Defense suppression benefits herbivores that have a monopoly on their feeding site but can backfire within natural communities

Glas, Joris J.; Alba, Juan M.; Simoni, Sauro; Villarroel, Carlos; Stoops, Marije; Schimmel, Bernardus C. J.; Schuurink, Robert C.; Sabelis, Maurice W.; Kant, Merijn R.

doi:10.1186/preaccept-2533843621365334

Cited by 33 publications

(104 citation statements)

References 33 publications

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“…Previously, we showed that mixing T. urticae and T. evansi from the start on the same leaf results in intermediate suppression of defenses (Alba et al, 2015). In nature, however, mites usually infest plants sequentially (Ferragut et al, 2013;Glas et al, 2014). Therefore, here we first allowed T. evansi to establish its feeding site and introduced T. urticae to the adjacent leaf tissue 2 d later, and vice versa.…”

Section: Introductionmentioning

confidence: 95%

Overcompensation of herbivore reproduction through hyper‐suppression of plant defenses in response to competition

et al. 2017

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Summary Spider mites are destructive arthropod pests on many crops. The generalist herbivorous mite Tetranychus urticae induces defenses in tomato (Solanum lycopersicum) and this constrains its fitness. By contrast, the Solanaceae‐specialist Tetranychus evansi maintains a high reproductive performance by suppressing tomato defenses. Tetranychus evansi outcompetes T. urticae when infesting the same plant, but it is unknown whether this is facilitated by the defenses of the plant.We assessed the extent to which a secondary infestation by a competitor affects local plant defense responses (phytohormones and defense genes), mite gene expression and mite performance.We observed that T. evansi switches to hyper‐suppression of defenses after its tomato host is also invaded by its natural competitor T. urticae. Jasmonate (JA) and salicylate (SA) defenses were suppressed more strongly, albeit only locally at the feeding site of T. evansi, upon introduction of T. urticae to the infested leaflet. The hyper‐suppression of defenses coincided with increased expression of T. evansi genes coding for salivary defense‐suppressing effector proteins and was paralleled by an increased reproductive performance.Together, these observations suggest that T. evansi overcompensates its reproduction through hyper‐suppression of plant defenses in response to nearby competitors. We hypothesize that the competitor‐induced overcompensation promotes competitive population growth of T. evansi on tomato.

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Section: Introductionmentioning

confidence: 95%

Overcompensation of herbivore reproduction through hyper‐suppression of plant defenses in response to competition

et al. 2017

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“…Odor cues emanating from infested plants were suggested to affect thrips choice, but no further studies on the mechanisms operating in these plant–thrips interactions have been described. Some studies have demonstrated that activation of plant defenses by other arthropod herbivores can affect thrips preference and survival (Delphia et al 2007), highlighting the central role of induced defenses in shaping the community of herbivores (Poelman et al 2008, Erb et al 2011, Glas et al 2014). …”

Section: Introductionmentioning

confidence: 99%

Induction of Jasmonic Acid-Associated Defenses by Thrips Alters Host Suitability for Conspecifics and Correlates with Increased Trichome Densities in Tomato

Escobar‐Bravo¹,

Klinkhamer²,

Leiss³

2017

Plant and Cell Physiology

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Plant defenses inducible by herbivorous arthropods can determine performance of subsequent feeding herbivores. We investigated how infestation of tomato (Solanum lycopersicum) plants with the Western flower thrips (Frankliniella occidentalis) alters host plant suitability and foraging decisions of their conspecifics. We explored the role of delayed-induced jasmonic acid (JA)-mediated plant defense responses in thrips preference by using the tomato mutant def-1, impaired in JA biosynthesis. In particular, we investigated the effect of thrips infestation on trichome-associated tomato defenses. The results showed that when offered a choice, thrips preferred non-infested plants over infested wild-type plants, while no differences were observed in def-1. Exogenous application of methyl jasmonate restored the repellency effect in def-1. Gene expression analysis showed induction of the JA defense signaling pathway in wild-type plants, while activating the ethylene signaling pathway in both genotypes. Activation of JA defenses led to increases in type-VI leaf glandular trichome densities in the wild type, augmenting the production of trichome-associated volatiles, i.e. terpenes. Our study revealed that plant-mediated intraspecific interactions between thrips are determined by JA-mediated defenses in tomato. We report that insects can alter not only trichome densities but also the allelochemicals produced therein, and that this response might depend on the magnitude and/or type of the induction.

