Two differentially expressed MATE factor genes from apple complement the Arabidopsis transparent testa12 mutant

Frank S, Keck M, Sagasser M, Niehaus K, Weisshaar B, Stracke R (2011)
Plant Biology 13(1): 42-50.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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Autor*in
Frank, SandraUniBi; Keck, MatthiasUniBi; Sagasser, MartinUniBi; Niehaus, KarstenUniBi; Weisshaar, BerndUniBi ; Stracke, RalfUniBi
Einrichtung
Fakultät für Biologie > Genetik und Genomik der Pflanzen
Fakultät für Biologie > Proteom- und Metabolomforschung
Centrum für Biotechnologie > Institut für Genomforschung und Systembiologie
Centrum für Biotechnologie > Arbeitsgruppe K. Niehaus
Centrum für Biotechnologie > Arbeitsgruppe B. Weisshaar
Abstract / Bemerkung
Proanthocyanidins (PAs) are a class of flavonoids with numerous functions in plant ecology and development, including protection against microbial infection, animal foraging and damage by UV light. PAs are also beneficial in the human diet and livestock farming, preventing diseases of the cardiovascular system and lowering the risk of cancer, asthma and diabetes. Apples (Malus x domestica Borkh.) are naturally rich in flavonoids, but the flavonoid content and composition varies significantly between cultivars. In this work, we applied knowledge from the model plant Arabidopsis thaliana, for which the main features of flavonoid biosynthesis have been elucidated, to investigate PA accumulation in apple. We identified functional homologues of the Multidrug And Toxic compound Extrusion (MATE) gene TRANSPARENT TESTA12 from A. thaliana using a comparative genomics approach. MdMATE1 and MdMATE2 were differentially expressed, and the function of the encoded proteins was verified by complementation of the respective A. thaliana mutant. In addition, MdMATE genes have a different gene structure in comparison to homologues from other species. Based on our findings, we propose that MdMATE1 and MdMATE2 are vacuolar flavonoid/H(+) -antiporters, active in PA accumulating cells of apple fruit. The identification of these flavonoid transporter genes expands our understanding of secondary metabolite biosynthesis and transport in apple, and is a prerequisite to improve the nutritional value of apples and apple-derived beverages.
Stichworte
transparent testa12 (tt12); flavonoid biosynthesis; Malus x domestica; MATE transporter; proanthocyanidins; Arabidopsis thaliana
Erscheinungsjahr
2011
Zeitschriftentitel
Plant Biology
Band
13
Ausgabe
1
Seite(n)
42-50
ISSN
1435-8603
Page URI
https://pub.uni-bielefeld.de/record/1896541

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Frank S, Keck M, Sagasser M, Niehaus K, Weisshaar B, Stracke R. Two differentially expressed MATE factor genes from apple complement the Arabidopsis transparent testa12 mutant. Plant Biology. 2011;13(1):42-50.
Frank, S., Keck, M., Sagasser, M., Niehaus, K., Weisshaar, B., & Stracke, R. (2011). Two differentially expressed MATE factor genes from apple complement the Arabidopsis transparent testa12 mutant. Plant Biology, 13(1), 42-50. https://doi.org/10.1111/j.1438-8677.2010.00350.x
Frank, Sandra, Keck, Matthias, Sagasser, Martin, Niehaus, Karsten, Weisshaar, Bernd, and Stracke, Ralf. 2011. “Two differentially expressed MATE factor genes from apple complement the Arabidopsis transparent testa12 mutant”. Plant Biology 13 (1): 42-50.
Frank, S., Keck, M., Sagasser, M., Niehaus, K., Weisshaar, B., and Stracke, R. (2011). Two differentially expressed MATE factor genes from apple complement the Arabidopsis transparent testa12 mutant. Plant Biology 13, 42-50.
Frank, S., et al., 2011. Two differentially expressed MATE factor genes from apple complement the Arabidopsis transparent testa12 mutant. Plant Biology, 13(1), p 42-50.
S. Frank, et al., “Two differentially expressed MATE factor genes from apple complement the Arabidopsis transparent testa12 mutant”, Plant Biology, vol. 13, 2011, pp. 42-50.
Frank, S., Keck, M., Sagasser, M., Niehaus, K., Weisshaar, B., Stracke, R.: Two differentially expressed MATE factor genes from apple complement the Arabidopsis transparent testa12 mutant. Plant Biology. 13, 42-50 (2011).
Frank, Sandra, Keck, Matthias, Sagasser, Martin, Niehaus, Karsten, Weisshaar, Bernd, and Stracke, Ralf. “Two differentially expressed MATE factor genes from apple complement the Arabidopsis transparent testa12 mutant”. Plant Biology 13.1 (2011): 42-50.

