Herbivore-Induced Changes in Tomato (Solanum lycopersicum) Primary Metabolism: A Whole Plant Perspective

Journal of Chemical Ecology

Volumn 37, Issue 12, 2011, Pages 1294-1303

  Steinbrenner, Adam D ^a,b   Gómez, Sara ^a,c   Osorio, Sonia ^d   Fernie, Alisdair R ^d   Orians, Colin M ^a  

^a TUFTS UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF RHODE ISLAND   (United States)

^d MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

Helicoverpa zea; Herbivory; Induced sequestration; Manduca sexta; Metabolomics; Resistance; Systemic responses; Tolerance

Indexed keywords

AMINO ACID; CONCENTRATION (COMPOSITION); ENERGY EFFICIENCY; FRUIT; HERBIVORY; METABOLISM; METABOLITE; PHYSIOLOGICAL RESPONSE; PLANT-HERBIVORE INTERACTION; TOLERANCE;

ANALYSIS OF VARIANCE; ANIMAL; ANTIBODY SPECIFICITY; ARTICLE; EVALUATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HERBIVORY; LARVA; MANDUCA; MASS FRAGMENTOGRAPHY; METABOLISM; METABOLOME; METHODOLOGY; MOTH; PHYSIOLOGY; PLANT LEAF; PLANT ROOT; PLANT STEM; SPECIES DIFFERENCE; TOMATO;

ANALYSIS OF VARIANCE; ANIMALS; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GENE EXPRESSION REGULATION, PLANT; HERBIVORY; LARVA; LYCOPERSICON ESCULENTUM; MANDUCA; METABOLOME; MOTHS; ORGAN SPECIFICITY; PLANT LEAVES; PLANT ROOTS; PLANT STEMS; SPECIES SPECIFICITY;

HELICOVERPA ZEA; LYCOPERSICON ESCULENTUM; MANDUCA SEXTA; SOLANUM;

EID: 84155194911     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-011-0042-1     Document Type: Article

References (59)

