NSFDEB-NERC; Collaborative Resource; A phytochemical "tug-of-war" and its impact on organismal diversification and niche occupancy in Caryophyllales

我们的工作旨在了解灌输植物的复杂的专门化代谢性状的逐步进化，并探索这些性状的进化如何影响开花植物随后的适应和多样化。为了解决这些问题，我们将重点关注开花植物目石竹目，它以对极端环境的非凡适应和来自氨基酸酪氨酸的代谢产物的异常高度多样性而被公认。我们的中心假设是，石竹目中酪氨酸的可获得性和丰度的变化导致了许多谱系特有的酪氨酸衍生代谢物的进化，而这些代谢产物反过来又深刻地影响了石竹目物种的适应性和多样性。为了验证这一假设，我们将为石竹目建立一个进化框架，该框架整合了转录、基因组和代谢数据集，以及宏观进化尺度上的特征进化模式。具体地说，我们将：1)进行广泛的调查，以确定酪氨酸衍生的代谢性状在石竹目中的出现和分布；2)检查这些酪氨酸衍生的代谢性状与组织适应不良和多样化模式的关联；以及3)确定导致这些代谢物生物合成的进化遗传机制。在拟议的工作完成后，我们预计将全面描述石竹目富含酪氨酸的新陈代谢的程度，定义它们与整个石竹目生物多样性模式的关联程度，并解决复杂酪氨酸衍生代谢途径背后的遗传路径的逐步进化组装。理解复杂性状的进化是生物学家面临的一个根本挑战，因为此类性状的逐步进化并不总是显而易见的。此外，复杂性状组合的不同阶段(如遗传、生化和形态)与随后的组织多样化模式之间的联系还没有得到很好的探索，方法论方法还处于起步阶段。随着基因组规模数据的整合，系统发育学的最新进展现在提供了及时的机会，将复杂特征的集合与特定谱系和特定生态位的生物多样性结合起来。专门化代谢物是在某些生态和进化背景下赋予适应性优势的化学物质。复杂的专门化代谢物背后的生物合成途径的阶梯性质确保了它们对于重建复杂性的阶梯进化特别容易处理。而特定代谢物的系统发育受限分布是解决复杂性状对生态位特定和线特定的组织适应和多样化的影响的基础。因此，我们的方法，使用石竹目丰富的酪氨酸专门化代谢作为模型系统，有可能导致对各种进化尺度上复杂性状进化组装的原因和结果的新的和基本的见解。

Our proposed work seeks to understand the step-wise evolution of complex specialized metabolic traits inflowering plants, and to explore how the evolution of such traits influence subsequent adaptation anddiversification in flowering plants. To address these questions, we will focus on the flowering plant orderCaryophyllales, which is well recognized for extraordinary adaptations to extreme environments andunusually high diversity of metabolites derived from the amino-acid Tyrosine. Our central hypothesis isthat changes in availability and abundance of Tyrosine in Caryophyllales has led to the evolution ofnumerous lineage-specific tyrosine-derived metabolites that in turn has profoundly influenced theadaptation and diversification of species within Caryophyllales. To test this hypothesis, we will build anevolutionary framework for Caryophyllales, that integrates transcriptomic, genomic, and metabolicdatasets, with patterns of trait evolution, on a macroevolutionary scale. Specifically, we will: 1) performan extensive survey to establish the occurrence and distribution of tyrosine-derived metabolic traits acrossCaryophyllales; 2) examine the association of these tyrosine-derived metabolic traits with organismaladaptation and diversification patterns; and 3) determine the evolutionary genetic mechanisms responsiblefor the biosynthesis of these metabolites. On completion of the proposed work, we expect to havecomprehensively described the extent of tyrosine-enriched metabolism in Caryophyllales, to have definedthe degree to which they are associated with organismal diversification patterns across Caryophyllales,and to have resolved the stepwise evolutionary assembly of the genetic pathways underlying complextyrosine-derived metabolic traits.Understanding the evolution of complex traits is a fundamental challenge for biologists, as the stepwisefashion by which such traits have evolved is not always readily apparent. Furthermore, the connectionsbetween the various stages of complex trait assembly (e.g. genetic, biochemical, and morphological) andsubsequent organismal diversification patterns are not well explored, with methodological approachesstill in their infancy. Recent advances in phylogenetics, with the integration of -omic scale data, nowprovide timely opportunities to marry the assembly of complex traits with lineage-specific and nichespecificorganismal diversification. Specialized metabolites are chemicals that confer adaptive advantagesin certain ecological and evolutionary contexts. The stepwise nature of the biosynthetic pathwaysunderlying complex specialized metabolites ensure that they are especially tractable for reconstructingstepwise evolution of complexity. While the phylogenetically restricted distributions of specializedmetabolites are fundamental to resolving the influence of complex traits on niche-specific and lineagespecificorganismal adaptation and diversification. Our approach, using the tyrosine-enriched specializedmetabolism in Caryophyllales as a model system, therefore has the potential to lead to new andfundamental insights into the causes and consequences of the evolutionary assembly of complex traits at avariety of evolutionary scales.