Biochemistry

Abstract

CS-6-5 - A Hidden Biochemical State that Facilitated the Evolution of Betalain Pigmentation

Sunday, July 15
4:38 PM - 4:58 PM

Plants synthesize numerous natural products, which play crucial roles in plant adaptation and human health. In contrast to well-documented diversification of specialized metabolic enzymes, little is known about the evolution of primary metabolic enzymes that provide precursors to various specialized metabolic pathways.
The plant order Caryophyllales (e.g. beet, quinoa, cactus) uniquely produces red/yellow betalain pigments that are derived from the aromatic amino acid L-tyrosine (Tyr) and replaced the otherwise ubiquitous phenylalanine (Phe)-derived anthocyanins. In most plants, Tyr production is strongly feedback regulated by Tyr at arogenate dehydrogenase (TyrA), which catalyzes the final step of Tyr biosynthesis. Here, we found that TyrA enzymes in Caryophyllales recently duplicated into two isoforms, one of which (TyrAα) exhibits relaxed sensitivity to Tyr inhibition. Notably, the de-regulated TyrAα emerged before the evolution of the betalain biosynthetic pathway. Metabolite profiling further revealed that other Tyr-derived compounds, such as dopamine and epinephrine derivatives, also accumulate in TyrAα-containing Caryophyllales species. Phylogeny-guided structure function analysis of TyrA enzymes from over one hundred of Caryophyllales transcriptome data identified key mutations responsible for the Tyr insensitivity of TyrAα enzymes. Finally, heterologous expression of beet TyrAα in various plants Nicotiana benthamiana and Arabidopsis thaliana resulted in hyper-accumulation of Tyr and decreased synthesis of Phe and Phe-derived metabolites including anthocyanins.

These results together suggest that de-regulation of Tyr biosynthesis redirected carbon flux from Phe to Tyr biosynthesis and provided a hidden evolutionary state for the subsequent evolution of novel specialized metabolic pathways—e.g. biosynthesis of betalain pigments and other Tyr-derived metabolites. Our finding also highlights the significance of upstream primary metabolic regulation for the diversification of specialized metabolism in plants, and provides novel engineering tools to improve the production of Tyr and Tyr-derived natural products, such as morphine alkaloid and vitamin E.

Co-Authors

Samuel Lopez-Nieves – University of Wisconsin-Madison Yang Ya – University of Minnesota Tao Feng – University of Cambridge Alfonso Timoneda – University of Cambridge Marcos Oliveira – Univeristy of Wisconsin-Madison Stephan Smith – University of Michigan Samuel F. Brockington – University of Cambridge

Hiroshi A. Maeda

Associate Professor
University of Wisconsin-Madison

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CS-6-5 - A Hidden Biochemical State that Facilitated the Evolution of Betalain Pigmentation



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