Defense Suppression through Interplant Communication Depends on the Attacking Herbivore Species

Abstract

In response to herbivory, plants emit volatile compounds that play important roles in plant defense. Herbivore-induced plant volatiles (HIPVs) can deter herbivores, recruit natural enemies, and warn other plants of possible herbivore attack. Following HIPV detection, neighboring plants often respond by enhancing their anti-herbivore defenses, but a recent study found that herbivores can manipulate HIPV-interplant communication for their own benefit and suppress defenses in neighboring plants. Herbivores induce species-specific blends of HIPVs and how these different blends affect the specificity of plant defense responses remains unclear. Here we assessed how HIPVs from zucchini plants (Cucurbita pepo) challenged with different herbivore species affect resistance in neighboring plants. Volatile “emitter” plants were damaged by one of three herbivore species: saltmarsh caterpillars (Estigmene acrea), squash bugs (Anasa tristis), or striped cucumber beetles (Acalymma vittatum), or were left as undamaged controls. Neighboring “receiver” plants were exposed to HIPVs or control volatiles and then challenged by the associated herbivore species. As measures of plant resistance, we quantified herbivore feeding damage and defense-related phytohormones in receivers. We found that the three herbivore species induced different HIPV blends from squash plants. HIPVs induced by saltmarsh caterpillars suppressed defenses in receivers, leading to greater herbivory and lower defense induction compared to controls. In contrast, HIPVs induced by cucumber beetles and squash bugs did not affect plant resistance to subsequent herbivory in receivers. Our study shows that herbivore species identity affects volatile-mediated interplant communication in zucchini, revealing a new example of herbivore defense suppression through volatile cues.

Undercover operation: Belowground insect herbivory modifies systemic plant defense and repels aboveground foraging insect herbivores

“…Squash bugs (Anasa tristis DeGeer) are another major pest of cucurbits that feed solely on aboveground plant tissues as both juveniles and adults (Doughty et al, 2016). As a piercing-sucking herbivore, squash bugs inflict markedly different damage on host plants than chewing cucumber beetles (Neal, 1993;Mauck et al, 2015;Marmolejo et al, 2021). Both squash bugs and cucumber beetles are native to North America, sharing a long coexistence history with zucchini squash (Shapiro and Mauck, 2018).…”

A Beneficial Plant-Associated Fungus Shifts the Balance toward Plant Growth over Resistance, Increasing Cucumber Tolerance to Root Herbivory

“…on specialists [ 43 ]. Striped cucumber beetles ( Acalymma vittatum ) are specialist herbivores of plants in the family Cucurbitaceae, and our previous research suggests indirect defenses (i.e., recruitment of herbivore-killing natural enemies with volatile compounds) may be more effective against cucumber beetles than other induced defenses (e.g., toxic metabolites) [ 44 , 45 ]. In this study, it appears that P. inflatum -induced changes to cucumber plant chemistry and/or nutrition positively affected the performance of specialist cucumber beetles, whereas in previous research with cotton, P. inflatum -associated plants were more resistant against generalist herbivores.…”

“…However, upon belowground herbivory by cucumber beetle larvae, these compounds were suppressed to levels like untreated control roots ( Figure 4 ). Although JA and SA are frequently associated with plant defense against herbivores [ 45 ] and pathogens [ 57 ], they can also be involved in signaling related to plant growth processes [ 34 , 58 , 59 ]. For example, in sunflowers, inhibition of JA increased lateral and primary root growth [ 60 ], whereas in tobacco, increased levels of JA inhibited root growth [ 55 , 56 ].…”

Improving Natural Enemy Selection in Biological Control through Greater Attention to Chemical Ecology and Host-Associated Differentiation of Target Arthropod Pests

“…Plant volatiles or other secondary metabolites convey the identity and suitability of a host plant to foraging herbivores. After locating a suitable host, herbivore feeding triggers the production of herbivore-induced plant volatiles (HIPVs), which are specific to the identity of the attacking herbivore [37]. Foraging herbivores can detect HIPVs and use these cues to assess the acceptability of a host plant [38][39][40].…”