The peroxidative cleavage of kaempferol contributes to the biosynthesis of the benzenoid moiety of ubiquinone in plants

Authors: SOUBEYRAND, ERIC - University Of Florida; JOHNSON, TIMOTHY - University Of Florida; LATIMER, SCOTT - University Of Florida; Block, Anna; KIM, JEONG-IM - University Of Florida; COLQUHOUN, THOMAS - University Of Florida; BUTELLI, EUGENIO - John Innes Center; MARTIN, CATHIE - John Innes Center; CHAPPLE, CLINT - Purdue University; BASSET, GILLES - University Of Florida

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/18/2018
Publication Date: 12/1/2018
Citation: Soubeyrand, E., Johnson, T.S., Latimer, S., Block, A.K., Kim, J., Colquhoun, T.A., Butelli, E., Martin, C., Chapple, C., Basset, G.J. 2018. The peroxidative cleavage of kaempferol contributes to the biosynthesis of the benzenoid moiety of ubiquinone in plants. The Plant Cell. 30:2910-2921. https://doi.org/10.1105/tpc.18.00688.
DOI: https://doi.org/10.1105/tpc.18.00688

Interpretive Summary: Human health is dependent upon numerous biochemical processes. The co-enzyme ubiquinone (Co-Q) is a compound that is important for human health due to its vital role in cellular respiration. Scientists from the University of Florida, ARS Gainesville, FL, Purdue University and the John Innes Center in the UK are working to uncover how plants make Co-Q with the goal to identify mechanisms to boost its production and enhance the nutritional value of plants. They have identified an unsuspected biosynthetic route for the production of Co-Q from the biosynthetic pathway that makes the UV protective/anti-oxidant compounds called flavonoids. This study reveals that upregulation of this pathway could lead to increased production of both Co-Q and flavonoids, two important nutraceuticals, making it an appealing target for crop improvement strategies.

Technical Abstract: Land plants possess the unique capacity to derive the benzenoid moiety of the vital respiratory cofactor, ubiquinone (coenzyme Q), from the metabolism of phenylpropanoids via the ß-oxidation of p-coumarate into 4-hydroxybenzoate. Approximately half of plant ubiquinone comes from this pathway; the origin of the other half, however, remains enigmatic. In this study, Phe-[Ring-13C6] feeding assays and gene network reconstructions uncovered the existence of a connection between the biosynthesis of ubiquinone and that of flavonoids. Ubiquinone quantification in a series of Arabidopsis knockouts corresponding to the central flavonoid biosynthetic pathway pinpointed the corresponding metabolic branch-point between the flavanone-3-hydroxylase and flavanone-3-hydroxylase catalyzed-reactions. Isotopic labeling and chemical rescue experiments demonstrated that B-ring of kaempferol is incorporated into ubiquinone. Furthermore, heme-dependent peroxidase activities were shown to be responsible for the cleavage of B-ring of kaempferol as 4-hydroxybenzoate. By contrast, kaempferol 3-ß-D-glucopyranoside, dihydrokaempferol, and naringenin were refractory to peroxidative cleavage. Collectively, these findings indicate that kaempferol contributes to the function of the plant mitochondrial respiratory chain, thus challenging the conventional notion that the role of flavonoids is restricted to secondary metabolism. Evidence is also shown that ubiquinone content of tomato fruits can be manipulated via deregulation of flavonoid biosynthesis.