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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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Phylogenetic relationships and gene orthology based on the genomes of 15 arthropod species. (A) phylogenetic relations of BPH to insects and other arthropods based on single-copy orthologous genes obtained from full genomes. Thirteen insect species were used for the analysis, including Bombyx mori, Danaus plexippus, Anopheles gambiae, Aedes aegypti, Drosophila melanogaster, Tribolium castaneum, Apis mellifera, Camponotus floridanus, Nasonia vitripennis, Pediculus humanus, Rhodnius prolixus, Nilaparvata lugens, and Acyrthosiphon pisum. Two Arthropoda animals (Daphnia pulex, Tetranychus urticae) were used as outgroup taxa. Branch lengths represents divergence times estimated by second codon positions of 318 single-copy genes (Table S17 in Additional file 1) using PhyML [80,81], with a gamma distribution across sites and an HKY85 substitution model. The branch supports were inferred based on approximate likelihood ratio test (aLRT) (B) Gene orthology comparison among the genomes of 15 arthropod species. Note: the order of the 15 species follows that in Figure 3A. 1:1:1 refers to single-copy gene orthologs found across all 15 lineages. N:N:N refers to multi-copy gene paralogs found across all 15 lineages. Diptera, Lepidoptera, Hymenoptera, Hemiptera, and Insect refer to taxon-specific genes that are present only in the relevant lineage. SD indicates species-specific genes in multiple copies. ND indicates species-specific genes in single copies.
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Fig3: Phylogenetic relationships and gene orthology based on the genomes of 15 arthropod species. (A) phylogenetic relations of BPH to insects and other arthropods based on single-copy orthologous genes obtained from full genomes. Thirteen insect species were used for the analysis, including Bombyx mori, Danaus plexippus, Anopheles gambiae, Aedes aegypti, Drosophila melanogaster, Tribolium castaneum, Apis mellifera, Camponotus floridanus, Nasonia vitripennis, Pediculus humanus, Rhodnius prolixus, Nilaparvata lugens, and Acyrthosiphon pisum. Two Arthropoda animals (Daphnia pulex, Tetranychus urticae) were used as outgroup taxa. Branch lengths represents divergence times estimated by second codon positions of 318 single-copy genes (Table S17 in Additional file 1) using PhyML [80,81], with a gamma distribution across sites and an HKY85 substitution model. The branch supports were inferred based on approximate likelihood ratio test (aLRT) (B) Gene orthology comparison among the genomes of 15 arthropod species. Note: the order of the 15 species follows that in Figure 3A. 1:1:1 refers to single-copy gene orthologs found across all 15 lineages. N:N:N refers to multi-copy gene paralogs found across all 15 lineages. Diptera, Lepidoptera, Hymenoptera, Hemiptera, and Insect refer to taxon-specific genes that are present only in the relevant lineage. SD indicates species-specific genes in multiple copies. ND indicates species-specific genes in single copies.

Mentions: We compared the annotated BPH genes with those of 12 insect and 2 other arthropod species with annotated genome sequences publically available, and identified 16,330 Treefam-method-defined BPH species-specific genes (59% of the whole gene set; Table 1, Figure 3B; Table S17 and Figure S11 in Additional file 1), indicating that only 40.8% of the 27,571 identified Nilaparvata protein-coding genes share detectable homology with other available Arthropoda proteomes. We also detected 2,421 conservative genes among all of the 15 genomes examined, including 318 strict single-copy orthologous genes (Table S17 in Additional file 1). A phylogenetic reconstruction using all 318 orthologs (of which the second codon positions comprise 219,780 sites) across the 15 arthropod taxa (Figure 3A; Figure S12 in Additional file 1) reveals that BPH is a sister taxon to the true bug R. prolixus, and together form a sister lineage to the pea aphid. The evidence for this relationship supports a monophyletic Hemiptera while rejecting ‘Homoptera’ [24].Figure 3


