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ARS Home » Plains Area » Manhattan, Kansas » Center for Grain and Animal Health Research » Hard Winter Wheat Genetics Research » Research » Publications at this Location » Publication #305442

Title: Avirulence effector discovery in a plant galling and plant parasitic arthropod, the Hessian fly (Mayetiola destructor)

item AGGARWAL, RAJAT - Purdue University
item SUBRAMANYAM, SUBHASHREE - Purdue University
item ZHAO, CHAOYANG - Purdue University
item Chen, Ming-Shun
item HARRIS, MARION - North Dakota State University
item STUART, JEFFREY - Purdue University

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/2/2014
Publication Date: 6/25/2014
Citation: Aggarwal, R., Subramanyam, S., Zhao, C., Chen, M., Harris, M.O., Stuart, J.J. 2014. Avirulence effector discovery in a plant galling and plant parasitic arthropod, the Hessian fly (Mayetiola destructor). PLoS One. 9(6):e100958.

Interpretive Summary: The Hessian fly is a major pest of wheat and is mainly controlled by deploying resistant wheat cultivars. However, wheat resistance to the Hessian fly is often short-lived, lasting for 3 to 6 years. To produce more durable resistance, we need to understand the molecular basis for Hessian fly resistance in wheat and for virulence in Hessian fly. This study identified an avirulence gene, named vH13, in Hessian fly. The gene encodes a small protein with a secretion signal peptide. Wild-type vH13 gene results in Hessian fly avirulence (death of insects) to plants containing the H13 resistance gene, whereas a mutated version of the gene confers Hessian fly virulence (survival of insects) to the otherwise resistant plants. These data clearly support the hypothesis that resistance requires recognition of effectors produced by the insects.

Technical Abstract: 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 effector-based strategy has evolved in multiple lineages of plant parasites, including arthropods.