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

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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.