Defence gene expression and phloem quality contribute to mesophyll and phloem resistance to aphids in wild barley

Abstract

Aphids, including the bird cherry-oat aphid (Rhopalosiphum padi), are significant agricultural pests. The wild relative of barley, Hordeum spontaneum 5 (Hsp5), has been described to be partially resistant to R. padi, with this resistance proposed to involve higher thionin and lipoxygenase gene expression. However, the specificity of this resistance to aphids and its underlying mechanistic processes are unknown. In this study, we assessed the specificity of Hsp5 resistance to aphids and analysed differences in aphid probing and feeding behaviour on Hsp5 and a susceptible barley cultivar (Concerto). We found that partial resistance in Hsp5 to R. padi extends to two other aphid pests of grasses. Using the electrical penetration graph technique, we show that partial resistance is mediated by phloem- and mesophyll-based resistance factors that limit aphid phloem ingestion. To gain insight into plant traits responsible for partial resistance, we compared non-glandular trichome density, defence gene expression, and phloem composition of Hsp5 with those of the susceptible barley cultivar Concerto. We show that Hsp5 partial resistance involves elevated basal expression of thionin and phytohormone signalling genes, and a reduction in phloem quality. This study highlights plant traits that may contribute to broad-spectrum partial resistance to aphids in barley.

A fitness cost resulting fromHamiltonella defensainfection is associated with altered probing and feeding behaviour inRhopalosiphum padi

“…Global analysis of aphid feeding patterns indicated that aphid feeding behaviour was significantly affected by plant identity (F 1,43 = 3.19; p = 0.017) and the interaction between endosymbiont presence and plant identity (F 1,43 = 2.71; p = 0.037). From the 72 parameters obtained, seven parameters were affected by plant identity alone (Table S1), however these parameters are not presented or discussed in detail here as we recently characterised R. padi feeding responses to plant identity in a separate study (see Leybourne et al 2019). In support of hypothesis 1, a total of 11 parameters were primarily influenced by endosymbiont infection, and these were mainly associated with stylet intracellular punctures and interaction with the phloem (Table 1; Fig.…”

“…A faster initiation of sustained feeding could explain the higher mass of H. defensa -infected nymphs on Concerto. However, it is likely that our observed reduction in nymph mass for both infected and uninfected nymphs when feeding on Hsp5 compared with those feeding on Concerto is due increased aphid resistance in Hsp5 (Leybourne et al, 2019). The rapid initiation of sustained feeding could be associated with other aphid fitness effects which are currently uncharacterised, such as the transmission or acquisition of phloem-limited viruses.…”

“…We recently characterised the partial-resistance mechanism of Hsp5 (Leybourne et al, 2019) and reported that partial-resistance involves mesophyll and phloem traits. These included an increased abundance of defensive thionins and a reduction in the availability of essential amino acids as mesophyll-derived and phloem-derived partial-resistance factors, respectively (Leybourne et al, 2019).…”

“…We recently characterised the partial-resistance mechanism of Hsp5 (Leybourne et al, 2019) and reported that partial-resistance involves mesophyll and phloem traits. These included an increased abundance of defensive thionins and a reduction in the availability of essential amino acids as mesophyll-derived and phloem-derived partial-resistance factors, respectively (Leybourne et al, 2019). These factors could underlie the decreased time aphids spent probing into plant tissue and the shorter duration of the initial probe into plant tissue, although the underlying processes causing these differential feeding patterns are currently unclear.…”

Partial-resistance against aphids in wild barley reduces the oviposition success of the generalist parasitoid,Aphidius colemaniViereck

“…We recently compared a modern domesticated cultivar of barley Hordeum vulgare (Linnaeus) cv. Concerto (Concerto) with a wild progenitor species possessing partial-resistance against aphids, H. spontaneum 5 (Linnaeus) (Hsp5) (L EYBOURNE et al 2019). We showed that partial-resistance in Hsp5 primarily involves mesophyll- and phloem-derived resistance factors, associated with increased defence gene expression and a reduction in phloem quality, respectively, which contribute to decreased aphid fitness (L EYBOURNE et al 2019).…”