelochemicals and caterpillar consumption of peppermint.Oecologia 78:112–114.Google Scholar
  140. Loomis, W.E. 1932. Growth-differentiation balance vs. carbohydrate-nitrogen ratio.Proc. Am. Soc. Hortic. Sci. 29:240–245.Google Scholar
  141. Lorio, P.L., Jr. 1986. Growth-differentiation balance: A basis for understanding southern pine beetle-tree interactions.For. Ecol. Manage. 14:259–273.Google Scholar
  142. Lorio, P.L., Jr. 1988. Growth differentiation-balance relationships in pines affect their resistance to bark beetles (Coleoptera: Scolytidae), pp. 73–92,in W.J. Mattson, J. Levieux, and C. Bernard-Dagan (eds.). Mechanisms of Woody Plant Defenses Against Insects, Search for Pattern. Springer-Verlag, New York.Google Scholar
  143. Loveys, B.R., Robinson, S.P., Brophy, J.J., andChacko, E.K. 1992. Mango sapburn: Components of fruit sap and their role in causing skin damage.Aust. J. Plant Physiol. 19:449–457.Google Scholar
  144. Mahlberg, P.G., Davis, D.G., Galitz, D.S., andManners, G.D. 1987. Laticifers and the classification ofEuphorbia: The chemotaxonomy ofEuphorbia esula L.Bot. J. Linn. Soc. 94:165–180.Google Scholar
  145. Mariani, P., Cappelletti, E.M., Campoccia, D., andBaldan, B. 1989. Oil cell ultrastructure and development inLiriodendron tulipifera L.Bot. Gaz. 150:391–396.Google Scholar
  146. Marner, F.-J., andKerp, B. 1992. Composition of iridals, unusual triterpenoids from sword-lilies, and the seasonal dependence of their content in various parts of differentIris species.Z. Naturforsch. 47c:21–25.Google Scholar
  147. Mathur, A.K., Ahuja, P.S., Pandey, B., Kukreja, A.K., andMandal, S. 1988. Screening and evaluation of somaclonal variations for quantitative and qualitative traits in an aromatic grass,Cymbopogon winterianus Jowitt.Plant Breeding 101:321–334.Google Scholar
  148. McCullough, D.G., andKulman, H.M. 1991. Differences in foliage quality of young jack pine (Pinus banksiana Lamb.) on burned and clearcut sites: Effects on jack pine budworm (Choristoneura pinus pinus Freeman).Oecologia 87:135–145.Google Scholar
  149. McDermitt, D.K., andLoomis, R.S. 1981. Elemental composition of biomass and its relation to energy content, growth efficiency, and growth yield.Ann. Bot. 48:275–290.Google Scholar
  150. McKey, D. 1979. The distribution of secondary compounds within plants, pp. 55–133,in G.A. Rosenthal and D.H. Janzen (eds.). Herbivores: Their Interaction with Secondary Plant Metabolites, 1st ed. Academic Press, New York.Google Scholar
  151. Merino, J., Field, C., andMooney, H.A. 1984. Construction and maintenance costs of Mediterranean-climate evergreen and deciduous leaves. II. Biochemical pathway analysis.Oecol. Plant. 5:211–229.Google Scholar
  152. Metivier, J., andViana, A.M. 1979. The effect of long and short day length upon the growth of whole plants and the level of soluble proteins, sugars, and stevioside in leaves ofStevia rebaudiana Bert.J. Exp. Bot. 30:1211–1222.Google Scholar
  153. Meyberg, M., Krohn, W., Brümmer, B., andKristen, U. 1991. Ultrastructure and secretion of glandular trichomes of tobacco leaves.Flora 185:357–363.Google Scholar
