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

Xue J, Zhou X, Zhang CX, Yu LL, Fan HW, Wang Z, Xu HJ, Xi Y, Zhu ZR, Zhou WW, Pan PL, Li BL, Colbourne JK, Noda H, Suetsugu Y, Kobayashi T, Zheng Y, Liu S, Zhang R, Liu Y, Luo YD, Fang DM, Chen Y, Zhan DL, Lv XD, Cai Y, Wang ZB, Huang HJ, Cheng RL, Zhang XC, Lou YH, Yu B, Zhuo JC, Ye YX, Zhang WQ, Shen ZC, Yang HM, Wang J, Wang J, Bao YY, Cheng JA - Genome Biol. (2014)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

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.

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Related in: MedlinePlus

The brown planthopper. (A) Short-winged (brachypterous) and long-winged (macropterous) female adults and nymph. (B) Schematic diagram of BPH distribution worldwide and possible northward migratory routes (arrows) in East China.
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Fig1: The brown planthopper. (A) Short-winged (brachypterous) and long-winged (macropterous) female adults and nymph. (B) Schematic diagram of BPH distribution worldwide and possible northward migratory routes (arrows) in East China.

Mentions: The brown planthopper (BPH), Nilaparvata lugens (Stål) (Hemiptera: Delphacidae) (Figure 1A), has become the most destructive pest for rice (Oryza sativa) - the major food source for half of the world’s population - since Asian farmers adopted green revolution technologies in the 1960s, that is, agricultural practices using genetically improved cultivars, synthetic fertilizers and pesticides [1]. BPH is equipped with special biological features that enable frequent outbreaks of it in condensed rice paddy fields, which have been used continuously for monoculture across large areas of Asia, under heavy use of nitrogen fertilizer and insecticides. Features contributing to the success of the insect include its mystical capacity to live on a sole host plant and to overcome host plant resistance, association with multiple endosymbionts, high fecundity, and long distance migration (Figure 1A,B). Although various new rice varieties with high resistance to BPH and new insecticides, as well as integrated pest management (IPM) programs, have been developed and implemented, Asian countries have continually experienced serious outbreaks of BPH in the new century. Approximately 10 to 20 million hectares of rice fields were destroyed by BPH through direct sucking and transmittal of ragged stunt virus and grassy stunt virus in 2005 [2,3].Figure 1


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

Xue J, Zhou X, Zhang CX, Yu LL, Fan HW, Wang Z, Xu HJ, Xi Y, Zhu ZR, Zhou WW, Pan PL, Li BL, Colbourne JK, Noda H, Suetsugu Y, Kobayashi T, Zheng Y, Liu S, Zhang R, Liu Y, Luo YD, Fang DM, Chen Y, Zhan DL, Lv XD, Cai Y, Wang ZB, Huang HJ, Cheng RL, Zhang XC, Lou YH, Yu B, Zhuo JC, Ye YX, Zhang WQ, Shen ZC, Yang HM, Wang J, Wang J, Bao YY, Cheng JA - Genome Biol. (2014)

The brown planthopper. (A) Short-winged (brachypterous) and long-winged (macropterous) female adults and nymph. (B) Schematic diagram of BPH distribution worldwide and possible northward migratory routes (arrows) in East China.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4269174&req=5

Fig1: The brown planthopper. (A) Short-winged (brachypterous) and long-winged (macropterous) female adults and nymph. (B) Schematic diagram of BPH distribution worldwide and possible northward migratory routes (arrows) in East China.
Mentions: The brown planthopper (BPH), Nilaparvata lugens (Stål) (Hemiptera: Delphacidae) (Figure 1A), has become the most destructive pest for rice (Oryza sativa) - the major food source for half of the world’s population - since Asian farmers adopted green revolution technologies in the 1960s, that is, agricultural practices using genetically improved cultivars, synthetic fertilizers and pesticides [1]. BPH is equipped with special biological features that enable frequent outbreaks of it in condensed rice paddy fields, which have been used continuously for monoculture across large areas of Asia, under heavy use of nitrogen fertilizer and insecticides. Features contributing to the success of the insect include its mystical capacity to live on a sole host plant and to overcome host plant resistance, association with multiple endosymbionts, high fecundity, and long distance migration (Figure 1A,B). Although various new rice varieties with high resistance to BPH and new insecticides, as well as integrated pest management (IPM) programs, have been developed and implemented, Asian countries have continually experienced serious outbreaks of BPH in the new century. Approximately 10 to 20 million hectares of rice fields were destroyed by BPH through direct sucking and transmittal of ragged stunt virus and grassy stunt virus in 2005 [2,3].Figure 1

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

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.

Show MeSH
Related in: MedlinePlus