Avirulence gene mapping in the Hessian fly (Mayetiola destructor) reveals a protein phosphatase 2C effector gene family

•The wheat-Hessian fly gene-for-gene interaction is corroborated.•A single candidate Hessian fly protein elicits H24-directed effector triggered immunity.•A family of secreted protein phosphatase-like effectors is revealed.

The genetic tractability of the Hessian fly (HF, Mayetiola destructor) provides an opportunity to investigate the mechanisms insects use to induce plant gall formation. Here we demonstrate that capacity using the newly sequenced HF genome by identifying the gene (vH24) that elicits effector-triggered immunity in wheat (Triticum spp.) seedlings carrying HF resistance gene H24. vH24 was mapped within a 230-kb genomic fragment near the telomere of HF chromosome X1. That fragment contains only 21 putative genes. The best candidate vH24 gene in this region encodes a protein containing a secretion signal and a type-2 serine/threonine protein phosphatase (PP2C) domain. This gene has an H24-virulence associated insertion in its promoter that appears to silence transcription of the gene in H24-virulent larvae. Candidate vH24 is a member of a small family of genes that encode secretion signals and PP2C domains. It belongs to the fraction of genes in the HF genome previously predicted to encode effector proteins. Because PP2C proteins are not normally secreted, our results suggest that these are PP2C effectors that HF larvae inject into wheat cells to redirect, or interfere, with wheat signal transduction pathways.

Graphical abstractFirst-instar Hessian fly larvae (A) use their microscopic mouthparts (m) to introduce secreted serine/threonine protein phosphatases (B) into wheat cells. These effectors presumably modulate wheat signal transduction pathways that alter seedling growth and development. (C) Susceptible seedlings (S) are stunted, but seedlings that detect the presence of an effector induce effector-triggered immunity (R) and grow normally.Figure optionsDownload full-size imageDownload as PowerPoint slide