Evolutionary tinkering with conserved components of a transcriptional regulatory network.
Evolutionary tinkering with conserved components of a transcriptional regulatory network.
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DOI：
10.1371/journal.pbio.1000329
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发表时间：
2010-03-09
期刊：
影响因子：
9.8
通讯作者：
Whiteway M
中科院分区：
文献类型：
--
作者：
Lavoie H;Hogues H;Mallick J;Sellam A;Nantel A;Whiteway M
通过分析相关酵母调节核糖体基因表达基本细胞过程的机制差异，揭示了进化可塑性的惊人水平。物种之间的基因表达差异是表型多样性的主要贡献者，但转录调控网络的潜在灵活性在很大程度上仍未被探索。核糖体调控子的转录是所有细胞的关键任务；在葡萄球菌中，转录因子Rap1、Fhl1、Ifh1和Hmo1形成一个多亚基复合物，控制核糖体基因的表达，而在白色念珠菌中，这种调节是由Tbf1和Cbf1控制的。在这里，我们使用全基因组转录因子作图分析了酿酒葡萄球菌和白色念珠菌中这一整套调控因子的每个同源成分的作用。我们观察到通用调节因子Cbf1、Hmo1、Rap1和Tbf1的结合谱发生了巨大变化，而Fhl1-Ifh1二聚体是两种真菌中唯一参与核糖体调节的成分：它在白色念珠菌中以Tbf1依赖的方式激活核糖体蛋白基因和rDNA表达，在酵母中以Rap1依赖的方式激活。我们发现控制两种相关酵母菌核糖体表达程序的转录调控网络在顺式和反式中被大量重塑。转录因子与细胞功能的连接、转录因子等级的运动、dna结合特异性和调控复合物的组装发生了变化，从而促进了真菌转录调控网络结构的全球变化。在大多数生命形式中，保守的代谢机制直接指导能量的生产和投资。然而，已经观察到编码这种机制的基因的转录调节的变化，并显示出物种之间的表型差异。在这里，我们表明，在不同的酵母物种中，控制中心代谢成分（在这种情况下是核糖体）表达的调节回路具有意想不到的进化可塑性水平。事实上，在酿酒酵母和白色念珠菌分离的进化过程中，大多数参与核糖体基因表达调控的转录因子都以新的方式被重复使用，从而产生转录网络结构的全局变化和新的核糖体调控复合物。
A surprising level of evolutionary plasticity is revealed by analysis of differences between related yeasts in the mechanisms regulating the essential cellular process of ribosomal gene expression. Gene expression variation between species is a major contributor to phenotypic diversity, yet the underlying flexibility of transcriptional regulatory networks remains largely unexplored. Transcription of the ribosomal regulon is a critical task for all cells; in S. cerevisiae the transcription factors Rap1, Fhl1, Ifh1, and Hmo1 form a multi-subunit complex that controls ribosomal gene expression, while in C. albicans this regulation is under the control of Tbf1 and Cbf1. Here, we analyzed, using full-genome transcription factor mapping, the roles, in both S. cerevisiae and C. albicans, of each orthologous component of this complete set of regulators. We observe dramatic changes in the binding profiles of the generalist regulators Cbf1, Hmo1, Rap1, and Tbf1, while the Fhl1-Ifh1 dimer is the only component involved in ribosomal regulation in both fungi: it activates ribosomal protein genes and rDNA expression in a Tbf1-dependent manner in C. albicans and a Rap1-dependent manner in S. cerevisiae. We show that the transcriptional regulatory network governing the ribosomal expression program of two related yeast species has been massively reshaped in cis and trans. Changes occurred in transcription factor wiring with cellular functions, movements in transcription factor hierarchies, DNA-binding specificity, and regulatory complexes assembly to promote global changes in the architecture of the fungal transcriptional regulatory network. Conserved metabolic machineries direct energy production and investment in most life forms. However, variation in the transcriptional regulation of the genes that encode this machinery has been observed and shown to contribute to phenotypic differences between species. Here, we show that the regulatory circuits governing the expression of central metabolic components (in this case the ribosomes) in different yeast species have an unexpected level of evolutionary plasticity. Most transcription factors involved in the regulation of expression of ribosomal genes have in fact been reused in new ways during the evolutionary time separating S. cerevisiae and C. albicans to generate global changes in transcriptional network structures and new ribosomal regulatory complexes.
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