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

瘿蚊是一种瘿蚊科的小苍蝇，由于它们有能力操纵植物发育形成瘿，被认为是自然界最专业化和最复杂的食草动物。瘿是一种植物结构，是对由瘿诱导剂产生的刺激作出反应而形成的，它可以是不显眼的营养组织，也可以是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，并激发了对物种形成、寄主选择和操纵等广泛主题的研究。然而，我们对这些事件所涉及的潜在机制的理解仍然存在重大差距。鉴于瘿蚊的草食性和特殊性，许多瘿蚊是破坏性的农业和林业害虫。瑞典蠓（Contarinia nasturtii）和油菜花蠓（C. brassicola）就是两个这样的例子，它们能够对十字花科作物（如西兰花、花椰菜、卷心菜、油菜花）造成重大损害。芸苔孔虫是科学上的新事物，直到2019年才被正式描述。而C. nasturtii原产于欧亚大陆，可以侵染芸苔科的多种植物物种和组织，C. brassicola被假设原产于北美，并且只知道侵染油菜籽（芸苔）的发育花蕾。系统发育证据还表明，虽然它们属于同一属，但这两个物种是远亲，而且每个物种都有更近的亲戚，这些亲戚都是非芸苔科专家。这表明C. nasturtii和C. brassicola可能经历了平行进化以使用相同的寄主植物。考虑到它们形成瘿的能力，以及它们的原生范围、被侵染的寄主植物/组织和害虫状况的差异，nasturtii和C. brassicola为研究寄主植物转移、选择和操纵的机制提供了一个独特的模型系统，这可能最终成为害虫形成的基础。这项NSERC基于发现的研究计划的长期目标是全面了解致病的芸苔科专家瘿蠓的进化。为了实现这一目标，我提出的研究将：1)对甘蓝的基因组进行注释，为进一步的转录组学和群体遗传分析创造资源；2)比较芸苔菌和纳氏恙虫的地理分布范围和寄主选择行为，探讨平行进化的可能机制；3)表征和比较nasturtii和C. brassicola参与宿主植物操纵的唾液腺效应物；4)建立拟南芥-拟南芥模型系统，探索蠓操纵的植物信号通路和防御反应。最终，通过该研究项目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.