Advertisement

Journal of Chemical Ecology

, Volume 37, Issue 12, pp 1294–1303 | Cite as

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

  • Adam D. Steinbrenner
  • Sara Gómez
  • Sonia Osorio
  • Alisdair R. Fernie
  • Colin M. Orians
Article

Abstract

Induced changes in primary metabolism are important plant responses to herbivory, providing energy and metabolic precursors for defense compounds. Metabolic shifts also can lead to reallocation of leaf resources to storage tissues, thus increasing a plant’s tolerance. We characterized whole-plant metabolic responses of tomato (Solanum lycopersicum) 24 h after leaf herbivory by two caterpillars (the generalist Helicoverpa zea and the specialist Manduca sexta) by using GC-MS. We measured 56 primary metabolites across the leaves, stems, roots, and apex, comparing herbivore-attacked plants to undamaged plants and mechanically damaged plants. Induced metabolic change, in terms of magnitude and number of individual concentration changes, was stronger in the apex and root tissues than in undamaged leaflets of damaged leaves, indicating rapid and significant whole-plant responses to damage. Helicoverpa zea altered many more metabolites than M. sexta across most tissues, suggesting an enhanced plant response to H. zea herbivory. Helicoverpa zea herbivory strongly affected concentrations of defense-related metabolites (simple phenolics and precursor amino acids), while M. sexta altered metabolites associated with carbon and nitrogen transport. We conclude that herbivory induces many systemic primary metabolic changes in tomato, and that changes often are specific to a single tissue or type of herbivore. The potential implications of primary metabolic changes are discussed in relation to resistance and tolerance.

Key Words

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

Notes

Acknowledgements

We thank B. Trimmer (Tufts University) and G. Felton (Pennsylvania State University) for provision of M. sexta and H. zea caterpillars, respectively. We thank T. Korpita for help during sample preparation and D. Marshall and B. Tavernia for statistical advice. F. Chew, G. Ellmore, N. van Dam, and two anonymous reviewers provided valuable comments on a previous version of the manuscript. ADS was supported by The Neubauer Scholars Program, The Paula Frazier Poskitt Memorial Scholarship, and the Astronaut Scholarship. This research was supported by the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service under USDA/CSREES grant 2007-35302-18351 to CMO.

Supplementary material

10886_2011_42_Fig4_ESM.jpg (9 kb)
Fig. S1

Plot of top two principal components from overall PCA (all tissues included) of 51 common, non-saturated metabolites. Points indicate individual plant tissue samples. Tissue groupings pool both herbivore-treated and control treatments. Total number of measured metabolites was 47 for leaves, 43 for stems, 43 for apex, and 35 for roots (see Fig. 1 for further information). (JPEG 8 kb)

10886_2011_42_MOESM1_ESM.tiff (2.1 mb)
High resolution (TIFF 2109 kb)
10886_2011_42_Fig5_ESM.jpg (32 kb)
Fig S2

Plots of top 2 principal components from tissue-specific principal component analysis. Points represent means for each treatment (see Fig. 1 for number of plant replicates measured per treatment). Standard deviations are shown on both axes. Total number of measured metabolites was 47 for leaves, 43 for stems, 43 for apex, and 35 for roots (see Fig. 1 for further information). (JPEG 31 kb)

10886_2011_42_MOESM2_ESM.tiff (5 mb)
High resolution (TIFF 5146 kb)
10886_2011_42_Fig6_ESM.jpg (52 kb)
Fig. S3

Mean relative concentration values of metabolites relative to mechanically damaged control means (1.0). Statistically significant differences from undamaged plants (Student’s t-test, P < 0.05) are highlighted with a shaded box. Sample size (number of plants) is given above each tissue-treatment combination. See Fig. 1 for samples sizes for mechanically damaged plants. Treatment labels: “Ms”, Manduca sexta herbivory, “Hz”, Helicoverpa zea herbivory. Nitrogen-transporting amino acids, abundant cellular sugars, amino acid products of the shikimate pathway, and components of phenylpropanoid metabolism are underlined and highlighted in bold. (JPEG 51 kb)

10886_2011_42_MOESM3_ESM.tiff (3.4 mb)
High resolution (TIFF 3478 kb)

