The role of protein effectors in plant–aphid interactions

Elzinga, Dezi; Jander, Georg

doi:10.1016/j.pbi.2013.06.018

Cited by 132 publications

(108 citation statements)

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“…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). However, although it has been proposed that aphids actively induce salicylic acid production to misdirect plant defenses (Walling, 2008), specific salivary effectors involved in this process have not yet been identified.…”

Section: Discussionmentioning

confidence: 99%

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: 99%

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

et al. 2015

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“…In response, herbivores have evolved the capacity to suppress and circumvent these plant defenses through the release of effectors (Elzinga and Jander, 2013). Plant cell walls (PCWs), for instance, are thick, rigid structures that consist mainly of a pectin-embedded network of cellulose and hemicellulose (Calderón-Cortés et al, 2012); these structures not only act as physical defenses against herbivores by enhancing the mechanical hardness of plant tissues but also reduce the digestibility of food for herbivores (Santiago et al, 2013), thereby functioning as the first layer of defense against herbivores.…”

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confidence: 99%

“…Thus, herbivore effectors play a central role in overcoming plant defenses and helping the herbivore establish a population on host plants. However, the mechanisms underlying the effector-mediated promotion of herbivore abilities to overcome plant defenses remain mostly unknown (Elzinga and Jander, 2013).…”

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“…Coagulable saliva forms salivary sheaths around the insect's stylets that help to stabilize and protect the stylets and may suppress plant defense responses to components of the watery saliva (Miles, 1999;Abdellatef et al, 2015). Watery saliva, which contains a mixture of amino acids, proteins, and digestive enzymes, assists in the digestion of plant material and helps suppress plant defense responses (Miles, 1968(Miles, , 1999Harmel et al, 2008;Carolan et al, 2009;Hogenhout and Bos, 2011;Nicholson et al, 2012;Elzinga and Jander, 2013). Thus, BPH saliva plays an important role in BPH feeding.…”

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confidence: 99%

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A Salivary Endo-β-1,4-Glucanase Acts as an Effector That Enables the Brown Planthopper to Feed on Rice

Chen

et al. 2017

Plant Physiol.

100

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ORCID IDs: 0000-0002-5714-7586 (J.Z.); 0000-0002-3262-6134 (Y.L.).The brown planthopper (BPH) Nilaparvata lugens is one of the most destructive insect pests on rice (Oryza sativa) in Asia. After landing on plants, BPH rapidly accesses plant phloem and sucks the phloem sap through unknown mechanisms. We discovered a salivary endo-b-1,4-glucanase (NlEG1) that has endoglucanase activity with a maximal activity at pH 6 at 37°C and is secreted into rice plants by BPH. NlEG1 is highly expressed in the salivary glands and midgut. Silencing NlEG1 decreases the capacity of BPH to reach the phloem and reduces its food intake, mass, survival, and fecundity on rice plants. By contrast, NlEG1 silencing had only a small effect on the survival rate of BPH raised on artificial diet. Moreover, NlEG1 secreted by BPH did not elicit the production of the defense-related signal molecules salicylic acid, jasmonic acid, and jasmonoyl-isoleucine in rice, although wounding plus the application of the recombination protein NlEG1 did slightly enhance the levels of jasmonic acid and jasmonoyl-isoleucine in plants compared with the corresponding controls. These data suggest that NlEG1 enables the BPH's stylet to reach the phloem by degrading celluloses in plant cell walls, thereby functioning as an effector that overcomes the plant cell wall defense in rice.

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“…The effector proteins from pathogenic bacteria and fungi induce and suppress plant immunity via a well-known process described by the zigzag theory (Jones and Dangl, 2006). Effectors are a group of proteins that translocate from microbes such as bacteria, fungi, and nematodes to host plants and animals (Elzinga and Jander, 2013). The major function of effectors is to modulate host immune responses though interactions with their counterpart proteins in the host plant.…”

Section: Introductionmentioning

confidence: 99%

Transient Expression of Whitefly Effectors in Nicotiana benthamiana Leaves Activates Systemic Immunity Against the Leaf Pathogen Pseudomonas syringae and Soil-Borne Pathogen Ralstonia solanacearum

Lee

Park

et al. 2018

Front. Ecol. Evol.

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Infestation of plants with the phloem-feeding whitefly Bemisia tabaci modulates root microbiota and both local and systemic immunity against microbial pathogens. Specifically, aboveground whitefly infestation suppresses pathogen propagation and symptom development caused by the soil-borne pathogens Agrobacterium tumefaciens and Ralstonia solanacearum in the root system through systemic signal transduction. Therefore, we hypothesized that secreted protein(s)/non-protein factors from whitefly saliva (referred to as candidate effectors) might function as insect determinants that activate systemic acquired resistance (SAR) in the host plant. Here, we intensively screened a cDNA library constructed from mRNA from whitefly feeding on Nicotiana benthamiana leaves and selected three candidate effectors 2G4, 2G5, and 6A10, that appear to reduce disease development caused by the aboveground pathogen Pseudomonas syringae pv. tabaci and the soil-borne pathogen R. solanacearum. Transient expression of the three candidate effector cDNAs in leaves primed the expression of SAR marker genes NbPR1a and NbPR2 in local and systemic leaves against P. syringae pv. tabaci, while leaf infiltration with 2G4 or 6A10 cDNA elicited strong defense priming of SAR markers following drench application of R. solanacearum on plant roots. In silico and qRT-PCR analyses revealed the presence of 2G5 and 6A10 transcripts in insect salivary glands. This is the first report of whitefly effectors that prime SAR against aboveground and belowground bacterial pathogens.

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The role of protein effectors in plant–aphid interactions

Cited by 132 publications

References 48 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

A Salivary Endo-β-1,4-Glucanase Acts as an Effector That Enables the Brown Planthopper to Feed on Rice

Transient Expression of Whitefly Effectors in Nicotiana benthamiana Leaves Activates Systemic Immunity Against the Leaf Pathogen Pseudomonas syringae and Soil-Borne Pathogen Ralstonia solanacearum

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