Ethylene contributes to potato aphid susceptibility in a compatible tomato host

Mantelin, Sophie; Bhattarai, Kishor K.; Kaloshian, Isgouhi

doi:10.1111/j.1469-8137.2009.02870.x

Cited by 46 publications

(58 citation statements)

References 72 publications

(94 reference statements)

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“…Alterations in ET also benefit aphids, increasing insect fecundity on infected plants and therefore the number of viruliferous aphids. Virus infection and aphid feeding have been shown to influence the production of ET (Love et al, 2005(Love et al, , 2007Kim et al, 2008;Mantelin et al, 2009;Chen et al, 2013;Haikonen et al, 2013;Mandadi et al, 2014;Mauck et al, 2014), though ET's role in vector-virusplant interactions has not yet been demonstrated. Virus-induced changes in ET responses may mediate vector-plant interactions more broadly and thus represent a conserved mechanism for increasing transmission by insect vectors across generations.…”

Section: Discussionmentioning

confidence: 99%

“…Increases in ET production following aphid feeding also have been reported in various plant-aphid interactions. However, ET production has been associated with both increased susceptibility and resistance to aphids (Miller et al, 1994;Argandoña et al, 2001;Mantelin et al, 2009;Lu et al, 2014;Wu et al, 2015). The role of ET in both plant-virus and plant-aphid interactions Figure 9.…”

Section: Discussionmentioning

confidence: 99%

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Disruption of Ethylene Responses by Turnip mosaic virus Mediates Suppression of Plant Defense against the Green Peach Aphid Vector

Casteel

Alwis²,

Bak³

et al. 2015

Plant Physiol.

146

129

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Plants employ diverse responses mediated by phytohormones to defend themselves against pathogens and herbivores. Adapted pathogens and herbivores often manipulate these responses to their benefit. Previously, we demonstrated that Turnip mosaic virus (TuMV) infection suppresses callose deposition, an important plant defense induced in response to feeding by its aphid vector, the green peach aphid (Myzus persicae), and increases aphid fecundity compared with uninfected control plants. Further, we determined that production of a single TuMV protein, Nuclear Inclusion a-Protease (NIa-Pro) domain, was responsible for changes in host plant physiology and increased green peach aphid reproduction. To characterize the underlying molecular mechanisms of this phenomenon, we examined the role of three phytohormone signaling pathways, jasmonic acid, salicylic acid, and ethylene (ET), in TuMV-infected Arabidopsis (Arabidopsis thaliana), with or without aphid herbivory. Experiments with Arabidopsis mutants ethylene insensitive2 and ethylene response1, and chemical inhibitors of ET synthesis and perception (aminoethoxyvinyl-glycine and 1-methylcyclopropene, respectively), show that the ET signaling pathway is required for TuMV-mediated suppression of Arabidopsis resistance to the green peach aphid. Additionally, transgenic expression of NIa-Pro in Arabidopsis alters ET responses and suppresses aphidinduced callose formation in an ET-dependent manner. Thus, disruption of ET responses in plants is an additional function of NIaPro, a highly conserved potyvirus protein. Virus-induced changes in ET responses may mediate vector-plant interactions more broadly and thus represent a conserved mechanism for increasing transmission by insect vectors across generations.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Disruption of Ethylene Responses by Turnip mosaic virus Mediates Suppression of Plant Defense against the Green Peach Aphid Vector

Casteel

Alwis²,

Bak³

et al. 2015

Plant Physiol.

146

129

View full text Add to dashboard Cite

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“…Furthermore, reduced population expansion was observed in green peach aphids (Myzus persicae) when raised on the Arabidopsis (Arabidopsis thaliana) constitutive expression of vegetative storage protein1 mutant constantly expressing JA responses, whereas the JA-insensitive mutant coronatine-insensitive1 supports more rapid growth of aphids than wild-type plants (Ellis et al, 2002;Mewis et al, 2005). Aphid infestation has been shown to trigger ET production (Mantelin et al, 2009). Elevated ET levels have been both positively and negatively correlated with plant resistance to aphids (Thompson and Goggin, 2006).…”

mentioning

confidence: 99%

“…Elevated ET levels have been both positively and negatively correlated with plant resistance to aphids (Thompson and Goggin, 2006). In tomato (Solanum lycopersicum), ET biosynthesis renders plants more susceptible to potato aphids (Macrosiphum euphorbiae; Mantelin et al, 2009). However, the Arabidopsis ET-insensitive mutant ein2 promotes performance of green peach aphids (Kettles et al, 2013), indicating that ET plays a defensive role in Arabidopsis.…”

mentioning

confidence: 99%

BOTRYTIS-INDUCED KINASE1 Modulates Arabidopsis Resistance to Green Peach Aphids via PHYTOALEXIN DEFICIENT4

