From induction to suppression: How to manipulate plant defenses

Plants have evolved traits, including induced defenses, to resist herbivores. However, some plant-eating spider mites (Tetranychus spp.) have adapted to plant defenses to maintain a high reproductive performance. From natural populations of two species of mites, T. urticae and T. evansi, three lines were selected and demonstrated to suppress induced defenses of tomato plants downstream from the accumulation of the defense-regulating hormones jasmonate (JA) and salicylate (SA), and independently of JA-SA crosstalk. When sharing a leaflet, the suppression by T. evansi is powerful enough to co-suppress the JA and SA responses induced by T. urticae mites that cannot suppress defenses (‘inducers’), thereby improving the reproductive performance of the latter. A subsequent analysis of the spatiotemporal dynamics of induction and suppression at the within leaflet scale revealed that these are predominantly local events. Furthermore, T. evansi was found to hyper-suppress defenses in response to the nearby presence of T. urticae competitors and this coincided with an increased reproductive performance of T. evansi, but not T. urticae. Hence, inducer mites do not always - or immediately - benefit from co-occurring suppressors. Zooming in further, inducer and suppressor T. urticae were shown to harbor different bacterial endosymbionts and removal of these bacteria with antibiotics affected mite performance, mite gene expression, mite feeding intensity, and tomato responses to mite feeding. Finally, genome-wide transcriptomic responses of tomato plants to feeding by suppressor and inducer mites were analyzed to identify T. evansi-responsive tomato promoters to use these to engineer an inducible resistance to suppressor mites.