title: 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.
authors: Department of Entomology, Purdue University, West Lafayette, IN 47097, USA.
authors: Chaoyang
authors: C
authors: Zhao
authors: Department of Entomology, Purdue University, West Lafayette, IN 47097, USA.
authors: Lucio Navarro
authors: LN
authors: Escalante
authors: 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.
authors: Hang
authors: H
authors: Chen
authors: Department of Entomology, Purdue University, West Lafayette, IN 47097, USA.
authors: Thiago R
authors: TR
authors: Benatti
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Jiaxin
authors: J
authors: Qu
authors: KSU Bioinformatics Center, Division of Biology, Kansas State University, Manhattan, KS 66506, USA.
authors: Sanjay
authors: S
authors: Chellapilla
authors: 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.
authors: Robert M
authors: RM
authors: Waterhouse
authors: Department of Biology, University of Rochester, Rochester, NY 14627, USA.
authors: David
authors: D
authors: Wheeler
authors: Department of Biology, Lund University, 223 62 Lund, Sweden.
authors: Martin N
authors: MN
authors: Andersson
authors: 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.
authors: Riyue
authors: R
authors: Bao
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Matthew
authors: M
authors: Batterton
authors: Department of Biological Sciences, University of Notre Dame, IN 46556, USA.
authors: Susanta K
authors: SK
authors: Behura
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Kerstin P
authors: KP
authors: Blankenburg
authors: 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.
authors: Doina
authors: D
authors: Caragea
authors: Department of Biology, National University of Ireland Maynooth, Maynooth, Ireland.
authors: James C
authors: JC
authors: Carolan
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Marcus
authors: M
authors: Coyle
authors: International Center for Agricultural Research in the Dry Areas (ICARDA), Rabat BP 6299, Morocco.
authors: Mustapha
authors: M
authors: El-Bouhssini
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Liezl
authors: L
authors: Francisco
authors: Department of Biological Sciences, Wayne State University, Detroit, MI 48202, USA.
authors: Markus
authors: M
authors: Friedrich
authors: Department of Botany, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.
authors: Navdeep
authors: N
authors: Gill
authors: KSU Bioinformatics Center, Division of Biology, Kansas State University, Manhattan, KS 66506, USA.
authors: Tony
authors: T
authors: Grace
authors: Center for Functional and Comparative Insect Genomics, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen, Denmark.
authors: Cornelis J P
authors: CJ
authors: Grimmelikhuijzen
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Yi
authors: Y
authors: Han
authors: Center for Functional and Comparative Insect Genomics, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen, Denmark.
authors: Frank
authors: F
authors: Hauser
authors: KSU Bioinformatics Center, Division of Biology, Kansas State University, Manhattan, KS 66506, USA.
authors: Nicolae
authors: N
authors: Herndon
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Michael
authors: M
authors: Holder
authors: 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.
authors: Panagiotis
authors: P
authors: Ioannidis
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: LaRonda
authors: L
authors: Jackson
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Mehwish
authors: M
authors: Javaid
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Shalini N
authors: SN
authors: Jhangiani
authors: USDA-ARS, Department of Entomology, Purdue University, West Lafayette, IN 47907, USA.
authors: Alisha J
authors: AJ
authors: Johnson
authors: KSU Bioinformatics Center, Division of Biology, Kansas State University, Manhattan, KS 66506, USA.
authors: Divya
authors: D
authors: Kalra
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Viktoriya
authors: V
authors: Korchina
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Christie L
authors: CL
authors: Kovar
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Fremiet
authors: F
authors: Lara
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Sandra L
authors: SL
authors: Lee
authors: USDA-ARS, Department of Entomology, Kansas State University, Manhattan, KS 66056, USA.
authors: Xuming
authors: X
authors: Liu
authors: Department of Biology, Lund University, 223 62 Lund, Sweden.
