Compatible plant-aphid interactions: How aphids manipulate plant responses

Giordanengo, Philippe; Brunissen, Laurence; Rustérucci, Christine; Vincent, Charles; Bel, Aart van; Dinant, Sylvie; Girousse, Christine; Faucher, Mireille; Bonnemain, Jean‐Louis

doi:10.1016/j.crvi.2010.03.007

Cited by 186 publications

(147 citation statements)

References 97 publications

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“…5B) and could account for the observed suppression of jasmonic acid signaling. Similar induction of salicylic acid-dependent gene expression has been reported in response to feeding by several other aphid species, including green peach aphid, cabbage aphid, greenbug aphid, and potato aphid (Giordanengo et al, 2010;Appel et al, 2014), suggesting that this may be a more general plant response to aphids. Aphids secrete a variety of proteins into the phloem as they are feeding (Elzinga and Jander, 2013), and some of these are known to suppress plant defense responses Bos et al, 2010;Elzinga et al, 2014).…”

Section: Discussionmentioning

confidence: 67%

Dynamic maize responses to aphid feeding are revealed by a time series of transcriptomic and metabolomic assays

et al. 2015

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(A.H.); 0000-0002-9675-934X (G.J.).As a response to insect attack, maize (Zea mays) has inducible defenses that involve large changes in gene expression and metabolism. Piercing/sucking insects such as corn leaf aphid (Rhopalosiphum maidis) cause direct damage by acquiring phloem nutrients as well as indirect damage through the transmission of plant viruses. To elucidate the metabolic processes and gene expression changes involved in maize responses to aphid attack, leaves of inbred line B73 were infested with corn leaf aphids for 2 to 96 h. Analysis of infested maize leaves showed two distinct response phases, with the most significant transcriptional and metabolic changes occurring in the first few hours after the initiation of aphid feeding. After 4 d, both gene expression and metabolite profiles of aphid-infested maize reverted to being more similar to those of control plants. Although there was a predominant effect of salicylic acid regulation, gene expression changes also indicated prolonged induction of oxylipins, although not necessarily jasmonic acid, in aphid-infested maize. The role of specific metabolic pathways was confirmed using Dissociator transposon insertions in maize inbred line W22. Mutations in three benzoxazinoid biosynthesis genes, Bx1, Bx2, and Bx6, increased aphid reproduction. In contrast, progeny production was greatly decreased by a transposon insertion in the single W22 homolog of the previously uncharacterized B73 terpene synthases TPS2 and TPS3. Together, these results show that maize leaves shift to implementation of physical and chemical defenses within hours after the initiation of aphid feeding and that the production of specific metabolites can have major effects in maize-aphid interactions.

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Section: Discussionmentioning

confidence: 67%

Dynamic maize responses to aphid feeding are revealed by a time series of transcriptomic and metabolomic assays

et al. 2015

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“…They also secrete watery saliva, both when probing into cells along the pathway and after penetrating the sieve elements with their stylet. The watery saliva contains calciumbinding proteins that suppress protein clogging and callose formation in the phloem, which would otherwise stop phloem transport (Giordanengo et al 2010). Aphids induce various responses in the plants.…”

Section: Introductionmentioning

confidence: 99%

The constitutive expression and induction of three β-1,3-glucanases by bird cherry-oat aphid in relation to aphid resistance in 15 barley breeding lines

Mehrabi

Åhman

Jonsson

2016

Arthropod-Plant Interactions

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In this study, 15 closely related barley genotypes were analyzed for the abundance of three b-1,3-glucanase transcripts immediately before and during infestation by the bird cherry-oat aphid (Rhopalosiphum padi L.). The barley lines are doubled haploid lines in backcross (BC) generations BC1 and BC2 from a cross between cultivar Lina and a wild barley accession. Previously, they have been characterized as susceptible (S) or resistant (R) to R. padi based on their ability to support nymphal growth. Here we also tested whether resistance was manifested as reduced aphid settling on the plants. Indeed, aphid numbers were lower on R than on S lines in all cases where there were significant differences between R and S lines. The choice of b-1,3-glucanase sequences is based on earlier results comparing two S and two R genotypes, suggesting that at least two of the three studied sequences are susceptibility factors. The comparisons of transcript abundance in plants with aphids showed for two of the b-1,3-glucanase sequences that there were several cases where an S genotype had significantly higher abundance than an R genotype, and in no case did an R line have significantly higher abundance than an S line. Thus, there was some support for the idea that b-1,3-glucanase sequences are susceptibility factors in the interaction between barley and R. padi.

