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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

Gene family expansions and contractions in the brown planthopper compared with other arthropod genomes. Numbers for expanded (green) and contracted (red) gene families are shown below branches or taxon names with percentages indicated by pie charts.
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Fig2: Gene family expansions and contractions in the brown planthopper compared with other arthropod genomes. Numbers for expanded (green) and contracted (red) gene families are shown below branches or taxon names with percentages indicated by pie charts.

Mentions: We predicted protein-coding genes using GENEWISE [17], an homology-based method referring to protein sequences from four representative insects and from human. We also used the programs GENSCAN [18] and AUGUSTUS [19] for additional ab initio gene predictions. These results were then combined using GLEAN to generate a consensus gene set [20]. A 2.47 Gbp RNA-seq data set was additionally used to complement the combined gene set. Finally, we created a reference gene set containing 27,571 protein-coding genes for BPH. Among the 15 arthropod genomes compared in this study, the numbers of predicted genes and species-specific genes in BPH were lower than in the pea aphid (Table 1), but higher than those of most other insects. The lack of accumulated knowledge on arthropod genomes in general might have attributed to the elevated species-specific gene components in BPH because sequenced arthropod genomes are limited and highly biased in phylogenetic coverage. For instance, the first sequenced crustacean, the waterflea (Daphnia pulex), has an unexpected proportion of unknown genes (36% of over 30,000 genes) when compared with other genomes [21]. Similarly, as most published insect genomes are from holometabolans, 37% of the predicted genes in the pea aphid (the first basal hemimetabolous species with sequenced genome) could not be matched to any known species [15]. Although the likelihood of overestimation during gene predictions cannot be completely ruled out, the pattern of elevated proportions of species-specific genes is shared among all hemipteran genomes (A. pisum, Rhodnius prolixus, and N. lugens (Figure 2). We expect that a higher level of homology can be discovered when additional genomes are sequenced for more hemipteran insects.Figure 2


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)

Gene family expansions and contractions in the brown planthopper compared with other arthropod genomes. Numbers for expanded (green) and contracted (red) gene families are shown below branches or taxon names with percentages indicated by pie charts.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig2: Gene family expansions and contractions in the brown planthopper compared with other arthropod genomes. Numbers for expanded (green) and contracted (red) gene families are shown below branches or taxon names with percentages indicated by pie charts.
Mentions: We predicted protein-coding genes using GENEWISE [17], an homology-based method referring to protein sequences from four representative insects and from human. We also used the programs GENSCAN [18] and AUGUSTUS [19] for additional ab initio gene predictions. These results were then combined using GLEAN to generate a consensus gene set [20]. A 2.47 Gbp RNA-seq data set was additionally used to complement the combined gene set. Finally, we created a reference gene set containing 27,571 protein-coding genes for BPH. Among the 15 arthropod genomes compared in this study, the numbers of predicted genes and species-specific genes in BPH were lower than in the pea aphid (Table 1), but higher than those of most other insects. The lack of accumulated knowledge on arthropod genomes in general might have attributed to the elevated species-specific gene components in BPH because sequenced arthropod genomes are limited and highly biased in phylogenetic coverage. For instance, the first sequenced crustacean, the waterflea (Daphnia pulex), has an unexpected proportion of unknown genes (36% of over 30,000 genes) when compared with other genomes [21]. Similarly, as most published insect genomes are from holometabolans, 37% of the predicted genes in the pea aphid (the first basal hemimetabolous species with sequenced genome) could not be matched to any known species [15]. Although the likelihood of overestimation during gene predictions cannot be completely ruled out, the pattern of elevated proportions of species-specific genes is shared among all hemipteran genomes (A. pisum, Rhodnius prolixus, and N. lugens (Figure 2). We expect that a higher level of homology can be discovered when additional genomes are sequenced for more hemipteran insects.Figure 2

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