Abstract 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：红藻作为研究真核生物基因丢失和基因组进化的模型

摘要 基因组进化通常从大小和复杂性随时间增长的角度来看待，以植物和动物为例。相比之下，基因组减少与生态潜力的缩小有关，例如在寄生虫和内共生体中。但是，核基因组减少是否也可以发生在自由生活的真核生物的主要辐射中，并可能支持它？这种现象的一个有趣例子是红藻（Rhodophyta）已经失去了许多保守的途径，例如鞭毛运动、巨自噬调节和基于光敏色素的光传感。在其超过 10 亿年的进化历史中，这种远古分化、物种丰富且具有重要生态意义的藻类谱系经历了至少两轮大规模的基因组减少。在这里，利用最近对基因组数据的分析，我们回顾了有关红藻核和细胞器基因库存以及质体编码的自催化内含子的进化轨迹的知识。我们将红藻的基因组进化与 Viridiplantae（绿藻和植物）进行比较和对比，这两者都是 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，即通过内共生基因转移减少红藻质体基因组大小会被红藻中紧凑核基因组的持续选择所抵消。最后，我们描述了剪接体内含子剪接装置如何在红藻中提供“行动中的进化”的例子，以及该谱系中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重要印记。我们的评论显示红藻是一种令人兴奋的，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尚待使用现代基因组、遗传和生化方法探索的未解决问题。在失去了大约 25% 的原始基因库存后，自由生活的真核生物的特殊谱系已经遍布许多水生栖息地，这一事实挑战我们阐明这一非凡壮举背后的机制。