Citronellol biosynthesis in pelargonium is a multistep pathway involving progesterone 5β-reductase and/or iridoid synthase-like enzymes - Archive ouverte HAL
Article Dans Une Revue Plant Physiology Année : 2024

Citronellol biosynthesis in pelargonium is a multistep pathway involving progesterone 5β-reductase and/or iridoid synthase-like enzymes

Sébastien Fiorucci
Frédéric Schiets

Résumé

Citronellol is a pleasant-smelling compound produced in rose (Rosa spp.) flowers and in the leaves of many aromatic plants, including pelargoniums (Pelargonium spp.). Although geraniol production has been well studied in several plants, citronellol biosynthesis has been documented only in crab-lipped spider orchid (Caladenia plicata) and its mechanism remains open to question in other species. We therefore profiled 10 pelargonium accessions using RNA sequencing and gas chromatography-MS analysis. Three enzymes from the progesterone 5β-reductase and/or iridoid synthase-like enzymes (PRISE) family were characterized in vitroand subsequently identified as citral reductases (named PhCIRs). Transgenic RNAi lines supported a role for PhCIRs in the biosynthesis of citronellol as well as in the production of mint-scented terpenes. Despite their high amino acid sequence identity, the 3 enzymes showed contrasting stereoselectivity, either producing mainly (S)-citronellal or a racemate of both (R)- and (S)-citronellal. Using site-directed mutagenesis, we identified a single amino acid substitution as being primarily responsible for the enzyme's enantioselectivity. Phylogenetic analysis of pelargonium PRISEs revealed 3 clades and 7 groups of orthologs. PRISEs from different groups exhibited differential affinities toward substrates (citral and progesterone) and cofactors (NADH/NADPH), but most were able to reduce both substrates, prompting hypotheses regarding the evolutionary history of PhCIRs. Our results demonstrate that pelargoniums evolved citronellol biosynthesis independently through a 3-step pathway involving PRISE homologs and both citral and citronellal as intermediates. In addition, these enzymes control the enantiomeric ratio of citronellol thanks to small alterations of the catalytic site.
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hal-04695870 , version 1 (16-09-2024)

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Laure Martinelli, Camille Bihanic, Aurélie Bony, Florence Gros, Corentin Conart, et al.. Citronellol biosynthesis in pelargonium is a multistep pathway involving progesterone 5β-reductase and/or iridoid synthase-like enzymes. Plant Physiology, 2024, 194 (2), pp.1006-1023. ⟨10.1093/plphys/kiad550⟩. ⟨hal-04695870⟩
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