Genomes of the rice pest brown planthopper and its endosymbionts reveal complex complementary contributions for host adaptation

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Genomes of the rice pest brown planthopper and its endosymbionts reveal complex complementary contributions for host adaptation. / Xue, Jian; Zhou, Xin; Zhang, Chuan-Xi; Yu, Li-Li; Fan, Hai-Wei; Wang, Zhuo; Xu, Hai-Jun; Xi, Yu; Zhu, Zeng-Rong; Zhou, Wen-Wu; Pan, Peng-Lu; Li, Bao-Ling; Colbourne, John K; Noda, Hiroaki; Suetsugu, Yoshitaka; Kobayashi, Tetsuya; Zheng, Yuan; Liu, Shanlin; Zhang, Rui; Liu, Yang; Luo, Ya-Dan; Fang, Dong-Ming; Chen, Yan; Zhan, Dong-Liang; Lv, Xiao-Dan; Cai, Yue; Wang, Zhao-Bao; Huang, Hai-Jian; Cheng, Ruo-Lin; Zhang, Xue-Chao; Lou, Yi-Han; Yu, Bing; Zhuo, Ji-Chong; Ye, Yu-Xuan; Zhang, Wen-Qing; Shen, Zhi-Cheng; Yang, Huan-Ming; Wang, Jian; Wang, Jun; Bao, Yan-Yuan; Cheng, Jia-An.

In: Genome Biol, Vol. 15, No. 12, 521, 03.12.2014.

Research output: Contribution to journalArticlepeer-review

Harvard

Xue, J, Zhou, X, Zhang, C-X, Yu, L-L, Fan, H-W, Wang, Z, Xu, H-J, Xi, Y, Zhu, Z-R, Zhou, W-W, Pan, P-L, Li, B-L, Colbourne, JK, Noda, H, Suetsugu, Y, Kobayashi, T, Zheng, Y, Liu, S, Zhang, R, Liu, Y, Luo, Y-D, Fang, D-M, Chen, Y, Zhan, D-L, Lv, X-D, Cai, Y, Wang, Z-B, Huang, H-J, Cheng, R-L, Zhang, X-C, Lou, Y-H, Yu, B, Zhuo, J-C, Ye, Y-X, Zhang, W-Q, Shen, Z-C, Yang, H-M, Wang, J, Wang, J, Bao, Y-Y & Cheng, J-A 2014, 'Genomes of the rice pest brown planthopper and its endosymbionts reveal complex complementary contributions for host adaptation', Genome Biol, vol. 15, no. 12, 521. https://doi.org/10.1186/s13059-014-0521-0

APA

Xue, J., Zhou, X., Zhang, C-X., Yu, L-L., Fan, H-W., Wang, Z., Xu, H-J., Xi, Y., Zhu, Z-R., Zhou, W-W., Pan, P-L., Li, B-L., Colbourne, J. K., Noda, H., Suetsugu, Y., Kobayashi, T., Zheng, Y., Liu, S., Zhang, R., ... Cheng, J-A. (2014). Genomes of the rice pest brown planthopper and its endosymbionts reveal complex complementary contributions for host adaptation. Genome Biol, 15(12), [521]. https://doi.org/10.1186/s13059-014-0521-0

Vancouver

Author

Xue, Jian ; Zhou, Xin ; Zhang, Chuan-Xi ; Yu, Li-Li ; Fan, Hai-Wei ; Wang, Zhuo ; Xu, Hai-Jun ; Xi, Yu ; Zhu, Zeng-Rong ; Zhou, Wen-Wu ; Pan, Peng-Lu ; Li, Bao-Ling ; Colbourne, John K ; Noda, Hiroaki ; Suetsugu, Yoshitaka ; Kobayashi, Tetsuya ; Zheng, Yuan ; Liu, Shanlin ; Zhang, Rui ; Liu, Yang ; Luo, Ya-Dan ; Fang, Dong-Ming ; Chen, Yan ; Zhan, Dong-Liang ; Lv, Xiao-Dan ; Cai, Yue ; Wang, Zhao-Bao ; Huang, Hai-Jian ; Cheng, Ruo-Lin ; Zhang, Xue-Chao ; Lou, Yi-Han ; Yu, Bing ; Zhuo, Ji-Chong ; Ye, Yu-Xuan ; Zhang, Wen-Qing ; Shen, Zhi-Cheng ; Yang, Huan-Ming ; Wang, Jian ; Wang, Jun ; Bao, Yan-Yuan ; Cheng, Jia-An. / Genomes of the rice pest brown planthopper and its endosymbionts reveal complex complementary contributions for host adaptation. In: Genome Biol. 2014 ; Vol. 15, No. 12.

