Origin and evolution of the nuclear auxin response system.
Origin and evolution of the nuclear auxin response system.
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DOI：
10.7554/elife.33399
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发表时间：
2018-03-27
期刊：
影响因子：
7.7
通讯作者：
Weijers D
中科院分区：
文献类型：
--
作者：
Mutte SK;Kato H;Rothfels C;Melkonian M;Wong GK;Weijers D
生长素是一种小信号分子，主要通过调节基因表达来控制陆地植物的许多发育过程。生长素反应蛋白是由具有不同功能的大家族所代表的，但它们的起源和进化都不清楚。在这里，我们使用深度系统基因组学方法来重建所有核生长素反应蛋白家族的起源和进化轨迹。我们发现，虽然所有的亚域都是古老的，但完整的生长素反应机制仅限于陆地植物。功能系统基因组学预测了反应系统特性进化的明确步骤，跨六个古老谱系的比较转录组学揭示了这些创新如何形成复杂的反应机制。对一种陆生植物的遗传分析揭示了古代非规范蛋白对生长素反应的意外贡献以及核心转录因子与生长素无关的功能。我们的研究为理解生长素信号的不同功能提供了一个功能进化框架。在所有的生命领域，信号分子，如激素，控制着生物体生命的许多方面，包括它们如何生长和发育。细胞有专门的蛋白质，可以识别信号分子，传递信息，并对信号做出反应，例如通过打开或关闭基因。这种反应系统通常由多个组成部分组成，并且，在整个进化过程中，这些反应组成部分经常被复制，以至于许多物种都有每个反应组成部分的多个不同版本。生长素是一种植物激素，控制着植物几乎所有的生长和发育过程，包括作物的许多产量性状。然而，没有人知道为什么它会参与这么多的过程。这部分是因为我们不清楚这种中枢信号分子的反应系统是如何诞生的，或者它是如何增加其复杂性的。为了解决这个问题，Mutte， Kato等人探索了超过1000种植物的遗传信息，包括藻类，它们跨越了7亿年的进化。他们的分析表明，所有生长素反应成分都是由更古老的基因片段组装而成的，但它们最初是在植物征服陆地时聚集在一起的。事实上，生长素的反应似乎是在一个现存的基因调节器之上发展起来的，这个基因调节器仍然存在于现代藻类中。Mutte， Kato等人随后使用实验来展示生长素反应成分的数量和类型的逐步增加如何在陆地植物中形成复杂的反应，并展示了古老的成分如何控制生长素反应。综上所述，这些发现为理解植物中生长素的许多功能以及它是如何产生的提供了一个框架。它们还展示了信号反应途径的复杂性是如何实现的，以及基因家族的多样性是如何进化的。对植物及其以外的其他反应系统的类似研究可能有助于揭示激素反应进化和基因调控系统多样化的共同原理。
The small signaling molecule auxin controls numerous developmental processes in land plants, acting mostly by regulating gene expression. Auxin response proteins are represented by large families of diverse functions, but neither their origin nor their evolution is understood. Here, we use a deep phylogenomics approach to reconstruct both the origin and the evolutionary trajectory of all nuclear auxin response protein families. We found that, while all subdomains are ancient, a complete auxin response mechanism is limited to land plants. Functional phylogenomics predicts defined steps in the evolution of response system properties, and comparative transcriptomics across six ancient lineages revealed how these innovations shaped a sophisticated response mechanism. Genetic analysis in a basal land plant revealed unexpected contributions of ancient non-canonical proteins in auxin response as well as auxin-unrelated function of core transcription factors. Our study provides a functional evolutionary framework for understanding diverse functions of the auxin signal. Across all kingdoms of life, signaling molecules like hormones, for example, control many aspects of the lives of organisms, including how they grow and develop. Cells have dedicated proteins that can recognize the signaling molecules, relay the information, and respond to the signal, for example by switching genes on or off. Such response systems usually consist of multiple components, and, throughout evolution, these response components have regularly been copied such that many species have multiple different versions of each one. Auxin is a plant hormone that controls virtually all growth and developmental processes in plants, including many yield traits in crops. However, no one knows why it is involved in so many processes. This is partly because it is not clear how the response system for this central signaling molecule was first born, or how it has increased in its complexity. To address this, Mutte, Kato et al. explored the genetic information of more than a thousand plant species, including algae, which span more than 700 million years of evolution. Their analysis showed that all auxin response components were assembled from pieces of much older genes, but that they first came together when plants conquered land. Indeed, the auxin response appears to have developed on top of a pre-existing genetic regulator that is still present in modern-day algae. Mutte, Kato et al. then used experiments to show how stepwise increases in the number and types of auxin response components have shaped sophisticated, complex responses in land plants, and to demonstrate how ancient components control auxin response. Together these findings provide a framework for understanding the many functions of auxin in plants, and how this came to be. They also show how complexity can be accomplished in a signal response pathway, and how diversity evolves in gene families. Similar studies on other response systems in plants and beyond are likely to help reveal common principles of hormone response evolution and diversification of gene regulation systems.