1. Agrawal, A. A. 2000. Specificity of induced resistance in wild radish: Causes and consequences for two specialist and two generalist caterpillars. Oikos 89: 493-500.
2. Arimura, G. I., Kopke, S., Kunert, M., Volpe, V., David, A., Brand, P., Dabrowska, P., Maffei, M. E., and Boland, W. 2008. Effects of feeding Spodoptera littoralis on lima bean leaves: IV. Diurnal and nocturnal damage differentially initiate plant volatile emission. Plant Physiol. 146: 965-973.
3. Arnold, T. M. and Schultz, J. C. 2002. Induced sink strength as a prerequisite for induced tannin biosynthesis in developing leaves of Populus. Oecologia 130: 585-593.
4. Babst, B. A., Ferrieri, R. A., Gray, D. W., Lerdau, M., Schlyer, D. J., Schueller, M., Thorpe, M. R., and Orians, C. M. 2005. Jasmonic acid induces rapid changes in carbon transport and partitioning in Populus. New Phytol. 167: 63-72.
5. Babst, B. A., Ferrieri, R. A., Thorpe, M. R., and Orians, C. M. 2008. Lymantria dispar herbivory induces rapid changes in carbon transport and partitioning in Populus nigra. Entomol. Exp. Appl. 128: 117-125.
6. Ballhorn, D. J., Kautz, S., and Lieberei, R. 2010. Comparing responses of generalist and specialist herbivores to various cyanogenic plant features. Entomol. Exp. Appl. 134: 245-259.
7. Beardmore, T., Wetzel, S., and Kalous, M. 2000. Interactions of airborne methyl jasmonate with vegetative storage protein gene and protein accumulation and biomass partitioning in Populus plants. Can. J. Forest Res. 30: 1106-1113.
8. Bhonwong, A., Stout, M., Attajarusit, J., and Tantasawat, P. 2009. Defensive role of tomato polyphenol oxidases against cotton bollworm (Helicoverpa armigera) and Beet Armyworm (Spodoptera exigua). J. Chem. Ecol. 35: 28-38.
9. Bi, J. L., Felton, G. W., Murphy, J. B., Howles, P. A., Dixon, R. A., and Lamb, C. J. 1997. Do plant phenolics confer resistance to specialist and generalist insect herbivores? J. Agric. Food Chem. 45: 4500-4504.
10. Bolton, M. D. 2009. Primary metabolism and plant defense-fuel for the fire. Mol. Plant Microbe Interact. 22: 487-97.
11. Chung, S. and Felton, G. 2011. Specificity of induced resistance in tomato gainst specialist lepidopteran and coleopteran Species. J. Chem. Ecol. 37: 378-386.
12. De Jong, T. J. and van der Meijden, E. 2000. On the correlation between allocation to defence and regrowth in plants. Oikos 88: 503-508.
13. Diezel, C., von Dahl, C. C., Gaquerel, E., and Baldwin, I. T. 2009. Different lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling. Plant Physiol. 150: 1576-1586.
14. Dixon, R. A. and Paiva, N. L. 1995. Stress-induced phenylpropanoid metabolism. Plant Cell 7: 1085-1097.
15. Erban, A., Schauer, N., Fernie, A. R., and Kopka, J. 2007. Nonsupervised construction and application of mass spectral and retention time index libraries from time-of-flight gas chromatography-mass spectrometry metabolite profiles. Meth. Mol. Biol. 358: 19-38.
16. Gómez, S. and Stuefer, J. 2006. Members only: induced systemic resistance to herbivory in a clonal plant network. Oecologia 147: 461-468.
17. Gómez, S., Ferrieri, R. A., Schueller, M., and Orians, C. M. 2010. Methyl jasmonate elicits rapid changes in carbon and nitrogen dynamics in tomato. New Phytol. 188: 835-834.
18. Halitschke, R., Schittko, U., Pohnert, G., Boland, W., and 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.
19. 11C in Nicotiana tabacum reveals insight into methyl jasmonate induced changes in metabolism. J. Chem. Ecol. 36: 1058-1067.
20. Herrmann, K. M. and Weaver, L. M. 1999. The shikimate pathway. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 473-503.
21. Hofmann, J., El Ashry, A. N., Anwar, S., Erban, A., Kopka, J., and Grundler, F. 2010. Metabolic profiling reveals local and systemic responses of host plants to nematode parasitism. Plant J 62: 1058-1071.
22. Howe, G. A. and Jander, G. 2008. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 59: 41-66.
23. Hummel, J., Selbig, J., Walther, D., and Kopka, J. 2007. The Golm Metabolome Database: a database for GC-MS based metabolite profiling, pp 75-95, in Nielsen J and Jewett M (eds.), Metabolomics: Springer Berlin/Heidelberg.
24. Isman, M. B. and Duffey, S. S. 1982. Toxicity of tomato phenolic compounds to the fruitworm, Heliothis zea. Entomol. Exp. Appl. 31: 370-376.
25. Iwasa, Y. O. H. and Kubo, T. 1997. Optimal size of storage for recovery after unpredictable disturbances. Evol. Ecol. 11: 41-65.
26. Kahl, J., Siemens, D. H., Aerts, R. J., Gäbler, R., Kühnemann, F., Preston, C. A., and Baldwin, I. T. 2000. Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore. Planta 210: 336-342.
27. Kaplan, F., Kopka, J., Haskell, D. W., Zhao, W., Schiller, K. C., Gatzke, N., Sung, D. Y., and Guy, C. L. 2004. Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol. 136: 4159-4168.
28. Karban, R. and Baldwin, I. T. 1997. Induced Responses to Herbivory. University of Chicago Press.
