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

Background: Sugar beets (Beta vulgaris L.) are grown worldwide and suffer economic loss annually due to curly top disease caused by the beet curly top virus (BCTV). The virus is spread by the beet leafhopper (BLH), Circulifer tenellus Baker. Current management strategies rely on chemical control and planting BCTV-resistant sugar beet genotypes. However, the genetic mechanism underlying BCTV resistance in sugar beet is unknown. This study aimed to determine these mechanisms by comparing a resistant (EL10) and susceptible (FC709-2) sugar beet genotype using host plant suitability (no-choice), host preference (choice) assays, and transcriptomic analysis.

Results: Host plant suitability assays revealed no significant differences in adult survival or nymph production between viruliferous and non-viruliferous BLH on either genotype, suggesting that BCTV resistance is not directly associated with reduced beet leafhopper fitness. However, host preference assays showed that viruliferous BLH preferred settling on the susceptible genotype, FC709-2, compared to the resistant genotype, EL10 whereas the non-viruliferous BLH showed no preference. RNA-sequencing analysis of BCTV-inoculated (viruliferous BLH-fed) and mock-inoculated (non-viruliferous BLH-fed) plants at day 1, 7, or 14 post-inoculations highlighted dynamic and contrasting responses between the two genotypes. The resistant genotype had differentially expressed transcripts (DETs) associated with jasmonic acid and abscisic acid biosynthesis and signaling. DETs associated with stress mitigation mechanisms and reduction in plant primary metabolic processes were also observed. In contrast, the susceptible genotype had DETs associated with opposing phytohormones like salicylic acid and auxin. Moreover, this genotype exhibited an upregulation in DETs involved in volatile organic compounds (VOCs) production and increased primary plant metabolic processes.

Conclusions: These results provide novel insight into the opposing transcriptional responses underlying BCTV resistance and susceptibility in sugar beet. 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.