Department of Ecology, Hubei Key Laboratory of Cell Homeostasis, College of Life Sciences, Wuhan University, Wuhan, China.
Department of Cell Biology, Hubei Key Laboratory of Cell Homeostasis, College of Life Sciences, Wuhan University, Wuhan, China.
Mol Biol Evol. 2020 Mar 1;37(3):786-798. doi: 10.1093/molbev/msz266.
Adaptations to different diets represent a hallmark of animal diversity. The diets of birds are highly variable, making them an excellent model system for studying adaptive evolution driven by dietary changes. To test whether molecular adaptations to diet have occurred during the evolution of birds, we examined a dietary enzyme alanine-glyoxylate aminotransferase (AGT), which tends to target mitochondria in carnivorous mammals, peroxisomes in herbivorous mammals, and both mitochondria and peroxisomes in omnivorous mammals. A total of 31 bird species were examined in this study, which included representatives of most major avian lineages. Of these, 29 have an intact mitochondrial targeting sequence (MTS) of AGT. This finding is in stark contrast to mammals, which showed a number of independent losses of the MTS. Our cell-based functional assays revealed that the efficiency of AGT mitochondrial targeting was greatly reduced in unrelated lineages of granivorous birds, yet it tended to be high in insectivorous and carnivorous lineages. Furthermore, we found that proportions of animal tissue in avian diets were positively correlated with mitochondrial targeting efficiencies that were experimentally determined, but not with those that were computationally predicted. Adaptive evolution of AGT mitochondrial targeting in birds was further supported by the detection of positive selection on MTS regions. Our study contributes to the understanding of how diet drives molecular adaptations in animals, and suggests that caution must be taken when computationally predicting protein subcellular targeting.
不同饮食的适应是动物多样性的一个标志。鸟类的饮食非常多样化，使它们成为研究饮食变化驱动的适应性进化的绝佳模型系统。为了测试鸟类进化过程中是否发生了分子适应饮食的现象，我们研究了一种饮食酶——丙氨酸-乙醛酸氨基转移酶（AGT），它往往在肉食性哺乳动物中靶向线粒体，在草食性哺乳动物中靶向过氧化物酶体，在杂食性哺乳动物中靶向线粒体和过氧化物酶体。在这项研究中，共检查了 31 种鸟类，其中包括大多数主要鸟类谱系的代表。在这些鸟类中，有 29 种具有完整的 AGT 线粒体靶向序列（MTS）。这一发现与哺乳动物形成鲜明对比，哺乳动物表现出许多 MTS 的独立缺失。我们的基于细胞的功能测定显示，在与granivorous 鸟类无关的谱系中，AGT 线粒体靶向的效率大大降低，但在昆虫食性和肉食性谱系中，其效率往往较高。此外，我们发现鸟类饮食中动物组织的比例与实验确定的但与计算预测的线粒体靶向效率呈正相关。在鸟类中，AGT 线粒体靶向的适应性进化进一步得到了 MTS 区域正选择检测的支持。我们的研究有助于理解饮食如何驱动动物的分子适应，并表明在计算预测蛋白质亚细胞靶向时必须谨慎。
