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 Gill; Tony Grace; Cornelis 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

doi:10.1016/j.cub.2014.12.057

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 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

Cell and Neurobiology

106 Citations (Scopus)

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 language	English
Journal	Current biology : CB
Volume	25
Issue number	5
Pages (from-to)	613-620
Number of pages	8
ISSN	0960-9822
DOIs	https://doi.org/10.1016/j.cub.2014.12.057
Publication status	Published - 2 Mar 2015

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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), 613-620. https://doi.org/10.1016/j.cub.2014.12.057

Zhao, C, Escalante, LN, Chen, H, Benatti, TR, Qu, J, Chellapilla, S, Waterhouse, RM, Wheeler, D, Andersson, MN, Bao, R, Batterton, M, Behura, SK, Blankenburg, KP, Caragea, D, Carolan, JC, Coyle, M, El-Bouhssini, M, Francisco, L, Friedrich, M, Gill, N, Grace, T, Grimmelikhuijzen, C, Han, Y, Hauser, F, Herndon, N, Holder, M, Ioannidis, P, Jackson, L, Javaid, M, Jhangiani, SN, Johnson, AJ, Kalra, D, Korchina, V, Kovar, CL, Lara, F, Lee, SL, Liu, X, Löfstedt, C, Mata, R, Mathew, T, Muzny, DM, Nagar, S, Nazareth, LV, Okwuonu, G, Ongeri, F, Perales, L, Peterson, BF, Pu, L-L, Robertson, HM, Schemerhorn, BJ, Scherer, SE, Shreve, JT, Simmons, D, Subramanyam, S, Thornton, RL, Xue, K, Weissenberger, GM, Williams, CE, Worley, KC, Zhu, D, Zhu, Y, Harris, MO, Shukle, RH, Werren, JH, Zdobnov, EM, Chen, M-S, Brown, SJ, Stuart, JJ & Richards, S 2015, 'A massive expansion of effector genes underlies gall-formation in the wheat pest Mayetiola destructor', Current biology : CB, vol. 25, no. 5, pp. 613-620. https://doi.org/10.1016/j.cub.2014.12.057

@article{4aacebce8ca54cc8aa76b8718f62797b,

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.",

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

year = "2015",

month = mar,

day = "2",

doi = "10.1016/j.cub.2014.12.057",

language = "English",

volume = "25",

pages = "613--620",

journal = "Current Biology",

issn = "0960-9822",

publisher = "Cell Press",

number = "5",

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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

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

PY - 2015/3/2

Y1 - 2015/3/2

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.

AB - 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.

U2 - 10.1016/j.cub.2014.12.057

DO - 10.1016/j.cub.2014.12.057

M3 - Journal article

C2 - 25660540

SN - 0960-9822

VL - 25

SP - 613

EP - 620

JO - Current Biology

JF - Current Biology

IS - 5

ER -

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

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