Resistance management in a native plant: Nicotine prevents herbivores from compensating for plant protease inhibitors

Ecology Letters

Volumn 10, Issue 6, 2007, Pages 499-511

  Steppuhn, Anke ^a   Baldwin, Ian T ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

Nicotiana attenuata; Plant defense; Secondary metabolites; Spodoptera exigua; Synergistic interaction; Tobacco; Trypsin proteinase inhibitors

Indexed keywords

NICOTINE; PROTEINASE INHIBITOR;

ALKALOID; CHEMICAL DEFENSE; HERBIVORE; MOTH; NATIVE SPECIES; RESISTANCE MANAGEMENT; TOBACCO;

ANIMAL; ARMYWORM; ARTICLE; METABOLISM; PHYSIOLOGY; TOBACCO;

ANIMALS; NICOTINE; PROTEASE INHIBITORS; SPODOPTERA; TOBACCO;

HEXAPODA; NICOTIANA ATTENUATA; NICOTIANA TABACUM; SPODOPTERA EXIGUA;

EID: 34248198418     PISSN: 1461023X     EISSN: 14610248     Source Type: Journal    
DOI: 10.1111/j.1461-0248.2007.01045.x     Document Type: Article

References (54)

1. Abdeen, A., Virgos, A., Olivella, E., Villanueva, J., Aviles, X., Gabarra, R. et al. (2005). Multiple insect resistance in transgenic tomato plants over-expressing two families of plant proteinase inhibitors. Plant Mol. Biol., 57, 189 202.
2. Appel, H.M. Martin, M.M. (1992). Significance of metabolic load in the evolution of host specificity in Manduca sexta. Ecology, 73, 216 228.
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. Bennett, R.N. Wallsgrove, R.M. (1994). Secondary metabolites in plant defense-mechanisms. New Phytol., 127, 617 633.
5. Berenbaum, M.R. (1985). Brementown revisited: interactions among allelochemicals in plants. Rec. Adv. Phytochem., 19 139 169.
6. Berenbaum, M. Neal, J.J. (1985). Synergism between myristicin and xanthotoxin, a naturally cooccurring plant toxicant. J. Chem. Ecol., 11, 1349 1358.
7. Berenbaum, M.R. Zangerl, A.R. (1993). Furanocoumarin metabolism in Papilio polyxenes: biochemistry, genetic variability, and ecological significance. Oecologia, 95, 370 375.
8. Birk, Y. (2003). Plant Protease Inhibitors; Significance in Nutrition, Plant Protection, Cancer Prevention and Genetic Engineering. Springer, Berlin.
9. Broadway, R.M. Duffey, S.S. (1988). The effect of plant protein quality on insect digestive physiology and the toxicity of plant proteinase inhibitors. J. Insect Physiol., 34, 1111 1117.
10. Bubner, B., Gase, K. Baldwin, I.T. (2004). Two-fold differences are the detection limit for determining transgene copy numbers in plants by real-time PCR. BMC Biotechnol., 4, 1 11.
11. Bubner, B., Gase, K., Berger, B., Link, D. Baldwin, I.T. (2006). Occurrence of tetraploidy in Nicotiana attenuata plants after Agrobacterium-mediated transformation is genotype specific but independent of polysomaty of explant tissue. Plant Cell Rep., 25, 668 675.
12. Cao, J., Zhao, J.Z., Tang, J.D., Shelton, A.M. Earle, E.D. (2002). Broccoli plants with pyramided cry1Ac and cry1C Bt genes control diamondback moths resistant to Cry1A and Cry1C proteins. Theor. Appl. Genet., 105, 258 264.
13. Chintapakorn, Y. Hamill, J.D. (2003). Antisense-mediated down-regulation of putrescine N-methyltransferase activity in transgenic Nicotiana tabacum L. can lead to elevated levels of anatabine at the expense of nicotine. Plant Mol. Biol., 53, 87 105.
14. Cloutier, C., Jean, C., Fournier, M., Yelle, S. Michaud, D. (2000). Adult Colorado potato beetles, Leptinotarsa decemlineata compensate for nutritional stress on oryzacystatin I-transgenic potato plants by hypertrophic behavior and over-production of insensitive proteases. Arch. Insect Biochem. Physiol., 44, 69 81.
15. van Dam, N.M., Horn, M., Mares, M. Baldwin, I.T. (2001). Ontogeny constrains systemic protease inhibitor response in Nicotiana attenuata. J. Chem. Ecol., 27, 547 568.
