Toxins from scratch? Diverse, multimodal gene origins in the predatory robber fly Dasypogon diadema indicate a dynamic venom evolution in dipteran insects
Toxins from scratch? Diverse, multimodal gene origins in the predatory robber fly Dasypogon diadema indicate a dynamic venom evolution in dipteran insects
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DOI：
10.1093/gigascience/giz081
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发表时间：
2019-07-01
期刊：
影响因子：
9.2
通讯作者：
von Reumont, Bjoern M.
中科院分区：
文献类型：
--
作者：
Drukewitz, Stephan Holger;Bokelmann, Lukas;von Reumont, Bjoern M.
背景：毒液和它们所含的毒素代表了在整个动物王国中无数次进化的分子适应。然而，形状毒液蛋白进化的过程知之甚少，因为缺乏全基因组数据可用于有毒物种的比较分析。结果如下：我们进行了广泛的比较毒理基因组学分析，以深入了解毒液进化的基因组机制，在强盗苍蝇（Asilidae）。我们首先测序了一个高质量的基因组草图的hyperteran狩猎强盗飞Dasypogon迪亚德马，分析其毒液的组合proteotranscriptomic方法，并比较我们的结果与最近描述的强盗飞毒液，以评估的一般组成和主要成分asilid毒液。然后，我们应用比较基因组学的方法，基于1个额外的asilid基因组，10个高质量的双翅目基因组，和2个鳞翅目外群基因组，揭示了进化机制和起源的确定毒液蛋白在强盗苍蝇。结论：虽然在非asilid基因组中鉴定了30种主要毒液蛋白中的15种的同源物，但剩余的15种高表达毒液蛋白似乎是强盗蝇所特有的。结果表明，D.迪亚德马可能以多模式方式进化，包括（i）基因复制后的新功能化，（ii）蛋白质的表达依赖性共选择，和（iii）具有神秘起源的asilid谱系特异性孤儿基因。这种孤儿基因的作用目前在进化基因组学中存在争议，但尚未在毒素进化的背景下进行讨论。我们的研究结果显示了一个意想不到的动态毒液进化asilid昆虫，这与唯一的其他昆虫toxicogenomic进化分析的结果，在寄生蜂（Hyplittera），毒素进化是由单基因co-option为主。这些发现支持了进一步基因组研究的重要性，以涵盖更多被忽视的有毒类群谱系，并了解孤儿基因作为毒液进化可能驱动因素的重要性。
Background: Venoms and the toxins they contain represent molecular adaptations that have evolved on numerous occasions throughout the animal kingdom. However, the processes that shape venom protein evolution are poorly understood because of the scarcity of whole-genome data available for comparative analyses of venomous species. Results: We performed a broad comparative toxicogenomic analysis to gain insight into the genomic mechanisms of venom evolution in robber flies (Asilidae). We first sequenced a high-quality draft genome of the hymenopteran hunting robber fly Dasypogon diadema, analysed its venom by a combined proteotranscriptomic approach, and compared our results with recently described robber fly venoms to assess the general composition and major components of asilid venom. We then applied a comparative genomics approach, based on 1 additional asilid genome, 10 high-quality dipteran genomes, and 2 lepidopteran outgroup genomes, to reveal the evolutionary mechanisms and origins of identified venom proteins in robber flies. Conclusions: While homologues were identified for 15 of 30 predominant venom protein in the non-asilid genomes, the remaining 15 highly expressed venom proteins appear to be unique to robber flies. Our results reveal that the venom of D. diadema likely evolves in a multimodal fashion comprising (i) neofunctionalization after gene duplication, (ii) expression-dependent co-option of proteins, and (iii) asilid lineage-specific orphan genes with enigmatic origin. The role of such orphan genes is currently being disputed in evolutionary genomics but has not been discussed in the context of toxin evolution. Our results display an unexpected dynamic venom evolution in asilid insects, which contrasts the findings of the only other insect toxicogenomic evolutionary analysis, in parasitoid wasps (Hymenoptera), where toxin evolution is dominated by single gene co-option. These findings underpin the significance of further genomic studies to cover more neglected lineages of venomous taxa and to understand the importance of orphan genes as possible drivers for venom evolution.