Effects of Plant Vascular Architecture on Aboveground–Belowground-Induced Responses to Foliar and Root Herbivores on Nicotiana tabacum

Abstract

Herbivores induce systemic changes in plant traits, and the strength of these induced responses is often associated with the degree of vascular connectivity that links damaged and undamaged plant tissues. Although this phenomenon is known to occur aboveground in leaves, it is unknown whether or not leaf–root induction similarly follows the vascular architecture of plants. To test for this possibility, we manipulated foliar and root herbivory on tobacco (Nicotiana tabacum) by the leaf-chewing insect Spodoptera exigua and the root-galling nematode Meloidogyne incognita. Subsequent changes in secondary chemistry (alkaloids and phenolics) were measured in leaves and roots that were orthostichous (vertically aligned) and nonorthostichous (opposite) from the herbivore-damaged tissues. Aboveground caterpillar herbivory elicited stronger secondary chemical responses in orthostichous compared with nonorthostichous plant tissues, although the magnitude of this difference was greater in leaves than roots. However, belowground nematode herbivory did not affect the secondary chemistry of tobacco leaves, despite inducing strong local responses in roots. Thus, plant vascular architecture can mediate the magnitude of systemic induction in roots as well as in leaves, with stronger responses in tissues that are more closely aligned. As a result, herbivores that co-occur on the same sector of plant (both aboveground and belowground) may be more likely to affect one another via induced responses than herbivores that occur on plant tissues sharing fewer resources.