MATE2 Mediates Vacuolar Sequestration of Flavonoid Glycosides and Glycoside Malonates in Medicago truncatula Page: 1,536
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The Plant Cell, Vol. 23: 1536-1555, April 2011, www.plantcell.org 2011 American Society of Plant Biologists
MATE2 Mediates Vacuolar Sequestration of Flavonoid
Glycosides and Glycoside Malonates in
Jian Zhao, David Huhman, Gail Shadle, Xian-Zhi He, Lloyd W. Sumner, Yuhong Tang, and Richard A. Dixon1
Plant Biology Division, Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401
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 3'-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
Anthocyanins and proanthocyanidins (PAs; also called con-
densed tannins) are abundant flavonoids found in seed coats,
leaves, fruits, flowers, and bark of many plant species (Ariga
et al., 1981; Gabetta et al., 2000; Gu et al., 2004; Dixon et al.,
2005). PAs and anthocyanins play protective roles against mi-
crobial pathogens, insect attack, and UV irradiation, and antho-
cyanins are commonly utilized to attract insect pollinators. For
humans, both classes of compounds have beneficial effects on
cardiac health, immunity, and longevity (Santos-Buelga and
Scalbert, 2000; Skibola and Smith, 2000), and the presence of
modest levels of PAs in the leaves and stems of protein-rich
forage crops is an important agronomic trait, as they protect
ruminant animals from pasture bloat, enhance ruminant nutrition,
and reduce protein degradation in silage (Lees, 1992).
Attempts to engineer PA production in the forage legume
alfalfa (Medicago sativa) have so far led to the accumulation of
anthocyanins rather than PAs (Peel et al., 2009). Flavan 3-ol-
derived PA oligomers and anthocyanins are derived from the
same precursors, anthocyanidins, and competition between
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findings presented in this article in accordance with the policy described
in the Instructions for Authors (www.plantcell.org) is: Richard A. Dixon
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these parallel pathways for metabolic flux might be an important
regulatory mechanism determining PA biosynthesis (Lepiniec
et al., 2006; Figure 1). Anthocyanidins (such as cyanidin, pelar-
gonidin, and delphinidin) from the flavonoid pathway can be
either immediately modified by glycosylation, acylation, and/or
methylation to generate diverse anthocyanins or further reduced
to generate flavan 3-ol precursors of PAs, such as epicatechin
formed by the action of anthocyanidin reductase (ANR; Figure 1;
Xie et al., 2003). Seeds of knockout mutants in ANR accumulate
many more anthocyanins than wild-type seeds (Marinova et al.,
2007b), and an inverse relationship between the expression of
ANR and anthocyanidin 3-O-glucosyltransferase has been dem-
onstrated for selective direction of cyanidin into either PA or
anthocyanin biosynthesis (Lee et al., 2005).
The family I glycosyltransferases UTG78G1 and UTG72L1
catalyze the glucosylation of anthocyanidins and epicatechin,
respectively (Modolo et al., 2007; Pang et al., 2008; Peel et al.,
2009). Glycosylation of epicatechin and cyanidin is essential for
their transport into the vacuole by the multidrug and toxin
extrusion transporters MATE1 and TT12 in the seed coats of
Medicago truncatula and Arabidopsis thaliana, respectively
(Marinova et al., 2007b; Zhao and Dixon, 2009; Figure 1). Many
flavonoid glycosides accumulate in the vacuole with acyl sub-
stituents on the sugar residues, but the exact function of the
acylation remains unclear. Whereas acylation with malonyl res-
idues has been suggested to be essential for the retention of
some glycosides within the vacuole (Matern et al., 1983), other
studies indicate the involvement of acylation in flavonoid trans-
port per se. For example, proton gradient-dependent vacuolar
uptake by unknown transporters of anthocyanidin-3-O-sinapoyl
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Zhao, Jian; Huhman, David; Shadle, Gail L.; He, Xian-Zhi; Sumner, Lloyd W.; Tang, Yuhong et al. MATE2 Mediates Vacuolar Sequestration of Flavonoid Glycosides and Glycoside Malonates in Medicago truncatula, article, April 2011; [Rockville, Maryland]. (digital.library.unt.edu/ark:/67531/metadc282595/m1/1/: accessed February 23, 2017), University of North Texas Libraries, Digital Library, digital.library.unt.edu; crediting UNT College of Arts and Sciences.