Abstract
Tomato plants are attacked by diverse herbivorous arthropods, including by cell-content-feeding mites, such as the extreme generalist Tetranychus urticae and specialists like Tetranychus evansi and Aculops lycopersici. Mite feeding induces plant defense responses that reduce mite performance. However, T. evansi and A. lycopersici suppress plant defenses via poorly understood mechanisms and, consequently, maintain a high performance on tomato. On a shared host, T. urticae 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 (T. urticae, T. evansi, A. lycopersici) or two species simultaneously (T. urticae plus T. evansi or T. urticae plus A. lycopersici). 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 T. urticae or A. lycopersici, respectively, only 0.1% was altered in T. evansi-infested plants. Transcriptome analysis of dual-infested leaves revealed that A. lycopersici primarily suppressed T. urticae-induced JA defenses, while T. evansi dampened T. urticae-triggered host responses on a transcriptome-wide scale. The latter suggests that T. evansi 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.
Highlights
Plants are usually attacked by multiple microbial and arthropod species, who attempt to consume them
Our results indicate that both specialist mites likely manipulate their host beyond the suppression of its defenses, as T. urticae-triggered tomato responses were dampened on a transcriptome-wide scale by T. evansi in dual-infested plants, and genes involved in cell cycle control and metabolite transport were up-regulated in leaves infested with A. lycopersici
We show that single infestations with specialist, defense-suppressing A. lycopersici or T. evansi both triggered the increased accumulation of jasmonic acid (JA)-Ile and SA, yet yielded very different transcriptomic changes in tomato leaves
Summary
Plants are usually attacked by multiple microbial and arthropod species, who attempt to consume them. The JA and SA signaling pathways interact, i.e., “crosstalk”, with each other as well as with signaling pathways of hormones that primarily regulate plant growth and development, presumably to fine-tune defense responses and to minimize growth-defense tradeoffs [5,6,7]. Both herbivores and pathogens have evolved various traits that enable them to overcome plant defenses [8], for instance by suppressing them through exploitation of the host’s hormonal crosstalk mechanisms or through sabotage of the host’s molecular machinery [9,10]
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