Understanding the evolution of adaptive traits has long been the central topic of evolutionary biology. But, elucidating their evolutionary history remains a big challenge, because it requires genomic information across closely related species, detailed knowledge on the genetic basis of adaptive traits, and availability of sophisticated phylogenomic tools. My work in this thesis provides new insights on this fascinating topic. First, I analyzed the evolution history of Nicotiana genomes. The results showed that the genomes experienced a whole-genome triplication (WGT) event and a repertoire of rapidly expanding transposable elements (TE) bloated the Nicotiana genomes. Phylogenomic analysis showed that the nicotine biosynthetic pathway gradually evolved from two duplicated ancient primary metabolic pathways followed by the rapid acquisition of root-specific gene expression. Second, the early defense signaling was analyzed in detail with six Nicotiana species. This analysis revealed a key gene co-expression network that is co-activated with herbivore associated elicitors induced by jasmonate acid accumulations. Again, the results showed that numerous TE insertions in regulatory regions and gene retention after the WGT are involved and promoted the evolution of this key network that might lead to increased network complexity and robustness. Finally, I developed an interactive platform: the Nicotiana attenuata Data Hub (NaDH). Genomic, phylogenetic, transcriptomic and metabolomic data were used to form this comprehensive toolbox which allows users to explore and visualize the complex datasets, infer gene functions and to reconstruct biosynthetic pathways. In conclusion, this dissertation sheds light on how gene duplications and TE insertions facilitate the evolution of multigene metabolic pathways in plants and will further enhance N. attenuata as a model organism for studying plant-environment interactions and the evolution of adaptive traits in plants.
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