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“…However, further investigations regarding the feeding strategy of the pest and host-plant response during compatible and incompatible interactions might provide useful information. Here, we will consider that a compatible interaction occurs when a pest is able to successfully feed and reproduce on its host-plant, while in incompatible interactions host resistance hamper or prevent the nutrition and development of the insect (Giordanengo et al 2010;Hogenhout and Bos 2011). Investigating how these interactions take place from both the insect and plant perspectives could help to infer how breeding and silvicultural practices might improve the management of tree pests based on host resistance.…”

Section: Genetic Diversity Of the Wpamentioning

confidence: 99%

“…It should therefore precede or be concomitant with the unveiling of resistance mechanisms. In a plantpest system, the analysis of compatible interactions implies to understand the feeding strategy of the pest and its consequences for the host at different scales, i.e., from cells or tissue to the entire tree level (Giordanengo et al 2010). Knowing in detail the feeding strategy of a pest is of prime importance since it is frequently related to the type of damage inflicted to the host-plant.…”

Section: In-depth Analysis Of Compatible Interactionsmentioning

confidence: 99%

Unraveling the tripartite interactions among the woolly poplar aphid, its host tree, and their environment: a lead to improve the management of a major tree plantation pest?

Sallé

Pointeau

Bankhead-Dronnet

et al. 2017

Annals of Forest Science

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Abstract& Key message For an optimal deployment of poplar resistance to the gall-inducing aphid Phloeomyzus passerinii, a laboratory susceptibility assay has been developed. The nature of aphid-tree interactions during compatible and incompatible situations has been studied in detail. This should help at identifying specific resistance markers and at testing effects of site conditions on tree-pest interactions. & Context P. passerinii is a major pest of poplar plantations in Europe, and the plantation of resistant poplar genotypes is regarded as the best long-term management strategy for this pest. This requires a sound knowledge of the interactions among the pest, its host and their environment. & Aims Here, we review the recent advances aiming at developing an optimal deployment of host resistance versus P. passerinii. & Results Investigations on aphid-host interactions demonstrated that P. passerinii induces pseudogalls within the bark of susceptible hosts. This results in a reduction of starch bark content during aphid outbreaks, which could be involved in tree death. The constitutive level of starch in the bark could be related to the tolerance level of trees. A susceptibility test has been designed for poplar genotypes, discriminating three categories of susceptibility depending on tree's ability to totally or partially inhibit pseudogall induction. The test still has several limitations however. It neither takes into account the large level of individual genetic diversity of the aphid in France, nor the environmental modulation of tree resistance and tolerance, while water deficit and fertilization could potentially affect these parameters. & Conclusion The hypotheses drawn regarding the processes leading to tree death or resistance should help at identifying resistance markers, and at testing effects of site conditions on tree-pest interactions.

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Compatible plant-aphid interactions: How aphids manipulate plant responses

Cited by 186 publications

References 97 publications

Dynamic maize responses to aphid feeding are revealed by a time series of transcriptomic and metabolomic assays

Dynamic maize responses to aphid feeding are revealed by a time series of transcriptomic and metabolomic assays

The constitutive expression and induction of three β-1,3-glucanases by bird cherry-oat aphid in relation to aphid resistance in 15 barley breeding lines

Unraveling the tripartite interactions among the woolly poplar aphid, its host tree, and their environment: a lead to improve the management of a major tree plantation pest?

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