  154. Mihaliak, C.A., andLincoln, D.E. 1989. Changes in leaf mono-and sesquiterpene metabolism with nitrate availability and leaf age inHeterotheca subaxillaris.J. Chem. Ecol. 15:1579–1588.Google Scholar
  155. Mihaliak, C.A., Gershenzon, J., andCroteau, R. 1991. Lack of rapid monoterpene turnover in rooted plants: Implications for theories of plant chemical defense.Oecologia 87:373–376.Google Scholar
  156. Monfar, M., Caelles, C., Balcells, L., Ferrer, A., Hegardt, F.G., andBoronat, A. 1990. Molecular cloning and characterization of plant 3-hydroxy-3-methylglutaryl coenzyme A reductase, pp. 83–97,in G.H.N. Towers and H.A. Stafford (eds.). Biochemistry of the Mevalonic Acid Pathway to Terpenoids, Recent Advances in Phytochemistry, Vol. 24. Plenum Press, New York.Google Scholar
  157. Morrow, P.A., andFox, L.R. 1980. Effects of variation inEucalyptus essential oil yield on insect growth and grazing damage.Oecologia 45:209–219.Google Scholar
  158. Muller, W.H. 1986. Allelochemical mechanisms in the inhibition of herbs by chaparral shrubs, pp. 189–199,in A.R. Putnam and C.-S. Tang (eds.). The Science of Allelopathy. John Wiley & Sons, New York.Google Scholar
  159. Munck, S.L., andCroteau, R. 1990. Purification and characterization of the sesquiterpene cyclase patchoulol synthase fromPogostemon cablin.Arch. Biochem. Biophys. 282:58–64.PubMedGoogle Scholar
  160. Muzika, R.M., Pregitzer, K.S., andHanover, J.W. 1989. Changes in terpene production following nitrogen fertilization of grand fir [Abies grandis (Dougl.) Lindl.] seedlings.Oecologia 80:485–489.Google Scholar
  161. Njar, V.C.O., Arnold, L.M., Banthorpe, D.V., Branch, S.A., Christie, A.C., andMarsh, D.C. 1989. Metabolism of exogenous monoterpenes and their epoxides in seedlings ofPinus pinaster Ait.J. Plant Physiol. 135:628–630.Google Scholar
  162. Ohigashi, H., Wagner, M.R., Matsumura, F., andBenjamin, D.M. 1981. Chemical basis of differential feeding behavior of the larch sawfly,Pristiphora erichsonii (Hartig).J. Chem. Ecol. 7:599–614.Google Scholar
  163. Paczkowski, C., andWojciechowski, Z.A. 1988. The occurrence of UDPG-dependent glucosyltransferase specific for sarsasapogenin inAsparagus officinalis.Phytochemistry 27:2743–2747.Google Scholar
  164. Paterson-Jones, J.C., Gilliland, M.G., andVan Staden, J. 1990. The biosynthesis of natural rubber.J. Plant Physiol. 136:257–263.Google Scholar
  165. Penning de Vries, F.W.T., Brunsting, A.H.M., andVan Laar, H.H. 1974. Products, requirements and efficiency of biosynthesis: A quantitative approach.J. Theor. Biol. 45:339–377.PubMedGoogle Scholar
  166. Platt, K.A., andThomson, W.W. 1992. Idioblast oil cells of avocado: Distribution, isolation, ultrastructure, histochemistry, and biochemistry.Int. J. Plant Sci. 153:301–310.Google Scholar
  167. Polonsky, J., Bhatnagar, S.C., Griffiths, D.C., Pickett, J.A., andWoodcock, C.M. 1989. Activity of quassinoids as antifeedants against aphids.J. Chem. Ecol. 15:993–998.Google Scholar
  168. Porter, J.W., andSpurgeon, S.L. (eds.) 1981. Biosynthesis of Isoprenoid Compounds, Vols. 1 and 2. John Wiley & Sons, New York, 558 pp. and 552 pp.Google Scholar
  169. Puritch, G.S., andNijholt, W.W. 1974. Occurrence of juvabione-related compounds in grand fir and Pacific silver fir infested by balsam woolly aphid.Can. J. Bot. 52:585–587.Google Scholar
