Small volatile lipophilic molecules induced belowground by aphid attack elicit a defensive response in neighbouring un-infested plants

Abstract

In pioneering studies on plant-aphid interactions, we have observed that Vicia faba plants infested by aphids can transmit signals via the rhizosphere that induce aboveground defence in intact, neighbouring plants. The aphid parasitoid Aphidius ervi is significantly attracted towards intact broad bean plants grown in a hydroponic solution previously harbouring Acyrtosiphon pisum-infested plants. To identify the rhizosphere signal(s) possibly mediating this belowground plant-plant communication, root exudates were collected using Solid-Phase Extraction (SPE) from 10-day old A. pisum-infested and un-infested Vicia faba plants hydroponically grown. To verify the ability of these root exudates to trigger defence mechanisms against the aphids we added them to V. fabae plants grown in hydroponic solution, and tested these plants in the wind-tunnel bioassay to assess their attractiveness towards the aphids’ parasitoids A. ervi. We identified three small volatile lipophilic molecules as plant defence elicitors: 1-octen-3-ol, sulcatone and sulcatol, in SPE extracts of A. pisum-infested broad bean plants. In wind tunnel assays, we recorded a significant increase in the attractiveness towards A. ervi of V. faba plants grown in hydroponic solution treated with these compounds, compared to plants grown in hydroponic treated with ethanol (control). Both 1-octen-3-ol and sulcatol have asymmetrically substituted carbon atoms at positions 3 and 2, respectively. Hence, we tested both their enantiomers alone or in mixture. We highlighted a synergistic effect on the level of attractiveness towards the parasitoid when testing the three compounds together in respect to the response recorded against them singly tested. These behavioural responses were supported by the characterization of headspace volatiles released by tested plants. These results shed new light on the mechanisms underlying plant-plant communication belowground and prompt the use of bio-derived semiochemicals for a sustainable protection of agricultural crops.

Belowground insect herbivory induces systemic volatile emissions that strengthen neighbouring plant resistance aboveground

“…Despite advances in understanding signalling between plants either aboveground or belowground, few studies have integrated across these ‘compartments’ when evaluating chemically mediated plant interactions, particularly in the context of insect herbivory. Intriguingly, aboveground insect herbivory was recently shown to systemically alter the release of belowground root exudates and HIPVs, which neighbouring roots detect and use to enhance their antiherbivore defences (Cascone, Vuts, Birkett, Dewhirst, et al, 2023; Cascone, Vuts, Birkett, Rasmann, et al, 2023). These findings demonstrate that systemic responses to insect herbivory can mediate interactions between plants, indicating that plant signalling spans across ‘compartments’ and plants interpret chemical information from neighbours to assess their risk of herbivory.…”

“…Relatedly, belowground herbivory can modulate systemic HIPV emissions from leaves that affect the foraging behaviours of aboveground herbivores (Sun et al, 2019) and natural enemies (Soler et al, 2007). Systemic HIPVs determine many plant‐mediated ecological interactions, but the extent to which neighbouring plants detect and/or respond to systemic HIPVs remains an open question (Cascone, Vuts, Birkett, Rasmann, et al, 2023). Considering many insect herbivore species feed belowground as larvae and aboveground as adults (Menacer et al, 2021), neighbouring plants may interpret belowground herbivore‐induced changes in systemic HIPVs as an early warning sign of aboveground herbivore attack.…”

Methyl‐salicylate: A surveillance system for triggering immunity in neighboring plants

“…These compounds are produced by the secretory cells of plants as a signal for defense upon being attacked by insects or microbes. Numerous reports have stated that VOCs containing MeSA are secreted by plants in response to aphid infestation, which is responsible for generating defense against insect and virus attacks, and also attracts predators to diminish the persistence of these insects on the plant (Cascone et al, 2023; Gong et al, 2023). MeSA is a key VOC secreted by many plant species and responsible for creating local and systemic acquired resistance against microbes and pathogens (Wenig et al, 2019; Gong et al, 2023).…”

“…Aphids are major pests for economically important crops, and they are also responsible for transmitting plant pathogenic viruses. The majority of plant viruses are transferred by members of aphids (Aphidoidea) and whiteflies (Aleyrodoidea), which are specialized for causing damage to cells and infect the target tissue phloem of the plants (Cascone et al, 2023), triggering the defense machinery in plants. In this commentary, we discuss the signaling role of methyl‐salicylate (MeSA) under attack by members of Aphidoidea in plants, which brings about systemically acquired resistance in the aphid‐infested plant as well as neighboring plants by acting as a long‐distance signaling molecule.…”