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

Abstract

BackgroundPlants have inducible defenses to combat attacking organisms. Hence, some herbivores have adapted to suppress these defenses. Suppression of plant defenses has been shown to benefit herbivores by boosting their growth and reproductive performance.ResultsWe observed in field-grown tomatoes that spider mites (Tetranychus urticae) establish larger colonies on plants already infested with the tomato russet mite (Aculops lycopersici). Using laboratory assays, we observed that spider mites have a much higher reproductive performance on russet mite-infested plants, similar to their performance on the jasmonic acid (JA)-biosynthesis mutant def-1. Hence, we tested if russet mites suppress JA-responses thereby facilitating spider mites. We found that russet mites manipulate defenses: they induce those mediated by salicylic acid (SA) but suppress those mediated by JA which would otherwise hinder growth. This suppression of JA-defenses occurs downstream of JA-accumulation and is independent from its natural antagonist SA. In contrast, spider mites induced both JA- and SA-responses while plants infested with the two mite species together display strongly reduced JA-responses, yet a doubled SA-response. The spider mite-induced JA-response in the presence of russet mites was restored on transgenic tomatoes unable to accumulate SA (nahG), but russet mites alone still did not induce JA-responses on nahG plants. Thus, indirect facilitation of spider mites by russet mites depends on the antagonistic action of SA on JA while suppression of JA-defenses by russet mites does not. Furthermore, russet mite-induced SA-responses inhibited secondary infection by Pseudomonas syringae (Pst) while not affecting the mite itself. Finally, while facilitating spider mites, russet mites experience reduced population growth.ConclusionsOur results show that the benefits of suppressing plant defenses may diminish within communities with natural competitors. We show that suppression of defenses via the JA-SA antagonism can be a consequence, rather than the cause, of a primary suppression event and that its overall effect is determined by the presence of competing herbivores and the distinct palette of defenses these induce. Thus, whether or not host-defense manipulation improves an herbivore’s fitness depends on interactions with other herbivores via induced-host defenses, implicating bidirectional causation of community structure of herbivores sharing a plant.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-014-0098-9) contains supplementary material, which is available to authorized users.

Size of predatory mites and refuge entrance determine success of biological control of the coconut mite

“…However, some herbivores can also benefit from plant structures to hide from predators (Magalhães et al 2007). For example, herbivores are known to live in between the scales of flower bulbs (Lesna et al 2004(Lesna et al , 2014, inside dense forests of leaf trichomes (van Houten et al 2013;Glas et al 2012Glas et al , 2014, and in shafts of grasses (Oldfield 1996;Lindquist and Oldfield 1996;Sabelis and Bruin 1996), which reduces the risk of predation.…”

Unraveling molecular mechanisms underlying plant defense in response to dual insect attack : studying density-dependent effects

“…It has been proposed that insects can manipulate plant defenses for their own benefit by modulating JA-SA crosstalk Zhu-Salzman et al, 2004;. This has also been reported for the tomato russet mite (Aculops lycopersici) that suppressed a harmful JA response by inducing SA signaling in tomato (Glas et al, 2014). A study using tomato plants infested by the mealybug Phenacoccus solenopsis also proposed the same mechanism (modification of JA-SA crosstalk) explaining the enhanced performance of P. solenopsis nymphs .…”

Drought-stressed tomato plants trigger bottom-up effects on key mite pests

“…urticae (Glas, 2014;Martel et al, 2015), and A. lycopersici (Glas, 2014), inducing both species the accumulation of OPDA, JA and JA-Ile (Glas, 2014;Glas et al, 2014;Alba et al, 2015).…”

“…The serine (PI-I, WIPI-II, JIP-21) aspartyl (CDI) and cysteine (CysPI) PI genes are induced by tetranychid mites in tomato but not by A. lycopersici (Li, et al, 2002;Kant et al, 2014;Glas, 2014;Glas et al, 2014;Alba et al 2015;Martel et al, 2015). Plant cysteine PIs are harmful for T. urticae (Santamaria et al, 2012(Santamaria et al, , 2015b been studied using some of these markers genes Alba et al, 2015).…”

“…A thin barrier of Lanolin (Sigma_aldrichChemie, Zwijndrecht, The Netherlands) was prepared, using a needleless syringe, around the petioles of the leaf to prevent the mites from escaping. The TRM population density was assessed at the two time points using the protocol described by Glas et al (2014). In brief, the three infested leaves of each plant were detached and washed one by one for 20 seconds in a single volume of 25 ml of Ethanol 100%.…”