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Parallel evolution of methyltransferases leads to vobasine biosynthesis in Tabernaemontana elegans and Catharanthus roseus

Farzana, M.; Richardson, M. B.; Deschenes, D. A. R.; Mai, Z.; Njoku, D. I.; Deslongchamps, G.; Qu, Y.

2024-07-29 biochemistry
10.1101/2024.07.28.605509 bioRxiv
Show abstract

Monoterpenoid indole alkaloids (MIA) are one of the largest and most complex alkaloid class in nature, boasting many clinically significant drugs such as anticancer vinblastine and antiarrhythmic ajmaline. Many MIAs undergo nitrogen N-methylation, altering their reactivity and affinity to the biological targets through a straightforward reaction. Remarkably, all known MIA N-methyltransferases (NMT) originate from the neofunctionalization of ancestral {gamma}-tocopherol C-methyltransferases ({gamma}TMTs), a phenomenon seemingly unique to the Apocynaceae family. In this study, we unveil and characterize a new {gamma}TMT-like enzyme from the plant Tabernaemontana elegans (toad tree): perivine N{beta}-methyltransferase (TePeNMT). TePeNMT and other homologs form a distinct clade in our phylogenetic study, setting them apart from other {gamma}TMTs and {gamma}TMT-like NMTs discovered to date. Enzyme kinetic experiments and enzyme homology modeling studies reveal the significant differences in enzyme active sites between TePeNMT and CrPeNMT, a previously characterized perivine N{beta}-methyltransferase from Catharanthus roseus (Madagascar periwinkle). Collectively, our findings suggest that parallel evolution of ancestral {gamma}TMTs may be responsible for the occurrence of perivine N-methylation in T. elegans and C. roseus.

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