Jasmonate-induced responses of Nicotiana sylvestris results in fitness costs due to impaired competitive ability for nitrogen

Journal of Chemical Ecology

Volumn 26, Issue 4, 2000, Pages 915-952

  Baldwin, Ian T ^a,b   Hamilton III, William ^c  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b UNIVERSITY AT BUFFALO   (United States)

^c SYRACUSE UNIVERSITY   (United States)

Author keywords

Allocation; Costs of defense; Growth; Induced defenses; Nicotiana sylvestris; Nicotine; Nitrogen; Reproduction

Indexed keywords

JASMONE; JASMONIC ACID; NICOTINE; NITROGEN;

ARTICLE; BIOMASS; COMPETITION; NITROGEN FIXATION; NONHUMAN; PLANT GROWTH; PLANT LEAF; PLANT SEED; REGULATORY MECHANISM; REPRODUCTION;

NICOTIANA SYLVESTRIS;

EID: 0034096525     PISSN: 00980331     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1005408208826     Document Type: Article

References (63)

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. BALDWIN, I. T. 1988. Damage-induced alkaloids in tobacco: Pot-bound plants are not inducible. J. Chem. Ecol. 14:1113-1120.
3. BALDWIN, I. T. 1998. Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc. Natl. Acad. Sci. USA 95:8113-8118.
4. BALDWIN, I. T. 1999. Inducible nicotine production in native Nicotiana as an example of adaptive phenotypic plasticity. J. Chem. Ecol. 25:3-30.
5. BALDWIN, I. T., and OHNMEISS, T. E. 1994. Swords into plowshares? Nicotiana sylvestris does not use nicotine as a nitrogen source under nitrogen-limited growth. Oecologia 98:385-392.
6. BALDWIN, I. T., and SCHMELZ, E. A. 1996. Immunological "memory" in the induced accumulation of nicotine in wild tobacco. Ecology 77:236-246.
7. 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.
8. 15N from nitrate to nicotine: Production and turnover of a damage-induced mobile defense. Ecology 75:1703-1713.
9. BALDWIN, I. T., SCHMELZ, 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.
10. BALDWIN, I. T., SCHMELZ, 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.
11. BALDWIN, I. T., ZHANG, Z.-P., DIAB, N., OHNMEISS, T. E., MCCLOUD, E. S., LYNDS, G. Y., and SCHMELZ, E. A. 1997. Quantification, correlations and manipulations of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris. Planta 201:397-404.
12. BALDWIN, I. T., GORHAM, D., SCHMELZ, E. A., LEWANDOWSKI, C., and LYNDS, G. Y. 1998. Allocation of nitrogen to an inducible defense and seed production in Nicotiana attenuata. Oecologia 115:541-552.
13. BALLARE, C. L., SCOPEL, A. L., and SANCHEZ, R. A. 1990. Far-red radiation reflected from adjacent leaves: An early signal of competition in plant canopies. Science 247:329-332.
14. BERGELSON, J., and PURRINGTON, C. B. 1996. Surveying patterns in the cost of resistance in plants. Am. Nat. 3:536-558.
15. 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.
16. BLOOM, A. J., and CHAPIN, F. S. 1985. Resource limitation in plants, an economic analogy. Annu. Rev. Ecol. Syst. 16:363-392.
17. BOODLEY, J. W., and SHELDRAKE, R. J. 1977. Cornell peat-lite mixes for commercial plant growing. Cornell Information Bulletin 43. Cornell University, Ithaca, New York.
18. BROWN, D. G. 1988. The cost of plant defense: an experimental analysis with inducible proteinase inhibitors in tomato. Oecologia 76:467-470.
19. COLEY, P. D., BRYANT, J. P., and CHAPIN, F. S. 1985. Resource availability and plant antiherbivore defense. Science 230:895-899.