16. De Leo, F., Bonade-Bottino, M.A., Ceci, L.R., Gallerani, R. Jouanin, L. (1998). Opposite effects on Spodoptera littoralis larvae of high expression level of a trypsin proteinase inhibitor in transgenic plants. Plant Physiol., 118, 997 1004.
17. Dyer, L.A., Dodson, C.D., Stireman, J.O., Tobler, M.A., Smilanich, A.M., Fincher, R.M. et al. (2003). Synergistic effects of three Piper amides on generalist and specialist herbivores. J. Chem. Ecol., 29, 2499 2514.
18. Feeny, P. (1976). Plant apparency and chemical defense. Recent Adv. Phytochem., 10, 1 40.
19. Felton, G.W., Broadway, R.M. Duffey, S.S. (1989). Inactivation of protease inhibitor activity by plant-derived quinones: complications for host-plant resistance against Noctuid herbivores. J. Insect Physiol., 35, 981 990.
20. Glendinning, J.I. (2002). How do herbivorous insects cope with noxious secondary plant compounds in their diet? Entomol. Exp. Appl., 104, 15 25.
21. Govenor, H.L., Schultz, J.C. Appel, H.M. (1997). Impact of dietary allelochemicals on gypsy moth (Lymantria dispar) caterpillars: importance of midgut alkalinity. J. Insect Physiol., 43, 1169 1175.
22. Green, E.S., Zangerl, A.R. Berenbaum, M.R. (2001). Effects of phytic acid and xanthotoxin on growth and detoxification in caterpillars. J. Chem. Ecol., 27, 1763 1773.
23. Halitschke, R. Baldwin, I.T. (2003). Antisense LOX expression increases herbivore performance by decreasing defense responses and inhibiting growth-related transcriptional reorganization in Nicotiana attenuata. Plant J., 36, 794 807.
24. Halitschke, R., Schittko, U., Pohnert, G., Boland, W. Baldwin, I.T. (2001). Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol., 125, 711 717.
25. Hermsmeier, D., Schittko, U. Baldwin, I.T. (2001). Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. I. Large-scale changes in the accumulation of growth- and defense-related plant mRNAs. Plant Physiol., 125, 683 700.
26. Hibi, N., Higashiguchi, S., Hashimoto, T. Yamada, Y. (1994). Gene-expression in tobacco low-nicotine mutants. Plant Cell, 6, 723 735.
27. Jones, C.G. (1983). Phytochemical variation, colonization and insect communities: the case of bracken fern (Pteridium aquilinum). In: Variable Plants and Herbivores in Natural and Managed Systems (eds. Denno, R.F. McClure, M.S.). Academic Press, New York, pp. 513 558.
28. Jongsma, M.A. Bolter, C. (1997). The adaptation of insects to plant protease inhibitors. J. Insect Physiol., 43, 885 895.
29. Jongsma, M.A., Bakker, P.L., Peters, J., Bosch, D. Stiekema, W.J. (1995). Adaptation of Spodoptera exigua larvae to plant proteinase inhibitors by induction of gut proteinase activity insensitive to inhibition. Proc. Natl Acad. Sci. USA, 92, 8041 8045.
30. Kang, J.-H., Wang, L. Baldwin, I.T. (2006). Silencing threonine deaminase and JAR1 homologue in Nicotiana attenuata impairs JA-isoleucine-mediated defense against the specialist herbivore Manduca sexta. Plant Cell, 18, 3303 3320.
31. Keinänen, M., Oldham, N.J. Baldwin, I.T. (2001). Rapid HPLC screening of jasmonate-induced increases in tobacco alkaloids, phenolics, and diterpene glycosides in Nicotiana attenuata. J. Agric. Food Chem., 49, 3553 3558.
32. Kessler, D. Baldwin, I.T. (2007). Making sense of nectar scents: the effects nectar secondary metabolites on floral visitors of N. attenuata. Plant J., 49, 840 854.
33. Kim, J.H. Mullin, C.A. (2003). Antifeedant effects of protease inhibitors on feeding behaviors of adult western corn rootworm (Diabrotica virgifera virgifera). J. Chem. Ecol., 29, 795 810.
34. Krügel, T., Lim, M., Gase, K., Halitschke, R. Baldwin, I.T. (2002). Agrobacterium-mediated transformation of Nicotiana attenuta, a model ecological expression system. Chemoecology, 12, 177 183.
