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

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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.

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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.

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Authors and Affiliations

  1. Department of Biology, Tufts University, Dana Hall, Medford, MA, 02155, USA

    Adam D. Steinbrenner, Sara Gómez & Colin M. Orians

  2. Department of Plant and Microbial Biology, University of California Berkeley, Koshland Hall, Berkeley, CA, 94709, USA

    Adam D. Steinbrenner

  3. Department of Biological Sciences, University of Rhode Island, Kingston, RI, 02881, USA

    Sara Gómez

  4. Max-Planck-Institut für Molekulare Pflanzenphysiologie, 14476, Potsdam-Golm, Germany

    Sonia Osorio & Alisdair R. Fernie

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  1. Adam D. Steinbrenner
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Correspondence to Adam D. Steinbrenner.

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Adam D. Steinbrenner and Sara Gómez contributed equally to this work.

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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)

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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)

High resolution (TIFF 5146 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)

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Steinbrenner, A.D., Gómez, S., Osorio, S. et al. Herbivore-Induced Changes in Tomato (Solanum lycopersicum) Primary Metabolism: A Whole Plant Perspective. J Chem Ecol 37, 1294–1303 (2011). https://doi.org/10.1007/s10886-011-0042-1

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