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Acylphloroglucinol biosynthesis in strawberry fruit

Song, Chuankui, Ring, Ludwig, Hoffmann, Thomas, Huang, Fong-Chin, Slovin, Janet P., Schwab, Wilfried
Plant physiology 2015 v.169 no.3 pp. 1656-1670
Fragaria ananassa, amino acids, anthocyanins, biosynthesis, catalysts, chalcone, condensation, diploidy, evolutionary adaptation, fruit crops, fruits, genes, genetic techniques and protocols, glucosides, isotope labeling, malonyl coenzyme A, metabolites, naringenin, naringenin-chalcone synthase, phenolic compounds, phytopharmaceuticals, proteins, ripening, strawberries, transgenic plants
Phenolics have health-promoting properties and are a major group of metabolites in fruit crops. Through reverse genetic analysis of the functions of four ripening-related genes in the octoploid strawberry, Fragaria Ă—ananassa, we discovered four acylphloroglucinol (APG)-glucosides as native strawberry fruit metabolites whose levels were differently regulated in the transgenic fruits. The biosynthesis of the APG aglycones was investigated by examination of the enzymatic properties of three recombinant F. vesca chalcone synthase (FvCHS) proteins. CHS is involved in anthocyanin biosynthesis during ripening. The diploid strawberry enzymes readily catalyzed the condensation of two intermediates in branched-chain amino acids metabolism, isovaleryl-CoA and isobutyryl-CoA, with three molecules of malonyl-CoA to form phlorisovalerophenone and phlorisobutyrophenone, respectively, and formed naringenin chalcone when 4-coumaroyl-CoA was used as starter molecule. Isovaleryl-CoA was the preferred starter substrate of FvCHS2-1. Suppression of CHS activity in both transient and stable CHS-silenced fruit resulted in a substantial decrease of APG glucosides and anthocyanins, and enhanced levels of volatiles derived from branched-chain amino acids. The proposed APG pathway was confirmed by feeding isotopically labeled amino acids. Thus, strawberry plants have the capacity to synthesize pharmaceutically important APGs using dual functional CHS/(phloriso)valerophenone synthases (VPS) that are expressed during fruit ripening. Duplication and adaptive evolution of CHS is the most probable scenario and might be generally applicable to other plants. The results highlight that important promiscuous gene function may be missed when annotation relies solely on in silico analysis.