  170. Putievsky, E., Ravid, U., Snir, N., andSanderovich, D. 1984. The essential oils from cultivated bay laurel.Isr. J. Bot. 33:47–52.Google Scholar
  171. Quispel, A., Svendsen, A.B., Schripsema, J., Baas, W.J., Erkelens, C., andLugtenburg, J. 1989. Identification of dipterocarpol as isolation factor for the induction of primary isolation ofFrankia from root nodules ofAlnus glutinosa (L.) Gaertner.Mol. Plant-Microbe Inter. 2:107–112.Google Scholar
  172. Rajaonarivony, J.I.M., Gershenzon, J., andCroteau, R. 1992. Characterization and mechanism of (4S)-limonene synthase, a monoterpene cyclase from the glandular trichomes of peppermint (Mentha × piperita).Arch. Biochem. Biophys. 296:49–57.PubMedGoogle Scholar
  173. Rausher, M.D. 1992. Natural selection and the evolution of plant-insect interactions, pp. 20–80,in B.D. Roitberg and M.B. Isman (eds.). Insect Chemical Ecology, An Evolutionary Approach. Chapman and Hall, New York.Google Scholar
  174. Regnier, F.E., Waller, G.R., Eisenbraun, E.J., andAuda, H. 1968. The biosynthesis of methylcyclopentane monoterpenoids. II. Nepetalactone.Phytochemistry 7:221–230.Google Scholar
  175. Reichardt, P.B., Bryant, J.P., Clausen, T.P., andWieland, G.D. 1984. Defense of winterdormant Alaska paper birch against snowshoe hares.Oecologia 65:58–69.Google Scholar
  176. Reichardt, P.B., Chapin, F.S., III, Bryant, J.P., Mattes, B.R., andClausen, T.P. 1991. Carbon/nutrient balance as a predictor of plant defense in Alaskan balsam poplar: Potential importance of metabolite turnover.Oecologia 88:401–406.Google Scholar
  177. Reynolds, A.G., andWardle, D.A. 1989. Influence of fruit microclimate on monoterpene levels of Gewürztraminer.Am. J. Enol. Vitic. 40:149–154.Google Scholar
  178. Rhoades, D.F. 1979. Evolution of plant chemical defense against herbivores, pp. 3–54,in G.A. Rosenthal and D.H. Janzen (eds.). Herbivores: their Interaction with Secondary Plant Metabolites, 1st ed. Academic Press, New York.Google Scholar
  179. Rogers, S., Wells, R., andRechsteiner, M. 1986. Amino acid sequences common to rapidly degraded proteins: The PEST hypothesis.Science 234:364–368.PubMedGoogle Scholar
  180. Ross, J.D., andSombrero, C. 1991. Environmental control of essential oil production in Mediterranean plants, pp. 83–94,in J.B. Harborne and F.A. Tomas-Barberan (eds.). Ecological Chemistry and Biochemistry of Plant Terpenoids, Annual Proceedings of the Phytochemical Society of Europe, Vol. 31. Clarendon Press, Oxford.Google Scholar
  181. Rousi, M., Tahvanainen, J., Henttonen, H., andUotila, I. 1993. Effect of shading and fertilization on resistance of winter-dormant birch (Betula pendula) to voles and hares.Ecology 74:30–38.Google Scholar
  182. Roy, A.T., andDe, D.N. 1992. Studies on differentiation of laticifers through light and electron microscopy inCalotropis gigantea (Linn.) R.Br.Ann. Bot. 70:443–449.Google Scholar
  183. Russin, W.A., Uchytil, T.F., Feistner, G., andDurbin, R.D. 1988. Developmental changes in content of foliar secretory cavities ofTagetes erecta (Asteraceae).Am. J. Bot. 75:1787–1793.Google Scholar
