Comparative analysis of diet-associated responses in two rice planthopper species

Abstract

Background: Host adaptation is the major determinant of insect diversification. However, knowledge of different host ranges in very close-related species remains scarce. The brown planthopper (Nilaparvata lugens, BPH) and small brown planthopper (Laodelphax striatellus, SBPH) are the most destructive insect pests belonging to Delphacidae. These two species differ in the host range (SBPH can well colonize on rice and wheat plants, while BPH survive on rice plants only), but the underlying mechanism still remains unknown. High-throughput sequencing technology provides a powerful approach for analyzing the association between gene expression changes and physiological responses of insects. Therefore, the gut transcriptomes were performed to elucidate the genes associated with host adaptation in planthoppers. Comparative analysis of planthoppers’ responses to different diets would improve our knowledge of host adaptation regarding herbivores insects.Results: In the present study, we analyzed the gene expression change of SBPH that transferred from rice plants to wheat plants in a short term (rSBPH vs tSBPH) and colonized on wheat plants for a long term (rSBPH vs wSBPH). The results showed that the majority of differentially expressed genes in SBPH showed similar expression change between short-term transfer and long-term colonization. Based on the comparative analysis of BPH and SBPH after transferring, genes associated with sugar transporters and heat shock proteins varied similarly. However, most of genes were differentially regulated between two species. The detoxification-related genes were upregulated in SBPH after transferring while downregulated in BPH under the same condition. Ribosomal-related genes were downregulated in SBPH after transferring while upregulated in BPH under the same condition.Conclusion: The results of this study provided evidence that host plants played dominant roles in shaping the gene expression, and unfitness of BPH on wheat plants might be determined within 24 hours after transferring. This study deepens our understanding of different host ranges regarding two planthopper species, which may provide a potential strategy for pest management.

Insight into different host range of three planthoppers by transcriptomic and microbiomic analysis

“…Our previous study has analysed the gut gene expression patterns of BPH and SBPH on rice and wheat plants (Huang et al ., 2020). To explore the potential mechanism underlying the different host adaptation in three planthopper species, we further analysed the responses of WBPH to rice and wheat hosts.…”

“…It is previously demonstrated that genes associated with sugar transporters and heat shock proteins showed similar expression trends; while most genes were reciprocally regulated between BPH and SBPH (Huang et al ., 2020). In this study, we found that sugar transporters (belonged to type I response genes) and heat shock proteins (belonged to type I or type III response genes) showed similar expression variation in three planthoppers, indicating that these genes played conserved roles in coping with host changes.…”

“…Host plants had non‐negligible impacts on genes associated with detoxification, transportation and amino acid metabolism in the three planthoppers (Table S6). The possible functions of these co‐regulated genes have been discussed in our previous work (Huang et al ., 2020). In this study, we found that proteasome‐associated genes were strikingly up‐regulated when WBPH transferred or colonized on wheat plants (belonged to type I responses), which was significantly different from that of BPH or SBPH.…”

“…By contrast, SBPH only move over short distances and feed on a variety of hosts, especially the wheat plants after rice harvest (Hong, 2017; He et al ., 2018). In our previous work, it is demonstrated that a majority of genes in BPH and SBPH were reciprocally regulated when these two planthoppers were transferred from rice to wheat plants (Huang et al ., 2020); besides, the CYP4DE1 gene was responsible for the successful adaptation of SBPH on wheat hosts (Huang et al ., 2018). However, it remains largely unexplored about the wheat adaptation of WBPH, which seldom feed on wheat plants in the wild condition but can utilize wheat plants as a food source.…”

“…This study aimed to investigate (1) the changes in gene expression of three planthoppers in coping with different plants; and (2) the influences of host plants on bacterial communities of three planthoppers. The gut gene expression patterns of BPH and SBPH in response to different host plants have been explored (Huang et al ., 2020). Therefore, we first profiled the gut gene expression patterns of WBPH that colonized rice plants (rWBPH), colonized wheat plants (wWBPH) and was transferred from rice to wheat plants (tWBPH) by transcriptomic sequencing.…”