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A massive expansion of effector genes underlies gall-formation in the wheat pest Mayetiola destructor.
Curr Biol. 2015 Mar 02; 25(5):613-20.CB

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.

Authors+Show Affiliations

Department of Entomology, Purdue University, West Lafayette, IN 47097, USA.Department of Entomology, Purdue University, West Lafayette, IN 47097, USA.Department of Entomology, Kansas State University, Manhattan, KS 66056, USA; The Research Institute of Resource Insects, Chinese Academy of Forestry, Bailongsi, Kunming 650224, People's Republic of China.Department of Entomology, Purdue University, West Lafayette, IN 47097, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.KSU Bioinformatics Center, Division of Biology, Kansas State University, Manhattan, KS 66506, USA.Department of Genetic Medicine and Development, University of Geneva Medical School, Rue Michel-Servet 1, 1211 Geneva, Switzerland; Swiss Institute of Bioinformatics, Rue Michel-Servet 1, 1211 Geneva, Switzerland; Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, 32 Vassar Street, Cambridge, MA 02139, USA; The Broad Institute of MIT and Harvard, 7 Cambridge Center, Cambridge, MA 02142, USA.Department of Biology, University of Rochester, Rochester, NY 14627, USA.Department of Biology, Lund University, 223 62 Lund, Sweden.The University of Chicago Bioinformatics Core, Biological Sciences Division, Center for Research Informatics, The University of Chicago, Chicago, IL 60637, USA; Department of Biological Sciences, Wayne State University, Detroit, MI 48202, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Department of Biological Sciences, University of Notre Dame, IN 46556, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.KSU Bioinformatics Center, Division of Biology, Kansas State University, Manhattan, KS 66506, USA; Department of Computer and Information Science, Kansas State University, Manhattan, KS 66506, USA.Department of Biology, National University of Ireland Maynooth, Maynooth, Ireland.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.International Center for Agricultural Research in the Dry Areas (ICARDA), Rabat BP 6299, Morocco.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Department of Biological Sciences, Wayne State University, Detroit, MI 48202, USA.Department of Botany, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.KSU Bioinformatics Center, Division of Biology, Kansas State University, Manhattan, KS 66506, USA.Center for Functional and Comparative Insect Genomics, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen, Denmark.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Center for Functional and Comparative Insect Genomics, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen, Denmark.KSU Bioinformatics Center, Division of Biology, Kansas State University, Manhattan, KS 66506, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Department of Genetic Medicine and Development, University of Geneva Medical School, Rue Michel-Servet 1, 1211 Geneva, Switzerland; Swiss Institute of Bioinformatics, Rue Michel-Servet 1, 1211 Geneva, Switzerland.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.USDA-ARS, Department of Entomology, Purdue University, West Lafayette, IN 47907, USA.KSU Bioinformatics Center, Division of Biology, Kansas State University, Manhattan, KS 66506, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.USDA-ARS, Department of Entomology, Kansas State University, Manhattan, KS 66056, USA.Department of Biology, Lund University, 223 62 Lund, Sweden.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.KSU Bioinformatics Center, Division of Biology, Kansas State University, Manhattan, KS 66506, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Department of Entomology, Purdue University, West Lafayette, IN 47097, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Department of Entomology, University of Illinois at Urbana-Champaign, 320 Morrill Hall, 505 South Goodwin Avenue, Urbana, IL 61801, USA.USDA-ARS, Department of Entomology, Purdue University, West Lafayette, IN 47907, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Department of Entomology, Purdue University, West Lafayette, IN 47097, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Department of Agronomy, Purdue University, West Lafayette, IN 47907, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.College of Life and Environment Sciences, Minzu University, Beijing 100081, China.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.USDA-ARS, Department of Agronomy, Purdue University, West Lafayette, IN 47907 USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.Department of Entomology, North Dakota State University, Fargo, ND 58108, USA.USDA-ARS, Department of Entomology, Purdue University, West Lafayette, IN 47907, USA.Department of Biology, University of Rochester, Rochester, NY 14627, USA.Department of Genetic Medicine and Development, University of Geneva Medical School, Rue Michel-Servet 1, 1211 Geneva, Switzerland; Swiss Institute of Bioinformatics, Rue Michel-Servet 1, 1211 Geneva, Switzerland.USDA-ARS, Department of Entomology, Kansas State University, Manhattan, KS 66056, USA.KSU Bioinformatics Center, Division of Biology, Kansas State University, Manhattan, KS 66506, USA.Department of Entomology, Purdue University, West Lafayette, IN 47097, USA.Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA. Electronic address: stephenr@bcm.edu.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