References

  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.Google Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  10. Bolton, M. D. 2009. Primary metabolism and plant defense—fuel for the fire. Mol. Plant Microbe Interact. 22:487–97.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  14. Dixon, R. A. and Paiva, N. L. 1995. Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  16. Gómez, S. and Stuefer, J. 2006. Members only: induced systemic resistance to herbivory in a clonal plant network. Oecologia 147:461–468.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  19. Hanik, N., Gómez, S., Best, M., Schueller, M., Orians, C. M., and Ferrieri, R. A. 2010. Partitioning of new carbon as 11C in Nicotiana tabacum reveals insight into methyl jasmonate induced changes in metabolism. J. Chem. Ecol. 36:1058–1067.PubMedCrossRefGoogle Scholar
  20. Herrmann, K. M. and Weaver, L. M. 1999. The shikimate pathway. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:473–503.PubMedCrossRefGoogle Scholar
  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.PubMedGoogle Scholar
  22. Howe, G. A. and Jander, G. 2008. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 59:41–66.PubMedCrossRefGoogle Scholar
  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.Google Scholar
  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.CrossRefGoogle Scholar
  25. Iwasa, Y. O. H. and Kubo, T. 1997. Optimal size of storage for recovery after unpredictable disturbances. Evol. Ecol. 11:41–65.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  28. Karban, R. and Baldwin, I. T. 1997. Induced Responses to Herbivory. University of Chicago Press.Google Scholar
  29. Kessler, A. and Baldwin, I. T. 2002. Plant responses to insect herbivory: The emerging molecular analysis. Annu. Rev. Plant Biol. 53:299–328.PubMedCrossRefGoogle Scholar
  30. Koo, A. J. K. and Howe, G. A. 2009. The wound hormone jasmonate. Phytochemistry 70:1571–1580.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  38. Orians, C., Thorn, A., and Gómez, S. 2011. Herbivore-induced resource sequestration in plants: why bother? Oecologia 167:1–9.PubMedCrossRefGoogle Scholar
  39. Pauwels, L., Inzé, D., and Goossens, A. 2009. Jasmonate-inducible gene: what does it mean? Trends Plant Sci. 14(2):87–91.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  41. Peiffer, M. and Felton, G. W. 2009. Do caterpillars secrete “oral secretions”? J. Chem. Ecol. 35:326–335.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  43. Roitsch, T. and González, M. C. 2004. Function and regulation of plant invertases: Sweet sensations. Trends Plant Sci. 9:606–613.PubMedCrossRefGoogle Scholar
  44. Rosenthal, G. A., and Berenbaum, M. R. 1992. Herbivores: Their Interactions with Secondary Plant Metabolites. Academic Press.Google Scholar
  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.CrossRefGoogle Scholar
  46. Schwachtje, J. and Baldwin, I. T. 2008. Why does herbivore attack reconfigure primary metabolism? Plant Physiol. 146:845–851.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  48. Smith, A. M. and Stitt, M. 2007. Coordination of carbon supply and plant growth. Plant, Cell Environ. 30:1126–1149.CrossRefGoogle Scholar
  49. Staswick, P. E. 1994. Storage proteins of vegetative plant tissues. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45:303–322.CrossRefGoogle Scholar
  50. Strauss, S. Y. 1991. Direct, indirect, and cumulative effects of three native herbivores on a shared host plant. Ecology 72:543–558.CrossRefGoogle Scholar
  51. Tiffin, P. 2000. Mechanisms of tolerance to herbivore damage:what do we know? Evol. Ecol. 14:523–536.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  55. Wink, M. and Theile, V. 2002. Alkaloid tolerance in Manduca sexta and phylogenetically related sphingids (Lepidoptera: Sphingidae). Chemoecology 12:29–46.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Adam D. Steinbrenner
    • 1
    • 2
  • Sara Gómez
    • 1
    • 3
  • Sonia Osorio
    • 4
  • Alisdair R. Fernie
    • 4
  • Colin M. Orians
    • 1
  1. 1.Department of BiologyTufts UniversityMedfordUSA
  2. 2.Department of Plant and Microbial BiologyUniversity of California BerkeleyBerkeleyUSA
  3. 3.Department of Biological SciencesUniversity of Rhode IslandKingstonUSA
  4. 4.Max-Planck-Institut für Molekulare PflanzenphysiologiePotsdam-GolmGermany

Personalised recommendations