Institute for Evolution and Biodiversity, University of Münster, Münster, Germany.
Department of Biological Sciences, University of Massachusetts, Lowell, MA, USA.
Heredity (Edinb). 2020 Aug;125(1-2):50-59. doi: 10.1038/s41437-020-0319-7. Epub 2020 Jun 4.
Eukaryotic genomes frequently acquire new protein-coding genes which may significantly impact an organism's fitness. Novel genes can be created, for example, by duplication of large genomic regions or de novo, from previously non-coding DNA. Either way, creation of a novel transcript is an essential early step during novel gene emergence. Most studies on the gain-and-loss dynamics of novel genes so far have compared genomes between species, constraining analyses to genes that have remained fixed over long time scales. However, the importance of novel genes for rapid adaptation among populations has recently been shown. Therefore, since little is known about the evolutionary dynamics of transcripts across natural populations, we here study transcriptomes from several tissues and nine geographically distinct populations of an ecological model species, the three-spined stickleback. Our findings suggest that novel genes typically start out as transcripts with low expression and high tissue specificity. Early expression regulation appears to be mediated by gene-body methylation. Although most new and narrowly expressed genes are rapidly lost, those that survive and subsequently spread through populations tend to gain broader and higher expression levels. The properties of the encoded proteins, such as disorder and aggregation propensity, hardly change. Correspondingly, young novel genes are not preferentially under positive selection but older novel genes more often overlap with F outlier regions. Taken together, expression of the surviving novel genes is rapidly regulated, probably via epigenetic mechanisms, while structural properties of encoded proteins are non-debilitating and might only change much later.
真核生物基因组经常获得新的蛋白质编码基因，这可能会显著影响生物体的适应性。新基因可以通过大片段基因组区域的复制或从头产生，从前非编码 DNA 产生。无论哪种方式，新转录本的产生都是新基因出现的早期关键步骤。迄今为止，大多数关于新基因增益和损失动态的研究都是在物种之间比较基因组，将分析局限于在长时间尺度上保持固定的基因。然而，新基因在种群间快速适应中的重要性最近已经得到证实。因此，由于人们对自然种群中转录本的进化动态知之甚少，我们在此研究了生态模式物种三刺鱼的九个地理上不同的种群的几个组织中的转录组。我们的研究结果表明，新基因通常以表达水平低和组织特异性高的转录本开始。早期的表达调控似乎是由基因体甲基化介导的。尽管大多数新的和表达范围狭窄的基因很快丢失，但那些存活下来并随后在种群中传播的基因往往会获得更广泛和更高的表达水平。编码蛋白的性质，如无序和聚集倾向，几乎不会改变。相应地，年轻的新基因不太可能受到正选择的影响，而较老的新基因更经常与 F 异常值区域重叠。总的来说，存活的新基因的表达被快速调控，可能是通过表观遗传机制，而编码蛋白的结构特性不会削弱，可能只会在很久之后才会改变。
