Inducible nicotine production in native Nicotiana as an example of adaptive phenotypic plasticity

Journal of Chemical Ecology

Volumn 25, Issue 1, 1999, Pages 3-30

  Baldwin, Ian T ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

Costs and benefits; Induced defense; Nicotine; Phenotypic plasticity; Post fire germination

Indexed keywords

NICOTINE;

ANTIHERBIVORE DEFENSE; FITNESS; PHENOTYPIC PLASTICITY; PHYTOCHEMISTRY;

ADAPTATION; ARTICLE; ENVIRONMENTAL FACTOR; NONHUMAN; ONTOGENY; PHENOTYPE; PLANT GROWTH; PLASTICITY;

DICOTYLEDONEAE; NICOTIANA;

EID: 0032913212     PISSN: 00980331     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1020880931488     Document Type: Article

References (100)

1. ADLER, F. R., and KARBAN, R. 1994. Defended fortresses or moving targets? Another model of inducible defenses inspired by military metaphors. Am. Nat. 144:813-832.
2. AGRAWAL, A. A. 1998. Induced responses to herbivory and increased plant performance. Science 279:1201-1202.
3. ALBORN, H. T., TURLINGS, T. C. J., JONES, T. H., STENHAGEN, G., LOUGHRIN, J. H., and TUMLINSON, J. H. 1997. An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945-949.
4. BALDWIN, I. T. 1988a. The alkaloidal responses of wild tobacco to real and simulated herbivory. Oecologia 77:378-381.
5. BALDWIN, I. T. 1988b. Damage-induced alkaloids in tobacco: Pot-bound plants are not inducible. J. Chem. Ecol. 14:1113-1120.
6. BALDWIN, I. T. 1988c. Short-term damage-induced increases in tobacco alkaloids protect plants. Oecologia 75:367-370.
7. BALDWIN, I. T. 1989. Mechanism of damaged-induced alkaloids in wild tobacco. J. Chem. Ecol. 15:1661-1680.
8. BALDWIN, I. T. 1991. Damage-induced alkaloids in wild tobacco, pp. 47-49, in M. J. Raupp and D. W. Tallamy (eds.). Phytochemical Induction by herbivores. John Wiley & Sons, New York.
9. BALDWIN, I. T. 1993. Chemical changes rapidly induced by folivory, pp. 1-23, in E. A. Bernay (ed.). Insect-Plant Interactions. CRC Press, Boca Raton, Florida.
10. BALDWIN, I. T. 1996. Methyl jasmonate-induced nicotine production in Nicotiana attenuata: Inducing defenses in the field without wounding. Entomol. Exp. Appl. 80:213-220.
11. BALDWIN, I. T. 1997. Allometric limits to the induced accumulation of nicotine in native tobacco. Plant Species Biol. 11:107-114.
12. BALDWIN, I. T. 1998. Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc. Natl. Acad. Sci. U.S.A. 95:8113-8118.
13. BALDWIN, I. T. 1999. The jasmonate cascade and the complexity of induced defense against herbivore attack, in M. Wink (ed.). The Role of Plant Secondary Metabolites and Their Utilization in Biotechnology. Sheffield Academic Press, Sheffied, UK. In press.
14. BALDWIN, I. T., and CALLAHAN, P. 1993. Autotoxicity and chemical defense: nicotine accumulation and carbon gain in solanaceous plants. Oecologia 94:534-541.
15. BALDWIN, I. T., nad KARB, M. J. 1995. Plasticity in allocation of nicotine to reproductive parts in Nicotiana attenuata. J. Chem. Ecol. 21:897-909.
16. BALDWIN, I. T., and MORSE, L. 1994. Up in smoke: II. Germination of Nicotiana attenuata in response to smoke-derived cues and nutrients in burned and unburned soils. J. Chem. Ecol. 20:2373-2391.
17. BALDWIN, I. T., and OHNMEISS, T. E. 1993. Alkaloidal responses to damage in Nicotiana native to North America. J. Chem. Ecol. 19:1143-1153.
