TY - JOUR
T1 - The peroxidative cleavage of kaempferol contributes to the biosynthesis of the benzenoid moiety of ubiquinone in plants
AU - Soubeyrand, Eric
AU - Johnson, Timothy S.
AU - Latimer, Scott
AU - Block, Anna
AU - Kim, Jeongim
AU - Colquhoun, Thomas A.
AU - Butelli, Eugenio
AU - Martin, Cathie
AU - Wilson, Mark A.
AU - Basseta, Gilles J.
N1 - Funding Information:
This work was supported by National Science Foundation grants (MCB-1608088 and MCB-1712608 to G.J.B.), and the USDA-ARS Floriculture and Nursery Research Initiative (to T.A.C.). The authors thank Pr. Joshua Widhalm at Purdue University for illuminating discussions about benzenoid metabolism, Pr. Clint Chapple at Purdue University for the gift of the ref3-4 and 4-cl3 knockouts, and Pr. Gloria K. Muday at Wake Forest University for the gift of the are mutant.
Funding Information:
This work was supported by National Science Foundation grants (MCB-1608088 and MCB-1712608 to G.J.B.), and the USDA-ARS Floriculture and Nursery Research Initiative (to T.A.C.).
Publisher Copyright:
© 2018 ASPB.
PY - 2018/12
Y1 - 2018/12
N2 - 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.
AB - 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.
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U2 - 10.1105/tpc.18.00688
DO - 10.1105/tpc.18.00688
M3 - Article
C2 - 30429224
AN - SCOPUS:85060628000
VL - 30
SP - 2910
EP - 2921
JO - Plant Cell
JF - Plant Cell
SN - 1040-4651
IS - 12
ER -