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)

Phylogenetic relationships and gene orthology based on the genomes of 15 arthropod species. (A) phylogenetic relations of BPH to insects and other arthropods based on single-copy orthologous genes obtained from full genomes. Thirteen insect species were used for the analysis, including Bombyx mori, Danaus plexippus, Anopheles gambiae, Aedes aegypti, Drosophila melanogaster, Tribolium castaneum, Apis mellifera, Camponotus floridanus, Nasonia vitripennis, Pediculus humanus, Rhodnius prolixus, Nilaparvata lugens, and Acyrthosiphon pisum. Two Arthropoda animals (Daphnia pulex, Tetranychus urticae) were used as outgroup taxa. Branch lengths represents divergence times estimated by second codon positions of 318 single-copy genes (Table S17 in Additional file 1) using PhyML [80,81], with a gamma distribution across sites and an HKY85 substitution model. The branch supports were inferred based on approximate likelihood ratio test (aLRT) (B) Gene orthology comparison among the genomes of 15 arthropod species. Note: the order of the 15 species follows that in Figure 3A. 1:1:1 refers to single-copy gene orthologs found across all 15 lineages. N:N:N refers to multi-copy gene paralogs found across all 15 lineages. Diptera, Lepidoptera, Hymenoptera, Hemiptera, and Insect refer to taxon-specific genes that are present only in the relevant lineage. SD indicates species-specific genes in multiple copies. ND indicates species-specific genes in single copies.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig3: Phylogenetic relationships and gene orthology based on the genomes of 15 arthropod species. (A) phylogenetic relations of BPH to insects and other arthropods based on single-copy orthologous genes obtained from full genomes. Thirteen insect species were used for the analysis, including Bombyx mori, Danaus plexippus, Anopheles gambiae, Aedes aegypti, Drosophila melanogaster, Tribolium castaneum, Apis mellifera, Camponotus floridanus, Nasonia vitripennis, Pediculus humanus, Rhodnius prolixus, Nilaparvata lugens, and Acyrthosiphon pisum. Two Arthropoda animals (Daphnia pulex, Tetranychus urticae) were used as outgroup taxa. Branch lengths represents divergence times estimated by second codon positions of 318 single-copy genes (Table S17 in Additional file 1) using PhyML [80,81], with a gamma distribution across sites and an HKY85 substitution model. The branch supports were inferred based on approximate likelihood ratio test (aLRT) (B) Gene orthology comparison among the genomes of 15 arthropod species. Note: the order of the 15 species follows that in Figure 3A. 1:1:1 refers to single-copy gene orthologs found across all 15 lineages. N:N:N refers to multi-copy gene paralogs found across all 15 lineages. Diptera, Lepidoptera, Hymenoptera, Hemiptera, and Insect refer to taxon-specific genes that are present only in the relevant lineage. SD indicates species-specific genes in multiple copies. ND indicates species-specific genes in single copies.
Mentions: We compared the annotated BPH genes with those of 12 insect and 2 other arthropod species with annotated genome sequences publically available, and identified 16,330 Treefam-method-defined BPH species-specific genes (59% of the whole gene set; Table 1, Figure 3B; Table S17 and Figure S11 in Additional file 1), indicating that only 40.8% of the 27,571 identified Nilaparvata protein-coding genes share detectable homology with other available Arthropoda proteomes. We also detected 2,421 conservative genes among all of the 15 genomes examined, including 318 strict single-copy orthologous genes (Table S17 in Additional file 1). A phylogenetic reconstruction using all 318 orthologs (of which the second codon positions comprise 219,780 sites) across the 15 arthropod taxa (Figure 3A; Figure S12 in Additional file 1) reveals that BPH is a sister taxon to the true bug R. prolixus, and together form a sister lineage to the pea aphid. The evidence for this relationship supports a monophyletic Hemiptera while rejecting ‘Homoptera’ [24].Figure 3

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