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Nematode Root Herbivory in Tomato Increases Leaf Defenses and Reduces Leaf Miner Oviposition and Performance

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Abstract

The outcome of plant-mediated interactions among herbivores from several feeding guilds has been studied intensively. However, our understanding on the effects of nematode root herbivory on leaf miner oviposition behavior and performance remain limited. In this study, we evaluated whether Meloidogyne incognita root herbivory affects Tuta absoluta oviposition preference on Solanum lycopersicum plants and the development of the resulting offspring. To investigate the M. incognita-herbivory induced plant systemic responses that might explain the observed biological effects, we measured photosynthetic rates, leaf trypsin protease inhibitor activities, and analyzed the profile of volatiles emitted by the leaves of root-infested and non-infested plants. We found that T. absoluta females avoided laying eggs on the leaves of root-infested plants, and that root infestation negatively affected the pupation process of T. absoluta. These effects were accompanied by a strong suppression of leaf volatile emissions, a decrease in photosynthetic rates, and an increase in the activity of leaf trypsin protease inhibitors. Our study reveals that root attack by nematodes can shape leaf physiology, and thereby increases plant resistance.

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Acknowledgements

We thank Jay Rosenheim, Ash Zemenick, Michael Culshaw-Maurer, Madelaine Venzon, Jeremy McNeil, Matthias Erb and Arne Janssen for critically reading the manuscript; and to FAPEMIG, CAPES, CNPq, and INCT–Semiochemicals on Agriculture for financial support. We also thank Felipe Lemos for helping with the GC measurments. CA was supported by FAPEMIG and CAPES (BPD-00065-14) and AP by FAPEMIG and CNPq.

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Authors and Affiliations

  1. Department of Entomology, Universidade Federal de Viçosa, Viçosa, Brazil

    Carla C. M. Arce, Natália S. Ribas, Paulo F. Cristaldo, Lívia M. S. Ataíde, Ângelo Pallini & Eraldo Lima

  2. Institute of Plant Sciences, University of Bern, Bern, Switzerland

    Carla C. M. Arce & Ricardo A. R. Machado

  3. Departament of Ecology, Universidade Federal do Sergipe, Aracaju, Brazil

    Paulo F. Cristaldo

  4. Institute of Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands

    Lívia M. S. Ataíde

  5. Department of Biology, Universidade Federal de Viçosa, Viçosa, Brazil

    Flávia M. Carmo

  6. Department of Phytopathology, Universidade Federal de Viçosa, Viçosa, Brazil

    Leandro G. Freitas

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  1. Carla C. M. Arce
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  2. Ricardo A. R. Machado
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  3. Natália S. Ribas
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  4. Paulo F. Cristaldo
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  6. Ângelo Pallini
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Correspondence to Carla C. M. Arce or Eraldo Lima.

Electronic supplementary material

Online Resource Fig. 1

Control and Meloidogyne incognita-infested tomato plants 20 d after nematode egg inoculation (PDF 484 kb)

Online Resource Fig. 2

Experimental set up for aboveground volatile collection (PDF 46 kb)

Online Resource Fig. 3

Total Ion chromatograms (TICs) from blank (empty glass chamber), control tomato plants and root-infested plants. Arrows highlight volatile compounds that statistically differed between treatments (1: α-pinene; 2: α-terpinene; 3: β-phellandrene; 4: β-caryophyllene; 5: α-humulene; 6: Unknown 1; 7: Unknown 2; 8: Unknown 3; and Internal Standard: N-heptyl-acetate). (PDF 234 kb)

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Arce, C.C.M., Machado, R.A.R., Ribas, N.S. et al. Nematode Root Herbivory in Tomato Increases Leaf Defenses and Reduces Leaf Miner Oviposition and Performance. J Chem Ecol 43, 120–128 (2017). https://doi.org/10.1007/s10886-016-0810-z

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