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

瘿蚊是瘿蚊科中的一种小型蝇类，由于其能够操纵植物发育形成瘿，因此被认为是自然界中最专门和复杂的食草动物。虫瘿是植物对虫瘿诱导物产生的刺激作出反应而形成的结构，其可以从不显眼的营养组织变化到类似刺或果实的复杂肿胀结构。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，并激发了对包括物种形成，宿主选择和操纵在内的广泛主题的研究。然而，在我们对这些事件所涉及的基本机制的理解方面仍然存在重大差距。 鉴于瘿蚊的食草性和专门性，许多瘿蚊是破坏性的农业和林业害虫。瑞典摇蚊Contarinia nasturtii和油菜花摇蚊C.芸苔属（brassicola）是两个这样的实例，其能够对花椰菜科作物（例如西兰花、花椰菜、卷心菜、油菜）造成显著损害。油菜Contarinia brassicola是一种新的科学，直到2019年才被正式描述。而C.旱金莲是欧亚大陆特有的一种害虫，可侵染菊科多种植物和组织。芸苔属被假设为原产于北美，并且仅已知侵染油菜（Brassicanapus）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，但这两个物种的亲缘关系较远，并且每个物种都有较近的亲属，这些亲属都是非菊科专家。这表明C。nasturtii和C.芸苔属可能经历了平行进化，以利用相同的宿主植物。鉴于它们形成虫瘿的能力以及它们在自然分布区、被侵染的寄主植物/组织和害虫状况方面的差异，C. nasturtii和C.芸苔属是研究寄主植物转移、选择和操纵机制的独特模式系统，这些机制可能最终成为害虫形成的基础。这个基于NSERC Discovery的研究计划的长期目标是全面了解传播害虫的十字花科专家Contarinia瘿蚊的进化。为了实现这一目标，我的研究工作将：1）注释C。为进一步的转录组学和群体遗传学研究提供了一个资源; 2）比较了甘蓝型油菜赤眼蜂的地理分布和寄主选择行为。brassicola和C. 3）比较并鉴定了C. nasturtii唾液腺中的效应子。nasturtii和C. brassicola参与寄主植物操纵; 4）发展一个C. nasturtii-Arabidopsis模式系统，探讨受蠓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有助于开发管理这些害虫的新策略。

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.