29. Kessler, A. and Baldwin, I. T. 2002. Plant responses to insect herbivory: The emerging molecular analysis. Annu. Rev. Plant Biol. 53: 299-328.
30. Koo, A. J. K. and Howe, G. A. 2009. The wound hormone jasmonate. Phytochemistry 70: 1571-1580.
31. Last, R. L., Jones, A. D., and Shachar-Hill, Y. 2007. Towards the plant metabolome and beyond. Nat. Rev. Mol. Cell Biol. 8: 167-174.
32. Lisec, J., Schauer, N., Kopka, J., Willmitzer, L., and Fernie, A. R. 2006. Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat. Protocols 1: 387-396.
33. Luedemann, A., Strassburg, K., Erban, A., and Kopka, J. 2008. TagFinder for the quantitative analysis of gas chromatography-mass spectrometry (GC-MS)-based metabolite profiling experiments. Bioinformatics 24: 732-737.
34. Morris, C. E. 1984. Electrophysiological effects of cholinergic agents on the CNS of a nicotine-resistant insect, the tobacco hornworm (Manduca sexta). J. Exp. Zool. 229: 361-374.
35. Musser, R. O., Hum-Musser, S. M., Eichenseer, H., Peiffer, M., Ervin, G., Murphy, J. B., and Felton, G. W. 2002. Caterpillar saliva beats plant defences. Nature 416: 599-600.
36. Orians, C. M., Pomerleau, J., and Ricco, R. 2000. Vascular architecture generates fine scale variation in systemic induction of proteinase inhibitors in tomato. J. Chem. Ecol. 26: 471-485.
37. Orians, C. M., Ardón, M., and Mohammad, B. A. 2002. Vascular architecture and patchy nutrient availability generate within-plant heterogeneity in plant traits important to herbivores. Am. J. Bot. 89: 270-278.
38. Orians, C., Thorn, A., and Gómez, S. 2011. Herbivore-induced resource sequestration in plants: why bother? Oecologia 167: 1-9.
39. Pauwels, L., Inzé, D., and Goossens, A. 2009. Jasmonate-inducible gene: what does it mean? Trends Plant Sci. 14(2): 87-91.
40. Peiffer, M. and Felton, G. W. 2005. The host plant as a factor in the synthesis and secretion of salivary glucose oxidase in larval Helicoverpa zea. Arch. Insect Biochem. Physiol. 58: 106-113.
41. Peiffer, M. and Felton, G. W. 2009. Do caterpillars secrete "oral secretions"? J. Chem. Ecol. 35: 326-335.
42. Rodriguez-Saona, C., Musser, R., Vogel, H., Hum-Musser, S., and Thaler, J. 2010. Molecular, biochemical, and organismal analyses of tomato plants simultaneously attacked by herbivores from two feeding guilds. J. Chem. Ecol. 36: 1043-1057.
43. Roitsch, T. and González, M. C. 2004. Function and regulation of plant invertases: Sweet sensations. Trends Plant Sci. 9: 606-613.
44. Rosenthal, G. A., and Berenbaum, M. R. 1992. Herbivores: Their Interactions with Secondary Plant Metabolites. Academic Press.
45. Schmidt, L., Schurr, U., and Röse, U. S. R. 2009. Local and systemic effects of two herbivores with different feeding mechanisms on primary metabolism of cotton leaves. Plant, Cell Environ. 32: 893-903.
46. Schwachtje, J. and Baldwin, I. T. 2008. Why does herbivore attack reconfigure primary metabolism? Plant Physiol. 146: 845-851.
47. Schwachtje, J., Minchin, P. E. H., Jahnke, S., van Dongen, J. T., Schittko, U., and Baldwin, I. T. 2006. SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proc. Natl. Acad. Sci. USA 103: 12935-12940.
48. Smith, A. M. and Stitt, M. 2007. Coordination of carbon supply and plant growth. Plant, Cell Environ. 30: 1126-1149.
49. Staswick, P. E. 1994. Storage proteins of vegetative plant tissues. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45: 303-322.
50. Strauss, S. Y. 1991. Direct, indirect, and cumulative effects of three native herbivores on a shared host plant. Ecology 72: 543-558.
51. Tiffin, P. 2000. Mechanisms of tolerance to herbivore damage: what do we know? Evol. Ecol. 14: 523-536.
52. van Dam, N. M. and Oomen, M. W. A. T. 2008. Root and shoot jasmonic acid applications differentially affect leaf chemistry and herbivore growth. Plant Signal. Behav. 3: 91-98.
53. Vos, M., Berrocal, S. M., Karamaouna, F., Hemerik, L., and Vet, L. E. M. 2001. Plant-mediated indirect effects and the persistence of parasitoid-herbivore communities. Ecol. Lett. 4: 38-45.
54. Wasternack, C., Stenzel, I., Hause, B., Hause, G., Kutter, C., Maucher, H., Neumerkel, J., Feussner, I., and Miersch, O. 2006. The wound response in tomato-Role of jasmonic acid. J. Plant Physiol. 163: 297-306.
55. Wink, M. and Theile, V. 2002. Alkaloid tolerance in Manduca sexta and phylogenetically related sphingids (Lepidoptera: Sphingidae). Chemoecology 12: 29-46.
56. Winz, R. A. and 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.
57. Zangerl, A. R. and Berenbaum, M. R. 1998. Damage-inducibility of primary and secondary metabolites in the wild parsnip (Pastinaca sativa). Chemoecology 8: 187-193.
58. Zarate, S. I., Kempema, L. A., and Walling, L. L. 2007. Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol. 143: 866-875.
59. Zhao, J., Davis, L. C., and Verpoorte, R. 2005. Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol. Adv. 23: 283-333.