8 Zitationen in Europe PMC

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The Vacuolar Transportome of Plant Specialized Metabolites.
de Brito Francisco R, Martinoia E., Plant Cell Physiol 59(7), 2018
PMID: 29452376
Transcriptomic evidence for the control of soybean root isoflavonoid content by regulation of overlapping phenylpropanoid pathways.
Dastmalchi M, Chapman P, Yu J, Austin RS, Dhaubhadel S., BMC Genomics 18(1), 2017
PMID: 28077078
Transcriptomic profiling of two Pak Choi varieties with contrasting anthocyanin contents provides an insight into structural and regulatory genes in anthocyanin biosynthetic pathway.
Zhang L, Xu B, Wu T, Yang Y, Fan L, Wen M, Sui J., BMC Genomics 18(1), 2017
PMID: 28399809
Global analysis of the MATE gene family of metabolite transporters in tomato.
Santos ALD, Chaves-Silva S, Yang L, Maia LGS, Chalfun-Júnior A, Sinharoy S, Zhao J, Benedito VA., BMC Plant Biol 17(1), 2017
PMID: 29084510
Molecular cloning and functional characterization of DkMATE1 involved in proanthocyanidin precursor transport in persimmon (Diospyros kaki Thunb.) fruit.
Yang S, Jiang Y, Xu L, Shiratake K, Luo Z, Zhang Q., Plant Physiol Biochem 108(), 2016
PMID: 27472890
The similar and different evolutionary trends of MATE family occurred between rice and Arabidopsis thaliana.
Wang L, Bei X, Gao J, Li Y, Yan Y, Hu Y., BMC Plant Biol 16(1), 2016
PMID: 27669820
Biosynthesis and metabolic engineering of anthocyanins in Arabidopsis thaliana.
Shi MZ, Xie DY., Recent Pat Biotechnol 8(1), 2014
PMID: 24354533
VvMATE1 and VvMATE2 encode putative proanthocyanidin transporters expressed during berry development in Vitis vinifera L.
Pérez-Díaz R, Ryngajllo M, Pérez-Díaz J, Peña-Cortés H, Casaretto JA, González-Villanueva E, Ruiz-Lara S., Plant Cell Rep 33(7), 2014
PMID: 24700246

59 References

Daten bereitgestellt von Europe PubMed Central.

