Barley transcriptome analyses upon interaction with different aphid species identify thionins contributing to resistance

Abstract

Aphids are phloem‐feeding insects that cause yield loss on a wide range of crops, including cereals such as barley. Whilst most aphid species are limited to one or few host species, some are able to reproduce on many plants belonging to different families. Interestingly, aphid probing behaviour can be observed on both host and non‐host species, indicating that interactions take place at the molecular level that may impact host range. Here, we aimed to gain insight into the interaction of barley with aphid species differing in their ability to infest this crop by analysing transcriptional responses. Firstly, we determined colonization efficiency, settlement and probing behaviour for the aphid species Rhopalosiphum padi, Myzus persicae and Myzus cerasi, which defined host, poor‐host and non‐host interactions, respectively. Analyses of barley transcriptional responses revealed gene sets differentially regulated upon the different barley–aphid interactions and showed that the poor‐host interaction with M. persicae resulted in the strongest regulation of genes. Interestingly, we identified several thionin genes strongly up‐regulated upon interaction with M. persicae, and to a lesser extent upon R. padi interaction. Ectopic expression of two of these genes in Nicotiana benthamiana reduced host susceptibility to M. persicae, indicating that thionins contribute to defences against aphids.

Plant resistance in different cell layers affects aphid probing and feeding behaviour during poor- and non-host interactions

“…Arabidopsis (Jaouannet et al, 2015). However, in both the M. persicae-barley poor-82 host interaction and the R. padi-Arabidopsis non-host interaction probing of the leaf 83 surface takes place (Escudero-Martinez et al, 2017, Jaouannet et al, 2015. In line 84 with our previous findings, choice assays showed that both aphid species will settle 85 on and interact with non-/poor-host plant species if given a choice, with 10% of 86 aphids found on non-/poor-hosts after 24h.…”

“…Prior to probing the leaf 15 surface aphid behaviour can be influenced by a range of these factors including leaf 16 colour, emitted volatile organic compounds and leaf surface components, such as 17 epicuticular waxes or trichomes (Doring, 2014, Doring & Chittka, 2007, Neal et al, 18 1990. Regardless of whether the aphid encounters a host or non-host plant species 19 their specialised mouthparts, known as stylets, are utilised to probe into the plant 20 tissue (Escudero-Martinez et al, 2017, Jaouannet et al, 2015, Powell et al, 2006. 21…”

“…Escudero-Martinez et al, 2017). However, our previous transcriptome analyses 343 showed induction of a barley gene encoding Phloem Protein 2-like (PP2), which is a 344 phloem specific lectin, with the induction being most pronounced during the barley-M.345 persicae interaction (Escudero-Martinez et al, 2017).…”

“…5C and 5D). It is likely that 326 this reduced phloem sap ingestion is responsible for the reduced M. persicae 327 performance on barley (Escudero-Martinez et al, 2017, Ramirez & Niemeyer, 2000. 328…”

“…aphids were placed on the plants) and that additional plant resistance 361 components that affect aphid choice may play a role in the interactions studied here 362 (Escudero-Martinez et al, 2017, Powell et al, 2006. For example, we previously 363 showed that the black cherry aphid (Myzus cerasi Fabricius), which infests cherry 364 trees as well as several herbaceous plants, displays only limited probing on non-host 365 barley plants, and does not settle on barley leaves (Escudero-Martinez et al, 2017), 366 pointing to a potential role of barley defences that act at the pre-probing level against 367 this aphid species (Nottingham et al, 1991). In addition, some plant induced volatile 368 compounds have been reported to be repellent to aphid pests and attractants of their 369 natural enemies (Dreyer & Jones, 1981, Mallinger et al, 2011, Turlings & Ton, 2006.…”