Malonylation is a key reaction in the metabolism of xenobiotic phenolic glucosides in Arabidopsis and tobacco

Taguchi, Goro; Ubukata, Takahisa; Nozue, Hatsumi; Kobayashi, Yuki; Takahi, Maki; Yamamoto, Haruhiko; Hayashida, Nobuaki

doi:10.1111/j.1365-313x.2010.04298.x

Cited by 96 publications

(90 citation statements)

References 38 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…However, the precise physiological function of flavonoid malonylation has yet to be defined (Boller and Wiemken, 1986;Springob et al, 2003;Luo et al, 2007;Yu et al, 2008). A role for malonylation in targeting compounds for vacuolar transport as opposed to extracellular secretion is supported by the recent demonstration that malonylation of xenobiotic phenolic glucosides leads to their preferential transport to the vacuole in Arabidopsis (Taguchi et al, 2010).…”

Section: Mate2 Preferentially Transports Malonylated Flavonoidsmentioning

confidence: 84%

MATE2 Mediates Vacuolar Sequestration of Flavonoid Glycosides and Glycoside Malonates inMedicago truncatula

et al. 2011

View full text Add to dashboard Cite

The majority of flavonoids, such as anthocyanins, proanthocyanidins, and isoflavones, are stored in the central vacuole, but the molecular basis of flavonoid transport is still poorly understood. Here, we report the functional characterization of a multidrug and toxin extrusion transporter (MATE2), from Medicago truncatula. MATE 2 is expressed primarily in leaves and flowers. Despite its high similarity to the epicatechin 39-O-glucoside transporter MATE1, MATE2 cannot efficiently transport proanthocyanidin precursors. In contrast, MATE2 shows higher transport capacity for anthocyanins and lower efficiency for other flavonoid glycosides. Three malonyltransferases that are coexpressed with MATE2 were identified. The malonylated flavonoid glucosides generated by these malonyltransferases are more efficiently taken up into MATE2-containing membrane vesicles than are the parent glycosides. Malonylation increases both the affinity and transport efficiency of flavonoid glucosides for uptake by MATE2. Genetic loss of MATE2 function leads to the disappearance of leaf anthocyanin pigmentation and pale flower color as a result of drastic decreases in the levels of various flavonoids. However, some flavonoid glycoside malonates accumulate to higher levels in MATE2 knockouts than in wild-type controls. Deletion of MATE2 increases seed proanthocyanidin biosynthesis, presumably via redirection of metabolic flux from anthocyanin storage.

show abstract

Section: Mate2 Preferentially Transports Malonylated Flavonoidsmentioning

confidence: 84%

MATE2 Mediates Vacuolar Sequestration of Flavonoid Glycosides and Glycoside Malonates inMedicago truncatula

et al. 2011

View full text Add to dashboard Cite

show abstract

“…The conserved HXXXD and DFGWG motifs are characteristic for almost all family members. So far, most of the characterized enzymes can be categorized into three functional classes: alcohol acetyl-transferases (Dudareva and Pichersky, 2000;D'Auria et al, 2002D'Auria et al, , 2007a, anthocyanin/flavonoid acyl-transferases (Suzuki et al, 2001;D'Auria et al, 2007b;Luo et al, 2007;Yu et al, 2008;Taguchi et al, 2010), and hydroxycinnamoyltransferases (Luo et al, 2009;Gou et al, 2009;Molina et al, 2009).…”

mentioning

confidence: 99%

ArabidopsisDeficient in Cutin FerulateEncodes a Transferase Required for Feruloylation of ω-Hydroxy Fatty Acids in Cutin Polyester

