Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom.
PLoS Comput Biol. 2024 Oct 1;20(10):e1012479. doi: 10.1371/journal.pcbi.1012479. eCollection 2024 Oct.
Plant viruses threaten food security and are often transmitted by insect vectors. Non-persistently transmitted (NPT) plant viruses are transmitted almost exclusively by aphids. Because virions attach to the aphid's stylet (mouthparts) and are acquired and inoculated via brief epidermal probes, the aphid-virus interaction is highly transient, with a very short aphid virus retention time. Many NPT viruses manipulate their host plant's phenotype to change aphid behaviour to optimise virus transmission. Epidemiological models of this have overlooked a key feature of aphid NPT virus retention: probing or feeding on a plant causes aphids to lose the virus. Furthermore, experimental studies suggest aphids could possibly inoculate multiple healthy plants within one infective period if they do not feed. Consequences of this for virus manipulation of host plant phenotype have not been explored. Our new compartmental epidemiological model includes both behaviour-based aphid dispersal and infectivity loss rates, and the ability of infective aphids to probe multiple plants before virus loss. We use our model to explore how NPT virus-induced host phenotypes affect epidemic outcomes, comparing these results to representative previous models. We find that previous models behave fundamentally differently and underestimate the benefit of an 'attract-and-deter' phenotype, where the virus induces increased aphid attraction to infected plants but deters them from prolonged feeding. Our results also highlight the importance of characterising NPT virus retention upon the aphid during probing. Allowing for multiple infective probes increases disease incidence and the effectiveness of virus manipulation, with implications for epidemic prediction and control.
植物病毒威胁着食品安全，通常通过昆虫媒介传播。非持久传播（NPT）的植物病毒几乎完全由蚜虫传播。由于病毒粒子附着在蚜虫的口针（口器）上，并通过短暂的表皮探测获得和接种，蚜虫-病毒的相互作用是高度短暂的，蚜虫病毒的保留时间非常短。许多 NPT 病毒操纵其宿主植物的表型，改变蚜虫的行为，以优化病毒传播。对这一点的流行病学模型忽略了蚜虫 NPT 病毒保留的一个关键特征：对植物的探测或取食会导致蚜虫失去病毒。此外，实验研究表明，如果蚜虫不取食，它们有可能在一个感染期内接种多个健康植物。这对病毒操纵宿主植物表型的后果尚未得到探讨。我们的新隔室流行病学模型包括基于行为的蚜虫扩散和感染性丧失率，以及感染性蚜虫在病毒丧失之前探测多个植物的能力。我们使用我们的模型来探讨 NPT 病毒诱导的宿主表型如何影响流行病结果，并将这些结果与有代表性的先前模型进行比较。我们发现，先前的模型表现出根本的不同，并低估了“吸引-驱赶”表型的益处，即在病毒诱导增加蚜虫对感染植物的吸引力的同时，又阻止它们长时间取食。我们的结果还强调了在探测过程中对蚜虫上的 NPT 病毒保留进行特征描述的重要性。允许多次感染性探测会增加疾病发病率和病毒操纵的有效性，这对流行病预测和控制具有重要意义。
