Avirulence Effector Discovery in a Plant Galling and Plant Parasitic Arthropod, the Hessian Fly (Mayetiola destructor)

Highly specialized obligate plant-parasites exist within several groups of arthropods (insects and mites). Many of these are important pests, but the molecular basis of their parasitism and its evolution are poorly understood. One hypothesis is that plant parasitic arthropods use effector proteins t...

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Main Authors: Aggarwal, Rajat, Subramanyam, Subhashree, Zhao, Chaoyang, Chen, Ming-Shun, Harris, Marion O., Stuart, Jeff J.
Format: Online
Language:English
Published: Public Library of Science 2014
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4071006/
id pubmed-4071006
recordtype oai_dc
spelling pubmed-40710062014-06-27 Avirulence Effector Discovery in a Plant Galling and Plant Parasitic Arthropod, the Hessian Fly (Mayetiola destructor) Aggarwal, Rajat Subramanyam, Subhashree Zhao, Chaoyang Chen, Ming-Shun Harris, Marion O. Stuart, Jeff J. Research Article Highly specialized obligate plant-parasites exist within several groups of arthropods (insects and mites). Many of these are important pests, but the molecular basis of their parasitism and its evolution are poorly understood. One hypothesis is that plant parasitic arthropods use effector proteins to defeat basal plant immunity and modulate plant growth. Because avirulence (Avr) gene discovery is a reliable method of effector identification, we tested this hypothesis using high-resolution molecular genetic mapping of an Avr gene (vH13) in the Hessian fly (HF, Mayetiola destructor), an important gall midge pest of wheat (Triticum spp.). Chromosome walking resolved the position of vH13, and revealed alleles that determine whether HF larvae are virulent (survive) or avirulent (die) on wheat seedlings carrying the wheat H13 resistance gene. Association mapping found three independent insertions in vH13 that appear to be responsible for H13-virulence in field populations. We observed vH13 transcription in H13-avirulent larvae and the salivary glands of H13-avirulent larvae, but not in H13-virulent larvae. RNA-interference-knockdown of vH13 transcripts allowed some H13-avirulent larvae to escape H13-directed resistance. vH13 is the first Avr gene identified in an arthropod. It encodes a small modular protein with no sequence similarities to other proteins in GenBank. These data clearly support the hypothesis that an effector-based strategy has evolved in multiple lineages of plant parasites, including arthropods. Public Library of Science 2014-06-25 /pmc/articles/PMC4071006/ /pubmed/24964065 http://dx.doi.org/10.1371/journal.pone.0100958 Text en https://creativecommons.org/publicdomain/zero/1.0/ This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration, which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Aggarwal, Rajat
Subramanyam, Subhashree
Zhao, Chaoyang
Chen, Ming-Shun
Harris, Marion O.
Stuart, Jeff J.
spellingShingle Aggarwal, Rajat
Subramanyam, Subhashree
Zhao, Chaoyang
Chen, Ming-Shun
Harris, Marion O.
Stuart, Jeff J.
Avirulence Effector Discovery in a Plant Galling and Plant Parasitic Arthropod, the Hessian Fly (Mayetiola destructor)
author_facet Aggarwal, Rajat
Subramanyam, Subhashree
Zhao, Chaoyang
Chen, Ming-Shun
Harris, Marion O.
Stuart, Jeff J.
author_sort Aggarwal, Rajat
title Avirulence Effector Discovery in a Plant Galling and Plant Parasitic Arthropod, the Hessian Fly (Mayetiola destructor)
title_short Avirulence Effector Discovery in a Plant Galling and Plant Parasitic Arthropod, the Hessian Fly (Mayetiola destructor)
title_full Avirulence Effector Discovery in a Plant Galling and Plant Parasitic Arthropod, the Hessian Fly (Mayetiola destructor)
title_fullStr Avirulence Effector Discovery in a Plant Galling and Plant Parasitic Arthropod, the Hessian Fly (Mayetiola destructor)
title_full_unstemmed Avirulence Effector Discovery in a Plant Galling and Plant Parasitic Arthropod, the Hessian Fly (Mayetiola destructor)
title_sort avirulence effector discovery in a plant galling and plant parasitic arthropod, the hessian fly (mayetiola destructor)
description Highly specialized obligate plant-parasites exist within several groups of arthropods (insects and mites). Many of these are important pests, but the molecular basis of their parasitism and its evolution are poorly understood. One hypothesis is that plant parasitic arthropods use effector proteins to defeat basal plant immunity and modulate plant growth. Because avirulence (Avr) gene discovery is a reliable method of effector identification, we tested this hypothesis using high-resolution molecular genetic mapping of an Avr gene (vH13) in the Hessian fly (HF, Mayetiola destructor), an important gall midge pest of wheat (Triticum spp.). Chromosome walking resolved the position of vH13, and revealed alleles that determine whether HF larvae are virulent (survive) or avirulent (die) on wheat seedlings carrying the wheat H13 resistance gene. Association mapping found three independent insertions in vH13 that appear to be responsible for H13-virulence in field populations. We observed vH13 transcription in H13-avirulent larvae and the salivary glands of H13-avirulent larvae, but not in H13-virulent larvae. RNA-interference-knockdown of vH13 transcripts allowed some H13-avirulent larvae to escape H13-directed resistance. vH13 is the first Avr gene identified in an arthropod. It encodes a small modular protein with no sequence similarities to other proteins in GenBank. These data clearly support the hypothesis that an effector-based strategy has evolved in multiple lineages of plant parasites, including arthropods.
publisher Public Library of Science
publishDate 2014
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4071006/
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