Distinct Signatures of Host Defense Suppression by Plant-Feeding Mites

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</p

Variation in life history traits and transcriptome associated with adaptation to diet shifts in the ladybird Cryptolaemus montrouzieri

Background: Despite the broad diet range of many predatory ladybirds, the mechanisms involved in their adaptation to diet shifts are not completely understood. Here, we explored how a primarily coccidophagous ladybird Cryptolaemus montrouzieri adapts to feeding on aphids. Results: Based on the lower survival rate, longer developmental time, and lower adult body weight and reproduction rate of the predator, the aphid Megoura japonica proved being less suitable to support C. montrouzieri as compared with the citrus mealybug Planococcus citri. The results indicated up-regulation of genes related to ribosome and translation in fourth instars, which may be related to their suboptimal development. Also, several genes related to biochemical transport and metabolism, and detoxification were up-regulated as a result of adaptation to the changes in nutritional and non-nutritional (toxic) components of the prey. Conclusion: Our results indicated that C. montrouzieri succeeded in feeding on aphids by regulation of genes related to development, digestion and detoxification. Thus, we argue that these candidate genes are valuable for further studies of the functional evolution of ladybirds led by diet shifts

Cross-talk between high light stress and plant defence to the two-spotted spider mite in Arabidopsis thaliana

Little is known about how plants deal with arthropod herbivores under the fluctuating light intensity and spectra which occur in natural environments. Moreover, the role of simultaneous stress such as excess light (EL) in the regulation of plant responses to herbivores is poorly characterized. In the current study, we focused on a mite-herbivore, specifically, the two-spotted spider mite (TSSM), which is one of the major agricultural pests worldwide. Our results showed that TSSM-induced leaf damage (visualized by trypan blue staining) and oviposition rate (measured as daily female fecundity) decreased after EL pre-treatment in wild-type Arabidopsis plants, but the observed responses were not wavelength specific. Thus, we established that EL pre-treatment reduced Arabidopsis susceptibility to TSSM infestation. Due to the fact that a portion of EL energy is dissipated by plants as heat in the mechanism known as non-photochemical quenching (NPQ) of chlorophyll fluorescence, we tested an Arabidopsis npq4-1 mutant impaired in NPQ. We showed that npq4-1 plants are significantly less susceptible to TSSM feeding activity, and this result was not dependent on light pre-treatment. Therefore, our findings strongly support the role of light in plant defence against TSSM, pointing to a key role for a photo-protective mechanism such as NPQ in this regulation. We hypothesize that plants impaired in NPQ are constantly primed to mite attack, as this seems to be a universal evolutionarily conserved mechanism for herbivores

The gut bacterial community affects immunity but not metabolism in a specialist herbivorous butterfly

1. Plant tissues often lack essential nutritive elements and may contain a range of secondary toxic compounds. As nutritional imbalance in food intake may affect the performances of herbivores, the latter have evolved a variety of physiological mechanisms to cope with the challenges of digesting their plant-based diet. Some of these strategies involve living in association with symbiotic microbes that promote the digestion and detoxification of plant compounds or supply their host with essential nutrients missing from the plant diet. In Lepidoptera, a growing body of evidence has, however, recently challenged the idea that herbivores are nutritionally dependent on their gut microbial community. It is suggested that many of the herbivorous Lepidopteran species may not host a resident microbial community, but rather a transient one, acquired from their environment and diet. Studies directly testing these hypotheses are however scarce and come from an even more limited number of species. 2. By coupling comparative metabarcoding, immune gene expression, and metabolomics analyses with experimental manipulation of the gut microbial community of prediapause larvae of the Glanville fritillary butterfly (Melitaea cinxia, L.), we tested whether the gut microbial community supports early larval growth and survival, or modulates metabolism or immunity during early stages of development. 3. We successfully altered this microbiota through antibiotic treatments and consecutively restored it through fecal transplants from conspecifics. Our study suggests that although the microbiota is involved in the up-regulation of an antimicrobial peptide, it did not affect the life history traits or the metabolism of early instars larvae. 4. This study confirms the poor impact of the microbiota on diverse life history traits of yet another Lepidoptera species. However, it also suggests that potential eco-evolutionary host-symbiont strategies that take place in the gut of herbivorous butterfly hosts might have been disregarded, particularly how the microbiota may affect the host immune system homeostasis.Peer reviewe

Reciprocal responses in the interaction between Arabidopsis and the cell-content feeding chelicerate herbivore spider mite

Most molecular-genetic studies of plant defense responses to arthropod herbivores have focused on insects. However, plant-feeding mites are also pests of diverse plants, and mites induce different patterns of damage to plant tissues than do well-studied insects (e.g. lepidopteran larvae or aphids). The two-spotted spidermite (Tetranychus urticae) is among the most significant mite pests in agriculture, feeding on a staggering number of plant hosts. To understand the interactions between spider mite and a plant at the molecular level, we examined reciprocal genome-wide responses of mites and its host Arabidopsis (Arabidopsis thaliana). Despite differences in feeding guilds, we found that transcriptional responses of Arabidopsis to mite herbivory resembled those observed for lepidopteran herbivores. Mutant analysis of induced plant defense pathways showed functionally that only a subset of induced programs, including jasmonic acid signaling and biosynthesis of indole glucosinolates, are central to Arabidopsis's defense to mite herbivory. On the herbivore side, indole glucosinolates dramatically increased mite mortality and development times. We identified an indole glucosinolate dose-dependent increase in the number of differentially expressedmite genes belonging to pathways associated with detoxification of xenobiotics. This demonstrates that spider mite is sensitive to Arabidopsis defenses that have also been associated with the deterrence of insect herbivores that are very distantly related to chelicerates. Our findings provide molecular insights into the nature of, and response to, herbivory for a representative of a major class of arthropod herbivores