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Background Host adaptation is the primary determinant of insect diversification. However, knowledge of different host ranges in closely related species remains scarce. The brown planthopper (Nilaparvata lugens, BPH) and the small brown planthopper (Laodelphax striatellus, SBPH) are the most destructive insect pests within the family Delphacidae. These two species differ in their host range (SBPH can well colonize rice and wheat plants, whereas BPH survives on only rice plants), but the underlying mechanism of this difference remains unknown. High-throughput sequencing provides a powerful approach for analyzing the association between changes in gene expression and the physiological responses of insects. Therefore, gut transcriptomes were performed to elucidate the genes associated with host adaptation in planthoppers. The comparative analysis of planthopper responses to different diets will improve our knowledge of host adaptation regarding herbivorous insects. Results In the present study, we analyzed the change in gene expression of SBPHs that were transferred from rice plants to wheat plants over the short term (rSBPH vs tSBPH) or were colonized on wheat plants over the long term (rSBPH vs wSBPH). The results showed that the majority of differentially expressed genes in SBPH showed similar changes in expression for short-term transfer and long-term colonization. Based on a comparative analysis of BPH and SBPH after transfer, the genes associated with sugar transporters and heat-shock proteins showed similar variation. However, most of the genes were differentially regulated between the two species. The detoxification-related genes were upregulated in SBPH after transfer from the rice plants to the wheat plants, but these genes were downregulated in BPH under the same conditions. In contrast, ribosomal-related genes were downregulated in SBPH after transfer, but these genes were upregulated in BPH under the same conditions. Conclusions The results of this study provide evidence that host plants played a dominant role in shaping gene expression and that the low fitness of BPH on wheat plants might be determined within 24 h after transfer. This study deepens our understanding of different host ranges for the two planthopper species, which may provide a potential strategy for pest management.

The cytochrome P450 monooxygenase (P450) gene family has an important role in detoxifying host plant allelochemicals and pesticides. In this study, we screened differentially expressed genes of the small brown planthopper (Laodelphax striatellus, SBPHs) that were reared for more than ten generations on rice and wheat plants, and found that only a few P450s were associated with host adaptation. LsCYP4DE1, whose expression was 9.5-fold higher in the wheat-adapted SBPH (wSBPH) than in the rice-adapted SBPH (rSBPH), appeared to have an important role in the colonization of wheat plants. Knocking down the expression of LsCYP4DE1 led to increased mortality, as well as decreased performance of SBPHs reared on wheat. However, no significant difference was found in dsLsCYP4DE1-treated SBPHs on rice plants. In addition, LsCYP4DE1 was potentially associated with pesticide tolerance, and suppression of its expression led to increased sensitivity to the pesticide ethiprole. Our results revealed potential roles of LsCYP4DE1 in wheat adaptation and ethiprole tolerance, and provide useful information for pest management.

Extracellular DNA, released by damaged plant cells, acts as a damage-associated molecular pattern (DAMP). We demonstrated previously that the small brown planthopper (Laodelphax striatellus, SBPH) secreted DNase II when feeding on artificial diets. However, the function of DNase II in insect feeding remained elusive. The influences of DNase II on SBPHs and rice plants were investigated by suppressing expression of DNase II or by application of heterogeneously expressed DNase II. We demonstrated that DNase II is mainly expressed in the salivary gland and is responsible for DNA-degrading activity of saliva. Knocking down the expression of DNase II resulted in decreased performance of SBPH reared on rice plants. The dsDNase II-treated SBPH did not influenced jasmonic acid (JA), salicylic acid (SA), ethylene (ET) pathways, but elicited a higher level of H2 O2 and callose accumulation. Application of heterogeneously expressed DNase II in DNase II-deficient saliva slightly reduced the wound-induced defence response. We propose a DNase II-based invading model for SBPH feeding on host plants, and provide a potential target for pest management.