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“…Antagonistic interactions between these pathways are well documented (Pieterse et al 2012). And a previous study attributed the observed enhancement of T. urticae performance in the presence of russet mites (Aculops lycopersici) to the attenuation of JA-defences because of JA-SA antagonism (Glass et al 2014)although Nachappa et al (2013) also reported positive effects of Tomato spotted wilt virus on T. urticae fecundity that did not appear to involve SA-JA crosstalk. In the current study, TYLCV and B. tabaci elicited significantly higher levels of SA and its associated marker gene (PR-1a) in combination than either induced in isolation (Figs 2c & 3d), and these levels were thus consistently higher in plants where T. urticae co-occurred with B. tabaci and TYLCV than in plants on which it co-occurred with either of these competitors separately (Figs 2c & 3d).…”

Section: Discussionmentioning

confidence: 94%

“…Total RNA was extracted and purified, and cDNA was synthesized as described by Su et al (2015a). To test the hypothesis that TYLCV infection suppresses T. urticae-induced JA-defences in B. tabaci-infested tomato, we measured defence responses in leaflets from T. urticae-infested and B. tabaci-infested plants by quantifying transcript levels of TYLCV influences plant-herbivore interactions 599 well-established JA-related and SA-related defence marker genes that are strongly induced by T. urticae feeding on tomato (Glass et al 2014;Alba et al 2015). Polyphenol oxidase-F (PPO-F), jasmonate-inducible protein 21 (JIP-21) and wound-induced proteinase inhibitor II (WIPI-II) were selected as JA-marker genes, while pathogenesis-related protein 1a (PR-1a) was selected as an SA-marker gene.…”

Section: Quantification Of Gene Expression By Qrt-pcrmentioning

confidence: 99%

“…Indeed, plant-mediated interactions between different herbivore speciesincluding both competition and facilitationare thought to be a major structuring force in arthropod communities (Denno et al 1995;Kaplan & Denno 2007). Ecological theory predicts that competition should be most intense when competing organisms belong to the same feeding guild (Denno et al 1995), but herbivores from different feeding guilds may also interact strongly via the induction of distinct, and potentially antagonistic, signal-transduction pathways (Kessler & Baldwin 2004;Viswanathan et al 2005;Thaler et al 2010;Bidart-Bouzat & Kliebenstein 2011;Ali & Agrawal 2014;Glass et al 2014). Thus, while the induction or suppression of plant defences may predictably reduce or increase an herbivore's reproductive performance when feeding in isolation, realized outcomes may be much less certain in the context of broader community interactions.…”

Section: Introductionmentioning

confidence: 99%

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Tomato yellow leaf curl virus differentially influences plant defence responses to a vector and a non‐vector herbivore

Mescher

Wang

et al. 2016

Plant Cell & Environment

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Plants frequently engage in simultaneous interactions with diverse classes of biotic antagonists. Differential induction of plant defence pathways by these antagonists, and interactions between pathways, can have important ecological implications; however, these effects are currently not well understood. We explored how Tomato yellow leaf curl virus (TYLCV) influenced the performance of its vector (Bemisia tabaci) and a non-vector herbivore (Tetranychus urticae) occurring separately or together on tomato plants (Solanum lycopersicum). TYLCV enhanced the performance of B. tabaci, although this effect was statistically significant only in the absence of T. urticae, which adversely affected B. tabaci performance regardless of infection status. In contrast, the performance of T. urticae was enhanced (only) by the combined presence of TYLCV and B. tabaci. Analyses of phytohormone levels and defence gene expression in wild-type tomatoes and various plant-defence mutants indicate that the enhancement of herbivore performance (for each species) entails the disruption of downstream defences in the jasmonic acid (JA) pathway. For T. urticae, this disruption appears to involve antagonistic effects of salicylic acid (SA), which is cumulatively induced to high levels by B. tabaci and TYLCV. In contrast, TYLCV was found to suppress JA-mediated responses to B. tabaci via mechanisms independent of SA.

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Defense suppression benefits herbivores that have a monopoly on their feeding site but can backfire within natural communities

Cited by 33 publications

References 33 publications

Overcompensation of herbivore reproduction through hyper‐suppression of plant defenses in response to competition

Overcompensation of herbivore reproduction through hyper‐suppression of plant defenses in response to competition

Induction of Jasmonic Acid-Associated Defenses by Thrips Alters Host Suitability for Conspecifics and Correlates with Increased Trichome Densities in Tomato

Tomato yellow leaf curl virus differentially influences plant defence responses to a vector and a non‐vector herbivore

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