Withycombe Jordan, Han Jinlong, MacWilliams Jacob, Dorn Kevin M, Nalam Vamsi J, Nachappa Punya
Department of Agricultural Biology, Colorado State University, Fort Collins, CO, 80523, USA.
Soil Management and Sugarbeet Research, USDA-ARS, Fort Collins, CO, 80523, USA.
BMC Genomics. 2024 Dec 23;25(1):1237. doi: 10.1186/s12864-024-11143-y.
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.
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.
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.
甜菜（Beta vulgaris L.）在全球范围内种植，每年因甜菜曲顶病毒（BCTV）引起的曲顶病而遭受经济损失。该病毒由甜菜叶蝉（BLH），即Circulifer tenellus Baker传播。目前的管理策略依赖于化学防治和种植抗BCTV的甜菜基因型。然而，甜菜对BCTV抗性的遗传机制尚不清楚。本研究旨在通过使用寄主植物适宜性（无选择）、寄主偏好（选择）试验以及转录组分析，比较抗性（EL10）和敏感（FC709 - 2）甜菜基因型来确定这些机制。
寄主植物适宜性试验表明，携带病毒和未携带病毒的BLH在两种基因型上的成虫存活率或若虫产量均无显著差异，这表明BCTV抗性与甜菜叶蝉适合度降低没有直接关联。然而，寄主偏好试验表明，与抗性基因型EL10相比，携带病毒的BLH更喜欢在敏感基因型FC709 - 2上栖息，而未携带病毒的BLH没有偏好。对接种BCTV（由携带病毒的BLH取食）和模拟接种（由未携带病毒的BLH取食）的植物在接种后第1、7或14天进行RNA测序分析，突出了两种基因型之间动态且相反的反应。抗性基因型具有与茉莉酸和脱落酸生物合成及信号传导相关的差异表达转录本（DETs）。还观察到与应激缓解机制和植物初级代谢过程减少相关的DETs。相比之下，敏感基因型具有与水杨酸和生长素等相反植物激素相关的DETs。此外，该基因型在参与挥发性有机化合物（VOCs）产生的DETs中表现出上调，并且植物初级代谢过程增加。
这些结果为甜菜对BCTV抗性和敏感性背后相反的转录反应提供了新的见解。了解和分类甜菜对BCTV感染的抗性或敏感性机制对研究人员和植物育种者有益，因为它为进一步探索寄主植物 - 病毒 - 载体相互作用提供了基础。
