The making of a pest - Understanding evolutionary mechanisms that underlie host plant specialization in gall midges

萤火虫是蝗科中的一种小苍蝇，被认为是自然界中最专门和最复杂的食草动物，因为它们有能力控制植物的发育来形成虫胆。虫胆是植物对由虫胆诱导剂产生的刺激的反应而形成的结构，从不明显的营养组织到复杂的类似刺或水果的膨胀结构，都有不同。数百年来，这种操纵植物生长的能力一直吸引着哲学家和科学家，并促使人们对包括物种形成、宿主选择和操纵在内的一系列主题进行研究。然而，在我们对这些事件涉及的基本机制的理解方面仍然存在重大差距。鉴于胆蚊的食草性和专业性，许多是破坏性的农业和林业害虫。瑞典吸浆虫Contarinia nasturtii和油菜花吸浆虫C.Brassicola就是两个这样的例子，能够对十字花科作物(如西兰花、花椰菜、卷心菜、油菜)造成重大损害。Brassicola Contarinia Brassicola是一个新的科学概念，直到2019年才被正式描述。虽然C.nasturtii原产于欧亚大陆，可以侵染十字花科中的多种植物和组织，但Brassicola被假设为原产于北美，仅已知侵染油菜(Brassica Napus)的发育中的花蕾。系统发育证据还表明，虽然它们属于同一属，但这两个物种是遥远的亲缘关系，每个物种都有更近的亲属，都不是十字花科专家。这表明甘蓝根结线虫和甘蓝根结线虫可能经历了使用相同寄主植物的平行进化。Nasturtii和Brassicola是研究寄主植物转移、选择和操纵机制的一种独特的模式系统，而寄主植物和寄主组织的寄主范围、侵染和虫害状况的差异可能最终导致害虫的形成。这个以NSERC Discovery为基础的研究计划的长期目标是全面了解瘟疫十字花科专家Contarinia gallmides的进化。为了实现这一目标，我提议的研究将：1)注释甘蓝型油菜基因组，为进一步的转录和种群遗传分析创造资源；2)比较甘蓝型油菜和甘蓝型油菜的地理范围和寄主选择行为，以考察平行进化的可能机制；3)表征和比较甘蓝型油菜和甘蓝型油菜唾液腺中参与寄主植物操纵的效应器；以及4)建立甘蓝型油菜-拟南芥模型系统，以探索寄主操纵的植物信号通路和防御反应。最终，通过这项研究计划获得的知识可能会使开发新的策略来管理这些害虫。

Gall midges, small flies in the Cecidomyiidae family, are considered natures most specialized and sophisticated herbivores, due to their ability to manipulate plant development to form galls. Galls are plant structures formed in response to stimuli produced by the gall-inducer, which can vary from inconspicuous nutritive tissues to elaborate swollen structures that resemble thorns or fruits. This ability to manipulate plant growth has fascinated philosophers and scientists for hundreds of years and spurred investigations on a wide array of subjects including speciation, host selection and manipulation. However, there are still major gaps in our understanding of the underlying mechanisms involved in these events. Given the herbivorous and specialized nature of gall midges, many are destructive agricultural and forestry pests. The swede midge, Contarinia nasturtii, and the canola flower midge, C. brassicola, are two such examples, capable of causing significant damage to Brassicaceae crops (e.g. broccoli, cauliflower, cabbage, canola). Contarinia brassicola is new-to-science, only being formally described in 2019. Whereas C. nasturtii is native to Eurasia, and can infest multiple plant species and tissues within the Brassicaceae, C. brassicola is hypothesized to be native to North America, and is only known to infest developing flower buds of canola (Brassica napus). Phylogenetic evidence also indicates that although they are in the same genus, the two species are distantly related and each have closer relatives that are non-Brassicaceae specialists. This suggests C. nasturtii and C. brassicola may have undergone parallel evolution to use the same host plants. Given their ability to form galls as well as differences in their native ranges, host plants/tissues infested, and pest status, C. nasturtii and C. brassicola represent a unique model system to investigate the mechanisms of host plant shifts, selection and manipulation, which may ultimately underlie the making of a pest. The long-term objective of this NSERC Discovery-based research program is to develop a comprehensive understanding of the evolution of pestiferous Brassicaceae-specialist Contarinia gall midges. To achieve this objective my proposed research will: 1) Annotate the genome of C. brassicola to create a resource for further transcriptomic and population genetic analyses; 2) Compare the geographic range and host selection behaviour of C. brassicola and C. nasturtii to examine possible mechanisms of parallel evolution; 3) Characterize and compare effectors in salivary glands of C. nasturtii and C. brassicola involved in host plant manipulation; and 4) Develop a C. nasturtii-Arabidopsis model system to explore the plant signaling pathways and defense responses which are manipulated by the midge. Ultimately, the knowledge gained through this research program may enable the development of novel strategies to manage these pests.