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Comparative Analysis of Different Host Adaptation in Two Rice Planthopper Species

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Comparative Analysis of Different Host Adaptation in Two Rice Planthopper Species Comparative analysis of different host adaptation in two rice planthopper species Hai-Jian Huang Ningbo University Jia-Rong Cui Nanjing Agricultural University Xiao-Yue Hong ( [email protected] ) https://orcid.org/0000-0002-5209-3961 Research article Keywords: Nilaparvata lugens, Laodelphax striatellus, Comparative transcriptome, Host adaptation Posted Date: September 23rd, 2019 DOI: https://doi.org/10.21203/rs.2.14809/v1 License: This work is licensed under a Creative Commons Attribution 4.0 International License. Read Full License Version of Record: A version of this preprint was published on August 17th, 2020. See the published version at https://doi.org/10.1186/s12864-020-06976-2. Page 1/24 Abstract Background The brown planthopper (Nilaparvata lugens, BPH) and small brown planthopper (Laodelphax striatellus, SBPH) are most destructive insect pests belonging to Delphacidae. These two species differ in host range, but the underlying mechanism remained unknown.Results In this work, we compared the gut transcriptome of two planthoppers that colonized on rice, colonized on wheat, and transferred from rice to wheat. We found that the majority of differentially expressed genes in SBPH were Type I responsive, which are plastic and evolved in the same direction. Genes associated with sugar transporters and heat shock proteins showed similar expression trends between BPH and SBPH. However, distinct gene expression variation were found after BPH and SBPH transferring from rice to wheat, with detoxifying-, ribosomal-, and amino acid metabolic-related genes reciprocally regulated.Conclusion The results of this study provide evidence that non-adaptation of BPH on wheat was determined within 24 h after transferring, with the majority of genes regulating in “wrong” way. In contrast, SBPH sophisticatedly response to wheat hosts, with the majority of genes plastic and evolved in same direction. Our study promotes our understanding on herbivore adapting to different food source, and might provide a potential strategy for pest management. Background Each herbivore uses specic host plants to complete their life cycle, and host range is the major determinant of insect diversication [1]. Herbivorous must uptake sucient amount of plant material to satisfy their nutritional demands and, at the meantime, they need to overcome a series of mechanical, chemical and protein-based defenses that posed by their sessile hosts [2, 3]. It is believed that successful host adaptation involves several essential traits of herbivorous insects, including sensing toward right plants, acquire nutrients while avoiding intoxication, and overcome plant defenses. Changes in these essential traits have been reported to cause failure of colonization or even new host specialization in several insect species [4-7]. The brown planthopper (Nilaparvata lugens, BPH) and small brown planthopper (Laodelphax striatellus, SBPH) are closely related insect pests belonging to Delphacidae. Although both planthoppers use rice as main food source, their host range differs. BPH is the monophagous that restricted to rice plants, while SBPH is oligophagous that can feed on rice, wheat, and other gramineous plants. The wider host range facilitates SBPH feeding on other hosts after rice harvest, which is critical for SBPH overwintering. Factors that potentially implicated in different host range of planthoppers have been investigated for decades. Denno & Roderick (1990) presumed that it might be chemical, but not physical barrier that prevent BPH feeding on non-adaptive plant, as the insects could still settle and insert their stylets into plants tissues [8]. Liu et al. (2011) found that feeding on different plants greatly inuence the activity of detoxication enzymes in SBPH, but have little impact on BPH [9], which was in agreement with expanded gene families of cytochrome P450 and ABC transporter in SBPH genome [10]. We further conrmed that upregulation of CYP4DE1 was responsible for successful adaptation of SBPH on wheat host, as LsCYP4DE1-knockdown SBPH showed decreased viability on wheat, but not on rice plant [11]. Page 2/24 Recently, the genomic information of both planthoppers and their host plants (Oryza sativa and Triticum aestivu) have become available [12], and provide an opportunity to study the mechanism of different host adaptation in these non-model insects. Midgut is one of the most important tissues that participated in diet digestion and allelochemical detoxication. Through “Omics” technologies, remodeling of gut physiology in response to different host plants have been investigated in several herbivorous species, especially the Lepidoptera insects. The