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

Carla C. M. Arce, Ricardo A. R. Machado, Natália S. Ribas, Paulo F. Cristaldo, Lívia M. S. Ataíde, Ângelo Pallini, Flávia M. Carmo, Leandro G. Freitas, Eraldo Lima

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.