Department of Entomology, Max Planck Institute for Chemical Ecology, Jena, Germany.
Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany.
Mol Biol Evol. 2019 May 1;36(5):930-941. doi: 10.1093/molbev/msz019.
Antagonistic chemical interactions between herbivorous insects and their host plants are often thought to coevolve in a stepwise process, with an evolutionary innovation on one side being countered by a corresponding advance on the other. Glucosinolate sulfatase (GSS) enzyme activity is essential for the Diamondback moth, Plutella xylostella, to overcome a highly diversified secondary metabolite-based host defense system in the Brassicales. GSS genes are located in an ancient cluster of arylsulfataselike genes, but the exact roles of gene copies and their evolutionary trajectories are unknown. Here, we combine a functional investigation of duplicated insect arylsulfatases with an analysis of associated nucleotide substitution patterns. We show that the Diamondback moth genome encodes three GSSs with distinct substrate spectra and distinct expression patterns in response to glucosinolates. Contrary to our expectations, early functional diversification of gene copies was not indicative of a coevolutionary arms race between host and herbivore. Instead, both copies of a duplicated arylsulfatase gene evolved concertedly in the context of an insect host shift to acquire novel detoxifying functions under positive selection, a pattern of duplicate gene retention that we call "concerted neofunctionalization."
植食性昆虫与其宿主植物之间的拮抗化学相互作用通常被认为是协同进化的，一方的进化创新会被另一方的相应进步所抵消。硫葡糖苷酶（GSS）酶活性对于小菜蛾 Plutella xylostella 克服 Brassicales 中高度多样化的基于次生代谢物的宿主防御系统至关重要。GSS 基因位于古老的芳基磺酸盐样基因簇中，但基因副本的确切作用及其进化轨迹尚不清楚。在这里，我们将重复的昆虫芳基磺酸盐酶的功能研究与相关核苷酸取代模式的分析相结合。我们表明，小菜蛾基因组编码三个具有不同底物谱和对硫葡糖苷不同表达模式的 GSS。与我们的预期相反，基因副本的早期功能多样化并不表明宿主和草食动物之间存在协同进化的军备竞赛。相反，在昆虫宿主转移的背景下，一个重复芳基磺酸盐基因的两个副本协同进化，在正选择下获得新的解毒功能，这种重复基因保留模式我们称之为“协同新功能化”。
