The role of cis regulatory evolution in maize domestication.

The role of cis regulatory evolution in maize domestication.
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DOI:
10.1371/journal.pgen.1004745
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发表时间:
2014-11
期刊:
影响因子:
4.5
通讯作者:
Doebley JF
Doebley JF
中科院分区:
生物学2区
文献类型:
--
作者:
Lemmon ZH;Bukowski R;Sun Q;Doebley JF

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顺式调控元件的修饰导致不同谱系之间的基因表达差异在进化中被认为是重要的。我们对玉米及其野生祖先teosinte的三种组织类型(穗、叶和茎)进行了基因组范围的顺式和反式调控差异分析。普遍存在的调控变异被观察到,大约70%的∼17,000个基因表明玉米和teosinte之间存在调控差异。然而,更少的基因(1,079个基因)显示出与所有采样的玉米和teosinte品系一致的顺式差异。对于这1,079个基因中的70%的∼,顺式差异是单个组织特有的。具有顺式调控差异的基因数量在耳朵组织中最多,在驯化过程中经历了形式上的剧烈变化。正如从驯化瓶颈预期的那样,玉米的顺式调控变异比teosinte小,玉米-teosinte顺式调控差异最大的基因缺失最大,这表明在驯化过程中对顺式调控差异进行了选择。在玉米驯化和改良过程中,与顺式调控元件的选择一致,具有顺式效应的基因与正选择下的基因有很强的相关性,而具有反式调控效应的基因则不相关。我们观察到一种定向偏向,即具有顺式差异的基因表现出比teosinte等位基因更高的玉米等位基因表达,这表明驯化有利于基因表达的上调。最后,这项工作记录了玉米和teosinte之间在三个组织的17,000多个基因中的顺式和反式调节变化。修饰顺式调控元件以产生基因表达水平、定位和时间上的差异是生物体进化分化适应的重要机制。为了检测玉米野生祖先teosinte在驯化过程中的基因调控变化,我们利用不同发育阶段的三种组织,对玉米和teosinte自交系及其F1代的等位基因特异性表达进行了研究。我们使用F1杂交种是第一次在驯化作物和野生祖先中进行研究,分析顺式和反式调节效应,以检查各种顺式和反式调节制度下基因的特征。我们发现了一致的顺式调控差异的证据,这种差异在大约4%的基因上区分了玉米和teosinte。这些基因与在驯化和作物改良过程中被选择的基因显著相关,表明顺式调控元件在玉米进化中发挥重要作用。这项工作为了解一种重要作物驯化过程中基因调控元件的进化提供了有价值的见解。
Gene expression differences between divergent lineages caused by modification of cis regulatory elements are thought to be important in evolution. We assayed genome-wide cis and trans regulatory differences between maize and its wild progenitor, teosinte, using deep RNA sequencing in F1 hybrid and parent inbred lines for three tissue types (ear, leaf and stem). Pervasive regulatory variation was observed with approximately 70% of ∼17,000 genes showing evidence of regulatory divergence between maize and teosinte. However, many fewer genes (1,079 genes) show consistent cis differences with all sampled maize and teosinte lines. For ∼70% of these 1,079 genes, the cis differences are specific to a single tissue. The number of genes with cis regulatory differences is greatest for ear tissue, which underwent a drastic transformation in form during domestication. As expected from the domestication bottleneck, maize possesses less cis regulatory variation than teosinte with this deficit greatest for genes showing maize-teosinte cis regulatory divergence, suggesting selection on cis regulatory differences during domestication. Consistent with selection on cis regulatory elements, genes with cis effects correlated strongly with genes under positive selection during maize domestication and improvement, while genes with trans regulatory effects did not. We observed a directional bias such that genes with cis differences showed higher expression of the maize allele more often than the teosinte allele, suggesting domestication favored up-regulation of gene expression. Finally, this work documents the cis and trans regulatory changes between maize and teosinte in over 17,000 genes for three tissues. Modification of cis regulatory elements to produce differences in gene expression level, localization, and timing is an important mechanism by which organisms evolve divergent adaptations. To examine gene regulatory change during the domestication of maize from its wild progenitor, teosinte, we assessed allele-specific expression in a collection of maize and teosinte inbreds and their F1 hybrids using three tissues from different developmental stages. Our use of F1 hybrids represents the first study in a domesticated crop and wild progenitor that dissects cis and trans regulatory effects to examine characteristics of genes under various cis and trans regulatory regimes. We find evidence for consistent cis regulatory divergence that differentiates maize from teosinte in approximately 4% of genes. These genes are significantly correlated with genes under selection during domestication and crop improvement, suggesting an important role for cis regulatory elements in maize evolution. This work provides valuable insight into the evolution of gene regulatory elements during the domestication of an important crop plant.
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