Plant viruses face many challenges in agricultural environments. Although crop fields appear to be abundant resources for these pathogens, it may be difficult for viruses to "escape" from crop environments prior to host senescence or harvesting. One way for viruses to increase the odds of persisting outside of agricultural fields across seasons is by evolving traits that increase transmission opportunities between crops and wild plant communities. There is accumulating evidence that some viruses can achieve this by manipulating crop plant phenotypes in ways that enhance transmission by vectors. Putative manipulations occur through alteration of plant cues (color, size, texture, foliar volatiles, in-leaf metabolites, defenses, and leaf cuticles) that mediate vector orientation, feeding, and dispersal behaviors. Virus effects on host phenotypes are not uniform but appear to exhibit convergence depending on virus traits underlying transmission, particularly the duration of probing and feeding required to acquire and inoculate distinct types of plant viruses. This shared congruence in manipulation strategies and mechanisms across divergent virus lineages suggests that such effects may be adaptive. To discern if this is the case, researchers must consider molecular and environmental constraints on virus evolution, including those imposed by insect vectors from organismal to landscape scales. In this review, we synthesize applied research on vector-borne virus transmission in laboratory and field settings to identify the main factors determining transmission opportunities for plant viruses, and thus, selection pressure to evolve manipulative traits. We then examine these outputs in the context of studies reporting putative instances of plant virus manipulation. Our synthesis reveals important disconnects between virus manipulation studies and actual selection pressures imposed by vectors in real-world contexts.

中文翻译：

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病毒-载体关联的综合揭示了植物病毒对宿主和载体操纵的研究中的重要缺陷。

植物病毒在农业环境中面临许多挑战。尽管作物田似乎是这些病原体的丰富资源，但病毒可能很难在宿主衰老或收获之前从作物环境中“逃脱”。病毒增加跨季节在农田外生存几率的一种方法是通过进化特征来增加作物和野生植物群落之间的传播机会。越来越多的证据表明，一些病毒可以通过以增强载体传播的方式操纵作物植物表型来实现这一目标。假定的操作通过改变植物线索（颜色、大小、质地、叶挥发物、叶内代谢物、防御和叶表皮）而发生，这些线索介导了载体定向、摄食和传播行为。病毒对宿主表型的影响并不统一，但似乎表现出趋同性，这取决于传播背后的病毒特征，特别是获取和接种不同类型植物病毒所需的探测和喂养的持续时间。这种跨不同病毒谱系的操纵策略和机制的共同一致性表明，这种影响可能是适应性的。为了辨别是否是这种情况，研究人员必须考虑病毒进化的分子和环境限制，包括昆虫载体从有机体到景观尺度施加的限制。在这篇综述中，我们综合了实验室和野外环境中媒介传播病毒传播的应用研究，以确定决定植物病毒传播机会的主要因素，从而确定进化操纵性状的选择压力。然后，我们在报告植物病毒操纵的假定实例的研究的背景下检查这些输出。我们的综合揭示了病毒操纵研究与载体在现实世界中施加的实际选择压力之间的重要脱节。