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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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Complementary metabolic pathways between the brown planthopper and its yeast-like symbiont. (A) Interactions of the amino acid biosynthetic pathways of BPH and YLS within the fat body (FB). The green and blue areas represent the BPH fat body and endosymbiont cell, respectively. Essential amino acids are represented by solid pink circles and non-essential amino acids by solid blue circles. YLS genes are represented by grey boxes labeled with Enzyme Commission numbers or enzyme names corresponding to the Kyoto Encyclopedia of Genes and Genomes (KEGG) annotation of the YLS genome. BPH genes are represented by red boxes. (B) Genes involved in nitrogen recycling and ammonia assimilation pathways. (C) Genes involved in the steroid biosynthesis pathway. In (B,C), YLS genes are represented by blue ovals with blue numbers representing Enzyme Commission codes corresponding to the KEGG annotation of the genome. BPH genes are represented by pink ovals with pink numbers. Genes identified in both the YLS and BPH genomes are represented by pink ovals with blue numbers. A nonsense mutation was found in the ERG5 gene (red asterisk).
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Fig4: Complementary metabolic pathways between the brown planthopper and its yeast-like symbiont. (A) Interactions of the amino acid biosynthetic pathways of BPH and YLS within the fat body (FB). The green and blue areas represent the BPH fat body and endosymbiont cell, respectively. Essential amino acids are represented by solid pink circles and non-essential amino acids by solid blue circles. YLS genes are represented by grey boxes labeled with Enzyme Commission numbers or enzyme names corresponding to the Kyoto Encyclopedia of Genes and Genomes (KEGG) annotation of the YLS genome. BPH genes are represented by red boxes. (B) Genes involved in nitrogen recycling and ammonia assimilation pathways. (C) Genes involved in the steroid biosynthesis pathway. In (B,C), YLS genes are represented by blue ovals with blue numbers representing Enzyme Commission codes corresponding to the KEGG annotation of the genome. BPH genes are represented by pink ovals with pink numbers. Genes identified in both the YLS and BPH genomes are represented by pink ovals with blue numbers. A nonsense mutation was found in the ERG5 gene (red asterisk).

Mentions: First, annotation of metabolic genes indicated that YLS is able to provide essential amino acids that BPH is unable to synthesize (Figure 4A). We inferred from the BPH genome that, as expected, the insect host lacks the ability to carry out de novo synthesis of 10 essential amino acids (arginine, histidine, isoleucine, leucine, lysine, methionine, phenylalanine, threonine, tryptophan, and valine). Whereas most animals obtain essential amino acids from food, BPH’s sole food source - rice phloem sap - does not provide these necessary nutrients [51]. Thus, it requires an additional supply source. Our YLS genome sequence analysis indicates that this fungal symbiont has evolved a reduced genome size, yet it retains amino acid synthetic pathways that are highly complementary to the host, providing the first genomic evidence that all the genes required for essential amino acid biosynthesis exist in the YLS genome (Table S24 in Additional file 1), and this explains why BPH can survive on artificial diets that are depleted of these critical nutrients [52].Figure 4


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)

Complementary metabolic pathways between the brown planthopper and its yeast-like symbiont. (A) Interactions of the amino acid biosynthetic pathways of BPH and YLS within the fat body (FB). The green and blue areas represent the BPH fat body and endosymbiont cell, respectively. Essential amino acids are represented by solid pink circles and non-essential amino acids by solid blue circles. YLS genes are represented by grey boxes labeled with Enzyme Commission numbers or enzyme names corresponding to the Kyoto Encyclopedia of Genes and Genomes (KEGG) annotation of the YLS genome. BPH genes are represented by red boxes. (B) Genes involved in nitrogen recycling and ammonia assimilation pathways. (C) Genes involved in the steroid biosynthesis pathway. In (B,C), YLS genes are represented by blue ovals with blue numbers representing Enzyme Commission codes corresponding to the KEGG annotation of the genome. BPH genes are represented by pink ovals with pink numbers. Genes identified in both the YLS and BPH genomes are represented by pink ovals with blue numbers. A nonsense mutation was found in the ERG5 gene (red asterisk).
© Copyright Policy - open-access
Related In: Results  -  Collection

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Fig4: Complementary metabolic pathways between the brown planthopper and its yeast-like symbiont. (A) Interactions of the amino acid biosynthetic pathways of BPH and YLS within the fat body (FB). The green and blue areas represent the BPH fat body and endosymbiont cell, respectively. Essential amino acids are represented by solid pink circles and non-essential amino acids by solid blue circles. YLS genes are represented by grey boxes labeled with Enzyme Commission numbers or enzyme names corresponding to the Kyoto Encyclopedia of Genes and Genomes (KEGG) annotation of the YLS genome. BPH genes are represented by red boxes. (B) Genes involved in nitrogen recycling and ammonia assimilation pathways. (C) Genes involved in the steroid biosynthesis pathway. In (B,C), YLS genes are represented by blue ovals with blue numbers representing Enzyme Commission codes corresponding to the KEGG annotation of the genome. BPH genes are represented by pink ovals with pink numbers. Genes identified in both the YLS and BPH genomes are represented by pink ovals with blue numbers. A nonsense mutation was found in the ERG5 gene (red asterisk).
Mentions: First, annotation of metabolic genes indicated that YLS is able to provide essential amino acids that BPH is unable to synthesize (Figure 4A). We inferred from the BPH genome that, as expected, the insect host lacks the ability to carry out de novo synthesis of 10 essential amino acids (arginine, histidine, isoleucine, leucine, lysine, methionine, phenylalanine, threonine, tryptophan, and valine). Whereas most animals obtain essential amino acids from food, BPH’s sole food source - rice phloem sap - does not provide these necessary nutrients [51]. Thus, it requires an additional supply source. Our YLS genome sequence analysis indicates that this fungal symbiont has evolved a reduced genome size, yet it retains amino acid synthetic pathways that are highly complementary to the host, providing the first genomic evidence that all the genes required for essential amino acid biosynthesis exist in the YLS genome (Table S24 in Additional file 1), and this explains why BPH can survive on artificial diets that are depleted of these critical nutrients [52].Figure 4

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