Volatile interactions between specific undamaged barley cultivars affect aphid feeding behavior and performance

Abstract

Recent studies have demonstrated that cultivar mixtures can reduce aphid plant acceptance and population development. It is still unknown as to which underlying mechanisms may contribute to this phenomenon. We investigated the effects of volatile interactions between undamaged barley cultivars on aphid feeding behavior and performance in the laboratory. Spring barley (Hordeum vulgare L.) cultivar Salome was exposed to volatiles from Fairytale (SeF), Anakin (SeA), or clean air (Se0). We used an electrical penetration graph to test the effect of exposure to neighbor volatiles on the feeding behavior and performance of bird cherry-oat aphids (Rhopalosiphum padi L.). We also assessed aphid relative growth rate, intrinsic rate of increase, and development time on exposed and unexposed Salome plants. Aphids spent significantly longer time on epidermis and mesophyll plant tissues on SeF than Se0, and no difference was observed between SeA and Se0. Significant decreases in the duration of phloem ingestion and phloem sustained ingestion were recorded in SeF showing that volatile-induced effects cause difficulty for aphids to feed. However, no differences in these variables were detected between SeA and Se0. We also observed reduced aphid relative growth rate and intrinsic rate of increase on SeF compared to Se0 and SeA. Our study demonstrated that, in a specific combination, exposure of one barley cultivar to volatiles from another one can change aphid feeding behavior and performance, probably due to changes in host plant properties/quality. Our results provide an insightful explanation of mechanisms responsible for the reduced aphid population development previously observed in the field.

Communication between undamaged plants can elicit changes in volatile emissions from neighbouring plants, thereby altering their susceptibility to aphids

“…Fairytale can induce responses in receiving plants which disrupt aphid feeding and reduce their performance (Kheam et al, 2023). In the field, the reduction of aphid populations observed in specific cultivar mixtures, such as Salome-Fairytale mixtures (Dahlin et al, 2018), is consistent with the mechanistic explanation proposed from the results of our laboratory experiments.…”

“…We used three different spring barley cultivars ( Hordeum vulgare L.) in this study including: cultivars Salome (Nordaat Saatzucht GmbH), Fairytale and Anakin (Sejet Plant Breeding), since some of these cultivars in combination can decrease aphid plant acceptance in the laboratory and lower population size in the field (Dahlin et al, 2018; Kheam et al, 2023). All three cultivars have different pedigrees: Auriga × (Publican × Beatrix) for Salome, Colston × (Receipt × Power) for Fairytale, and (Tumbler × Response) for Anakin.…”

“…One of those potential biological alternatives against aphids could be based on the effects of plant–plant communication via volatile interactions in genotypically diverse cultivar mixtures. Previous studies reported that plant–plant communication in certain cultivar mixtures can increase the resilience of the crop to insect pests (Dahlin et al, 2018; Grettenberger & Tooker, 2016; Kheam et al, 2023; Shoffner & Tooker, 2013). Field studies showed that significant decreases in aphid populations were observed in the mixtures of Salome and Fairytale barley cultivars as compared to their pure stands.…”

“…Volatiles from onion plants can induce changes in potato volatile emissions making them less attractive to aphids in the laboratory and field experiments (Ninkovic et al, 2013). Previous studies further suggest a high specificity of such volatile-based plant-plant interactions depending on the species or even cultivar identity of interacting plants (Karban et al, 2006;Kheam et al, 2023;Ninkovic et al, 2013). For example, volatiles emitted from one specific barley cultivar significantly affect biomass allocation in another cultivar, leading to increased root biomass production, while other cultivars do not (Ninkovic, 2003).…”

“…Laboratory studies showed that the volatile interactions reduced plant acceptance by aphids in Salome exposed to Fairytale (SeF), but not in Salome exposed to Anakin (SeA) (Dahlin et al, 2018). Additionally, aphid feeding behaviour was disrupted and performance was reduced in SeF, but not in SeA (Kheam et al, 2023). The results of these studies suggest that plant–plant volatile interactions between specific cultivars may contribute to changes in host plants that make them less suitable for aphids.…”