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Suppression of Plant Defenses by Herbivorous Mites Is Not Associated with Adaptation to Host Plants.

ABSTRACT: Some herbivores suppress plant defenses, which may be viewed as a result of the coevolutionary arms race between plants and herbivores. However, this ability is usually studied in a one-herbivore-one-plant system, which hampers comparative studies that could corroborate this hypothesis. Here, we extend this paradigm and ask whether the herbivorous spider-mite Tetranychus evansi, which suppresses the jasmonic-acid pathway in tomato plants, is also able to suppress defenses in other host plants at different phylogenetic distances from tomatoes. We test this using different plants from the Solanales order, namely tomato, jimsonweed, tobacco, and morning glory (three Solanaceae and one Convolvulaceae), and bean plants (Fabales). First, we compare the performance of T. evansi to that of the other two most-commonly found species of the same genus, T. urticae and T. ludeni, on several plants. We found that the performance of T. evansi is higher than that of the other species only on tomato plants. We then showed, by measuring trypsin inhibitor activity and life history traits of conspecific mites on either clean or pre-infested plants, that T. evansi can suppress plant defenses on all plants except tobacco. This study suggests that the suppression of plant defenses may occur on host plants other than those to which herbivores are adapted.

SUBMITTER: Paulo JT

PROVIDER: S-EPMC6032058 | biostudies-literature | 2018 Jun

REPOSITORIES: biostudies-literature

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Suppression of Plant Defenses by Herbivorous Mites Is Not Associated with Adaptation to Host Plants.

Paulo Jéssica T JT Godinho Diogo P DP Silva Anabela A Branquinho Cristina C Magalhães Sara S

International journal of molecular sciences 20180615 6

Some herbivores suppress plant defenses, which may be viewed as a result of the coevolutionary arms race between plants and herbivores. However, this ability is usually studied in a one-herbivore-one-plant system, which hampers comparative studies that could corroborate this hypothesis. Here, we extend this paradigm and ask whether the herbivorous spider-mite <i>Tetranychus evansi</i>, which suppresses the jasmonic-acid pathway in tomato plants, is also able to suppress defenses in other host pl ...[more]

PMID: 29914126

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Project description: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.

Project description:BackgroundPlants respond to herbivore damage with the release of volatile organic compounds (VOCs). This indirect defense can cause ecological costs when herbivores themselves use VOCs as cues to localize suitable host plants. Can VOCs reliably indicate food plant quality to herbivores?MethodologyWe determined the choice behavior of herbivorous beetles (Chrysomelidae: Gynandrobrotica guerreroensis and Cerotoma ruficornis) when facing lima bean plants (Fabaceae: Phaseolus lunatus) with different cyanogenic potential, which is an important constitutive direct defense. Expression of inducible indirect defenses was experimentally manipulated by jasmonic acid treatment at different concentrations. The long-distance responses of male and female beetles to the resulting induced plant volatiles were investigated in olfactometer and free-flight experiments and compared to the short-distance decisions of the same beetles in feeding trials.ConclusionFemale beetles of both species were repelled by VOCs released from all induced plants independent of the level of induction. In contrast, male beetles were repelled by strongly induced plants, showed no significant differences in choice behavior towards moderately induced plants, but responded positively to VOCs released from little induced plants. Thus, beetle sex and plant VOCs had a significant effect on host searching behavior. By contrast, feeding behavior of both sexes was strongly determined by the cyanogenic potential of leaves, although females again responded more sensitively than males. Apparently, VOCs mainly provide information to these beetles that are not directly related to food quality. Being induced by herbivory and involved in indirect plant defense, such VOCs might indicate the presence of competitors and predators to herbivores. We conclude that plant quality as a food source and finding a potentially enemy-free space is more important for female than for male insect herbivores, whereas the presence of a slightly damaged plant can help males to localize putative mating partners.

Project description:When plants detect herbivores they strengthen their defenses. As a consequence, some herbivores evolved the means to suppress these defenses. Research on induction and suppression of plant defenses usually makes use of particular life stages of herbivores. Yet many herbivorous arthropods go through development cycles in which their successive stages have different characteristics and lifestyles. Here we investigated the interaction between tomato defenses and different herbivore developmental stages using two herbivorous spider mites, i.e., Tetranychus urticae of which the adult females induce defenses and T. evansi of which the adult females suppress defenses in Solanum lycopersicum (tomato). First, we monitored egg-to-adult developmental time on tomato wild type (WT) and the mutant defenseless-1 (def-1, unable to produce jasmonate-(JA)-defenses). Then we assessed expression of salivary effector genes (effector 28, 84, SHOT2b, and SHOT3b) in the consecutive spider mite life stages as well as adult males and females. Finally, we assessed the extent to which tomato plants upregulate JA- and salicylate-(SA)-defenses in response to the consecutive mite developmental stages and to the two sexes. The consecutive juvenile mite stages did not induce JA defenses and, accordingly, egg-to-adult development on WT and def-1 did not differ for either mite species. Their eggs however appeared to suppress the SA-response. In contrast, all the consecutive feeding stages upregulated SA-defenses with the strongest induction by T. urticae larvae. Expression of effector genes was higher in the later developmental stages. Comparing expression in adult males and females revealed a striking pattern: while expression of effector 84 and SHOT3b was higher in T. urticae females than in males, this was the opposite for T. evansi. We also observed T. urticae females to upregulate tomato defenses, while T. evansi females did not. In addition, of both species also the males did not upregulate defenses. Hence, we argue that mite ontogenetic niche shifts and stage-specific composition of salivary secreted proteins probably together determine the course and efficiency of induced tomato defenses.

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Suppression of Plant Defenses by Herbivorous Mites Is Not Associated with Adaptation to Host Plants.

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Suppression of Plant Defenses by Herbivorous Mites Is Not Associated with Adaptation to Host Plants.

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