20. DUDLEY, S. A., and SCHMITT, J. 1996. Testing the adaptive plasticity hypothesis: Density dependent selection on manipulated stem length in Impatiens capensis. Am. Nat. 147:445-465.
21. EULER, M., and BALDWIN, I. T. 1996. The chemistry of defense and apparency in the corollas of Nicotiana attenuata. Oecologia 107:102-112.
22. FEENY, P. 1976. Plant apparency and chemical defense. Recent Adv. Phytochem. 10:1-40.
23. FINEBLUM, W. L., and RAUSHER, M. D. 1995. Tradeoff between resistance and tolerance to herbivore damage in a morning glory. Nature 377:517-520.
24. GIVNISH, T. J. 1986. Economics of biotic interactions, pp. 667-679 in T. J. Givnish (ed.). On the Economy of Plant Form and Function. Cambridge University Press, Cambridge.
25. GÖRSCHEN, E., DUNAEVA, M., HAUSE, B., REEH, I., WASTERNACK, C., and PARTHIER, B. 1997a. Expression of the ribosome-inactivating protein JIP60 from barley in transgenic tobacco leads to an abnormal phenotype and alterations on the level of translation. Planta 202:470-473.
26. GÖRSCHEN, E., DUNAEVA, M., REEH, L., and WASTERNACK, C. 1997b. Overexpression of the jasmonate-inducible 23 KDA protein (JIP23) from bailey in transgenic tobacco leads to the repression of leaf proteins. FEBS Lett. 419:58-62.
27. GOULD, S. J., and LEWONTIN, R. C. 1979. The spandrels of San Marco and the Panglossian paradigm: A critique of the adaptationist programme. Proc. R. Soc. London B 205:581-598.
28. HARVELL, C. D. 1986. The ecology and evolution of inducible defenses in a marine bryozoan: Cues, costs, and consequences. Am. Nat. 128:810-823.
29. HAUKIOJA, E., and HAKALA, T. 1975. Herbivore cycles and periodic outbreaks. Formulation of a general hypothesis. Rep. Kevo Subarct. Res. Stn. 12:1-9.
30. HERMS, D. A., and MATTSON, W. J. 1992. The dilemma of plants: to grow or defend. Q. Rev. Biol. 67:283-335.
31. HOWE, G. A., LIGHTNER, J., BROWSE, J., and RYAN, C. A. 1986. An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell 8:2067-2077.
32. JACINTO, T., MCGURL, B., FRANCESCHI, V., DELANO-FREIER, J., and RYAN, C. A. 1997. Tomato prosystemin promoter gene in transgenic tomato plants. Planta 203:406-412.
33. KARBAN, R., and BALDWIN, I. T. 1997. Induced Responses to Herbivory, University of Chicago Press, Chicago.
34. LYNDS, G. Y., and BALDWIN, I. T. 1998. Fire, nitrogen, and defensive plasticity. Oecologia 115:531-540.
35. MCCLOUD, E. S., and BALDWIN, I. T. 1997. Herbivory and caterpillar régurgitants amplify the wound-induced increases in jasmonic acid but not nicotine in Nicotiana sylvestris. Planta 203:430-435.
36. MCCONN, M., CREELMAN, R. A., BELL, E., MULLET, J. E., and BROWSE, J. 1997. Jasmonate is essential for insect defense in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 4:5473-5477.
37. MCGURL, B., PEARCE, G., OROZCO-CARDENAS, M., and RYAN, C. A. 1992. Structure, expression, and antisense inhibition of the systemin precursor gene. Science 255:1570-1573.
38. MCKEY, D. 1974. Adaptive patterns in alkaloid physiology. Am. Nat. 108:305-320.
39. MCKEY, D. 1979. The distribution of secondary compounds within plants, pp. 56-133-56-133, in G. A. Rosenthal and D. H. Janzen (eds.). Herbivores: Their Interaction with Secondary Plant Metabolites. Academic Press, New York.
40. MOLE, S. 1994. Trade-offs and constraints in plant-herbivore defense theory: A life-history perspective. Oikos 71:3-12.