et al. 2011

View full text Add to dashboard Cite

The cuticle is a complex aliphatic polymeric layer connected to the cell wall and covers surfaces of all aerial plant organs. The cuticle prevents nonstomatal water loss, regulates gas exchange, and acts as a barrier against pathogen infection. The cuticle is synthesized by epidermal cells and predominantly consists of an aliphatic polymer matrix (cutin) and intracuticular and epicuticular waxes. Cutin monomers are primarily C 16 and C 18 unsubstituted, v-hydroxy, and a,v-dicarboxylic fatty acids. Phenolics such as ferulate and p-coumarate esters also contribute to a minor extent to the cutin polymer. Here, we present the characterization of a novel acyl-coenzyme A (CoA)-dependent acyl-transferase that is encoded by a gene designated Deficient in Cutin Ferulate (DCF). The DCF protein is responsible for the feruloylation of v-hydroxy fatty acids incorporated into the cutin polymer of aerial Arabidopsis (Arabidopsis thaliana) organs. The enzyme specifically transfers hydroxycinnamic acids using v-hydroxy fatty acids as acyl acceptors and hydroxycinnamoyl-CoAs, preferentially feruloyl-CoA and sinapoyl-CoA, as acyl donors in vitro. Arabidopsis mutant lines carrying DCF loss-of-function alleles are devoid of rosette leaf cutin ferulate and exhibit a 50% reduction in ferulic acid content in stem insoluble residues. DCF is specifically expressed in the epidermis throughout all green Arabidopsis organs. The DCF protein localizes to the cytosol, suggesting that the feruloylation of cutin monomers takes place in the cytoplasm.The cuticle, a complex polymeric layer connected to the cell wall of epidermal cells, covers the surfaces of all aerial plant organs. The cuticle prevents nonstomatal water loss, regulates gas exchange, acts as a barrier against pathogen infection, and prevents organ fusions (Lolle et al., 1998;Sieber et al., 2000). The plant cuticle is synthesized by epidermal cells and predominantly consists of a lipophilic polymer matrix (cutin) and intracuticular and epicuticular waxes. Cutin monomers are primarily aliphatic C 16 and C 18 unsubstituted, v-hydroxy, and a,v-dicarboxylic fatty acids. Polyhydroxy fatty acids, fatty alcohols, phenolic acids such as ferulic and p-coumaric acid, and glycerol may also contribute to cutin composition in different plant species (Baker and Martin, 1963;Kolattukudy, 1980;Pollard et al., 2008;Samuels et al., 2008;Schreiber, 2010).In Arabidopsis (Arabidopsis thaliana), several enzymes have been identified to be involved in cutin monomer synthesis and polymerization processes, such as glycerol-3-phosphate acyl-transferases 4 and 8 (Li et al., 2007), Bodyguard (Kurdyukov et al., 2006), and Defective in Cuticular Ridges (DCR), a BAHD family enzyme involved in cutin polyester synthesis in Arabidopsis roots, flowers, and seeds. DCR mutant lines are characterized by an almost complete lack of 9 (10),16-dihydroxy-hexadecanoic acid, a major component of the flower cutin polymer, accompanied by several cuticle-associated phenotypic alterations in response to abiotic stresses (e.g. impa...

show abstract

“…Malonyl-CoA is the precursor for the de novo synthesis and elongation of fatty acids (Baud et al, 2003(Baud et al, , 2004 as well as the formation of flavonoids, isoflavonoids, stilbenoids (Peer et al, 2001), and many malonylated compounds, including malonylated 1-aminocyclopropane-1-carboxylic acid, D-amino acids, and flavonoid glycosides (Liu et al, 1984;Taguchi et al, 2010). In eukaryotic cells, it has been generally accepted that malonylCoA is formed almost exclusively by acetyl-CoA carboxylase (ACCase; EC 6.4.1.2) that catalyzes the ATP-dependent formation of malonyl-CoA from acetyl-CoA and bicarbonate.…”

Section: Introductionmentioning

confidence: 99%

Malonyl-CoA Synthetase, Encoded by ACYL ACTIVATING ENZYME13, Is Essential for Growth and Development of Arabidopsis

et al. 2011

View full text Add to dashboard Cite

Malonyl-CoA is the precursor for fatty acid synthesis and elongation. It is also one of the building blocks for the biosynthesis of some phytoalexins, flavonoids, and many malonylated compounds. In plants as well as in animals, malonyl-CoA is almost exclusively derived from acetyl-CoA by acetyl-CoA carboxylase (EC 6.4.1.2). However, previous studies have suggested that malonyl-CoA may also be made directly from malonic acid by malonyl-CoA synthetase (EC 6.2.1.14). Here, we report the cloning of a eukaryotic malonyl-CoA synthetase gene, Acyl Activating Enzyme13 (AAE13; At3g16170), from Arabidopsis thaliana. Recombinant AAE13 protein showed high activity against malonic acid (K m = 529.4 ± 98.5 μM; V m = 24.0 ± 2.7 μmol/mg/min) but little or no activity against other dicarboxylic or fatty acids tested. Exogenous malonic acid was toxic to Arabidopsis seedlings and caused accumulation of malonic and succinic acids in the seedlings. aae13 null mutants also grew poorly and accumulated malonic and succinic acids. These defects were complemented by an AAE13 transgene or by a bacterial malonyl-CoA synthetase gene under control of the AAE13 promoter. Our results demonstrate that the malonyl-CoA synthetase encoded by AAE13 is essential for healthy growth and development, probably because it is required for the detoxification of malonate.

show abstract

Malonylation is a key reaction in the metabolism of xenobiotic phenolic glucosides in Arabidopsis and tobacco

Cited by 96 publications

References 38 publications

MATE2 Mediates Vacuolar Sequestration of Flavonoid Glycosides and Glycoside Malonates inMedicago truncatula

MATE2 Mediates Vacuolar Sequestration of Flavonoid Glycosides and Glycoside Malonates inMedicago truncatula

ArabidopsisDeficient in Cutin FerulateEncodes a Transferase Required for Feruloylation of ω-Hydroxy Fatty Acids in Cutin Polyester

Malonyl-CoA Synthetase, Encoded by ACYL ACTIVATING ENZYME13, Is Essential for Growth and Development of Arabidopsis

Contact Info

Product

Resources

About