Genome evolution is usually viewed through the lens of growth in size and complexity over time, exemplified by plants and animals. In contrast, genome reduction is associated with a narrowing of ecological potential, such as in parasites and endosymbionts. But, can nuclear genome reduction also occur in, and potentially underpin a major radiation of free-living eukaryotes? An intriguing example of this phenomenon is provided by the red algae (Rhodophyta) that have lost many conserved pathways such as for flagellar motility, macroautophagy regulation, and phytochrome based light sensing. This anciently diverged, species-rich, and ecologically important algal lineage has undergone at least two rounds of large-scale genome reduction during its >1 billion-year evolutionary history. Here, using recent analyses of genome data, we review knowledge about the evolutionary trajectory of red algal nuclear and organelle gene inventories and plastid encoded autocatalytic introns. We compare and contrast Rhodophyta genome evolution to Viridiplantae (green algae and plants), both of which are members of the Archaeplastida, and highlight their divergent paths. We also discuss evidence for the speculative hypothesis that reduction in red algal plastid genome size through endosymbiotic gene transfer is counteracted by ongoing selection for compact nuclear genomes in red algae. Finally, we describe how the spliceosomal intron splicing apparatus provides an example of “evolution in action” in Rhodophyta and how the overall constraints on genome size in this lineage has left significant imprints on this key step in RNA maturation. Our review reveals the red algae to be an exciting, yet under-studied model that offers numerous novel insights as well as many unanswered questions that remain to be explored using modern genomic, genetic, and biochemical methods. The fact that a speciose lineage of free-living eukaryotes has spread throughout many aquatic habitats after having lost about 25% of its primordial gene inventory challenges us to elucidate the mechanisms underlying this remarkable feat.

中文翻译：

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当少即是多时：红藻作为研究真核生物基因损失和基因组进化的模型

基因组进化通常是随着时间的推移，随着大小和复杂性的增长而观察到的，例如动植物。相反，基因组减少与生态潜力的缩小相关，例如寄生虫和共生共生体。但是，核基因组的减少还会发生在自由生存的真核生物的主要辐射中，并有可能成为其支撑吗？红藻（Rhodophyta）提供了这种现象的一个有趣示例，该红藻已经失去了许多保守的途径，例如鞭毛运动，宏观自噬调节和基于植物色素的光感测。这个古老的，物种丰富且具有重要生态意义的藻类谱系在其超过10亿年的进化历史中经历了至少两轮大规模的基因组减少。在这里，使用对基因组数据的最新分析，我们审查有关红藻核和细胞器基因清单和质体编码的自催化内含子的进化轨迹的知识。我们比较和对比红藻植物基因组进化与Viridiplantae（绿藻和植物），这两个都是Archaeplastida的成员，并突出了它们的不同路径。我们还讨论了推测性假设的证据，即通过内生共生基因转移减少红藻质体基因组大小的减少，是通过对红藻中紧致核基因组的持续选择来抵消的。最后，我们描述了剪接体内含子剪接设备如何在红藻中提供“作用进化”的例子，以及该谱系中对基因组大小的总体限制如何在RNA成熟的这一关键步骤上留下了重要的印记。我们的评论显示，红藻令人兴奋，尚未得到充分研究的模型，它提供了许多新颖的见解以及许多未解决的问题，仍有待使用现代基因组学，遗传学和生化方法进行探索。在失去了大约25％的原始基因库存后，自由生存的真核生物的特定谱系已经传播到许多水生生境中，这一事实向我们阐明了这一非凡成就的机理提出了挑战。