18. BALDWIN, I. T., and OHNMEISS, T. E. 1994a. Coordination of photosynthetic and alkaloidal responses to damage in uninducible and inducible Nicotiana sylvestris. Ecology 75:1003-1014.
19. BALDWIN, I. T., and OHNMEISS, T. E. 1994b. Swords into plowshares? Nicotiana sylvestris does not use nicotine as a nitrogen source under nitrogen-limited growth. Oecologia 98:385-392.
20. BALDWIN, I. T., and SCHMELZ, E. A. 1994. Constraints on an induced defense: The role of canopy area. Oecologia 97:424-430.
21. BALDWIN, I. T., and SCHMELZ, E. A. 1996. Immunological "memory" in the induced accumulation of nicotine in wild tobacco. Ecology 77:236-246.
22. BALDWIN, I. T., SIMS, C. L., and KEAN, S. E. 1990. The reproductive consequences associated with inducible alkaloidal responses in wild tobacco. Ecology 71:252-262.
23. BALDWIN, I. T., OESCH, R. C., MERHIGE, P. M., and HAYES, K. 1993. Damage-induced root nitrogen metabolism in Nicotiana sylvestris: Testing C/N predictions for alkaloid production. J. Chem. Ecol. 19:3029-3043.
24. 15N from nitrate to nicotine: Production and turnover of a damage-induced mobile defense. Ecology 75:1703-1713.
25. BALDWIN, I. T., SCHEMLZ, E. A., and OHNMEISS, T. E. 1994b. Wound-induced changes in root and shoot jasmonic acid pools correlate with induced nicotine synthesis in Nicotiana sylvestris Spegazzini and Comes. J. Chem. Ecol. 20:2139-2157.
26. BALDWIN, I. T., STASZAK-KOZINSKI, L., and DAVIDSON, R. 1994c. Up in smoke: I. Smoke-derived germination cues for the postfire annual Nicotiana attenuata Torr. Ex. Watson. J. Chem. Ecol. 20:2345-2371.
27. BALDWIN, I. T., SCHEMLZ, E. A., and ZHANG, Z.-P. 1996. Effects of octadecanoid metabolites and inhibitors on induced nicotine accumulation in Nicotiana sylvestris. J. Chem. Ecol. 22:61-73.
28. BALDWIN, I. T., PRESTON, C. A., EULER, M. A., and GORHAM, D. 1997a. Patterns and consequences of benzyl acetone floral emissions from Nicotiana attenuata plants. J. Chem. Ecol. 23:2327-2343.
29. BALDWIN, I. T., ZHANG, Z.-P., DIAB, N., OHNMEISS, T. E., E. S., M., LYNDS, G. Y., and SCHMELZ, E. A. 1997b. Quantification, correlations and manipulations of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris. Planta 201:397-404.
30. BALDWIN, I. T., GORHAM, D., SCHMELZ, E. A., LEWANDOWSKI, C., and LYNDS, G. Y. 1998. Allocation of nitrogen to an inducible defense and seed in Nicotiana attenuata. Oecologia 115:541-552.
31. BARBOSA, P., GROSS, P., and KEMPER, J. 1991. Influence of plant allelochemicals on the tobacco hornworm and its parasitoid, Cotesia congregata. Ecology 72:1567-1575.
32. BAZZAZ, F. A., CHIARIELLO, N. R., COLEY, P. D., and PITELKA, L. F. 1987. Allocating resources to reproduction and defense. BioScience 37:58-67.
33. BENDER, C., and PALMER, D. 1996. Biosynthesis of coronatine, a thermoregulated phytotoxin produced by the phytopathogen Pseudomonas syringae. Arch. Microbiol. 166:71-75.
34. BERGEY, D. R., HOWE, G. A., and RYAN, C. A. 1996. Polypeptide signaling for plants defensive genes exhibits analogies to defense signaling in animals. Proc. Natl. Acad. Sci. U.S.A. 93:12053-12058.