41. OHNMEISS, T. E., and BALDWIN, I. T. 1994. The allometry of nitrogen allocation to growth and an inducible defense under nitrogen-limited growth. Ecology 75:995-1002.
42. 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.
43. OROZCO-CARDENAS, M., MCGURL, B., and RYAN, C. A. 1993. Expression of an antisense prosystemin gene in tomato plants reduces resistance toward Manduca sexta larvae. Proc. Natl. Acad. Sci. U.S.A. 90:8273-8276.
44. PEARCE, G., JOHNSON, S., STRYDOM, D., and RYAN, C. A. 1991. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253:895-898.
45. RAUSHER, M. D. 1996. Genetic analysis of coevolution between plants and their natural enemies. Trends Genet. 12:212-217.
46. REEKIE, E. G., and BAZZAZ, F. A. 1987. Reproductive efforts in plants. 1. Carbon allocation to reproduction. Am. Nat. 129:897-906.
47. 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. Academic Press, New York.
48. RHOADES, D. F. 1983. Responses of alder and willow to attack by tent caterpillar's and webworms: evidence for pheromonal sensitivity of willows, pp. 55-68, in P. A. Hedin (ed.). Plant Resistance to Insects. American Chemical Society, Washington, D.C.
49. RHOADES, D. F., and CATES, R. G. 1976. Towards a general theory of plant antiherbivore chemistry. Recent Adv. Phytochem. 10:168-213.
50. ROSENTHAL, J. P., and KOTANEN, P. M. 1994. Terrestrial plant tolerance to herbivory. TREE 9:145-148.
51. SCHWINNTNG, S., and WEINER, J. 1998. Mechanisms determining the degree of size asymmetry in competition among plants. Oecologia 113:447-455.
52. 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.
53. STAMP, N. E. 1992. The theory of plant-insect interactions on the inevitable brink of resynthesis. Bull. Ecol. Soc. Am. 73:28-34.
54. STRAUSS, S. Y. 1997. Floral characters link herbivores, pollinators, and plant fitness. Ecology 78:1640-1645.
55. THALER, J. S., STOUT, M. J., KARBAN, R., and DUFFEY, S. S. 1996. Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field. J. Chem. Ecol. 22:1767-1779.
56. VAN DAM, N. M., and BALDWIN, I. T. 1998. Costs of jasmonate-induced responses in plants competing for limited resources. Ecol. Lett. 1:30-33.
57. VAN DER MEIJDEN, E., WIJN, M., and VERKAAR, H. J. 1988. Defense and regrowth, alternative plant strategies in the struggle against herbivores. Oikos 51:355-363.
58. WASTERNACK, C., and PARTHIER, B. 1997. Jasmonate-signalled plant gene expression. TIPS 2:302-307.
59. WASTERNACK, C., ORTEL, B., MIERSCH, O., KRAMELL, R., BEALE, M., GREULICH, F., FEUSSNER, I., HAUSE, B., KRUMM, T., BOLAND, W., and PARTHIER, B. 1998. Diversity in octadecanoid-induced gene expression of tomato. J. Plant Physiol. 152:1-8.
60. WILLIAMS, M. M., JORDAN, N., and YERKES, C. 1995. The fitness costs of triazine resistance in jimsonweed (Datura stramonium L.). Am. Midl. Nat. 133:131-137.
61. YU, J. Q., and MATSUI, Y. 1994. Phytoxic Substances in Root Exudates of Cucumber (Cucumis sativus L.). J. Chem. Ecol. 20:21-32.
62. ZANGERL, A. Z., ARNTZ, A. M., and BERENBAUM, M. R. 1997. Physiological price of an induced chemical defense - photosynthesis, respiration, biosynthesis, and growth. Oecologia 109:433-441.
63. 14C]jasmonic acid from leaves to roots mimics wound-induced changes in endogenous jasmonic acid pools in Nicotiana sylvestris. Planta 203:436-441.