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

<div><p>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 (<i>Avr</i>) gene discovery is a reliable method of effector identification, we tested this hypothesis using high-resolution molecular genetic mapping of an <i>Avr</i> gene (<i>vH13</i>) in the Hessian fly (HF, <i>Mayetiola destructor</i>), an important gall midge pest of wheat (<i>Triticum</i> spp.). Chromosome walking resolved the position of <i>vH13</i>, and revealed alleles that determine whether HF larvae are virulent (survive) or avirulent (die) on wheat seedlings carrying the wheat <i>H13</i> resistance gene. Association mapping found three independent insertions in <i>vH13</i> that appear to be responsible for <i>H13</i>-virulence in field populations. We observed <i>vH13</i> transcription in <i>H13</i>-avirulent larvae and the salivary glands of <i>H13</i>-avirulent larvae, but not in <i>H13</i>-virulent larvae. RNA-interference-knockdown of <i>vH13</i> transcripts allowed some <i>H13</i>-avirulent larvae to escape <i>H13</i>-directed resistance. <i>vH13</i> is the first <i>Avr</i> 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.</p>