Bibtex

@article{061a7a0bf95d435c84c7ac49ccc607d6,
title = "Genomes of the rice pest brown planthopper and its endosymbionts reveal complex complementary contributions for host adaptation",
abstract = "BACKGROUND: The brown planthopper, Nilaparvata lugens, the most destructive pest of rice, is a typical monophagous herbivore that feeds exclusively on rice sap, which migrates over long distances. Outbreaks of it have re-occurred approximately every three years in Asia. It has also been used as a model system for ecological studies and for developing effective pest management. To better understand how a monophagous sap-sucking arthropod herbivore has adapted to its exclusive host selection and to provide insights to improve pest control, we analyzed the genomes of the brown planthopper and its two endosymbionts.RESULTS: We describe the 1.14 gigabase planthopper draft genome and the genomes of two microbial endosymbionts that permit the planthopper to forage exclusively on rice fields. Only 40.8% of the 27,571 identified Nilaparvata protein coding genes have detectable shared homology with the proteomes of the other 14 arthropods included in this study, reflecting large-scale gene losses including in evolutionarily conserved gene families and biochemical pathways. These unique genomic features are functionally associated with the animal's exclusive plant host selection. Genes missing from the insect in conserved biochemical pathways that are essential for its survival on the nutritionally imbalanced sap diet are present in the genomes of its microbial endosymbionts, which have evolved to complement the mutualistic nutritional needs of the host.CONCLUSIONS: Our study reveals a series of complex adaptations of the brown planthopper involving a variety of biological processes, that result in its highly destructive impact on the exclusive host rice. All these findings highlight potential directions for effective pest control of the planthopper.",
keywords = "Adaptation, Biological, Animals, Arthropods, Asia, Bacteria, Evolution, Molecular, Genome, Insect, Genomics, Hemiptera, Herbivory, Host Specificity, Molecular Sequence Data, Multigene Family, Oryza, Phylogeny, Sequence Homology, Nucleic Acid, Symbiosis, Brown Planthopper, Fosmid Library, Fosmid Clone, Peritrophic Matrix, Unannotated Gene",
author = "Jian Xue and Xin Zhou and Chuan-Xi Zhang and Li-Li Yu and Hai-Wei Fan and Zhuo Wang and Hai-Jun Xu and Yu Xi and Zeng-Rong Zhu and Wen-Wu Zhou and Peng-Lu Pan and Bao-Ling Li and Colbourne, {John K} and Hiroaki Noda and Yoshitaka Suetsugu and Tetsuya Kobayashi and Yuan Zheng and Shanlin Liu and Rui Zhang and Yang Liu and Ya-Dan Luo and Dong-Ming Fang and Yan Chen and Dong-Liang Zhan and Xiao-Dan Lv and Yue Cai and Zhao-Bao Wang and Hai-Jian Huang and Ruo-Lin Cheng and Xue-Chao Zhang and Yi-Han Lou and Bing Yu and Ji-Chong Zhuo and Yu-Xuan Ye and Wen-Qing Zhang and Zhi-Cheng Shen and Huan-Ming Yang and Jian Wang and Jun Wang and Yan-Yuan Bao and Jia-An Cheng",
year = "2014",
month = dec,
day = "3",
doi = "10.1186/s13059-014-0521-0",
language = "English",
volume = "15",
journal = "Genome Biology",
issn = "1474-7596",
publisher = "BioMed Central",
number = "12",

}

RIS

TY - JOUR

T1 - Genomes of the rice pest brown planthopper and its endosymbionts reveal complex complementary contributions for host adaptation

