Biochemistry and Molecular Basis of Intracellular Flavonoid Transport in Plants

Abstract

Flavonoids are a biochemically diverse group of specialized metabolites in plants that are derived from phenylalanine. While the biosynthesis of the flavonoid aglycone is highly conserved across species and well characterized, numerous species-specific decoration steps and their relevance remained largely unexplored. The flavonoid biosynthesis takes place at the cytosolic side of the endoplasmatic reticulum (ER), but accumulation of various flavonoids was observed in the central vacuole. A universal explanation for the subcellular transport of flavonoids has eluded researchers for decades. Current knowledge suggests that a glutathione S-transferase-like protein (ligandin) protects anthocyanins and potentially proanthocyanidin precursors during the transport to the central vacuole. ABCC transporters and to a lower extend MATE transporters sequester anthocyanins into the vacuole. Glycosides of specific proanthocyanidin precursors are sequestered through MATE transporters. A P-ATPase in the tonoplast and potentially other proteins generate the proton gradient that is required for the MATE-mediated antiport. Vesicle-mediated transport of flavonoids from the ER to the vacuole is considered as an alternative or additional route.

Keywords: ABCC; MATE; anthocyanins; flavones; flavonoid accumulation; flavonoid biosynthesis; flavonoid transport; flavonols; ligandin; proanthocyanidins.

Figure 1

(a) Simplified illustration of the flavonoid biosynthesis. CHS (chalcone synthase), CHI (chalcone isomerase), FNS (flavone synthase), FLS (flavonol synthase), F3H (flavanone 3-hydroxylase), F3′H (flavonoid 3′-hydroxylase), F3′5′H (flavonoid 3′5′-hydroxylase), DFR (dihydroflavonol 4-reductase), ANS (anthocyanidin synthase), LAR (leucoanthocyanidin reductase), ANR (anthocyanidin reductase), UGT (UDP-dependent glycosyltransferase), AT (BAHD acyltransferase), and MT (methyltransferase). The successive decoration of anthocyanins with sugar moieties, acyl groups, and methyl groups is indicated by a circle with the names of the responsible enzymes. (b) Chemical structure of a flavylium sekeleton of anthocyanidins. Frequently modified positions are highlighted with red dots.

Figure 2

Simplified illustration of the intracellular flavonoid transport pathways. ABCC (ATP-binding cassette (ABC) subfamily C), ABCG (ABC subfamily G), MATE (Multidrug And Toxin Extrusion transporter), BTL-like (bilitranslocase-like), GFS9/TT9 (Green Fluorescent Seed 9/Transparent Testa 9), EXO70B1 (exocyst complex component), ER (Endoplasmatic Reticulum) and AVI (anthocyanin vacuolar inclusion). Strength of lines indicates the assumed relevance of these transport pathways.

Figure 3

Simplified summary of potential flavonoid transport routes and the involved agents. Example genes are named if the involvement in the transport of the respective compound was reported. Aglycones are not included in this table, because they might be able to pass membranes by diffusion. Vesicle transport is indicated by a dot, the lack of transport ability is indicated by a minus, a lack of knowledge about the transport ability is indicated by a question mark.