expression patterns of gut-associated transcripts, including digestive and detoxifying enzymes, transporters, immune and peritrophic genes were reported to be substantially altered when worms exposed to novel diets [13-15]. For generalist worms, profoundly transcriptional changes would be occurred in guts to overcome detrimental effects of plant secondary metabolites; while, for specialist worms, a specic detoxication system avoids activation of a general stress response and minimized the metabolic costs [13, 16], which, on the other hand, might restrain a specialist from adapting to a novel phytotoxin [2]. Our previous work demonstrated that genes associated with wheat adaptation were dramatically remodeled in gut compared with other tissues [11]. It was intriguing to unveil the role of midgut in planthoppers adapting to different hosts. In this study, we compared the performance of BPH and SBPH on different hosts, and proled the global gene expression pattern of SBPH that colony on rice (rSBPH), colonized on wheat (wSBPH), transferred from rice to wheat (tSBPH) by transcriptomic sequencing. The differentially expressed genes (DEGs) that exhibited plastic response and evolved response to wheat plants were classied into four Types. We found that the majority of these genes in SBPH were Type I responsive, which are plastic and evolved in the same direction. In addition, the transcriptomes of BPH that colony on rice (rBPH) and transferred from rice to wheat (tBPH) were also investigated. By comparative analysis, the possible mechanism of different host range of BPH and SBPH were illustrated. Results Performance of planthoppers on rice and wheat plants BPH can well colonize on rice plants, but not on wheat plants, with only the rice-colonized BPH strain (rBPH) generated in laboratory conditions. In contrast, SBPH could successfully colonize on both rice and wheat plants, and two SBPH strains (rSBPH and wSBPH) were maintained in our laboratory for more than 30 generations. Survival analysis demonstrated that more than 90% of rBPH survived on rice plant for 12 days, which is signicantly higher than that on wheat plant (LT50=6.1 day) or provided with water only (LT50=3.3 day) (Fig. 1A). These results indicated that BPH could only survived on wheat sap for short time, but not for long time. For SBPH, both rSBPH and wSBPH can survive on rice and wheat plant successfully (Fig. 1B), in accordance with previous reports [17]. Overview of RNA sequencing data Page 3/24 To explore the mechanism underlying different host adaptation of two planthoppers on wheat plants, guts of planthoppers that colony on rice (rSBPH and rBPH) or wheat plants (wSBPH), or transfer from rice to wheat plants (tSBPH and tBPH) were isolated and underwent Illumina HiSeq2500 sequencing. A total of 15 libraries were generated, with clean reads exceeding 45 million in each library. The clean reads were mapped to their reference genomes [10, 18], respectively. For BPH, there were 75% to 83% clean reads mapped to reference genome. For SBPH, the percentages of mapped clean reads ranged from 60% to 66%. Saturation analysis showed that the number of detected genes decreased as the number of reads increased, and library capacity reached saturation when the number of sequence reads approached 20.0 million (Fig. S1, Supporting information). Principal component analysis (PCA) demonstrated that the three replicates of each treatment were well clustered (Fig. 2). In SBPH, the expression pattern of wSBPH and tSBPH were close-related when compared with that of rSBPH, indicating that host plants have non- negligible inuence on gene expression. Analysis of differentially expressed genes (DEGs) Gene expression changes were analyzed by comparing rice-colony planthopper to transfer planthopper (tSBPH_vs_rSBPH and tBPH_vs_rBPH) and rice-colony planthopper to wheat-colony planthopper (wSBPH_vs_rSBPH) using a threshold of >2 fold change and an FDR adjusted p-value <0.05. For rice- colony planthoppers transferring to wheat, a total of 2,877 and 2,638 genes were differentially expressed in SBPH and BPH, respectively (Fig. 3). There were 2,373 genes up-regulated and 505 genes down- regulated when rSBPH transferred to wheat (Table S1). Among them, genes participated in signal transduction (i.e., Hippo signaling pathway, MAPK signaling pathway, FoxO signaling pathway, IL-17 signaling pathway) were signicantly upregulated. CYP4DE1, which was found to mediate wheat adaptation and ethiprole tolerance in SBPH [11], was also induced after transferring (Fig. 4). In contrast, 71 genes related to ribosomal proteins and 48 genes related to oxidative phosphorylation were signicantly downregulated, indicating a decreased protein production and energy metabolism (Fig. 5). Other genes, such as serine proteinase, sugar transporter, cytochrome c oxidase, and ATP synthase were also downregulated.
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