Genes Expressed Differentially in Hessian Fly Larvae Feeding in Resistant and Susceptible Plants

Abstract

The Hessian fly, Mayetiola destructor, is a destructive pest of wheat worldwide and mainly controlled by deploying resistant cultivars. In this study, we investigated the genes that were expressed differentially between larvae in resistant plants and those in susceptible plants through RNA sequencing on the Illumina platform. Informative genes were 11,832, 14,861, 15,708, and 15,071 for the comparisons between larvae in resistant versus susceptible plants for 0.5, 1, 3, and 5 days, respectively, after larvae had reached the feeding site. The transcript abundance corresponding to 5401, 6902, 8457, and 5202 of the informative genes exhibited significant differences (p ≤ 0.05) in the respective paired comparisons. Overall, genes involved in nutrient metabolism, RNA and protein synthesis exhibited lower transcript abundance in larvae from resistant plants, indicating that resistant plants inhibited nutrient metabolism and protein production in larvae. Interestingly, the numbers of cytochrome P450 genes with higher transcript abundance in larvae from resistant plants were comparable to, or higher than those with lower transcript abundance, indicating that toxic chemicals from resistant plants may have played important roles in Hessian fly larval death. Our study also identified several families of genes encoding secreted salivary gland proteins (SSGPs) that were expressed at early stage of 1st instar larvae and with more genes with higher transcript abundance in larvae from resistant plants. Those SSGPs are candidate effectors with important roles in plant manipulation.

Comparative Hessian Fly Larval Transcriptomics Provides Novel Insight into Host and Nonhost Resistance

“…DEGs encoding enzymes in the TCA pathway were represented in our RNA-Seq data by 18 genes ( Figure 14 ). These results are consistent with the expression profiles of genes involved in citric acid cycle and energy metabolism in Hessian fly Biotype GP reported previously [ 33 ]. A higher percentage of genes from this pathway were differentially expressed in virulent larvae feeding on the susceptible wheat line Newton as compared to avirulent larvae feeding on the resistant wheat line Molly [ 33 ].…”

“…RNA-Seq identified several transcriptional changes occurring in Biotype L larvae feeding on both host wheat and nonhost Bd plants. It was necessary to investigate comparisons between the Biotype L larvae on wheat since the previous study [ 33 ] on virulent and avirulent larvae feeding on susceptible (Newton) and resistant (Molly) host wheat, respectively, used the GP (Great Plains) biotype, making a direct comparison with transcriptome changes in Biotype L larvae on nonhost Bd less ideal. Therefore, our current study attempts to directly compare the transcriptome of Biotype L larvae feeding on host wheat and nonhost Bd plants.…”

“…Our RNA-Seq results for DEGs belonging to the cytochrome P450 class revealed that the avirulent larvae had higher transcript abundance of these genes than V3 and Bd3. A previous transcriptome study for the GP Hessian fly biotype revealed 8–10% more genes encoding cytochrome P450s had greater transcript abundance in avirulent larvae feeding on resistant plants as compared to virulent larvae feeding on susceptible plants [ 33 ]. However, amongst up-regulated genes, around 26% of cytochrome P450 genes were up-regulated in V3 compared to 12% in A3 and 24% in Bd3, suggesting that virulent larvae and larvae on Bd plants are able to detoxify more plant-derived allelochemicals than the avirulent larvae can.…”

“…These include genes encoding carboxylestarase, cytochrome P450 (CYP450), glutathione S-transferase (GST), and uridine diphosphate (UDP)-glycosyltransferase (UGT) [38,39]. Increased accumulation of transcripts encoding these detoxification enzymes have been documented previously in other insects [40], as well as virulent Hessian fly larvae feeding on susceptible host wheat [33,[41][42][43]. The transcriptome of A3, V3, and Bd3 larvae revealed differential expression of all four detoxification enzyme classes with 6, 15, 14, and 42 DEGs encoding UGT, carboxylesterase, GST, and CYP450, respectively (Figure 6).…”

“…Illumina RNA-Sequencing (RNA-Seq) was performed on Biotype L larvae feeding on nonhost Bd plants and on avirulent and virulent Biotype L larvae feeding on resistant and susceptible host wheat, respectively. Although a previous study has been undertaken characterizing the differentially expressed genes (DEGs) in Hessian fly larvae, the study was carried out using the Great Plains biotype and only compared transcriptomes of larvae feeding on resistant and susceptible wheat plants, but not nonhost plants [ 33 ]. Our objective was to use the comparative transcriptomics data to understand the molecular mechanisms that are employed by the Hessian fly larvae when they are challenged with different biotic factors presented by resistant and susceptible host wheat and nonhost Bd plants.…”