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Differential localization of Hessian fly candidate effectors in resistant and susceptible wheat plants.

ABSTRACT: Hessian fly Mayetiola destructor is a notorious pest of wheat. Previous studies suggest that Hessian fly uses effector-based mechanisms to attack wheat plants during parasitism, but no direct evidence has been reported to support this postulation. Here, we produced recombinant proteins for five Family-1 candidate effectors and antibodies. Indirect immunostaining and western blots were carried out to examine the localization of Hessian fly Family-1 proteins in plant and insect tissues. Confocal images revealed that Family-1 putative effectors were exclusively produced in the basal region of larval salivary glands, which are directly linked to the mandibles' ducts for effector injection. The five Family-1 proteins were detected in infested host plants on western blots. Indirect immunostaining of sectioned host tissues around the feeding site revealed strikingly different localization patterns between resistant and susceptible plants. In susceptible plants, the Family-1 proteins penetrated from the feeding cell into deep tissues, indicative of movement between cells during nutritive cell formation. In contrast, the Hessian fly proteins were primarily limited to the initially attacked cells in resistant plants. The limitation of effectors' spread in resistant plants was likely due to wall strengthening and rapid hypersensitive cell death. Cell death was found in Nicotiana benthamiana in association with hypersensitive reaction triggered by the Family-1 effector SSGP-1A2. Our finding represents a significant progress in visualizing insect effectors in host tissues and mechanisms of plant resistance and susceptibility to gall midge pests.

SUBMITTER: Aljbory Z

PROVIDER: S-EPMC7428492 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Differential localization of Hessian fly candidate effectors in resistant and susceptible wheat plants.

Aljbory Zainab Z Aikins Michael J MJ Park Yoonseong Y Reeck Gerald R GR Chen Ming-Shun MS

Plant direct 20200814 8

Hessian fly <i>Mayetiola destructor</i> is a notorious pest of wheat. Previous studies suggest that Hessian fly uses effector-based mechanisms to attack wheat plants during parasitism, but no direct evidence has been reported to support this postulation. Here, we produced recombinant proteins for five Family-1 candidate effectors and antibodies. Indirect immunostaining and western blots were carried out to examine the localization of Hessian fly Family-1 proteins in plant and insect tissues. Con ...[more]

PMID: 32818166

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Project description:BackgroundHessian fly (Mayetiola destructor), a member of the gall midge family, is one of the most destructive pests of wheat (Triticum aestivum) worldwide. Probing of wheat plants by the larvae results in either an incompatible (avirulent larvae, resistant plant) or a compatible (virulent larvae, susceptible plant) interaction. Virulent larvae induce the formation of a nutritive tissue, resembling the inside surface of a gall, in susceptible wheat. These nutritive cells are a rich source of proteins and sugars that sustain the developing virulent Hessian fly larvae. In addition, on susceptible wheat, larvae trigger a significant increase in levels of amino acids including proline and glutamic acid, which are precursors for the biosynthesis of ornithine and arginine that in turn enter the pathway for polyamine biosynthesis.ResultsFollowing Hessian fly larval attack, transcript abundance in susceptible wheat increased for several genes involved in polyamine biosynthesis, leading to higher levels of the free polyamines, putrescine, spermidine and spermine. A concurrent increase in polyamine levels occurred in the virulent larvae despite a decrease in abundance of Mdes-odc (ornithine decarboxylase) transcript encoding a key enzyme in insect putrescine biosynthesis. In contrast, resistant wheat and avirulent Hessian fly larvae did not exhibit significant changes in transcript abundance of genes involved in polyamine biosynthesis or in free polyamine levels.ConclusionsThe major findings from this study are: (i) although polyamines contribute to defense in some plant-pathogen interactions, their production is induced in susceptible wheat during interactions with Hessian fly larvae without contributing to defense, and (ii) due to low abundance of transcripts encoding the rate-limiting ornithine decarboxylase enzyme in the larval polyamine pathway the source of polyamines found in virulent larvae is plausibly wheat-derived. The activation of the host polyamine biosynthesis pathway during compatible wheat-Hessian fly interactions is consistent with a model wherein the virulent larvae usurp the polyamine biosynthesis machinery of the susceptible plant to acquire nutrients required for their own growth and development.

Dataset Information

Differential localization of Hessian fly candidate effectors in resistant and susceptible wheat plants.

Publications

Differential localization of Hessian fly candidate effectors in resistant and susceptible wheat plants.

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