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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.

SUBMITTER: Xue J

PROVIDER: S-EPMC4269174 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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

Xue Jian J Zhou Xin X Zhang Chuan-Xi CX Yu Li-Li LL Fan Hai-Wei HW Wang Zhuo Z Xu Hai-Jun HJ Xi Yu Y Zhu Zeng-Rong ZR Zhou Wen-Wu WW Pan Peng-Lu PL Li Bao-Ling BL Colbourne John K JK Noda Hiroaki H Suetsugu Yoshitaka Y Kobayashi Tetsuya T Zheng Yuan Y Liu Shanlin S Zhang Rui R Liu Yang Y Luo Ya-Dan YD Fang Dong-Ming DM Chen Yan Y Zhan Dong-Liang DL Lv Xiao-Dan XD Cai Yue Y Wang Zhao-Bao ZB Huang Hai-Jian HJ Cheng Ruo-Lin RL Zhang Xue-Chao XC Lou Yi-Han YH Yu Bing B Zhuo Ji-Chong JC Ye Yu-Xuan YX Zhang Wen-Qing WQ Shen Zhi-Cheng ZC Yang Huan-Ming HM Wang Jian J Wang Jun J Bao Yan-Yuan YY Cheng Jia-An JA

Genome biology 20141203 12

<h4>Background</h4>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 selectio ...[more]

PMID: 25609551

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Project description:Brown planthopper (Nilaparvata lugens Stål, BPH) is one of the most destructive insects affecting rice production. To better understand the physiological mechanisms of how rice responds to BPH feeding, we analyzed BPH-induced transcriptomic and metabolic changes in leaf sheaths of both BPH-susceptible and -resistant rice varieties. Our results demonstrated that the resistant rice reduced the settling, feeding and growth of BPH. Metabolic analyses indicated that BPH infestation caused more drastic overall metabolic changes in the susceptible variety than the resistant rice. Differently accumulated metabolites (DAMs) belonging to flavonoids were downregulated in the susceptible rice but upregulated in resistant variety. Transcriptomic analyses revealed more differentially expressed genes (DEGs) in susceptible rice than resistant rice, and DEGs related to stimulus were significantly upregulated in resistant rice but downregulated in susceptible rice. Combined analyses of transcriptome and metabolome showed that many DEGs and DAMs were enriched in phenylpropane biosynthesis, flavonoid biosynthesis, and plant hormone signal transduction. We conducted correlation analyses of DEGs and DAMs in these pathways and found a high correlation between DEGs and DAMs. Then, we found that the contents of endogenous indole 3-acetic acid (IAA) in resistant rice was lower than that of susceptible rice after BPH feeding, while the salicylic acid (SA) content was the opposite. For functional analysis, an exogenous application of IAA decreased rice resistance to BPH, but the exogenous application of SA increased resistance. In addition, biochemical assessment and quantitative PCR analysis showed that the lignin content of resistant accession was constitutively higher than in susceptible accession. By adding epigallocatechin, the substrate of anthocyanidin reductase (ANR), to the artificial diet decreased the performance of BPH. We first combined a transcriptome-metabolome-wide association study (TMWAS) on rice resistance to BPH in this study. We demonstrated that rice promoted resistance to BPH by inducing epigallocatechin and decreasing IAA. These findings provided useful transcriptomic and metabolic information for understanding the rice-BPH interactions.

Dataset Information

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

Publications

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

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