Transcriptomic profiling reveals distinct plant responses to beet curly top virus (BCTV) infection in resistant and susceptible sugar beet genotypes

Authors: WITHYCOMBE, JORDAN - Colorado State University; HAN, JINLONG - Colorado State University; MACWILLIAMS, JACOB - Colorado State University; Dorn, Kevin; NALAM, VAMSI - Colorado State University; NACHAPPA, PUNYA - Colorado State University

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/9/2024
Publication Date: 12/23/2024
Citation: Withycombe, J., Han, J., MacWilliams, J., Dorn, K.M., Nalam, V., Nachappa, P. 2024. Transcriptomic profiling reveals distinct plant responses to beet curly top virus (BCTV) infection in resistant and susceptible sugar beet genotypes. BMC Genomics. 25. Article e1237. https://doi.org/10.1186/s12864-024-11143-y.
DOI: https://doi.org/10.1186/s12864-024-11143-y

Interpretive Summary: Sugar beets are the source of over half the table sugar produced in the United States. For nearly a century, plant breeders have worked to improve disease resistance in sugar beet to the many pests and pathogens that threaten yields. The viral disease Beet Curly Top has historically threatened American beet sugar production, and been a central breeding target for both public and private plant breeders. While improved resistance to the Beet Curly Top has been developed, very little is known about the mechanism that underlies this resistance. USDA-ARS scientists alongside collaborators at Colorado State University identified specific plant responses to this important disease, along with finding that the insect vector of the Beet Curly Top Virus preferred to settle on susceptible lines when given a choice. These results helped identify critical gene expression patterns in response to infection with the Beet Curly Top Virus. These molecular signatures underly the genetic differences in lines with improved resistance to Beet Curly Top Virus. The results of this study will be useful for deepening our understanding of the interaction between sugar beet, an important viral disease, and its insect vector.

Technical Abstract: Sugar beets (Beta vulgaris L.) are grown across world and suffer economic loss annually to curly top disease caused by the beet curly top virus (BCTV). The virus is spread by the beet leafhopper (BLH), Circulifer tenellus. Current management strategies for BCTV rely on chemical control and planting BCTV-resistant sugar beet varieties. However, the underlying genetic mechanism surrounding resistance in sugar beet is unknown. The goal of this study was to determine the nature of BCTV resistance in a resistant (EL10) and susceptible (FC709-2) genotype of sugar beet using host plant suitability and host preference insect assays and characterize the transcriptional response to BCTV in both genotypes using RNA-sequencing. In host plant suitability assays, there was no difference in survival of BLH adults, or the number of nymphs produced on either genotype. In host preference assays, virus-infected BLH preferred to settle on the susceptible genotype compared to the resistant genotype. RNA-sequencing was performed on mock-inoculated and BCTV-inoculated plants from each genotype on day 1, 7, or 14 post inoculation. The results showed that both plant genotypes had a dynamic response to BCTV infection over time and there was minimal overlap in the transcriptomic responses of the two genotypes. The resistant genotype had DETs associated with phytohormone production including jasmonic acid and abscisic acid, along with proteins linked to stress reduction and the downregulation of plant primary metabolic processes. Contrastingly, the susceptible genotype had DETs associated with opposing phytohormones like salicylic acid and auxins, as well as the production of volatile organic compounds and an increase of primary plant metabolic processes. In summary, these results provide novel insights into the opposing responses in the transcriptional response of a resistant and susceptible genotype of sugar beet to BCTV infection. Understanding and classifying the mechanisms of resistance or susceptibility to BCTV infection in sugar beet is beneficial to researchers and plant breeders as it provides a basis for further exploration of the host plant-virus-vector interactions.