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. 2024 Feb 7;14(2):jkad289.
doi: 10.1093/g3journal/jkad289.

High-quality genome of the zoophytophagous stink bug, Nesidiocoris tenuis, informs their food habit adaptation

Tomofumi Shibata  1   2 , Masami Shimoda  2 , Tetsuya Kobayashi  1 , Hiroshi Arai  1 , Yuta Owashi  1 , Takuya Uehara  1
Affiliations

High-quality genome of the zoophytophagous stink bug, Nesidiocoris tenuis, informs their food habit adaptation

Tomofumi Shibata et al. G3 (Bethesda). .

Abstract

The zoophytophagous stink bug, Nesidiocoris tenuis, is a promising natural enemy of micro-pests such as whiteflies and thrips. This bug possesses both phytophagous and entomophagous food habits, enabling it to obtain nutrition from both plants and insects. This trait allows us to maintain its population density in agricultural fields by introducing insectary plants, even when the pest prey density is extremely low. However, if the bugs' population becomes too dense, they can sometimes damage crop plants. This dual character seems to arise from the food preferences and chemosensation of this predator. To understand the genomic landscape of N. tenuis, we examined the whole genome sequence of a commercially available Japanese strain. We used long-read sequencing and Hi-C analysis to assemble the genome at the chromosomal level. We then conducted a comparative analysis of the genome with previously reported genomes of phytophagous and hematophagous stink bugs to focus on the genetic factors contributing to this species' herbivorous and carnivorous tendencies. Our findings suggest that the gustatory gene set plays a pivotal role in adapting to food habits, making it a promising target for selective breeding. Furthermore, we identified the whole genomes of microorganisms symbiotic with this species through genomic analysis. We believe that our results shed light on the food habit adaptations of N. tenuis and will accelerate breeding efforts based on new breeding techniques for natural enemy insects, including genomics and genome editing.

Keywords: IPM; food habit; natural enemy; zoophytophagous.

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Conflict of interest statement

Conflicts of interest The authors declare no conflicts of interest.

Figures

Fig. 1.
Fig. 1.
Overviews of the life history of Nesidiocoris tenuis and the pipeline used for genome analysis. a) Adult male of Nesidiocoris tenuis on a tomato leaf, b) schematic picture of the bug’s zoophytophagy, and c) pipeline of genome assembly and analysis. Cylindrical icons indicate read data and arrows show flow of processed data. The software used and the version in this pipeline are summarized in Supplementary Table 1.
Fig. 2.
Fig. 2.
Comparisons of repeated sequences and genome landscapes in hemipteran chromosomes. a) Comparison of repeated sequences from this study and from that of Ferguson et al. (2021), b) Venn diagram analysis of all annotated genes in Nesidiocoris tenuis (Nt) with Apolygus lucorum (Al), Pachypeltis micranthus (Pm), and Cimex lectularius (Cl), and c) synteny analysis of Nt with Al and Pm.
Fig. 3.
Fig. 3.
Phylogenetic analysis of symbiotic microorganisms. Phylogenetic trees based on the 16S rRNA genes of Spiroplasma and Rickettsia were inferred using the maximum likelihood method on the basis of the Kimura two-parameter model with 1,000 bootstrap replicates. Bootstrap values <60% are not shown, and accession numbers are given after each operational taxonomic unit. a) Phylogenetic tree of Spiroplasma, based on 1,477 positions of the 16S rRNA coding region. The classification of Spiroplasma is represented on the right side and grouped into the citri–poulsonii clade. The outgroup is Erysipelothrix larvae and the scale bar indicates 0.02 substitutions per site. b) Phylogenetic tree of Rickettsia, based on 1,402 positions of the 16S rRNA coding region. The classification of Rickettsia is represented on the right side and grouped into the bellii clade. The outgroup is Orientia tsutsugamushi and the scale bar indicates 0.02 substitutions per site.
Fig. 4.
Fig. 4.
Comparison of annotated genes in closely related hemipteran species. a) Phylogenetic tree of closely related stink bugs and b) comparison of the number of annotated genes. Colors representing species in the left panel a) correspond to those in the right panel b). c) Comparison of chemosensory receptor genes. Abbreviations are as follows: ND, unclustered genes specific to each species; SD, species-specific genes with multiple gene copies; Miridae, Miridae-genus-specific genes; N-N-N, multicopy universal genes; 1-1-1, single-copy universal genes.
Fig. 5.
Fig. 5.
Phylogenetic analysis of chemosensory genes. Phylogenetic trees of a) olfactory and b) gustatory genes. Black circles indicate branches with bootstrap values of 80% or higher. The gray highlights indicate a clade consisting of three species from Miridae (Apolygus lucorum, Nesidiocoris tenuis, and Pachypeltis micranthus), while the green highlights represent a clade comprising four species with herbivorous feeding habits (A. lucorum, N. tenuis, P. micranthus, and Orius laevigatus). Each clade is characterized by the presence of at least five genes. Commonly found insect chemosensory receptor genes, such as olfactory coreceptor (Orco) and sweet, bitter, and CO2 GRs are shown.
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