The subgenus Tillandsia (Bromeliaceae) belongs to one of the fastest radiating clades in the plant kingdom and is characterised by the repeated evolution of Crassulacean acid metabolism (CAM). Despite its complex genetic basis, this water-conserving trait has evolved independently across many plant families and is regarded as a key innovation trait and driver of ecological diversification in Bromeliaceae. By producing high-quality genome assemblies of a Tillandsia species pair displaying divergent photosynthetic phenotypes, and combining genome-wide investigations of synteny, transposable element (TE) dynamics, sequence evolution, gene family evolution and temporal differential expression, we were able to pinpoint the genomic drivers of CAM evolution in Tillandsia. Several large-scale rearrangements associated with karyotype changes between the two genomes and a highly dynamic TE landscape shaped the genomes of Tillandsia. However, our analyses show that rewiring of photosynthetic metabolism is mainly obtained through regulatory evolution rather than coding sequence evolution, as CAM-related genes are differentially expressed across a 24-hour cycle between the two species but are not candidates of positive selection. Gene orthology analyses reveal that CAM-related gene families manifesting differential expression underwent accelerated gene family expansion in the constitutive CAM species, further supporting the view of gene family evolution as a driver of CAM evolution.

中文翻译：

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CAM 进化与爆炸性凤梨科植物辐射中的基因家族扩张有关

铁兰亚属（凤梨科）属于植物界辐射最快的分支之一，其特征是景天酸代谢（CAM）的重复进化。尽管其遗传基础复杂，但这种保水性状已在许多植物科中独立进化，并被视为凤梨科生态多样化的关键创新性状和驱动力。通过对显示不同光合表型的空气凤梨物种对进行高质量的基因组组装，并结合对同线性、转座元件（TE）动力学、序列进化、基因家族进化和时间差异表达的全基因组研究，我们能够查明铁兰 CAM 进化的基因组驱动因素。与两个基因组之间核型变化相关的几次大规模重排和高度动态的 TE 景观塑造了空气凤梨的基因组。然而，我们的分析表明，光合代谢的重新布线主要是通过调控进化而不是编码序列进化获得的，因为CAM相关基因在两个物种之间的24小时周期内差异表达，但不是正选择的候选者。基因直系同源分析表明，在 CAM 组成物种中，表现出差异表达的 CAM 相关基因家族经历了加速的基因家族扩张，进一步支持了基因家族进化作为 CAM 进化驱动因素的观点。