  184. Russin, W.A., Uchytil, T.F., andDurbin, R.D. 1992. Isolation of structurally intact secretory cavities from leaves of African marigold,Tagetes erecta L. (Asteraceae).Plant. Sci. 85:115–119.Google Scholar
  185. Schindler, T., andKotzias, D. 1989. Comparison of monoterpene volatilization and leaf-oil composition of conifers.Naturwissenschaften 76:475–476.Google Scholar
  186. Schnepf, E. 1974. Gland cells, pp. 331–357,in A.W. Robards (ed.). Dynamic Aspects of Plant Ultrastructure. McGraw-Hill, New York.Google Scholar
  187. Schulze-Siebert, D. andSchultz, G. 1987. Full autonomy in isoprenoid synthesis in spinach chloroplasts.Plant Physiol. Biochem. 25:145–153.Google Scholar
  188. Scora, R.W., andMann, J.D. 1967. Essential oil synthesis inMonarda punctata.Lloydia 30:236–241.Google Scholar
  189. Seaman, F., Bohlmann, F., Zdero, C., andMabry, T.J. 1990. Diterpenes of Flowering Plants, Compositae (Asteraceae). Springer-Verlag, New York, 638 pp.Google Scholar
  190. Seigler, D., andPrince, P.W. 1976. Secondary compounds in plants: Primary functions.Am. Nat. 110:101–105.Google Scholar
  191. Shomer, I., andErner, Y. 1989. The nature of oleocellosis in citrus fruits.Bot. Gaz. 150:281–288.Google Scholar
  192. Simms, E.L. 1992. Costs of plant resistance to herbivory, pp. 392–425,in R.S. Fritz and E.L. Simms (eds.). Plant Resistance to Herbivores and Pathogens: Ecology, Evolution, and Genetics. University of Chicago Press, Chicago.Google Scholar
  193. Simms, E.L., andFritz, R.S. 1990. The ecology and evolution of host-plant resistance to insects.Trends Ecol. Evol. 5:356–360.Google Scholar
  194. Simms, E.L., andRausher, M.D. 1987. Costs and benefits of plant resistance to herbivory.Am. Nat. 130:570–581.Google Scholar
  195. Singh, N., andLuthra, R. 1987. Sucrose metabolism and essential oil accumulation during lemongrass (Cymbopogon flexuosus Stapf.) leaf development.Plant Sci. 57:127–133.Google Scholar
  196. Singh, N., Luthra, R., andSangwan, R.S. 1990. Oxidative pathways and essential oil biosynthesis in the developingCymbopogon flexuosus leaf.Plant Physiol. Biochem. 28:703–710.Google Scholar
  197. Singh, N., Luthra, R., andSangwan, R.S. 1991. Mobilization of starch and essential oil biogenesis during leaf ontogeny of lemongrass (Cymbopogon flexuosus Stapf.).Plant Cell Physiol. 32:803–811.Google Scholar
  198. Singh, V.P., Chatterjee, B.N., andSingh, D.V. 1989. Response of mint species to nitrogen fertilization.J. Agric. Sci. 113:267–271.Google Scholar
  199. Skogsmyr, I., andFagerstrom, T. 1992. The cost of anti-herbivory defence: An evaluation of some ecological and physiological factors.Oikos 64:451–457.Google Scholar
  200. Smyrl, T.G., andLemaguer, M. 1980. Solubilities of terpenic essential oil components in aqueous solutions.J. Chem. Eng. Data 25:150–152.Google Scholar
  201. Spencer, A., Hamill, J.D., andRhodes, M.J.C. 1993. In vitro biosynthesis of monoterpenes byAgrobacterium transformed shoot cultures of twoMentha species.Phytochemistry 32:911–919.Google Scholar
  202. Stahl-Biskup, E., andWichtmann, E.-M. 1991. Composition of the essential oils from roots of some Apiaceae in relation to the development of their oil duct systems.Flavour Fragr. J. 6:249–255.Google Scholar
