Biochemistry and Molecular Basis of Intracellular Flavonoid Transport in Plants

Overview

Journal Plants (Basel)

Date 2022 Apr 12

PMID 35406945

Authors

Boas Pucker

Dirk Selmar

Affiliations

Soon will be listed here.

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.

Citing Articles

Deciphering the anthocyanin metabolism gene network in tea plant (Camellia sinensis) through structural equation modeling.

Xia P, Chen M, Chen L, Yang Y, Ma L, Bi P BMC Genomics. 2024; 25(1):1093.

PMID: 39548396 PMC: 11568573. DOI: 10.1186/s12864-024-11012-8.

Downregulation of a Phi class glutathione -transferase gene in transgenic torenia yielded pale flower color.

Akagi M, Nakamura N, Tanaka Y Plant Biotechnol (Tokyo). 2024; 41(2):147-151.

PMID: 39463771 PMC: 11500598. DOI: 10.5511/plantbiotechnology.24.0409a.

Insights into physiological roles of flavonoids in plant cold acclimation.

Kitashova A, Lehmann M, Schwenkert S, Munch M, Leister D, Nagele T Plant J. 2024; 120(5):2269-2285.

PMID: 39453687 PMC: 11629739. DOI: 10.1111/tpj.17097.

Thermopriming Induces Time-Limited Tolerance to Salt Stress.

Korner T, Zinkernagel J, Rohlen-Schmittgen S Int J Mol Sci. 2024; 25(14).

PMID: 39062938 PMC: 11277441. DOI: 10.3390/ijms25147698.

Genetic factors explaining anthocyanin pigmentation differences.

Marin-Recinos M, Pucker B BMC Plant Biol. 2024; 24(1):627.

PMID: 38961369 PMC: 11221117. DOI: 10.1186/s12870-024-05316-w.

References

Appelhagen I, Nordholt N, Seidel T, Spelt K, Koes R, Quattrochio F . TRANSPARENT TESTA 13 is a tonoplast P3A -ATPase required for vacuolar deposition of proanthocyanidins in Arabidopsis thaliana seeds. Plant J. 2015; 82(5):840-9. DOI: 10.1111/tpj.12854. View

Pelletier M, Murrell J, Shirley B . Characterization of flavonol synthase and leucoanthocyanidin dioxygenase genes in Arabidopsis. Further evidence for differential regulation of "early" and "late" genes. Plant Physiol. 1997; 113(4):1437-45. PMC: 158268. DOI: 10.1104/pp.113.4.1437. View

Yang S, Jiang Y, Xu L, Shiratake K, Luo Z, Zhang Q . Molecular cloning and functional characterization of DkMATE1 involved in proanthocyanidin precursor transport in persimmon (Diospyros kaki Thunb.) fruit. Plant Physiol Biochem. 2016; 108:241-250. DOI: 10.1016/j.plaphy.2016.07.016. View

Marinova K, Pourcel L, Weder B, Schwarz M, Barron D, Routaboul J . The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+ -antiporter active in proanthocyanidin-accumulating cells of the seed coat. Plant Cell. 2007; 19(6):2023-38. PMC: 1955721. DOI: 10.1105/tpc.106.046029. View

Dai X, Zhuang J, Wu Y, Wang P, Zhao G, Liu Y . Identification of a Flavonoid Glucosyltransferase Involved in 7-OH Site Glycosylation in Tea plants (Camellia sinensis). Sci Rep. 2017; 7(1):5926. PMC: 5517534. DOI: 10.1038/s41598-017-06453-z. View

Pollastri M . Overview on the Rule of Five. Curr Protoc Pharmacol. 2012; Chapter 9:Unit 9.12. DOI: 10.1002/0471141755.ph0912s49. View

Kitamura S, Akita Y, Ishizaka H, Narumi I, Tanaka A . Molecular characterization of an anthocyanin-related glutathione S-transferase gene in cyclamen. J Plant Physiol. 2012; 169(6):636-42. DOI: 10.1016/j.jplph.2011.12.011. View

