Distinct Signatures of Host Defense Suppression by Plant-Feeding Mites

Abstract

Tomato plants are attacked by diverse herbivorous arthropods, including by cell-content-feeding mites, such as the extreme generalist <i>Tetranychus urticae</i> and specialists like <i>Tetranychus evansi</i> and <i>Aculops lycopersici</i>. Mite feeding induces plant defense responses that reduce mite performance. However, <i>T. evansi</i> and <i>A. lycopersici</i> suppress plant defenses via poorly understood mechanisms and, consequently, maintain a high performance on tomato. On a shared host, <i>T. urticae</i> can be facilitated by either of the specialist mites, likely due to the suppression of plant defenses. To better understand defense suppression and indirect plant-mediated interactions between herbivorous mites, we used gene-expression microarrays to analyze the transcriptomic changes in tomato after attack by either a single mite species (<i>T. urticae</i>, <i>T. evansi</i>, <i>A. lycopersici</i>) or two species simultaneously (<i>T. urticae</i> plus <i>T. evansi</i> or <i>T. urticae</i> plus <i>A. lycopersici</i>). Additionally, we assessed mite-induced changes in defense-associated phytohormones using LC-MS/MS. Compared to non-infested controls, jasmonates (JAs) and salicylate (SA) accumulated to higher amounts upon all mite-infestation treatments, but the response was attenuated after single infestations with defense-suppressors. Strikingly, whereas 8 to 10% of tomato genes were differentially expressed upon single infestations with <i>T. urticae</i> or <i>A. lycopersici</i>, respectively, only 0.1% was altered in <i>T. evansi</i>-infested plants. Transcriptome analysis of dual-infested leaves revealed that <i>A. lycopersici</i> primarily suppressed <i>T. urticae</i>-induced JA defenses, while <i>T. evansi</i> dampened <i>T. urticae</i>-triggered host responses on a transcriptome-wide scale. The latter suggests that <i>T. evansi</i> not solely down-regulates plant gene expression, but rather directs it back towards housekeeping levels. Our results provide valuable new insights into the mechanisms underlying host defense suppression and the plant-mediated facilitation of competing herbivores.