  203. Sukhov, G.V. 1958. The use of radiocarbon in the study of biosynthesis of terpenes, pp. 535–547,in R.C. Extermann (ed.). Radioisotopes in Scientific Research. Pergamon Press, New York.Google Scholar
  204. Swiezewska, E., Dallner, G., Andersson, B., andErnster, L. 1993. Biosynthesis of ubiquinone and plastoquinone in the endoplasmic reticulum-Golgi membranes of spinach leaves.J. Biol. Chem. 268:1494–1499.PubMedGoogle Scholar
  205. Tabata, M., Tanaka, S., Cho, H.J., Uno, C., Shimakura, J., Ito, M., Kamisako, W., andHonda, C. 1993. Production of anti-allergic triterpene, bryonolic acid, by plant cell cultures.J. Nat. Prod. 56:165–174.PubMedGoogle Scholar
  206. Takabayashi, J., Dicke, M., andPosthumus, M.A. 1991. Induction of indirect defence against spider-mites in uninfested lima bean leaves.Phytochemistry 30:1459–1462.Google Scholar
  207. Tallamy, D.W., andRaupp, M.J. (eds.). 1991. Phytochemical Induction by Herbivores. John Wiley & Sons, New York, 431 pp.Google Scholar
  208. Tanaka, S., Yamaura, T., Shigemoto, R., andTabata, M. 1989. Phytochrome-mediated production of monoterpenes in thyme seedlings.Phytochemistry 28:2955–2957.Google Scholar
  209. Thomson, W.W., Platt-Aloia, K.A., andEndress, A.G. 1976. Ultrastructure of oil gland development in the leaf ofCitrus sinensis L.Bot. Gaz. 137:330–340.Google Scholar
  210. Threlfall, D.R., andWhitehead, I.M. 1991. Terpenoid phytoalexins: Aspects of biosynthesis, catabolism, and regulation, pp. 159–208,in J.B. Harborne and F.A. Tomas-Barberan (eds.). Ecological Chemistry and Biochemistry of Plant Terpenoids, Annual Proceedings of the Phytochemical Society of Europe, Vol. 31. Clarendon Press, Oxford.Google Scholar
  211. Tingey, D.T., Turner, D.P., andWeber, J.A. 1991. Factors controlling the emissions of monoterpenes and other volatile organic compounds, pp. 93–119,in T.D. Sharkey, E.A. Holland, and H.A. Mooney (eds.). Trace Gas Emissions by Plants. Academic Press, San Diego.Google Scholar
  212. Tisdale, R.A., andNebeker, T.E. 1992. Resin flow as a function of height along the bole of loblolly pine.Can. J. Bot. 70:2509–2511.Google Scholar
  213. Towers, G.H.N., andStafford, H.A. (eds.). 1990. Biochemistry of the Mevalonate Pathway to Terpenoids, Recent Advances in Phytochemistry, Vol. 24. Plenum Press, New York, 341 pp.Google Scholar
  214. Tuomi, J., Niemela, P., Chapin, F.S., III, Bryant, J.P., andSiren, S. 1988. Defensive responses of trees in relation to their carbon/nutrient balance, pp. 57–72,in W.J. Mattson, J. Levieux, and C. Bernard-Dagan (eds.). Mechanisms of Woody Plant Defenses Against Insects, Search for Pattern. Springer-Verlag, New York.Google Scholar
  215. Tyson, B.J., Dement, W.A., andMooney, H.A. 1974. Volatilisation of terpenes fromSalvia mellifera.Nature 252:119–120.Google Scholar
  216. Van Wassenhove, F.A., Dirinck, P.J., Schamp, N.M., andVulsteke, G.A. 1990. Effect of nitrogen fertilizers on celery volatiles.J. Agric. Food Chem. 38:220–226.Google Scholar
  217. Vierstra, R.D. 1993. Protein degradation in plants.Annu. Rev. Plant Physiol. Plant Mol. Biol. 44:385–410.Google Scholar