authors: Christer
authors: C
authors: Löfstedt
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Robert
authors: R
authors: Mata
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Tittu
authors: T
authors: Mathew
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Donna M
authors: DM
authors: Muzny
authors: KSU Bioinformatics Center, Division of Biology, Kansas State University, Manhattan, KS 66506, USA.
authors: Swapnil
authors: S
authors: Nagar
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Lynne V
authors: LV
authors: Nazareth
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Geoffrey
authors: G
authors: Okwuonu
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Fiona
authors: F
authors: Ongeri
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Lora
authors: L
authors: Perales
authors: Department of Entomology, Purdue University, West Lafayette, IN 47097, USA.
authors: Brittany F
authors: BF
authors: Peterson
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Ling-Ling
authors: LL
authors: Pu
authors: Department of Entomology, University of Illinois at Urbana-Champaign, 320 Morrill Hall, 505 South Goodwin Avenue, Urbana, IL 61801, USA.
authors: Hugh M
authors: HM
authors: Robertson
authors: USDA-ARS, Department of Entomology, Purdue University, West Lafayette, IN 47907, USA.
authors: Brandon J
authors: BJ
authors: Schemerhorn
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Steven E
authors: SE
authors: Scherer
authors: Department of Entomology, Purdue University, West Lafayette, IN 47097, USA.
authors: Jacob T
authors: JT
authors: Shreve
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: DeNard
authors: D
authors: Simmons
authors: Department of Agronomy, Purdue University, West Lafayette, IN 47907, USA.
authors: Subhashree
authors: S
authors: Subramanyam
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Rebecca L
authors: RL
authors: Thornton
authors: College of Life and Environment Sciences, Minzu University, Beijing 100081, China.
authors: Kun
authors: K
authors: Xue
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: George M
authors: GM
authors: Weissenberger
authors: USDA-ARS, Department of Agronomy, Purdue University, West Lafayette, IN 47907 USA.
authors: Christie E
authors: CE
authors: Williams
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Kim C
authors: KC
authors: Worley
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Dianhui
authors: D
authors: Zhu
authors: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
authors: Yiming
authors: Y
authors: Zhu
authors: Department of Entomology, North Dakota State University, Fargo, ND 58108, USA.
authors: Marion O
authors: MO
authors: Harris
authors: USDA-ARS, Department of Entomology, Purdue University, West Lafayette, IN 47907, USA.
authors: Richard H
authors: RH
authors: Shukle
authors: Department of Biology, University of Rochester, Rochester, NY 14627, USA.
authors: John H
authors: JH
authors: Werren
authors: 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.
authors: Evgeny M
authors: EM
authors: Zdobnov
authors: USDA-ARS, Department of Entomology, Kansas State University, Manhattan, KS 66056, USA.
authors: Ming-Shun
authors: MS
authors: Chen
authors: KSU Bioinformatics Center, Division of Biology, Kansas State University, Manhattan, KS 66506, USA.
authors: Susan J
authors: SJ
authors: Brown
authors: Department of Entomology, Purdue University, West Lafayette, IN 47097, USA.
authors: Jeffery J
authors: JJ
authors: Stuart
authors: 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.
authors: Stephen
authors: S
authors: Richards
mesh_terms: D000220:Adaptation, Biological / Q000235:genetics; D000595:Amino Acid Sequence; D000818:Animals; D001483:Base Sequence; D002875:Chromosomes / Q000235:genetics*; D004175:Diptera / Q000235:genetics* / Q000378:metabolism; D007814:Larva / Q000378:metabolism; D008957:Models, Genetic; D008969:Molecular Sequence Data; D005810:Multigene Family / Q000235:genetics*; D010802:Phylogeny; D010941:Plant Tumors / Q000235:genetics*; D017422:Sequence Analysis, DNA; D017385:Sequence Homology; D012726:Sexual Behavior, Animal / Q000502:physiology; D014908:Triticum / Q000469:parasitology*; D020798:Two-Hybrid System Techniques; D044767:Ubiquitin-Protein Ligases / Q000235:genetics
chemical_list: D044767:Ubiquitin-Protein Ligases