25660540

Citation

Zhao, Chaoyang, et al. "A Massive Expansion of Effector Genes Underlies Gall-formation in the Wheat Pest Mayetiola Destructor." Current Biology : CB, vol. 25, no. 5, 2015, pp. 613-20.
Zhao C, Escalante LN, Chen H, et al. A massive expansion of effector genes underlies gall-formation in the wheat pest Mayetiola destructor. Curr Biol. 2015;25(5):613-20.
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 : CB, 25(5), 613-20. https://doi.org/10.1016/j.cub.2014.12.057
Zhao C, et al. A Massive Expansion of Effector Genes Underlies Gall-formation in the Wheat Pest Mayetiola Destructor. Curr Biol. 2015 Mar 2;25(5):613-20. PubMed PMID: 25660540.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - A massive expansion of effector genes underlies gall-formation in the wheat pest Mayetiola destructor. AU - Zhao,Chaoyang, AU - Escalante,Lucio Navarro, AU - Chen,Hang, AU - Benatti,Thiago R, AU - Qu,Jiaxin, AU - Chellapilla,Sanjay, AU - Waterhouse,Robert M, AU - Wheeler,David, AU - Andersson,Martin N, AU - Bao,Riyue, AU - Batterton,Matthew, AU - Behura,Susanta K, AU - Blankenburg,Kerstin P, AU - Caragea,Doina, AU - Carolan,James C, AU - Coyle,Marcus, AU - El-Bouhssini,Mustapha, AU - Francisco,Liezl, AU - Friedrich,Markus, AU - Gill,Navdeep, AU - Grace,Tony, AU - Grimmelikhuijzen,Cornelis J P, AU - Han,Yi, AU - Hauser,Frank, AU - Herndon,Nicolae, AU - Holder,Michael, AU - Ioannidis,Panagiotis, AU - Jackson,LaRonda, AU - Javaid,Mehwish, AU - Jhangiani,Shalini N, AU - Johnson,Alisha J, AU - Kalra,Divya, AU - Korchina,Viktoriya, AU - Kovar,Christie L, AU - Lara,Fremiet, AU - Lee,Sandra L, AU - Liu,Xuming, AU - Löfstedt,Christer, AU - Mata,Robert, AU - Mathew,Tittu, AU - Muzny,Donna M, AU - Nagar,Swapnil, AU - Nazareth,Lynne V, AU - Okwuonu,Geoffrey, AU - Ongeri,Fiona, AU - Perales,Lora, AU - Peterson,Brittany F, AU - Pu,Ling-Ling, AU - Robertson,Hugh M, AU - Schemerhorn,Brandon J, AU - Scherer,Steven E, AU - Shreve,Jacob T, AU - Simmons,DeNard, AU - Subramanyam,Subhashree, AU - Thornton,Rebecca L, AU - Xue,Kun, AU - Weissenberger,George M, AU - Williams,Christie E, AU - Worley,Kim C, AU - Zhu,Dianhui, AU - Zhu,Yiming, AU - Harris,Marion O, AU - Shukle,Richard H, AU - Werren,John H, AU - Zdobnov,Evgeny M, AU - Chen,Ming-Shun, AU - Brown,Susan J, AU - Stuart,Jeffery J, AU - Richards,Stephen, Y1 - 2015/02/05/ PY - 2014/10/30/received PY - 2014/12/07/revised PY - 2014/12/23/accepted PY - 2015/2/10/entrez PY - 2015/2/11/pubmed PY - 2016/1/15/medline SP - 613 EP - 20 JF - Current biology : CB JO - Curr Biol VL - 25 IS - 5 N2 - 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. SN - 1879-0445 UR - https://www.unboundmedicine.com/medline/citation/25660540/A_massive_expansion_of_effector_genes_underlies_gall_formation_in_the_wheat_pest_Mayetiola_destructor_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S0960-9822(14)01695-9 DB - PRIME DP - Unbound Medicine ER -