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

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          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.

          Abstract

          Non‐host and poor‐host resistance to aphids is poorly understood and is key for development of novel crop resistances to insect pests. Here, we used barley as a monocot model crop plant to study the interaction with aphid species that differ in their ability to infest and analysed barley transcriptional responses during interactions. Our work provides insights into how barley responds to different types of aphid interactions. Importantly, we identified barley genes contributing to plant defences against aphids.

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          The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity.

          In plants, reactive oxygen species (ROS) associated with the response to pathogen attack are generated by NADPH oxidases or apoplastic peroxidases. Antisense expression of a heterologous French bean (Phaseolus vulgaris) peroxidase (FBP1) cDNA in Arabidopsis thaliana was previously shown to diminish the expression of two Arabidopsis peroxidases (peroxidase 33 [PRX33] and PRX34), block the oxidative burst in response to a fungal elicitor, and cause enhanced susceptibility to a broad range of fungal and bacterial pathogens. Here we show that mature leaves of T-DNA insertion lines with diminished expression of PRX33 and PRX34 exhibit reduced ROS and callose deposition in response to microbe-associated molecular patterns (MAMPs), including the synthetic peptides Flg22 and Elf26 corresponding to bacterial flagellin and elongation factor Tu, respectively. PRX33 and PRX34 knockdown lines also exhibited diminished activation of Flg22-activated genes after Flg22 treatment. These MAMP-activated genes were also downregulated in unchallenged leaves of the peroxidase knockdown lines, suggesting that a low level of apoplastic ROS production may be required to preprime basal resistance. Finally, the PRX33 knockdown line is more susceptible to Pseudomonas syringae than wild-type plants. In aggregate, these data demonstrate that the peroxidase-dependent oxidative burst plays an important role in Arabidopsis basal resistance mediated by the recognition of MAMPs.
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            Myzus persicae (green peach aphid) salivary components induce defence responses in Arabidopsis thaliana.

            Myzus persicae (green peach aphid) feeding on Arabidopsis thaliana induces a defence response, quantified as reduced aphid progeny production, in infested leaves but not in other parts of the plant. Similarly, infiltration of aphid saliva into Arabidopsis leaves causes only a local increase in aphid resistance. Further characterization of the defence-eliciting salivary components indicates that Arabidopsis recognizes a proteinaceous elicitor with a size between 3 and 10 kD. Genetic analysis using well-characterized Arabidopsis mutants shows that saliva-induced resistance against M. persicae is independent of the known defence signalling pathways involving salicylic acid, jasmonate and ethylene. Among 78 Arabidopsis genes that were induced by aphid saliva infiltration, 52 had been identified previously as aphid-induced, but few are responsive to the well-known plant defence signalling molecules salicylic acid and jasmonate. Quantitative PCR analyses confirm expression of saliva-induced genes. In particular, expression of a set of O-methyltransferases, which may be involved in the synthesis of aphid-repellent glucosinolates, was significantly up-regulated by both M. persicae feeding and treatment with aphid saliva. However, this did not correlate with increased production of 4-methoxyindol-3-ylmethylglucosinolate, suggesting that aphid salivary components trigger an Arabidopsis defence response that is independent of this aphid-deterrent glucosinolate.
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              Premature leaf senescence modulated by the Arabidopsis PHYTOALEXIN DEFICIENT4 gene is associated with defense against the phloem-feeding green peach aphid.

              Aphids, which are phloem-feeding insects, cause extensive loss of plant productivity and are vectors of plant viruses. Aphid feeding causes changes in resource allocation in the host, resulting in an increase in flow of nutrients to the insect-infested tissue. We hypothesized that leaf senescence, which is involved in the programmed degradation of cellular components and the export of nutrients out of the senescing leaf, could be utilized by plants to limit aphid growth. Using Arabidopsis (Arabidopsis thaliana) and green peach aphid (GPA; Myzus persicae Sulzer), we found that GPA feeding induced premature chlorosis and cell death, and increased the expression of SENESCENCE ASSOCIATED GENES (SAGs), all hallmarks of leaf senescence. Hypersenescence was accompanied by enhanced resistance against GPA in the Arabidopsis constitutive expresser of PR genes5 and suppressor of SA insensitivity2 mutant plants. In contrast, resistance against GPA was compromised in the phytoalexin deficient4 (pad4) mutant plant. The PAD4 gene, which is expressed at elevated level in response to GPA feeding, modulates the GPA feeding-induced leaf senescence. In comparison to the wild-type plant, GPA feeding-induced chlorophyll loss, cell death, and SAG expression were delayed in the pad4 mutant. Although PAD4 is associated with camalexin synthesis and salicylic acid (SA) signaling, camalexin and SA signaling are not important for restricting GPA growth; growth of GPA on the camalexin-biosynthesis mutant, pad3, and the SA deficient2 and NahG plants and the SA-signaling mutant, nonexpresser of PR genes1, were comparable to that on the wild-type plant. Our results suggest that PAD4 modulates the activation of senescence in the aphid-infested leaves, which contributes to basal resistance to GPA.
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                Author and article information

                Contributors
                j.bos@dundee.ac.uk
                Journal
                Plant Cell Environ
                Plant Cell Environ
                10.1111/(ISSN)1365-3040
                PCE
                Plant, Cell & Environment
                John Wiley and Sons Inc. (Hoboken )
                0140-7791
                1365-3040
                18 July 2017
                November 2017
                : 40
                : 11 , Special Issue on Photomorphogenesis ( doiID: 10.1111/pce.v40.11 )
                : 2628-2643
                Affiliations
                [ 1 ] Cell and Molecular Sciences The James Hutton Institute Dundee DD2 5DA UK
                [ 2 ] Division of Plant Sciences, School of Life Sciences University of Dundee Dundee DD2 5DA UK
                Author notes
                [*] [* ]Correspondence: J. I. B. Bos. e‐mail: j.bos@ 123456dundee.ac.uk
                Author information
                http://orcid.org/0000-0002-5876-0331
                http://orcid.org/0000-0003-0866-324X
                http://orcid.org/0000-0003-3222-8643
                Article
                PCE12979 PCE-17-0107.R1
                10.1111/pce.12979
                6084319
                28452058
                b42d157d-bcef-4550-8eba-22dc6da48074
                © 2017 The Authors Plant, Cell & Environment Published by John Wiley & Sons Ltd

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 30 September 2016
                : 10 April 2017
                : 20 April 2017
                Page count
                Figures: 6, Tables: 0, Pages: 16, Words: 8401
                Funding
                Funded by: Royal Society of Edinburgh (personal fellowship)
                Funded by: European Research Council
                Award ID: 310190‐APHIDHOST
                Categories
                Original Article
                Original Articles
                Custom metadata
                2.0
                pce12979
                November 2017
                Converter:WILEY_ML3GV2_TO_NLMPMC version:version=5.4.4 mode:remove_FC converted:09.08.2018

                Plant science & Botany
                herbivore,host range,plant defence,transcriptomics
                Plant science & Botany
                herbivore, host range, plant defence, transcriptomics

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