35. BLECHERT, S., BRODSCHELM, W., HÖLDER, S., KAMMERER, L., KUTCHAN, T. M., MÜLLER, J. M., XIA, Z. Q., and ZENK, M. H. 1995. The octadecanoic pathways: Signal molecules for the regulation of secondary pathways. Proc. Natl. Acad. Sci. U.S.A. 92:4099-4105.
36. BLECHERT, S., BOCKELMANN, C., BRÜMMER, O., FÜßLEIN, M., GUNDLACH, H., HAIDER, G., HÖLDER, S., KUTCHAN, T. M., WEILER, E. W., and ZENK, M. H. 1997. Structural separation of biological activities of jasmonates and related compounds. J. Chem. Soc. 23:3549-3559.
37. BOWERS, M. D. 1988. Chemistry and coevolution: Iriidoid glycosides, plants and herbivorous insects, pp. 133-166, in K. C. Spencer (ed.). Chemical Mediation of Coevolution. Academic Press, New York.
38. BRYANT, J. P., CHAPIN, F. S., and KLEIN, D. R. 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357-368.
39. CREELMAN, R. A., and MULLET, J. E. 1997. Biosynthesis and action of jasmonates in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:355-381.
40. DAWSON, R. F. 1942. Accumulation of nicotine in reciprocal grafts of tomato and tobacco. Am. J. Bot. 29:66-71.
41. DEMORAES, C. M., LEWIS, W. J., PARE, P. W. ALBORN, H. T., and TUMLINSON, J. H. 1998. Herbivore-infested plants selectively attract parasitoids. Nature 393:570-573.
42. DEWITT, T. J., SIH, A., and WILSON, D. S. 1998. Costs and limits of phenotypic plasticity. TREE 13:77-81.
43. EISNER, T. E., and MEINWALD, J. 1995. The chemistry of sexual selection. Proc. Natl. Acad. Sci. U.S.A. 92:50-55.
44. EULER, M., and BALDWIN, I. T. 1996. The chemistry of defense and apparency in the corollas of Nicotiana attenuata. Oecologia 107:102-112.
45. FARMER, E. E., and RYAN, C. A. 1990. Interplant communication: Airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc. Natl. Acad. Sci. U.S.A. 87:7713-7716.
46. FARMER, E. E., and RYAN, C. A. 1992. Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4:129-134.
47. FETH, F., WAGNER, R., and WAGNER, K. G. 1986. Regulation in tobacco callus of enzyme activities of the nicotine pathway I. The route from ornithine to methylpyrroline. Planta 168:402-407.
48. FINEBLUM, W. L., and RAUSHER, M. D. 1995. Tradeoff between resistance and tolerance to herbivore damage in a morning glory. Nature 377:517-520.
49. FOWLER, S. V., and LAWTON, J. H. 1985. Rapidly induced defenses and talking trees: The devil's advocate position. Am. Nat. 126:181-195.
50. 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. CRC Press, Boca Raton, Florida.
51. HASLAM, E. 1986. Secondary metabolism - fact and fiction. Nat. Prod. Rep. 3:217-249.
52. HERMS, D. A., and MATTSON, W. J. 1992. The dilemma of plants: to grow or defend. Q. Rev. Biol. 67:283-335.
53. HIBI, N., HIGASHIGUCHI, S., HASHIMOTO, T., and YAMADA, Y. 1994. Gene expression in tobacco low-nicotine mutants. Plant Cell 6:723-735.
54. KARBAN, R. 1993. Costs and benefits of induced resistance and plant density for a native shrub, Gossypium thurberi. Ecology 74:9-19.
55. KARBAN, R., and BALDWIN, I. T. 1997. Induced Responses to Herbivory. Chicago University Press, Chicago.
56. KARBAN, R., and MYERS, J. H. 1989. Induced plant responses to herbivory. Annu. Rev. Ecol. Syst. 20:331-348.
57. KOIWA, H., BRESSAN, R. A., and HASEGAWA, P. M. 1997. Regulation of protease inhibitors and plant defense. TIPS 2:379-383.
58. KRISCHIK, V. A., BARBOSA, P., and REICHELDERFER, C. 1988. Three trophic level interactions: Allelochemicals, Manduca sexta (L.), and Bacillus thuringiensis var. kurstaki Berliner. Environ. Entomol. 17:476-482.
