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      Heterodera avenae GLAND5 Effector Interacts With Pyruvate Dehydrogenase Subunit of Plant to Promote Nematode Parasitism

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          Abstract

          Heterodera avenae mainly infects cereal crops and causes severe economic losses. Many studies have shown that parasitic nematodes can secrete effector proteins to suppress plant immune responses and then promote parasitism. In this study, we showed that HaGland5, a novel effector of H. avenae, was exclusively expressed in dorsal esophageal gland cell of nematode, and up-regulated in the early parasitic stage. Transgenic Arabidopsis thaliana lines expressing HaGland5 were significantly more susceptible to H. schachtii than wild-type control plants. Conversely, silencing of HaGland5 through barley stripe mosaic virus-medicated host-induced gene silencing technique substantially reduced the infection of H. avenae in wheat. Moreover, HaGland5 could suppress the plant defense responses, including the repression of plant defense-related genes, reducing deposition of cell wall callose and the burst of reactive oxygen species. Mass spectrometry, co-immunoprecipitation, and firefly luciferase complementation imaging assays confirmed that HaGland5 interacted specifically with Arabidopsis pyruvate dehydrogenase subunit (AtEMB3003).

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          Most cited references52

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          A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense.

          Selection pressure exerted by insects and microorganisms shapes the diversity of plant secondary metabolites. We identified a metabolic pathway for glucosinolates, known insect deterrents, that differs from the pathway activated by chewing insects. This pathway is active in living plant cells, may contribute to glucosinolate turnover, and has been recruited for broad-spectrum antifungal defense responses. The Arabidopsis CYP81F2 gene encodes a P450 monooxygenase that is essential for the pathogen-induced accumulation of 4-methoxyindol-3-ylmethylglucosinolate, which in turn is activated by the atypical PEN2 myrosinase (a type of beta-thioglucoside glucohydrolase) for antifungal defense. We propose that reiterated enzymatic cycles, controlling the generation of toxic molecules and their detoxification, enable the recruitment of glucosinolates in defense responses.
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            HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis.

            Powdery mildew fungi are obligate biotrophic pathogens that only grow on living hosts and cause damage in thousands of plant species. Despite their agronomical importance, little direct functional evidence for genes of pathogenicity and virulence is currently available because mutagenesis and transformation protocols are lacking. Here, we show that the accumulation in barley (Hordeum vulgare) and wheat (Triticum aestivum) of double-stranded or antisense RNA targeting fungal transcripts affects the development of the powdery mildew fungus Blumeria graminis. Proof of concept for host-induced gene silencing was obtained by silencing the effector gene Avra10, which resulted in reduced fungal development in the absence, but not in the presence, of the matching resistance gene Mla10. The fungus could be rescued from the silencing of Avra10 by the transient expression of a synthetic gene that was resistant to RNA interference (RNAi) due to silent point mutations. The results suggest traffic of RNA molecules from host plants into B. graminis and may lead to an RNAi-based crop protection strategy against fungal pathogens.
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              Phytopathogen effectors subverting host immunity: different foes, similar battleground.

              Phytopathogenic bacteria, fungi, and oomycetes invade and colonize their host plants through distinct routes. These pathogens secrete diverse groups of effector proteins that aid infection and establishment of different parasitic lifestyles. Despite this diversity, a comparison of different plant-pathogen systems has revealed remarkable similarities in the host immune pathways targeted by effectors from distinct pathogen groups. Immune signaling pathways mediated by pattern recognition receptors, phytohormone homeostasis or signaling, defenses associated with host secretory pathways and pathogen penetrations, and plant cell death represent some of the key processes controlling disease resistance against diverse pathogens. These immune pathways are targeted by effectors that carry a wide range of biochemical functions and are secreted by completely different pathogen groups, suggesting that these pathways are a common battleground encountered by many plant pathogens. Copyright © 2012 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                04 June 2019
                2019
                : 10
                : 1241
                Affiliations
                Department of Plant Pathology and MOA Key Laboratory of Pest Monitoring and Green Management, China Agricultural University , Beijing, China
                Author notes

                Edited by: Holger Heuer, Julius Kühn-Institut, Germany

                Reviewed by: Kan Zhuo, South China Agricultural University, China; Aska Goverse, Wageningen University & Research, Netherlands

                *Correspondence: Heng Jian, hengjian@ 123456cau.edu.cn

                This article was submitted to Plant Microbe Interactions, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2019.01241
                6558007
                31214156
                e8e0cc8c-9284-4cc3-8b3d-71a687367af9
                Copyright © 2019 Yang, Pan, Chen, Yang, Liu and Jian.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 26 December 2018
                : 17 May 2019
                Page count
                Figures: 7, Tables: 0, Equations: 0, References: 65, Pages: 12, Words: 0
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                heterodera avenae,effector,hagland5,pyruvate dehydrogenase subunit,defense signaling pathways

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