Department of Entomology and Nematology, University of California, Davis, CA, 95616, USA.
US Department of Agriculture, Agricultural Research Service, Salinas, CA, 93905, USA.
Sci Rep. 2022 May 19;12(1):8429. doi: 10.1038/s41598-022-12618-2.
There is widespread evidence of plant viruses manipulating behavior of their insect vectors as a strategy to maximize infection of plants. Often, plant viruses and their insect vectors have multiple potential host plant species, and these may not overlap entirely. Moreover, insect vectors may not prefer plant species to which plant viruses are well-adapted. In such cases, can plant viruses manipulate their insect vectors to preferentially feed and oviposit on plant species, which are suitable for viral propagation but less suitable for themselves? To address this question, we conducted dual- and no-choice feeding studies (number and duration of probing events) and oviposition studies with non-viruliferous and viruliferous [carrying beet curly top virus (BCTV)] beet leafhoppers [Circulifer tenellus (Baker)] on three plant species: barley (Hordeum vulgare L.), ribwort plantain (Plantago lanceolata L.), and tomato (Solanum lycopersicum L.). Barley is not a host of BCTV, whereas ribwort plantain and tomato are susceptible to BCTV infection and develop a symptomless infection and severe curly top symptoms, respectively. Ribwort plantain plants can be used to maintain beet leafhopper colonies for multiple generations (suitable), whereas tomato plants cannot be used to maintain beet leafhopper colonies (unsuitable). Based on dual- and no-choice experiments, we demonstrated that BCTV appears to manipulate probing preference and behavior by beet leafhoppers, whereas there was no significant difference in oviposition preference. Simulation modeling predicted that BCTV infection rates would to be higher in tomato fields with barley compared with ribwort plantain as a trap crop. Simulation model results supported the hypothesis that manipulation of probing preference and behavior may increase BCTV infection in tomato fields. Results presented were based on the BCTV-beet leafhopper pathosystem, but the approach taken (combination of experimental studies with complementary simulation modeling) is widely applicable and relevant to other insect-vectored plant pathogen systems involving multiple plant species.
有广泛的证据表明，植物病毒会操纵其昆虫媒介的行为，以此作为最大限度感染植物的策略。通常，植物病毒及其昆虫媒介有多个潜在的宿主植物物种，这些物种并不完全重叠。此外，昆虫媒介可能不会偏好对其适应良好的植物物种。在这种情况下，植物病毒能否操纵其昆虫媒介优先取食和产卵于适合病毒传播但对自身不利的植物物种上？为了解决这个问题，我们进行了双选择和无选择取食研究（探测事件的数量和持续时间）以及非传毒和传毒[携带甜菜曲顶病毒（BCTV）]叶蝉[Circulifer tenellus（Baker）]在三种植物上的产卵研究：大麦（Hordeum vulgare L.）、车前草（Plantago lanceolata L.）和番茄（Solanum lycopersicum L.）。大麦不是 BCTV 的宿主，而车前草和番茄易受 BCTV 感染，分别表现出无症状感染和严重曲顶症状。车前草植物可用于维持叶蝉群体的多代繁殖（适合），而番茄植物则不能用于维持叶蝉群体（不适合）。基于双选择和无选择实验，我们证明 BCTV 似乎操纵了叶蝉的探测偏好和行为，而在产卵偏好方面没有显著差异。模拟模型预测，与车前草作为诱捕作物相比，在番茄田中种植大麦会导致 BCTV 感染率更高。模拟模型结果支持了这样一种假设，即操纵探测偏好和行为可能会增加番茄田中 BCTV 的感染率。呈现的结果基于 BCTV-叶蝉病理系统，但所采用的方法（实验研究与互补模拟建模的结合）具有广泛的适用性，与涉及多个植物物种的其他昆虫媒介植物病原体系统相关。
