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

Abstract

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.

Keywords: Comparative transcriptome; Diet-associated responses; Host adaptation; Laodelphax striatellus; Nilaparvata lugens.

Fig. 1

Survival of planthoppers on rice and wheat plants. a The survival of rBPHs colonizing rice plants, transferred to wheat plants, and provided with water only. b The survival of rSBPH colonizing on rice plants and transferred to wheat plants, and wSBPH colonizing wheat plants. Light shades indicate 95% confidence intervals. Different letters signify significant different survival distributions among each treatment group at P < 0.05 according to the log-rank test

Fig. 2

The number of differentially expressed genes in planthoppers that feed on different hosts. The differentially expressed genes were analyzed by comparing tSBPH to rSBPH, wSBPH to rSBPH, and tBPH to rBPH based on a threshold of > 2-fold change and an FDR-adjusted p-value of < 0.05

Fig. 3

Classification of DEGs in SBPH based on their expression patterns. The expression patterns of identified DEGs in SBPH can be classified into four types: Type I, expression changed in the same direction for short-term transfer and long-term colonization; Type II, expression changed in the opposite direction for short-term transfer and long-term colonization; Type III, expression changed in the short-term transfer, but not in the long-term colonization; Type IV, expression changed in the long-term colonization, but not in the short-term transfer. The number of genes belonging to each type is listed following the heat map. The red and green boxes represent up- and down-regulated genes, respectively, in tSBPH and wSBPH relative to those of rSBPH. The white boxes represent genes that did not change

Fig. 4

Correlation between transcriptomic data and qPCR results in SBPH. The relative expression level of each gene was determined by qPCR (blue) and was compared with the expression of the transcriptomic data (green). a UDP-glucuronosyltransferase, b venom serine carboxypeptidase-like, c sugar transporter, d maltase 2-like, e 60S ribosomal protein, f 40S ribosomal protein, g nucleotide exchange factor SIL1 I, h peroxisomal biogenesis factor 3-like, i 70 kDa heat shock protein, j peptide transporter family 2-like, k cytochrome P450, l ABC transporter of evm. TU.Contig86.54, m ABC transporter of evm. TU.Contig58.174

Fig. 5

Correlation between transcriptomic data and qPCR results in BPH. The relative expression level of each gene was determined by qPCR (blue) and was compared with the expression of the transcriptomic data (green). a cryptopsoridial mucin, b facilitated trehalose transporter Tret1-like of NLU013658.1, c serine proteinase stubble, d peptide methionine sulfoxide reductase, e elongation of very long chain fatty acids protein, f ABC transporter of NLU003498.1, g ABC transporter of NLU013034.1, h cytochrome P450 6A20, i cytochrome P450 4C3, j cuticle protein 16.5-like I, k facilitated trehalose transporter Tret1-like of NLU003716.1, l chemosensory protein 12, m lipid storage droplets surface-binding protein, n small heat shock protein, o 60S ribosomal protein, p 40S ribosomal protein, q heat shock protein