Journal of Chemical Ecology

, Volume 36, Issue 10, pp 1043–1057

Molecular, Biochemical, and Organismal Analyses of Tomato Plants Simultaneously Attacked by Herbivores from Two Feeding Guilds

  • Cesar R. Rodriguez-Saona
  • Richard O. Musser
  • Heiko Vogel
  • Sue M. Hum-Musser
  • Jennifer S. Thaler
Article

DOI: 10.1007/s10886-010-9854-7

Cite this article as:
Rodriguez-Saona, C.R., Musser, R.O., Vogel, H. et al. J Chem Ecol (2010) 36: 1043. doi:10.1007/s10886-010-9854-7

Abstract

Previous work identified aphids and caterpillars as having distinct effects on plant responses to herbivory. We sought to decipher these interactions across different levels of biological organization, i.e., molecular, biochemical, and organismal, with tomato plants either damaged by one 3rd-instar beet armyworm caterpillar (Spodoptera exigua), damaged by 40 adult potato aphids (Macrosiphum euphorbiae), simultaneous damaged by both herbivores, or left undamaged (controls). After placing insects on plants, plants were transferred to a growth chamber for 5 d to induce a systemic response. Subsequently, individual leaflets from non-damaged parts of plants were excised and used for gene expression analysis (microarrays and quantitative real-time PCR), C/N analysis, total protein analysis, proteinase inhibitor (PI) analysis, and for performance assays. At the molecular level, caterpillars up-regulated 56 and down-regulated 29 genes systemically, while aphids up-regulated 93 and down-regulated 146 genes, compared to controls. Although aphids induced more genes than caterpillars, the magnitude of caterpillar-induced gene accumulation, particularly for those associated with plant defenses, was often greater. In dual-damaged plants, aphids suppressed 27% of the genes regulated by caterpillars, while caterpillars suppressed 66% of the genes regulated by aphids. At the biochemical level, caterpillars induced three-fold higher PI activity compared to controls, while aphids had no effects on PIs either alone or when paired with caterpillars. Aphid feeding alone reduced the foliar C/N ratio, but not when caterpillars also fed on the plants. Aphid and caterpillar feeding alone had no effect on the amount of protein in systemic leaves; however, both herbivores feeding on the plant reduced the amount of protein compared to aphid-damaged plants. At the organismal level, S. exigua neonate performance was negatively affected by prior caterpillar feeding, regardless of whether aphids were present or absent. This study highlights areas of concordance and disjunction between molecular, biochemical, and organismal measures of induced plant resistance when plants are attacked by multiple herbivores. In general, our data produced consistent results when considering each herbivore separately but not when considering them together.

Key Words

Inducible responses Herbivore performance C/N Proteinase inhibitors Microarrays qRT-PCR Decoy hypothesis Jasmonic acid Salicylic acid Pathogen defense 

Supplementary material

10886_2010_9854_MOESM1_ESM.xls (112 kb)
Supplemental Material Table S1shows mean expression for all treatments and probabilities for one-way ANOVA and t-test comparison for each treatment. This list includes only those genes where herbivory significantly up- or down-regulated gene expression (P ≤ 0.05) and changed gene expression by at least 2-fold compared to controls. Treatments are A=non-wounded control (NW); B=aphid feeding (aphid), C=caterpillar feeding (caterpillar), and D=caterpillar and aphid feeding (caterpillar and aphid). (XLS 112 kb)

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Cesar R. Rodriguez-Saona
    • 1
  • Richard O. Musser
    • 2
  • Heiko Vogel
    • 3
  • Sue M. Hum-Musser
    • 2
  • Jennifer S. Thaler
    • 4
  1. 1.Department of Entomology, Philip E. Marucci Center for Blueberry and Cranberry Research & ExtensionRutgers UniversityChatsworthUSA
  2. 2.Department of Biological SciencesWestern Illinois UniversityMacombUSA
  3. 3.Department of EntomologyMax Planck Institute for Chemical EcologyJenaGermany
  4. 4.Departments of Entomology and Ecology & Evolutionary BiologyCornell UniversityIthacaUSA

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