A draft Diabrotica virgifera virgifera genome: insights into control and host plant adaption by a major maize pest insect

Authors: Coates, Brad; WALDEN, KIM - University Of Illinois; LATA, DIMPAL - Illinois Institute Of Technology; VELLICHIRAMMAL, NEETHA - University Of Nebraska; MITCHELL, ROBERT - University Of Wisconsin; ANDERSSON, MARTIN - Lund University; MCKAY, RACHEL - University Of Wisconsin; LORENZEN, MARCE - North Carolina State University; GRUBBS, NATHANIEL - North Carolina State University; WANG, YU-HUI - North Carolina State University; HAN, JINLONG - North Carolina State University; XUAN, JING LI - North Carolina State University; WILLADSEN, PETER - University Of Nebraska; WANG, HUICHUN - University Of Nebraska; French, Bryan; Bansal, Raman; Sedky, Sammy; SOUZA, DARIANE - University Of Florida; BUNN, DAKOTA - Illinois Institute Of Technology; MEINKE, LANCE - University Of Nebraska; MILLER, NICHOLAS - Illinois Institute Of Technology; SIEGFRIED, BLAIR - University Of Florida; Sappington, Thomas; ROBERTSON, HUGH - University Of Illinois

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/4/2022
Publication Date: 1/13/2023
Citation: Coates, B.S., Walden, K.O., Lata, D., Vellichirammal, N.N., Mitchell, R.F., Andersson, M.N., Mckay, R., Lorenzen, M.D., Grubbs, N., Wang, Y., Han, J., Xuan, J., Willadsen, P., Wang, H., French, B.W., Bansal, R., Sedky, S.F., Souza, D., Bunn, D., Meinke, L.J., Miller, N.J., Siegfried, B.D., Sappington, T.W., Robertson, H.M. 2023. A draft Diabrotica virgifera virgifera genome: insights into control and host plant adaption by a major maize pest insect. BMC Genomics. 24. Article 19. https://doi.org/10.1186/s12864-022-08990-y.
DOI: https://doi.org/10.1186/s12864-022-08990-y

Interpretive Summary: Western corn rootworm (WCR) larvae feed on roots of corn and closely-related grasses. The resulting damage can cause economically significant yield loss to corn and the biofuel crop Miscanthus, reducing producer profits. WCR is difficult to control due to widespread resistance to multiple insecticides and adaptation to natural plant defenses. WCR larvae develop at different rates when feeding on roots of different host plants, affecting their ability to reach adulthood. The basis for these differences is unknown. ARS scientists along with a team of university collaborators examined genes identified from sequences in the WCR genome that, in other insects, are involved in responses to insecticides and host plant defenses, and in attraction of egg-laying adults to host plants. Differences in gene expression were identified among WCR larvae fed either on roots of corn (preferred host), Miscanthus (alternate host), switchgrass (marginal host), sorghum (non-host), or were starved. Expression of genes involved in cell stress responses was highest in larvae fed switchgrass or sorghum, or when starved. Fewer genes were expressed differently in WCR fed the preferred host (corn) compared to the alternate host (Miscanthus). Knowledge that expression of genes involved in stress responses and metabolism changes when feeding on different host plants provides insight into mechanisms by which WCR adapt to host plant defenses. This research will be used by university, government, and industry scientists to help assess and manage the threat posed by corn pests to new biofuel crops, and to target key genes in developing novel pest management tools.

Technical Abstract: Host plant adaptations determine the range of crops damaged by arthropod pests and their impacts on agricultural production. The host range of Diabrotica virgifera virgifera (western corn root worm) (Coleoptera: Chrysomelidae) is restricted to Zea mays and a few grasses. Resistance of D. v. virgifera to crop rotation practices and multiple insecticides contributes to difficulties controlling this pest in cultivated maize. A 2.42-Gb draft D. v. virgifera genome assembly, Dvir_v2.0, was constructed using a short shotgun read strategy, and scaffolded using transcriptome-guided and linked read data. K-mer analysis indicated a genome repeat content of = 61.5%. Ortholog assignments for Dvir_2.0 RefSeq models predict a greater number of D. v. virgifera-specific gene duplications than in other Coleoptera, including expansions in the ATP binding cassette transporter and chemosensory gene families. A majority of annotated D. v. virgifera cytochrome P450s belong to CYP4, 6, and 9 clades, which are associated with insecticide resistance in other insects. 5,404 differentially-expressed transcripts were detected between D. v. virgifera larvae fed maize roots compared to an alternative host (Miscanthus), a marginal host (Panicum virgatum), a poor host (Sorghum bicolor) and starvation treatments, with 1,908 transcripts shared across treatments. The fewest differentially expressed genes were predicted for maize compared to Miscanthus. Differentially-regulated transcripts in larvae fed maize compared to the other hosts were enriched for putative spliceosome and proteosome, and intracellular transport functions. General stress pathway functions were unique and enriched among up-regulated larval transcripts in marginal host, poor host, and starvation responses, compared to responses to primary (maize) and alternate hosts. Our study suggests that adaptations of D. v. virgifera larvae to feeding on an alternate host plant invoke fewer transcriptional changes compared to marginal or poor hosts. The shared up-regulation of stress response pathways between marginal host, poor host, and starvation treatments may reflect nutrient deprivation, and not a response to host plant defenses. This study provides insight into transcriptomic responses to larval feeding on different host plants, and genomic resources for future research on this economically significant pest of maize.