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

Eric Soubeyrand, Timothy S. Johnson, Scott Latimer, Anna Block, Jeongim Kim, Thomas A. Colquhoun, Eugenio Butelli, Cathie Martin, Mark A. Wilson, Gilles J. Basseta

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

Land plants possess the unique capacity to derive the benzenoid moiety of the vital respiratory cofactor, ubiquinone (coenzyme Q), from phenylpropanoid metabolism via b-oxidation of p-coumarate to form 4-hydroxybenzoate. Approximately half of the ubiquinone in plants comes from this pathway; the origin of the rest remains enigmatic. In this study, Phe-[Ring-13 C6] feeding assays and gene network reconstructions uncovered a connection between the biosynthesis of ubiquinone and that of flavonoids in Arabidopsis (Arabidopsis thaliana). Quantification of ubiquinone in Arabidopsis and tomato (Solanum lycopersicum) mutants in flavonoid biosynthesis pinpointed the corresponding metabolic branch-point as lying between flavanone-3-hydroxylase and flavonoid-39-hydroxylase. Further isotopic labeling and chemical rescue experiments demonstrated that the B-ring of kaempferol is incorporated into ubiquinone. Moreover, heme-dependent peroxidase activities were shown to be responsible for the cleavage of B-ring of kaempferol to form 4-hydroxybenzoate. By contrast, kaempferol 3-b-D-glucopyranoside, dihydrokaempferol, and naringenin were refractory to peroxidative cleavage. Collectively, these data indicate that kaempferol contributes to the biosynthesis of a vital respiratory cofactor, resulting in an extraordinary metabolic arrangement where a specialized metabolite serves as a precursor for a primary metabolite. Evidence is also provided that the ubiquinone content of tomato fruits can be manipulated via deregulation of flavonoid biosynthesis.

Original languageEnglish (US)
Pages (from-to)2910-2921
Number of pages12
JournalPlant Cell
Volume30
Issue number12
DOIs
StatePublished - Dec 2018

Fingerprint

Ubiquinone
ubiquinones
kaempferol
biosynthesis
Flavonoids
flavonoids
Lycopersicon esculentum
Arabidopsis
tomatoes
Embryophyta
metabolites
naringenin
Gene Regulatory Networks
embryophytes
Solanum lycopersicum
phenylpropanoids
heme
Mixed Function Oxygenases
Heme
Peroxidase

ASJC Scopus subject areas

  • Plant Science
  • Cell Biology

Cite this

Soubeyrand, E., Johnson, T. S., Latimer, S., Block, A., Kim, J., Colquhoun, T. A., ... Basseta, G. J. (2018). The peroxidative cleavage of kaempferol contributes to the biosynthesis of the benzenoid moiety of ubiquinone in plants. Plant Cell, 30(12), 2910-2921. https://doi.org/10.1105/tpc.18.00688

The peroxidative cleavage of kaempferol contributes to the biosynthesis of the benzenoid moiety of ubiquinone in plants. / Soubeyrand, Eric; Johnson, Timothy S.; Latimer, Scott; Block, Anna; Kim, Jeongim; Colquhoun, Thomas A.; Butelli, Eugenio; Martin, Cathie; Wilson, Mark A.; Basseta, Gilles J.

In: Plant Cell, Vol. 30, No. 12, 12.2018, p. 2910-2921.

Research output: Contribution to journalArticle

Soubeyrand, E, Johnson, TS, Latimer, S, Block, A, Kim, J, Colquhoun, TA, Butelli, E, Martin, C, Wilson, MA & Basseta, GJ 2018, 'The peroxidative cleavage of kaempferol contributes to the biosynthesis of the benzenoid moiety of ubiquinone in plants', Plant Cell, vol. 30, no. 12, pp. 2910-2921. https://doi.org/10.1105/tpc.18.00688
Soubeyrand, Eric ; Johnson, Timothy S. ; Latimer, Scott ; Block, Anna ; Kim, Jeongim ; Colquhoun, Thomas A. ; Butelli, Eugenio ; Martin, Cathie ; Wilson, Mark A. ; Basseta, Gilles J. / The peroxidative cleavage of kaempferol contributes to the biosynthesis of the benzenoid moiety of ubiquinone in plants. In: Plant Cell. 2018 ; Vol. 30, No. 12. pp. 2910-2921.
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