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 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.

A non‐vector herbivore indirectly increases the transmission of a vector‐borne virus by reducing plant chemical defences

“…As noted in the introduction, a previous study suggested that T. urticae infestation may reduce flavonoid levels in tomato plants (Schimmel et al, ). Here, we did not find that T. urticae reduced overall flavonoid levels in tomato.…”

“…Furthermore, JA enhanced flavonoid production probably via MYB transcription factors in which MYC2 was shown to have a positive role (Dombrecht et al, ). However, T. urticae feeding resulted in the upregulation of the multiple MYC repressor JASMONATE ZIM DOMAIN (JAZ)‐encoding genes in tomato (Schimmel et al, ), which suggested repression of the flavonoid biosynthetic pathway by T. urticae . Moreover, recent studies indicated that T. urticae infestation upregulated the expression of genes encoding 4‐coumarate‐CoA ligase (Schimmel et al, ; Zhang, Bouwmeester, & Kappers, ), and this enzyme is involved in the final step of the phenylpropanoid pathway to precede SA biosynthesis (Chen, Zheng, Huang, Lai, & Fan, ).…”

“…However, T. urticae feeding resulted in the upregulation of the multiple MYC repressor JASMONATE ZIM DOMAIN (JAZ)‐encoding genes in tomato (Schimmel et al, ), which suggested repression of the flavonoid biosynthetic pathway by T. urticae . Moreover, recent studies indicated that T. urticae infestation upregulated the expression of genes encoding 4‐coumarate‐CoA ligase (Schimmel et al, ; Zhang, Bouwmeester, & Kappers, ), and this enzyme is involved in the final step of the phenylpropanoid pathway to precede SA biosynthesis (Chen, Zheng, Huang, Lai, & Fan, ). Thus, we also hypothesize that the flavonoid biosynthesis is restricted or reduced upon T. urticae herbivory because the production of SA induced by T. urticae diverts a substantial part of the precursors available to SA biosynthesis.…”

“…Su et al, ). Fourth, another recent study found that several genes encoding positive regulators of flavonoids were downregulated in tomato leaves infested with T. urticae , suggesting that the production of flavonoids may be decreased in T. urticae ‐infested tomato plants (Schimmel et al, ).…”

Tetranychusevansi spider mite populations suppress tomato defenses to varying degrees

“…T. evansi suppress tomato defense downstream of plant hormone accumulation, such that the plant's expression of defense‐associated genes is downregulated to the benefit of the herbivore (Alba et al, 2015; Ataide et al, 2016; Sarmento, Lemos, Bleeker, et al, 2011). In the course of the infestation, such suppression can temporarily result in expression levels of defense genes at or below the plant's housekeeping levels (Sarmento, Lemos, Bleeker, et al, 2011) but for most of the time in an intermediate level of induction (Alba et al, 2015; Schimmel et al, 2018). This suppression is mediated by secreted salivary effector proteins (Jonckheere et al, 2016; Villarroel et al, 2016) that restrain the defense response to levels of induction low enough for the mite to tolerate (Ataide et al, 2016), independent of herbivore‐associated bacteria (Staudacher et al, 2017).…”