Lei

Finlayson

Salzman³

et al. 2014

Plant Physiology

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BOTRYTIS-INDUCED KINASE1 (BIK1) plays important roles in induced defense against fungal and bacterial pathogens in Arabidopsis (Arabidopsis thaliana). Its tomato (Solanum lycopersicum) homolog is required for host plant resistance to a chewing insect herbivore. However, it remains unknown whether BIK1 functions in plant defense against aphids, a group of insects with a specialized phloem sap-feeding style. In this study, the potential role of BIK1 was investigated in Arabidopsis infested with the green peach aphid (Myzus persicae). In contrast to the previously reported positive role of intact BIK1 in defense response, loss of BIK1 function adversely impacted aphid settling, feeding, and reproduction. Relative to wild-type plants, bik1 displayed higher aphid-induced hydrogen peroxide accumulation and more severe lesions, resembling a hypersensitive response (HR) against pathogens. These symptoms were limited to the infested leaves. The bik1 mutant showed elevated basal as well as induced salicylic acid and ethylene accumulation. Intriguingly, elevated salicylic acid levels did not contribute to the HR-like symptoms or to the heightened aphid resistance associated with the bik1 mutant. Elevated ethylene levels in bik1 accounted for an initial, short-term repellence. Introducing a loss-of-function mutation in the aphid resistance and senescence-promoting gene PHYTOALEXIN DEFICIENT4 (PAD4) into the bik1 background blocked both aphid resistance and HR-like symptoms, indicating bik1-mediated resistance to aphids is PAD4 dependent. Taken together, Arabidopsis BIK1 confers susceptibility to aphid infestation through its suppression of PAD4 expression. Furthermore, the results underscore the role of reactive oxygen species and cell death in plant defense against phloem sap-feeding insects.

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“…Therefore, other techniques are required to elucidate gene function. Virusinduced gene silencing (VIGS) offers an attractive alternative (Mitra et al, 2008;Pandey and Baldwin, 2008;Mantelin et al, 2009). Initially, VIGS was almost exclusively performed in the model plant species Nicotiana benthamiana by using vectors derived from tobacco mosaic virus (TMV) (Kumagai et al, 1995), potato virus X (Ratcliff et al, 1997), and tobacco rattle virus (TRV) (Ratcliff et al, 2001;Liu et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

Silencing Defense Pathways in Arabidopsis by Heterologous Gene Sequences from Brassica oleracea Enhances the Performance of a Specialist and a Generalist Herbivorous Insect

et al. 2011

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The jasmonic acid (JA) signaling pathway and defensive secondary metabolites such as glucosinolates are generally considered to play central roles in the defense of brassicaceous plants against herbivorous insects. To determine the function of specific plant genes in plant-insect interactions, signaling or biosynthetic mutants are needed. However, mutants are not yet available for brassicaceous plants other than Arabidopsis thaliana, e.g., cabbage (Brassica oleracea). We employed virus-induced gene silencing (VIGS) by using tobacco rattle virus (TRV) to knock down the endogenous expression of lipoxygenase (LOX), an upstream enzyme of the JA pathway and thioglucoside glucohydrolase: myrosinase (TGG1/TGG2), a hydrolytic enzyme that catalyzes the release of defensive volatile products originating from glucosinolates, in Arabidopsis thaliana. This was done by using the heterologous gene sequences from B. oleracea. Silencing these genes in A. thaliana plants is efficient and specific. Only 18 nucleotides with 100% identity between the trigger (BoMYR) and the target (AtTGG1/2) sequence are sufficient to achieve gene silencing. LOX-silenced plants showed significantly reduced AtLOX2 transcript accumulation after Pieris rapae larval feeding. TGG-silenced plants exhibited significantly lower TGG1/TGG2 transcript levels only after shorter larval feeding. The inhibition of TGG1/TGG2 transcript accumulation via gene silencing may be overruled by longer larval feeding. Specialist P. rapae larvae developed significantly better on both types of silenced plants than on empty vector (EV) control plants, while generalist Mamestra brassicae larvae developed significantly better on the TGG1/TGG2 silenced plants than on EV control plants. This shows that not only the generalist herbivore but also the Brassicaceae-specialist P. rapae is negatively affected by the ability of brassicaceous plants to produce their specific secondary metabolites, i.e., glucosinolates. Our results demonstrate the important roles of AtLOX2 and AtTGG1/TGG2 genes, which were silenced by heterologous gene sequences from B. oleracea BoLOX and BoMYR, in A. thaliana resistance to the specialist P. rapae and the generalist M. brassicae.

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Ethylene contributes to potato aphid susceptibility in a compatible tomato host

Cited by 46 publications

References 72 publications

Disruption of Ethylene Responses by Turnip mosaic virus Mediates Suppression of Plant Defense against the Green Peach Aphid Vector

Disruption of Ethylene Responses by Turnip mosaic virus Mediates Suppression of Plant Defense against the Green Peach Aphid Vector

BOTRYTIS-INDUCED KINASE1 Modulates Arabidopsis Resistance to Green Peach Aphids via PHYTOALEXIN DEFICIENT4

Silencing Defense Pathways in Arabidopsis by Heterologous Gene Sequences from Brassica oleracea Enhances the Performance of a Specialist and a Generalist Herbivorous Insect

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