Although native to North America, the invasion of the aphid-like grape phylloxera Daktulosphaira vitifoliae across the globe altered the course of grape cultivation. For the past 150 years, viticulture relied on grafting-resistant North American Vitis species as rootstocks, thereby limiting genetic stocks tolerant to other stressors such as pathogens and climate change. Limited understanding of the insect genetics resulted in successive outbreaks across the globe when rootstocks failed. Here we report the 294-Mb genome of D. vitifoliae as a basic tool to understand host plant manipulation, nutritional endosymbiosis, and enhance global viticulture. Using a combination of genome, RNA, and population resequencing, we found grape phylloxera showed high duplication rates since its common ancestor with aphids, but similarity in most metabolic genes, despite lacking obligate nutritional symbioses and feeding from parenchyma. Similarly, no enrichment occurred in development genes in relation to viviparity. However, phylloxera evolved > 2700 unique genes that resemble putative effectors and are active during feeding. Population sequencing revealed the global invasion began from the upper Mississippi River in North America, spread to Europe and from there to the rest of the world. The grape phylloxera genome reveals genetic architecture relative to the evolution of nutritional endosymbiosis, viviparity, and herbivory. The extraordinary expansion in effector genes also suggests novel adaptations to plant feeding and how insects induce complex plant phenotypes, for instance galls. Finally, our understanding of the origin of this invasive species and its genome provide genetics resources to alleviate rootstock bottlenecks restricting the advancement of viticulture.

中文翻译：

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葡萄根瘤蚜的基因组序列为了解标志性害虫的进化、适应和入侵途径提供了见解。


虽然原产于北美，但类似蚜虫的葡萄根瘤蚜 Daktulosphaira vitifoliae 在全球范围内的入侵改变了葡萄种植的进程。在过去的 150 年里，葡萄栽培依赖抗嫁接的北美葡萄品种作为砧木，从而限制了对病原体和气候变化等其他压力源的耐受性。由于对昆虫遗传学的了解有限，当砧木失败时，导致全球范围内连续爆发昆虫。在这里，我们报告了 294 Mb 的 D. vitifolie 基因组，作为了解宿主植物操纵、营养内共生和增强全球葡萄栽培的基本工具。结合基因组、RNA和群体重测序，我们发现葡萄根瘤蚜自其与蚜虫的共同祖先以来表现出很高的重复率，但大多数代谢基因相似，尽管缺乏专性营养共生和从薄壁组织获取营养。同样，与胎生相关的发育基因也没有发生富集。然而，根瘤蚜进化出了超过 2700 个独特的基因，这些基因类似于假定的效应子，并且在进食过程中活跃。种群测序显示，全球入侵从北美密西西比河上游开始，蔓延到欧洲，再从那里传播到世界其他地区。葡萄根瘤蚜基因组揭示了与营养内共生、胎生和草食性进化相关的遗传结构。效应基因的异常扩展也表明对植物进食的新适应以及昆虫如何诱导复杂的植物表型，例如虫瘿。最后，我们对这种入侵物种的起源及其基因组的了解为缓解限制葡萄栽培进步的砧木瓶颈提供了遗传资源。