Pourcel L, Routaboul J, Kerhoas L, Caboche M, Lepiniec L, Debeaujon I . TRANSPARENT TESTA10 encodes a laccase-like enzyme involved in oxidative polymerization of flavonoids in Arabidopsis seed coat. Plant Cell. 2005; 17(11):2966-80. PMC: 1276023. DOI: 10.1105/tpc.105.035154. View

Ichino T, Fuji K, Ueda H, Takahashi H, Koumoto Y, Takagi J . GFS9/TT9 contributes to intracellular membrane trafficking and flavonoid accumulation in Arabidopsis thaliana. Plant J. 2014; 80(3):410-23. DOI: 10.1111/tpj.12637. View

10.

Martens S, Forkmann G, Britsch L, Wellmann F, Matern U, Lukacin R . Divergent evolution of flavonoid 2-oxoglutarate-dependent dioxygenases in parsley. FEBS Lett. 2003; 544(1-3):93-8. DOI: 10.1016/s0014-5793(03)00479-4. View

11.

Offen W, Martinez-Fleites C, Yang M, Kiat-Lim E, Davis B, Tarling C . Structure of a flavonoid glucosyltransferase reveals the basis for plant natural product modification. EMBO J. 2006; 25(6):1396-405. PMC: 1422153. DOI: 10.1038/sj.emboj.7600970. View

12.

Hu B, Zhao J, Lai B, Qin Y, Wang H, Hu G . LcGST4 is an anthocyanin-related glutathione S-transferase gene in Litchi chinensis Sonn. Plant Cell Rep. 2016; 35(4):831-43. DOI: 10.1007/s00299-015-1924-4. View

13.

Behrens C, Smith K, Iancu C, Choe J, Dean J . Transport of Anthocyanins and other Flavonoids by the Arabidopsis ATP-Binding Cassette Transporter AtABCC2. Sci Rep. 2019; 9(1):437. PMC: 6345954. DOI: 10.1038/s41598-018-37504-8. View

14.

Frangne N, Eggmann T, Koblischke C, Weissenbock G, Martinoia E, Klein M . Flavone glucoside uptake into barley mesophyll and Arabidopsis cell culture vacuoles. Energization occurs by H(+)-antiport and ATP-binding cassette-type mechanisms. Plant Physiol. 2002; 128(2):726-33. PMC: 148933. DOI: 10.1104/pp.010590. View

15.

Gomez C, Conejero G, Torregrosa L, Cheynier V, Terrier N, Ageorges A . In vivo grapevine anthocyanin transport involves vesicle-mediated trafficking and the contribution of anthoMATE transporters and GST. Plant J. 2011; 67(6):960-70. DOI: 10.1111/j.1365-313X.2011.04648.x. View

16.

Debeaujon I, Peeters A, Leon-Kloosterziel K, Koornneef M . The TRANSPARENT TESTA12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. Plant Cell. 2001; 13(4):853-71. PMC: 135529. DOI: 10.1105/tpc.13.4.853. View

17.

Luo J, Nishiyama Y, Fuell C, Taguchi G, Elliott K, Hill L . Convergent evolution in the BAHD family of acyl transferases: identification and characterization of anthocyanin acyl transferases from Arabidopsis thaliana. Plant J. 2007; 50(4):678-95. DOI: 10.1111/j.1365-313X.2007.03079.x. View

18.

Grotewold E, Chamberlin M, Snook M, Siame B, Butler L, Swenson J . Engineering secondary metabolism in maize cells by ectopic expression of transcription factors. Plant Cell. 1998; 10(5):721-40. PMC: 144024. View

19.

Alseekh S, de Souza L, Benina M, Fernie A . The style and substance of plant flavonoid decoration; towards defining both structure and function. Phytochemistry. 2020; 174:112347. DOI: 10.1016/j.phytochem.2020.112347. View

20.

Petrussa E, Braidot E, Zancani M, Peresson C, Bertolini A, Patui S . Plant flavonoids--biosynthesis, transport and involvement in stress responses. Int J Mol Sci. 2013; 14(7):14950-73. PMC: 3742282. DOI: 10.3390/ijms140714950. View