Location of the proanthocyanidins in the barley grain
Aastrup, Carlsberg Research Communications 49(), 1984
The Arabidopsis TDS4 gene encodes leucoanthocyanidin dioxygenase (LDOX) and is essential for proanthocyanidin synthesis and vacuole development.
Abrahams S, Lee E, Walker AR, Tanner GJ, Larkin PJ, Ashton AR., Plant J. 35(5), 2003
PMID: 12940955
Structure and expression of an asparaginyl-tRNA synthetase gene located on chromosome IV of Arabidopsis thaliana and adjacent to a novel gene of 15 exons
Aubourg, Biochimica et Biophysica Acta-Gene Structure and Expression 1398(), 1998
The DEAD box RNA helicase family in Arabidopsis thaliana.
Aubourg S, Kreis M, Lecharny A., Nucleic Acids Res. 27(2), 1999
PMID: 9862990
Retroviruses and retrotransposons: the role of reverse transcription in shaping the eukaryotic genome.
Baltimore D., Cell 40(3), 1985
PMID: 2578883
A plasma membrane H+-ATPase is required for the formation of proanthocyanidins in the seed coat endothelium of Arabidopsis thaliana
Baxter, Proceedings of the National Academy of Sciences USA 102(), 2005
Mutations in UDP-Glucose:sterol glucosyltransferase in Arabidopsis cause transparent testa phenotype and suberization defect in seeds.
DeBolt S, Scheible WR, Schrick K, Auer M, Beisson F, Bischoff V, Bouvier-Nave P, Carroll A, Hematy K, Li Y, Milne J, Nair M, Schaller H, Zemla M, Somerville C., Plant Physiol. 151(1), 2009
PMID: 19641030
Apple phytochemicals and their health benefits
Boyer, Nutritional Journal 3(), 2004
[GeneBee-NET: An Internet based server for biopolymer structure analysis]
Brodskii LI, Ivanov VV, Kalaidzidis IaL, Leontovich AM, Nikolaev VK, Feranchuk SI, Drachev VA., Biokhimiia 60(8), 1995
PMID: 7578577
A catalogue of splice junction and putative branch point sequences from plant introns.
Brown JW., Nucleic Acids Res. 14(24), 1986
PMID: 3808952
Three distinct modes of intron dynamics in the evolution of eukaryotes.
Carmel L, Wolf YI, Rogozin IB, Koonin EV., Genome Res. 17(7), 2007
PMID: 17495008
TRANSPARENT TESTA 12 genes from Brassica napus and parental species: cloning, evolution, and differential involvement in yellow seed trait.
Chai YR, Lei B, Huang HL, Li JN, Yin JM, Tang ZL, Wang R, Chen L., Mol. Genet. Genomics 281(1), 2008
PMID: 19018571
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
Clough SJ, Bent AF., Plant J. 16(6), 1998
PMID: 10069079
The TRANSPARENT TESTA12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium.
Debeaujon I, Peeters AJ, Leon-Kloosterziel KM, Koornneef M., Plant Cell 13(4), 2001
PMID: 11283341
Proanthocyanidin-accumulating cells in Arabidopsis testa: regulation of differentiation and role in seed development.
Debeaujon I, Nesi N, Perez P, Devic M, Grandjean O, Caboche M, Lepiniec L., Plant Cell 15(11), 2003
PMID: 14555692
Tannin analysis of food products.
Deshpande SS, Cheryan M, Salunkhe DK., Crit Rev Food Sci Nutr 24(4), 1986
PMID: 3536314
Review of apple flavor--state of the art.
Dimick PS, Hoskin JC., Crit Rev Food Sci Nutr 18(4), 1983
PMID: 6354595
Proanthocyanidins--a final frontier in flavonoid research?
Dixon RA, Xie DY, Sharma SB., New Phytol. 165(1), 2005
PMID: 15720617
The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation.
Durrett TP, Gassmann W, Rogers EE., Plant Physiol. 144(1), 2007
PMID: 17351051
High-performance liquid chromatography with diode-array detection for the determination of phenolic compounds in peel and pulp from different apple varieties.
Escarpa A, Gonzalez MC., J Chromatogr A 823(1-2), 1998
PMID: 9818410
Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10.
Espley RV, Hellens RP, Putterill J, Stevenson DE, Kutty-Amma S, Allan AC., Plant J. 49(3), 2006
