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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.

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