A Systems Approach Uncovers Restrictions for Signal Interactions Regulating Genome-wide Responses to Nutritional Cues in Arabidopsis

As sessile organisms, plants must cope with multiple and combined variations of signals in their environment. However, very few reports have studied the genome-wide effects of systematic signal combinations on gene expression. Here, we evaluate a high level of signal integration, by modeling genome-wide expression patterns under a factorial combination of carbon (C), light (L), and nitrogen (N) as binary factors in two organs (O), roots and leaves. Signal management is different between C, N, and L and in shoots and roots. For example, L is the major factor controlling gene expression in leaves. However, in roots there is no obvious prominent signal, and signal interaction is stronger. The major signal interaction events detected genome wide in Arabidopsis roots are deciphered and summarized in a comprehensive conceptual model. Surprisingly, global analysis of gene expression in response to C, N, L, and O revealed that the number of genes controlled by a signal is proportional to the magnitude of the gene expression changes elicited by the signal. These results uncovered a strong constraining structure in plant cell signaling pathways, which prompted us to propose the existence of a “code” of signal integration.

作为固着生物，植物必须应对环境中多种且复合的信号变化。然而，目前鲜有研究探讨系统性信号组合对基因表达的全基因组层面影响。本研究通过构建二分类因子——碳（Carbon, C）、光（Light, L）与氮（Nitrogen, N）——在根与叶两类器官（Organ, O）中的析因组合下的全基因组表达模式模型，以此评估高水平的信号整合程度。碳、氮与光的信号调控模式在两类器官中存在显著差异：光是调控叶片基因表达的核心因子，但在根系中则无明显的主导信号，且信号间的互作效应更强。本研究解析并通过综合概念模型总结了拟南芥（Arabidopsis）根系全基因组范围内检测到的主要信号互作事件。令人意外的是，针对碳、氮、光及器官类型的基因表达全局分析显示，受某一信号调控的基因数量，与该信号诱导的基因表达变化幅度呈正相关。上述研究结果揭示了植物细胞信号通路中存在极强的约束性结构，这促使我们提出存在一套“信号整合编码”的假说。