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

Zhao, Chaoyang; Escalante, Lucio Navarro; Chen, Hang; Benatti, Thiago R.; Qu, Jiaxin; Chellapilla, Sanjay; Waterhouse, Robert M.; Wheeler, David; Andersson, Martin N LU and Bao, Riyue, et al. (2015) In Current Biology 25(5). p.613-620
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... (More)
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. (Less)
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Current Biology
volume
25
issue
5
pages
613 - 620
publisher
Elsevier
external identifiers
  • pmid:25660540
  • wos:000350708800024
  • scopus:84924812260
ISSN
1879-0445
DOI
10.1016/j.cub.2014.12.057
project
Sex pheromone biosynthesis and odorant receptors in gall midges
language
English
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2bea7618-4a4a-461b-9a82-966b6e4ea9fb (old id 5147256)
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2015-03-03 08:38:09
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@article{2bea7618-4a4a-461b-9a82-966b6e4ea9fb,
  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 (<i>Mayetiola destructor</i>; 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       = {Zhao, Chaoyang and Escalante, Lucio Navarro and Chen, Hang and Benatti, Thiago R. and Qu, Jiaxin and Chellapilla, Sanjay and Waterhouse, Robert M. and Wheeler, David and Andersson, Martin N and Bao, Riyue and Batterton, Matthew and Behura, Susanta K and Blankenburg, Kerstin P and Caragea, Doina and Carolan, James C and Coyle, Marcus and El-Bouhssini, Mustapha and Francisco, Liezl and Friedrich, Markus and Gill, Navdeep and Grace, Tony and Grimmelikhuijzen, Cornelis J P and Han, Yi and Hauser, Frank and Herndon, Nicolae and Holder, Michael and Ioannidis, Panagiotis and Jackson, LaRonda and Javaid, Mehwish and Jhangiani, Shalini N and Johnson, Alisha J and Kalra, Divya and Korchina, Viktoriya and Kovar, Christie L and Lara, Fremiet and Lee, Sandra L and Liu, Xuming and Löfstedt, Christer and Mata, Robert and Mathew, Tittu and Muzny, Donna M and Nagar, Swapnil and Nazareth, Lynne V and Okwuonu, Geoffrey and Ongeri, Fiona and Perales, Lora and Peterson, Brittany F and Pu, Ling-Ling and Robertson, Hugh M and Schemerhorn, Brandon J and Scherer, Steven E and Shreve, Jacob T and Simmons, DeNard and Subramanyam, Subhashree and Thornton, Rebecca L and Xue, Kun and Weissenberger, George M and Williams, Christie E and Worley, Kim C and Zhu, Dianhui and Zhu, Yiming and Harris, Marion O and Shukle, Richard H and Werren, John H and Zdobnov, Evgeny M and Chen, Ming-Shun and Brown, Susan J and Stuart, Jeffery J and Richards, Stephen},
  issn         = {1879-0445},
  language     = {eng},
  number       = {5},
  pages        = {613--620},
  publisher    = {Elsevier},
  series       = {Current Biology},
  title        = {A massive expansion of effector genes underlies gall-formation in the wheat pest <i>Mayetiola destructor</i>},
  url          = {http://dx.doi.org/10.1016/j.cub.2014.12.057},
  volume       = {25},
  year         = {2015},
}