A massive expansion of effector genes underlies gall-formation in the wheat pest mayetiola destructor

Chaoyang Zhao, Lucio Navarro Escalante, Hang Chen, Thiago R. Benatti, Jiaxin Qu, Sanjay Chellapilla, Robert M. Waterhouse, David Wheeler, Martin N. Andersson, Riyue Bao, Matthew Batterton, Susanta K. Behura, Kerstin P. Blankenburg, Doina Caragea, James C. Carolan, Marcus Coyle, Mustapha El-Bouhssini, Liezl Francisco, Markus Friedrich, Navdeep GillTony Grace, Cornelis J.P. Grimmelikhuijzen, Yi Han, Frank Hauser, Nicolae Herndon, Michael Holder, Panagiotis Ioannidis, Laronda Jackson, Mehwish Javaid, Shalini N. Jhangiani, Alisha J. Johnson, Divya Kalra, Viktoriya Korchina, Christie L. Kovar, Fremiet Lara, Sandra L. Lee, Xuming Liu, Christer Löfstedt, Robert Mata, Tittu Mathew, Donna M. Muzny, Swapnil Nagar, Lynne V. Nazareth, Geoffrey Okwuonu, Fiona Ongeri, Lora Perales, Brittany F. Peterson, Ling Ling Pu, Hugh M. Robertson, Brandon J. Schemerhorn, Steven E. Scherer, Jacob T. Shreve, Denard Simmons, Subhashree Subramanyam, Rebecca L. Thornton, Kun Xue, George M. Weissenberger, Christie E. Williams, Kim C. Worley, Dianhui Zhu, Yiming Zhu, Marion O. Harris, Richard H. Shukle, John H. Werren, Evgeny M. Zdobnov, Ming Shun Chen, Susan J. Brown, Jeffery J. Stuart, Stephen Richards

Research output: Contribution to journalArticle

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.

Original languageEnglish (US)
Pages (from-to)613-620
Number of pages8
JournalCurrent Biology
Volume25
Issue number5
DOIs
StatePublished - Mar 2 2015

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Fingerprint Dive into the research topics of 'A massive expansion of effector genes underlies gall-formation in the wheat pest mayetiola destructor'. Together they form a unique fingerprint.

  • Cite this

    Zhao, C., Escalante, L. N., Chen, H., Benatti, T. R., Qu, J., Chellapilla, S., Waterhouse, R. M., Wheeler, D., Andersson, M. N., Bao, R., Batterton, M., Behura, S. K., Blankenburg, K. P., Caragea, D., Carolan, J. C., Coyle, M., El-Bouhssini, M., Francisco, L., Friedrich, M., ... Richards, S. (2015). A massive expansion of effector genes underlies gall-formation in the wheat pest mayetiola destructor. Current Biology, 25(5), 613-620. https://doi.org/10.1016/j.cub.2014.12.057