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


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Chaoyang Zhao, Lucio Navarro Escalante, Hang Chen, Thiago Benatti, Jiaxin Qu, Sanjay Chellapilla, Robert Waterhouse, David Wheeler, Martin Andersson, Riyue Bao, Matthew Batterton, Susanta Behura, Kerstin Blankenburg, Doina Caragea, James Carolan, Marcus Coyle, Mustapha El Bouhssini, Liezl Francisco, Markus Friedrich, Navdeep Gill, Tony Grace, Cornelis Grimmelikhuijzen, Yi Han, Frank Hauser, Nicolae Herndon, Michael Holder, Panagiotis Ioannidis, LaRonda Jackson, Mehwish Javaid, Shalini Jhangiani, Alisha Johnson, Divya Kalra, Viktoriya Korchina, Christie Kovar, Fremiet Lara, Sandra Lee, Xuming Liu, Christer Löfstedt, Robert Mata, Tittu Mathew, Donna Muzny, Swapnil Nagar, Lynne Nazareth, Geoffrey Okwuonu, Fiona Ongeri, Lora Perales, Brittany Peterson, Ling-Ling Pu, Hugh Robertson, Brandon Schemerhorn, Steven Scherer, Jacob Shreve, DeNard Simmons, Subhashree Subramanyam, Rebecca Thornton, Kun Xue, George Weissenberger, Christie Williams, Kim Worley, Dianhui Zhu, Yiming Zhu, Marion O. Harris, Richard Shukle, John Werren, Evgeny Zdobnov, Ming-Shun Chen, Susan Brown, Jeffery Stuart, Stephen Richards. (5/2/2015). A Massive Expansion of Effector Genes Underlies Gall-Formation in the Wheat Pest Mayetiola destructor. Current Biology, 25 (5), pp. 613-620.
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.

Author(s) ORCID(s)

El Bouhssini, Mustapha