59. LYNDS, G. Y., and BALDWIN, I. T. 1998. Fire, nitrogen, and defensive plasticity. Oecologia In press.
60. MALCOLM, S. B., and ZALUCKI, M. P. 1996. Milkweed latex and cardenolide induction may resolve the lethal plant defence paradox. Entomol. Exp. Appl. 80:193-196.
61. MAURICIO, R., RAUSHER, M. D., and BURDICK, D. S. 1997. Variation in the defense strategies of plants: Are resistance and tolerance mutually exclusive? Ecology 78:1301-1311.
62. MCCLOUD, E. S., and BALDWIN, I. T. 1997. Herbivory and caterpillar regurgitants amplify the wound-induced increases in jasmonic cid but not nicotine in Nicotiana sylvestris. Planta 203:430-435.
63. MCKEY, D. 1979. The distribution of secondary compounds within plants, pp. 56-133, in G. A. Rosenthal and D. H. Janzen (eds.). Herbivores: Their Interaction with Secondary Plant Metabolites. Academic Press, New York.
64. MIZUSAKI, S., TANABE, Y., NOGUCHI, M., and TAMAKI, E. 1973. Activities of ornithine decarboxylase, putrescine N-methyltransferase and N-methylputrescine oxidase in tobacco roots in relation to nicotine biosynthesis. Plant Cell Physiol. 14:103-110.
65. MOLE, S. 1994. Trade-offs and constraints in plant-herbivore defense theory: A life-history perspective. Oikos 71:3-12.
66. MURRAY, C. L., QUAGLIA, M., ARNANSON, J. T., and MORRIS, C. E. 1994. A putative nicotine pump at the metabolic blood-brain barrier of the tobacco hornworm. J. Neurobiol. 25:23-34.
67. NOWACKI, E., JURZYSTA, M., GORSKI, P., NOWACKA, D., and WALLER, G. R. 1976. Effect of nitrogen nutrition on alkaloidd metabolism in plants. Biochem. Physiol. Pflanzen 169:231-240.
68. OHNMEISS, T. E., and BALDWIN, I. T. 1994. The allometry of nitrogen allocation to growth and an inducible defense under nitrogen-limtied growth. Ecology 75:995-1002.
69. OHNMEISS, T., MCCLOUD, E. S., LYNDS, G. Y., and BALDWIN, I. T. 1997. Within-plant relationships among wounding, jasmonic acid, and nicotine: Implications for defense in Nicotiana sylvestris. new Phytol. 137:441-452.
70. PARR, J. C., and THURSTON, R. 1972. Toxicity of nicotine in synthetic diets to larvae of the tobacco hornworm. Ann. Entomol. Soc. Am. 65:1185-1188.
71. PIGLIUCCI, M., SCHLICHTING, C. D., JONES, C. S., and SCHWENK, K. 1996. Developmental reaction norms: The interaction among allometry, ontogeny and plasticity. Plant Spec. Biol. 11:69-85.
72. PRESTON, C. A., and BALDWIN, I. T. 1999. Positive and negative signals regulate germination in the post-fire annual, Nicotiana attenuata. Ecology In press.
73. RABE, E. 1990. The functional significance of the accumulation of nitrogen-containing compounds. J. Hortic. Sci. 65:231-243.
74. RUSHER, M. D. 1996. Genetic analysis of coevolution between plants and their natural enemies. Trends Genet. 12:212-217.
75. REEVE, H. K., and SHERMAN, P. W. 1993. Adaptation and the goals of evolutionary research. Q. Rev. Biol. 68:1-32.
76. ROSENTHAL, J. P., and KOTANEN, P. M. 1994. Terrestrial plant tolerance to herbivory. TREE 9:145-148.
77. ROWELL-RATHIER, M., and PASTEELS, J. M. 1992. Third trophic level influences of plant allelochemical, pp. 243-277, in G. A. Rosenthal and M. R. Berenbaum (eds.). Herbivores: Their Interactions with Secondary Plant Metabolites. Academic Press, New York.
