Plant volatiles induced by herbivore eggs prime defences and mediate shifts in the reproductive strategy of receiving plants

Abstract

Plants can detect cues associated with the risk of future herbivory and modify defence phenotypes accordingly; however, our current understanding is limited both with respect to the range of early warning cues to which plants respond and the nature of the responses. Here we report that exposure to volatile emissions from plant tissues infested with herbivore eggs promotes stronger defence responses to subsequent herbivory in two Brassica species. Furthermore, exposure to these volatile cues elicited an apparent shift from growth to reproduction in Brassica nigra, with exposed plants exhibiting increased flower and seed production, but reduced leaf production, relative to unexposed controls. Our results thus document plant defence priming in response to a novel environmental cue, oviposition‐induced plant volatiles, while also showing that plant responses to early warning cues can include changes in both defence and life‐history traits.

Plant volatiles mediate evolutionary interactions between plants and tephritid flies and are evolutionarily more labile than non‐volatile defenses

“…This oversight is somewhat surprising because plant volatiles can be extremely important to host choice of herbivores within the Hymenoptera, Lepidoptera, Coleoptera, Hemiptera and Diptera (Benelli et al., 2013; Fraser et al., 2003; Li et al., 2017; Ninkovic et al., 2003; Wei et al., 2006). These herbivores can locate host plants by recognizing either species‐specific compounds or specific ratios of ubiquitous volatile compounds (Bruce et al., 2005), whereas plants can defend against herbivores by varying their volatile compound composition (Pashalidou et al., 2020; Ruther & Kleier, 2005). For example, Zu et al.…”

Arabidopsis, tobacco, nightshade and elm take insect eggs as herbivore alarm and show similar transcriptomic alarm responses

“…Plants can boost (prime) their defences against insect herbivory when they perceive cues that indicate a risk of herbivore attack prior to the feeding damage. Among these cues are feeding- or insect egg-induced plant volatiles from neighbouring plants 1 – 4 , insect sex pheromones 5 , 6 or insect egg deposition 7 . Plants respond to priming cues with transcriptional, phytohormonal and metabolic changes 7 – 9 .…”

“…VPS2, MYC2 ) SA: Increased SA levels Enhanced expression of SA-related genes (e.g. PR2 ) 4 , 16 , 68 – 71 Other Brassicaceae a Pieris brassicae Reduced larval weight and higher mortality Prolonged development until pupation Fabaceae Vicia faba Halyomorpha halys Reduced nymph weight 15 Solanaceae Nicotiana attenuata Manduca sexta Reduced antimicrobial activity in the hemolymph Increased levels of caffeoyl putrescine Increased TPI activity JA: Increased MYB8 expression 19 , 20 Spodoptera exigua Reduced larval weight and higher mortality Increased levels of caffeoyl putrescine JA: Increased MYB8 expression Solanum lycopersicum Helicoverpa zea JA: Increased JA levels Enhanced expression of PIN2 18 Solanum dulcamara Spodoptera exigua Reduced larval weight and higher mortality Stronger expression of genes involved in the phenylpropanoid pathways, e.g. anthocyanins JA, SA and ABA levels were not affected by prior egg deposition 22 Ulmaceae Ulmus minor Xanthogaleruca luteola Higher larval mortality Increase...…”

Sensory co‐evolution: The sex attractant of a gall‐making fly primes plant defences, but female flies recognize resulting changes in host‐plant quality

“…Plants tend to produce two types of defences as follows: constitutive defences, which are expressed constantly, and induced defences, which plants deploy only in response to specific environmental cues, often directly associated with herbivore feeding (Dicke & Hilker, 2003). It is also increasingly clear that plants respond to cues that precede herbivore attack, typically through defence priming, which does not entail the immediate deployment of defences, but rather results in stronger or faster defence induction in response to subsequent attack (Frost, Mescher, Carlson, & De Moraes, 2008;Mauch-Mani et al, 2017;Pashalidou et al, 2020). In S. altissima, defence responses mediated by the jasmonic acid pathway are primed by exposure to conophthorin, the primary component of the putative sex pheromone emitted by E. solidaginis males (Helms et al, 2013(Helms et al, , 2017.…”