Convergent evolution of the UbiA prenyltransferase family underlies the independent acquisition of furanocoumarins in plants

Abstract

Furanocoumarins (FCs) are plant-specialized metabolites with potent allelochemical properties. The distribution of FCs is scattered with a chemotaxonomical tendency towards four distant families with highly similar FC pathways. The mechanism by which this pathway emerged and spread in plants has not been elucidated. Furanocoumarin biosynthesis was investigated in Ficus carica (fig, Moraceae), focusing on the first committed reaction catalysed by an umbelliferone dimethylallyltransferase (UDT). Comparative RNA-seq analysis among latexes of different fig organs led to the identification of a UDT. The phylogenetic relationship of this UDT to previously reported Apiaceae UDTs was evaluated.The expression pattern of F. carica prenyltransferase 1 (FcPT1) was related to the FC contents in different latexes. Enzymatic characterization demonstrated that one of the main functions of FcPT1 is UDT activity. Phylogenetic analysis suggested that FcPT1 and Apiaceae UDTs are derived from distinct ancestors, although they both belong to the UbiA superfamily. These findings are supported by significant differences in the related gene structures.This report describes the identification of FcPT1 involved in FC biosynthesis in fig and provides new insights into multiple origins of the FC pathway and, more broadly, into the adaptation of plants to their environments.

A new P450 involved in the furanocoumarin pathway underlies a recent case of convergent evolution

“…CYP76F112 was shown to be a selective and efficient enzyme that interacts with high specificity and affinity with DMS. Moreover, CYP76F112 is preferentially expressed in petiole latex (Table S6), which is consistent with both the repartition of linear furanocoumarins in F. carica (Kitajima et al ., 2018) and the expression patterns of FcPT1 (Munakata et al ., 2020). Taken together, these results led us to conclude that the conversion of DMS into marmesin described here might be the primary physiological function of CYP76F112.…”

“…For instance, DMS is necessary for the biosynthesis of downstream furanocoumarins (Fig. 1b) and its biosynthesis is supported by Fc PT1 activity (Munakata et al ., 2020). However, it has never been described in Ficus phytochemical analyses.…”

Parallel evolution of UbiA superfamily proteins into aromaticO-prenyltransferases in plants

“…However, the transcript corresponding to c22985_g1_i1 seems to be nonfunctional, due to the lack of a coding region containing the second aspartate-rich motif that is essential for prenylation reactions in UbiA proteins 24,25 . In silico analysis predicted that the polypeptides CpPT1 and CpPT2 each include two aspartate-rich motifs, multiple transmembrane regions, and transit peptides (TPs), all of which are characteristics of plant UbiA PT proteins [20][21][22][23] ( Supplementary Fig. 3).…”

“…Coumarin and FC derivatives without a hydroxy group at C5 or C8, as well as molecules in other phenolic classes (No. [19][20][21][22][23][24][25], were not recognized as substrates.…”

“…21), flavonoids(22)(23)(24) and homogentisic acid(25) were tested as possible prenyl acceptor substrates of CpPT1. Dimethylallyl diphosphate (DMAPP), geranyl diphosphate (GPP), and farnesyl diphosphate (FPP) were tested as possible prenyl donor substrates.…”