A Massive Expansion of Effector Genes Underlies Gall-Formation in the Wheat Pest Mayetiola destructor

Abstract

Gall-forming arthropods are highly specialized herbivores that, in combination with their hosts, produce extended phenotypes with unique morphologies [1]. Many are economically important, and others have improved our understanding of ecology and adaptive radiation [2]. However, the mechanisms that these arthropods use to induce plant galls are poorly understood. We sequenced the genome of the Hessian fly (Mayetiola destructor; Diptera: Cecidomyiidae), a plant parasitic gall midge and a pest of wheat (Triticum spp.), with the aim of identifying genic modifications that contribute to its plant-parasitic lifestyle. Among several adaptive modifications, we discovered an expansive reservoir of potential effector proteins. Nearly 5% of the 20,163 predicted gene models matched putative effector gene transcripts present in the M. destructor larval salivary gland. Another 466 putative effectors were discovered among the genes that have no sequence similarities in other organisms. The largest known arthropod gene family (family SSGP-71) was also discovered within the effector reservoir. SSGP-71 proteins lack sequence homologies to other proteins, but their structures resemble both ubiquitin E3 ligases in plants and E3-ligase-mimicking effectors in plant pathogenic bacteria. SSGP-71 proteins and wheat Skp proteins interact in vivo. Mutations in different SSGP-71 genes avoid the effector-triggered immunity that is directed by the wheat resistance genes H6 and H9. Results point to effectors as the agents responsible for arthropod-induced plant gall formation.

The Salivary Protein Repertoire of the Polyphagous Spider Mite Tetranychus urticae: A Quest for Effectors

“…Arthropod effector proteins are characterized by the presence of a Nterminal SP, directing them to the secretory pathway, and their encoding genes show signatures of rapid evolution (poor sequence similarity with other genera, multiple gene copies, and high rates of non-synonymous nucleotide mutations) (131)(132)(133)(134). Because of the highly specific function of effectors, variable expression levels depending on the host plant could also be indicative of a context-dependent function (108).…”

The Conformation of a Plasma Membrane-Localized Somatic Embryogenesis Receptor Kinase Complex Is Altered by a Potato Aphid-Derived Effector

“…To date, three insect-derived avirulence effectors have been identified from the Dipteran Hessian fly Mayetiola destructor (Aggarwal et al, 2014;Zhao et al, 2015). However, their cognate R genes have not yet been cloned and the mechanism of recognition of these effectors is not known (Harris et al, 2015;Stuart, 2015).…”

Crop domestication, global human-mediated migration, and the unresolved role of geography in pest control

“…Breeding for high levels of plant resistance may be more effective against generalist herbivores than specialist herbivores, because chewing specialist herbivores may already possess the biochemical pathways to detoxify specialized toxins (Gols et al, 2008;Shlichta et al, 2014). For sap-sucking and galling herbivores, continued efforts to breed for defense could be very important but the sustainability of resistance could be short-lived, because plants and herbivores appear to be engaged in reciprocal defense and virulence responses (Smith and Chuang, 2014;Habachi-Houimli et al, 2015;Zhao et al, 2015). Finally, for natural enemies that have adapted to domestication crops, it would be useful to understand how to increase their effectiveness.…”