78. SAUNDERS, J. W., and BUSH, L. P. 1979. Nicotine biosynthetic enzyme activities in Nicotiana tabacum genotypes with different alkaloids levels. Plant Physiol. 64:236-240.
79. SCHEINER, S. M. 1993. Genetics and evolution of phenotypic plasiticity. Annu. Rev. Ecol. Syst. 24:35-68.
80. SCHLICHTING, C. D. 1986. The evolution of phenotypic plasticity in plants. Annu. Rev. Ecol. Syst. 17:667-693.
81. SCHMITT, J., MCCORMAC, A. C., and SMITH, H. 1995. A test of the adaptive plasticity hypothesis using transgenic and mutant plants disabled in phytochrome-mediated elongation responses to neighbors. Am. Nat. 146:937-953.
82. SELF, L. S., and GUTHRIE, F. E. 1964. Adaptation of tobacco homworms to the ingestion of nicotine. J. Insect Physiol. 10:907-914.
83. SIMMS, E. L. 1992. Costs of plant resistance to herbivores, 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.
84. SMILEY, J. T., HORN, J. M., and RANK, N. E. 1985. Ecological effects of salicin at three trophic levels: New problems from old adaptations. Science 229:649-651.
85. SNYDER, M. J., and GLENDINNING, J. I. 1996. Causal connection between detoxification enzyme activity and consumption of a toxic plant compound. J. Comp. Physiol. A. 179:255-261.
86. SRAUSS, S. Y. 1997. Floral characters link herbivores, pollinators, and plant fitness. Ecology 78:1640-1645.
87. SULTAN, S. E. 1992. Phenotypic plasticity and the neo-Darwinian legacy. Evol. Trends Plant 6:61-71.
88. TAKABAYASHI, J., and DICKE, M. 1996. Plant-carnivore mutualism through herbivore-induced carnivore attractants. TIPS 1:109-113.
89. TALLAMY, D. W., and RAUPP, M. J. 1991. Phytochemical Induction by Herbivores. John Wiley & Sons, New York.
90. THOMPSON, J. 1991. Phenotypic plasticity as a component of evolutionary change. TREE 6:246-249.
91. TUOMI, J., NIEMELÄ, P., HAUKIOJA, E., SIRÉN, S., and NEUVONEN, S. 1984. Nutrient stress: An explanation for plant anti-herbivore responses to defoliation. Oecologia 61:208-210.
92. TURLINGS, T. C. J., TUMLINSON, J. H., and LEWIS, W. J. 1990. Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251-1253.
93. TURLINGS, T. C. J., LOUGHRIN, J. H., MCCALL, P. J., RÖSE, U. S. R., LEWIS, W. J., and TUMLINSON, J. H. 1995. How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc. Natl. Acad. Sci. U.S.A. 92:4169-4174.
94. VAN DAM, N. M., and BALDWIN, I. T. 1998. Costs of jasmonate-induced responses in plants competing for limited resources. Ecol. Lett. In press.
95. VAN DER MEIJDEN, E., WUN, M., and VERKAAR, H. J. 1988. Defense and regrowth, alternative plant strategies in the struggle against herbivores. Oikos 51:355-363.
96. WAGNER, R., FETH, F., and WAGNER, K. G. 1986. The regulation of enzyme activities of the nicotine pathway in tobacco. Physiol. Plant. 68:667-672.
97. WASTERNACK, C., and PARTHIER, B. 1997. Jasmonate-signalled plant gene expression. TIPS 2:302-307.
98. WEILER, E. W. 1997. Octadecanoid-mediated signal transduction in higher plants. Naturwissenschaften 84:340-349.
99. ZANGERL, A. R., and BAZZAZ, 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.
100. 14C]jasmonic acid from leaves to roots mimics wound-induced changes in endogenous jasmonic acid pools in Nicotiana sylvestris. Planta 203:436-441.