AU - Xue, Jian

AU - Zhou, Xin

AU - Zhang, Chuan-Xi

AU - Yu, Li-Li

AU - Fan, Hai-Wei

AU - Wang, Zhuo

AU - Xu, Hai-Jun

AU - Xi, Yu

AU - Zhu, Zeng-Rong

AU - Zhou, Wen-Wu

AU - Pan, Peng-Lu

AU - Li, Bao-Ling

AU - Colbourne, John K

AU - Noda, Hiroaki

AU - Suetsugu, Yoshitaka

AU - Kobayashi, Tetsuya

AU - Zheng, Yuan

AU - Liu, Shanlin

AU - Zhang, Rui

AU - Liu, Yang

AU - Luo, Ya-Dan

AU - Fang, Dong-Ming

AU - Chen, Yan

AU - Zhan, Dong-Liang

AU - Lv, Xiao-Dan

AU - Cai, Yue

AU - Wang, Zhao-Bao

AU - Huang, Hai-Jian

AU - Cheng, Ruo-Lin

AU - Zhang, Xue-Chao

AU - Lou, Yi-Han

AU - Yu, Bing

AU - Zhuo, Ji-Chong

AU - Ye, Yu-Xuan

AU - Zhang, Wen-Qing

AU - Shen, Zhi-Cheng

AU - Yang, Huan-Ming

AU - Wang, Jian

AU - Wang, Jun

AU - Bao, Yan-Yuan

AU - Cheng, Jia-An

PY - 2014/12/3

Y1 - 2014/12/3

N2 - BACKGROUND: The brown planthopper, Nilaparvata lugens, the most destructive pest of rice, is a typical monophagous herbivore that feeds exclusively on rice sap, which migrates over long distances. Outbreaks of it have re-occurred approximately every three years in Asia. It has also been used as a model system for ecological studies and for developing effective pest management. To better understand how a monophagous sap-sucking arthropod herbivore has adapted to its exclusive host selection and to provide insights to improve pest control, we analyzed the genomes of the brown planthopper and its two endosymbionts.RESULTS: We describe the 1.14 gigabase planthopper draft genome and the genomes of two microbial endosymbionts that permit the planthopper to forage exclusively on rice fields. Only 40.8% of the 27,571 identified Nilaparvata protein coding genes have detectable shared homology with the proteomes of the other 14 arthropods included in this study, reflecting large-scale gene losses including in evolutionarily conserved gene families and biochemical pathways. These unique genomic features are functionally associated with the animal's exclusive plant host selection. Genes missing from the insect in conserved biochemical pathways that are essential for its survival on the nutritionally imbalanced sap diet are present in the genomes of its microbial endosymbionts, which have evolved to complement the mutualistic nutritional needs of the host.CONCLUSIONS: Our study reveals a series of complex adaptations of the brown planthopper involving a variety of biological processes, that result in its highly destructive impact on the exclusive host rice. All these findings highlight potential directions for effective pest control of the planthopper.

AB - BACKGROUND: The brown planthopper, Nilaparvata lugens, the most destructive pest of rice, is a typical monophagous herbivore that feeds exclusively on rice sap, which migrates over long distances. Outbreaks of it have re-occurred approximately every three years in Asia. It has also been used as a model system for ecological studies and for developing effective pest management. To better understand how a monophagous sap-sucking arthropod herbivore has adapted to its exclusive host selection and to provide insights to improve pest control, we analyzed the genomes of the brown planthopper and its two endosymbionts.RESULTS: We describe the 1.14 gigabase planthopper draft genome and the genomes of two microbial endosymbionts that permit the planthopper to forage exclusively on rice fields. Only 40.8% of the 27,571 identified Nilaparvata protein coding genes have detectable shared homology with the proteomes of the other 14 arthropods included in this study, reflecting large-scale gene losses including in evolutionarily conserved gene families and biochemical pathways. These unique genomic features are functionally associated with the animal's exclusive plant host selection. Genes missing from the insect in conserved biochemical pathways that are essential for its survival on the nutritionally imbalanced sap diet are present in the genomes of its microbial endosymbionts, which have evolved to complement the mutualistic nutritional needs of the host.CONCLUSIONS: Our study reveals a series of complex adaptations of the brown planthopper involving a variety of biological processes, that result in its highly destructive impact on the exclusive host rice. All these findings highlight potential directions for effective pest control of the planthopper.

KW - Adaptation, Biological

KW - Animals

KW - Arthropods

KW - Asia

KW - Bacteria

KW - Evolution, Molecular

KW - Genome, Insect

KW - Genomics

KW - Hemiptera

KW - Herbivory

KW - Host Specificity

KW - Molecular Sequence Data

KW - Multigene Family

KW - Oryza

KW - Phylogeny

KW - Sequence Homology, Nucleic Acid

KW - Symbiosis

KW - Brown Planthopper

KW - Fosmid Library

KW - Fosmid Clone

KW - Peritrophic Matrix

KW - Unannotated Gene

U2 - 10.1186/s13059-014-0521-0

DO - 10.1186/s13059-014-0521-0

M3 - Article

C2 - 25609551

VL - 15

JO - Genome Biology

JF - Genome Biology

SN - 1474-7596

IS - 12

M1 - 521

ER -