Beet curly top virus affects vector biology: The first transcriptome analysis of the beet leafhopper

Authors: HAN, JINLONG - Colorado State University; CUI, MEIHUA - Colorado State University; WITHYCOMBE, JORDAN - Colorado State University; SCHMIDTBAUER, MAX - Colorado State University; CHIGINSKY, JUDITH - Colorado State University; NEHER, OLIVER - Amalgamated Sugar Company; Strausbaugh, Carl; Majumdar, Raj; NALAM, V. J. - Colorado State University; NACHAPPA, PUNYA - Colorado State University

Submitted to: Journal of General Virology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/10/2024
Publication Date: 7/29/2024
Citation: Han, J., Cui, M., Withycombe, J., Schmidtbauer, M., Chiginsky, J., Neher, O., Strausbaugh, C.A., Majumdar, R., Nalam, V., Nachappa, P. 2024. Beet curly top virus affects vector biology: The first transcriptome analysis of the beet leafhopper. Journal of General Virology. 105(7):1-15. https://doi.org/10.1099/jgv.0.002012.
DOI: https://doi.org/10.1099/jgv.0.002012

Interpretive Summary: Beet curly top virus (BCTV) is a major yield limiting factor that negatively impacts sugar beet yield and overall sucrose production. The virus is vectored by beet leafhopper (BLH) that not only infects sugar beet but many other commercially important crops such as common beans, pepper, hemp, spinach, and tomatoes. Controlling BLH is primarily achieved through insecticide seed treatment with neonicotinoids which are on the verge of being banned in the U.S. due to environmental concerns. Future strategies to control BLH mediated BCTV transmission will require the knowledge of other BLH gene targets that are critical for BCTV acquisition and transmission during their interaction. Using recently sequenced BLH genome and global gene expression assay, we have identified key BLH genes that could be critical during its interaction with the virus. The data presented here will help in designing future strategies to control BCTV symptoms and reduce economic losses in crop plants that are highly susceptible to this virus.

Technical Abstract: Curly top disease, caused by beet curly top virus (BCTV), is one of the most serious viral diseases affecting sugar beets in western United States. The virus is exclusively transmitted by the beet leafhopper (BLH, Circulifer tenellus) in a circulative and non-propagative manner. Despite the growing knowledge base on virus-vector interactions, our understanding of the molecular interactions between BCTV and BLH is hampered by limited information regarding the virus impact on the vector and the absence of genomic and transcriptomic resources for BLH. Our study unveils the significant impact of BCTV on both the performance and transcriptome response of BLHs. Viruliferous BLHs had higher fecundity than non-viruliferous counterparts, which was evidenced by up-regulation of differentially expressed transcripts (DETs) associated with the development, viability, and fertility of germline and embryos in viruliferous insects. In contrast, most DETs associated with muscle movement and locomotor activities were down-regulated in viruliferous insects, implying potential behavioral modifications by BCTV. Additionally, a great proportion of differentially expressed transcripts related to innate immunity and detoxification was up-regulated in viruliferous insects. Viral infection also induced notable alterations in primary metabolisms, including energy metabolism namely glucosidases, lipid digestion and transport, and protein degradation, along with other cellular functions, particularly in chromatin remodeling and DNA repair. To our knowledge, this study represents the first comprehensive transcriptome analysis for BLH. Our findings provide new insights into the multifaceted effects of viral infection on various biological processes in BLH, revealing key molecular players in both virus manipulation of vector biology and the vector’s defensive strategies resulting from their long-term association.