35. Lara, P., Ortego, F., Gonzalez-Hidalgo, E., Castanera, P., Carbonero, P. Diaz, I. (2000). Adaptation of Spodoptera exigua (Lepidoptera: Noctuidae) to barley trypsin inhibitor BTI-CMe expressed in transgenic tobacco. Transgenic Res., 9, 169 178.
36. Nelson, A.C. Kursar, T.A. (1999). Interactions among plant defense compounds: a method for analysis. Chemoecology, 9, 81 92.
37. Parr, J.C. Thurston, R. (1972). Toxicity of nicotine in synthetic diets to larvae of the tobacco hornworm. Ann. Entomol. Soc. Am., 65, 1158 1188.
38. Pohlon, E. Baldwin, I.T. (2001). Artificial diets 'capture' the dynamics of jasmonate-induced defenses in plants. Entomol. Exp. Appl., 100, 127 130.
39. Rayapuram, C. Baldwin, I.T. (2006). Using nutritional indices to study LOX3-dependent insect resistance. Plant Cell Environ., 29, 1585 1594.
40. Rhoades, D.F. Cates, R.G. (1976). Toward a general theory of plant antiherbivore chemistry. Recent Adv. Phytochem., 10, 168 213.
41. Schmidt, S. Baldwin, I.T. (2006). Systemin in black nightshade (Solanum nigrum): the tomato-homologous polypeptide does not mediate direct defense responses. Plant Physiol., 142, 1751 1758.
42. Simpson, S.J. Simpson, C.L. (1990). The mechanisms of nutritional compensation of phytophagous Insects. In: Insect-Plant Interactions (ed. Bernays, E.A.). CRC Press, Boca Raton, pp. 111 160.
43. Simpson, S.J., Raubenheimer, D. Chambers, P.G. (1995). The mechanisms of nutritional homeostasis. In: Regulatory Mechanisms in Insect Feeding (eds. Chapman, R.F. de Boer, G.). Chapman & Hall, New York, pp. 251 277.
44. Steppuhn, A., Gase, K., Krock, B., Halitschke, R. Baldwin, I.T. (2004). Nicotine's defensive function in nature. PLoS Biol., 2, 1074 1080.
45. Voelckel, C., Krügel, T., Gase, K., Heidrich, N., van Dam, N.M., Winz, R. et al. (2001). Anti-sense expression of putrescine N-methyltransferase confirms defensive role of nicotine in Nicotiana sylvestris against Manduca sexta. Chemoecology, 11, 121 126.
46. Waldbauer, G. (1968). The consumption and utilization of food by insects. Adv. Insect Physiol., 5, 229 288.
47. Waterman, P.G. Mole, S. (1989). Extrinsic factors influencing production of secondary metabolites in plants. In: Insect-Plant Interactions (ed. Bernays, E.A.). CRC Press, Boca Raton, FL, pp. 107 134.
48. Winterer, J. Bergelson, J. (2001). Diamondback moth compensatory consumption of protease inhibitor-transformed plants. Mol. Ecol., 10, 1069 1074.
49. Winz, R.A. Baldwin, I.T. (2001). Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. IV. Insect-induced ethylene reduces jasmonate-induced nicotine accumulation by regulating putrescine N-methyltransferase transcripts. Plant Physiol., 125, 2189 2202.
50. Zavala, J.A., Patankar, A.G. Baldwin, I.T. (2004a). Manipulation of endogenous trypsin proteinase inhibitor production in Nicotiana attenuata demonstrates their function as antiherbivore defenses. Plant Physiol., 134, 1181 1190.
51. Zavala, J.A., Patankar, A.G., Gase, K. Baldwin, I.T. (2004b). Constitutive and inducible trypsin proteinase inhibitor production incurs large fitness costs in Nicotiana attenuata. Proc. Natl Acad. Sci. USA, 101, 1607 1612.
52. Zhao, J.Z., Cao, J., Li, Y.X., Collins, H.L., Roush, R.T., Earle, E.D. et al. (2003). Transgenic plants expressing two Bacillus thuringiensis toxins delay insect resistance evolution. Nat. Biotechnol., 21, 1493 1497.
53. Zhu-Salzman, K., Ahn, J.E., Salzman, R.A., Koiwa, H., Shade, R.E. Balfe, S. (2003a). Fusion of a soybean cysteine protease inhibitor and a legume lectin enhances anti-insect activity synergistically. Agric. For. Entomol., 5, 317 323.
54. Zhu-Salzman, K., Koiwa, H., Salzman, R.A., Shade, R.E. Ahn, J.E. (2003b). Cowpea bruchid Callosobruchus maculatus uses a three-component strategy to overcome a plant defensive cysteine protease inhibitor. Insect Mol. Biol., 12, 135 145.