  218. Vogeli, U., andChappell, J. 1990. Regulation of a sesquiterpene cyclase in cellulase-treated tobacco cell suspension cultures.Plant Physiol. 94:1860–1866.Google Scholar
  219. Wagschal, K., Savage, T.J., andCroteau, R. 1991. Isotopically sensitive branching as a tool for evaluating multiple product formation by monoterpene cyclases.Tetrahedron 47:5933–5944.Google Scholar
  220. Waterman, P.G., andMole, S. 1989. Extrinsic factors influencing production of secondary metabolites in plants, pp. 107–134,in E.A. Bernays (ed.). Insect-Plant Interactions, Vol. 1, CRC Press, Boca Raton, Florida.Google Scholar
  221. Weidenhamer, J.D., Macias, F.A., Fischer, N.H., andWilliamson, G.B. 1993. Just how insoluble are monoterpenes?J. Chem. Ecol. 19:1799–1807.Google Scholar
  222. Werker, E., andFahn, A. 1981. Secretory hairs ofInula viscosa (L.) Ait.—development, ultrastructure, and secretion.Bot. Gaz. 142:461–476.Google Scholar
  223. Werker, E., Ravid, U., andPutievsky, E. 1985. Structure of glandular hairs and identification of the main components of their secreted material in some species of the Labiatae.Isr. J. Bot. 34:31–45.Google Scholar
  224. Werker, E., Putievsky, E., Ravid, U., Dudai, N., andKatzir, I. 1993. Glandular hairs and essential oil in developing leaves ofOcimum basilicum L. (Lamiaceae).Ann. Bot. 71:43–50.Google Scholar
  225. West, C.A. 1981. Biosynthesis of diterpenes, pp. 375–411,in J.W. Porter and S.L. Spurgeon (eds.). Biosynthesis of Isoprenoid Compounds, Vol. 1. John Wiley & Sons, New York.Google Scholar
  226. Williams, K., Percival, F., Merino, J., andMooney, H.A. 1987. Estimation of tissue construction cost from heat of combustion and organic nitrogen content.Plant Cell Environ. 10:725–734.Google Scholar
  227. Yamaura, T., Tanaka, S., andTabata, M. 1989. Light-dependent formation of glandular trichomes and monoterpenes in thyme seedlings.Phytochemistry 28:741–744.Google Scholar
  228. Yates, J.L., andPeckol, P. 1993. Effects of nutrient availability and herbivory on polyphenolics in the seaweedFucus vesiculosus.Ecology 74:1757–1766.Google Scholar
  229. Zambou, K., Spyropoulos, C.G., Chinou, I., andKontos, F. 1993. Saponin-like substances inhibit α-galactosidase production in the endosperm of fenugreek seeds, a possible regulatory role in endosperm galactomannan degradation.Planta 189:207–212.Google Scholar
  230. Zangerl, A.R., andBazzaz, F.A. 1992. Theory and pattern in plant defense allocation, pp. 363–391,in R.S. Fritz and E.L. Simms (eds.). Plant Resistance to Herbivores and Pathogens: Ecology, Evolution, and Genetics. University of Chicago Press, Chicago.Google Scholar
  231. Zimowski, J. 1991. Occurrence of a glucosyltransferase specific for solanidine in potato plants.Phytochemistry 30:1827–1831.Google Scholar
  232. Zimowski, J. 1992. Specificity and some other properties of cytosolic and membranous UDPGlc: 3ß-hydroxysteroid glucosyltransferases fromSolanum tuberosum leaves.Phytochemistry 31:2977–2981.Google Scholar

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© Plenum Publishing Corporation 1994

Authors and Affiliations

  • Jonathan Gershenzon
    • 1
  1. 1.Institute of Biological ChemistryWashington State UniversityPullman

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