Department of Biology, Lund University, Sölvegatan 37, SE-223 62, Lund, Sweden.
Department of Organismic and Evolutionary Biology, Harvard University, 16 Divinity Avenue, Cambridge, MA, 02138, USA.
BMC Biol. 2021 Apr 23;19(1):83. doi: 10.1186/s12915-021-01001-8.
Defining the origin of genetic novelty is central to our understanding of the evolution of novel traits. Diversification among fatty acid desaturase (FAD) genes has played a fundamental role in the introduction of structural variation in fatty acyl derivatives. Because of its central role in generating diversity in insect semiochemicals, the FAD gene family has become a model to study how gene family expansions can contribute to the evolution of lineage-specific innovations. Here we used the codling moth (Cydia pomonella) as a study system to decipher the proximate mechanism underlying the production of the ∆8∆10 signature structure of olethreutine moths. Biosynthesis of the codling moth sex pheromone, (E8,E10)-dodecadienol (codlemone), involves two consecutive desaturation steps, the first of which is unusual in that it generates an E9 unsaturation. The second step is also atypical: it generates a conjugated diene system from the E9 monoene C intermediate via 1,4-desaturation.
Here we describe the characterization of the FAD gene acting in codlemone biosynthesis. We identify 27 FAD genes corresponding to the various functional classes identified in insects and Lepidoptera. These genes are distributed across the C. pomonella genome in tandem arrays or isolated genes, indicating that the FAD repertoire consists of both ancient and recent duplications and expansions. Using transcriptomics, we show large divergence in expression domains: some genes appear ubiquitously expressed across tissue and developmental stages; others appear more restricted in their expression pattern. Functional assays using heterologous expression systems reveal that one gene, Cpo_CPRQ, which is prominently and exclusively expressed in the female pheromone gland, encodes an FAD that possesses both E9 and ∆8∆10 desaturation activities. Phylogenetically, Cpo_CPRQ clusters within the Lepidoptera-specific ∆10/∆11 clade of FADs, a classic reservoir of unusual desaturase activities in moths.
Our integrative approach shows that the evolution of the signature pheromone structure of olethreutine moths relied on a gene belonging to an ancient gene expansion. Members of other expanded FAD subfamilies do not appear to play a role in chemical communication. This advises for caution when postulating the consequences of lineage-specific expansions based on genomics alone.
确定遗传新颖性的起源是我们理解新性状进化的核心。脂肪酸去饱和酶（FAD）基因的多样化在脂肪酸衍生物结构变异的引入中发挥了基本作用。由于其在产生昆虫信息素多样性方面的核心作用，FAD 基因家族已成为研究基因家族扩张如何有助于谱系特异性创新进化的模型。在这里，我们使用苹果蠹蛾（Cydia pomonella）作为研究系统，以破译产生金小蜂属昆虫中∆8∆10 特征结构的近因机制。苹果蠹蛾性信息素（E8，E10）-十二碳二烯醇（codlemone）的生物合成涉及两个连续的去饱和步骤，第一个步骤不同寻常，因为它产生了 E9 不饱和键。第二步也很典型：它通过 1,4-去饱和作用将 E9 单烯 C 中间体转化为共轭二烯系统。
在这里，我们描述了在 codlemone 生物合成中起作用的 FAD 基因的特征。我们鉴定了 27 个 FAD 基因，这些基因对应于昆虫和鳞翅目昆虫中鉴定的各种功能类别。这些基因在 C. pomonella 基因组中串联排列或孤立基因分布，表明 FAD 库由古老和近代的重复和扩张组成。使用转录组学，我们显示了表达域的巨大差异：一些基因在组织和发育阶段普遍表达；其他基因的表达模式则更为局限。使用异源表达系统的功能测定表明，一个基因 Cpo_CPRQ 在雌性信息素腺中高度且专门表达，该基因编码的 FAD 具有 E9 和 ∆8∆10 去饱和活性。系统发育分析表明，Cpo_CPRQ 聚类在鳞翅目特异性 ∆10/∆11 分支的 FAD 中，这是鳞翅目中不寻常去饱和酶活性的经典库。
我们的综合方法表明，金小蜂属昆虫特征性信息素结构的进化依赖于属于古老基因扩张的基因。其他扩张的 FAD 亚家族的成员似乎在化学通讯中不起作用。因此，仅基于基因组推断谱系特异性扩张的后果时应谨慎。