PMID: 17181777
T-DNA insertion mutagenesis in Arabidopsis: mutational spectrum
Feldmann, The Plant Journal 1(), 1991
Control of carpel and fruit development in Arabidopsis.
Ferrandiz C, Pelaz S, Yanofsky MF., Annu. Rev. Biochem. 68(), 1999
PMID: 10872453
An aluminum-activated citrate transporter in barley.
Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K, Katsuhara M, Takeda K, Ma JF., Plant Cell Physiol. 48(8), 2007
PMID: 17634181
ExPASy: The proteomics server for in-depth protein knowledge and analysis.
Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A., Nucleic Acids Res. 31(13), 2003
PMID: 12824418
Grapevine MATE-type proteins act as vacuolar H+-dependent acylated anthocyanin transporters.
Gomez C, Terrier N, Torregrosa L, Vialet S, Fournier-Level A, Verries C, Souquet JM, Mazauric JP, Klein M, Cheynier V, Ageorges A., Plant Physiol. 150(1), 2009
PMID: 19297587
Characterization of highly polymerized procyanidins in cider apple (Malus sylvestris var. kermerrien) skin and pulp
Guyot, Phytochemistry 44(), 1997
Procyanidins are the most abundant polyphenols in dessert apples at maturity
Guyot, Lebensmittel-Wissenschaften und Technologie 35(), 2002
The multidrug/oligosaccharidyl-lipid/polysaccharide (MOP) exporter superfamily.
Hvorup RN, Winnen B, Chang AB, Jiang Y, Zhou XF, Saier MH Jr., Eur. J. Biochem. 270(5), 2003
PMID: 12603313
Evolutionary relationship of plant catalase genes inferred from exon-intron structures: isozyme divergence after the separation of monocots and dicots
Iwamoto, Theoretical and Applied Genetics 97(), 1998
Analysis of the subcellular localization, function, and proteolytic control of the Arabidopsis cyclin-dependent kinase inhibitor ICK1/KRP1.
Jakoby MJ, Weinl C, Pusch S, Kuijt SJ, Merkle T, Dissmeyer N, Schnittger A., Plant Physiol. 141(4), 2006
PMID: 16766674
Global gene expression analysis of apple fruit development from the floral bud to ripe fruit.
Janssen BJ, Thodey K, Schaffer RJ, Alba R, Balakrishnan L, Bishop R, Bowen JH, Crowhurst RN, Gleave AP, Ledger S, McArtney S, Pichler FB, Snowden KC, Ward S., BMC Plant Biol. 8(), 2008
PMID: 18279528
Genetic control of flavonoid biosynthesis in barley
Jende-Strid, Hereditas 119(), 1993
TRANSPARENT TESTA 19 is involved in the accumulation of both anthocyanins and proanthocyanidins in Arabidopsis.
Kitamura S, Shikazono N, Tanaka A., Plant J. 37(1), 2004
PMID: 14675436
High rate of recent intron gain and loss in simultaneously duplicated Arabidopsis genes.
Knowles DG, McLysaght A., Mol. Biol. Evol. 23(8), 2006
PMID: 16720694
The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector
Koncz, Molecular & General Genetics 204(), 1986
Mutations affecting the testa colour in Arabidopsis
Koornneef, Arabidopsis Information Services 27(), 1990
Clustal W and Clustal X version 2.0.
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG., Bioinformatics 23(21), 2007
PMID: 17846036
How introns influence and enhance eukaryotic gene expression.
Le Hir H, Nott A, Moore MJ., Trends Biochem. Sci. 28(4), 2003
PMID: 12713906
Genetics and biochemistry of seed flavonoids.
Lepiniec L, Debeaujon I, Routaboul JM, Baudry A, Pourcel L, Nesi N, Caboche M., Annu Rev Plant Biol 57(), 2006
PMID: 16669768
Identification of QTLs involved in the resistance to South American leaf blight (Microcyclus ulei) in the rubber tree.
Lespinasse D, Grivet L, Troispoux V, Rodier-Goud M, Pinard F, Seguin M., Theor. Appl. Genet. 100(6), 2000
PMID: IND22064132
A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum.
Magalhaes JV, Liu J, Guimaraes CT, Lana UG, Alves VM, Wang YH, Schaffert RE, Hoekenga OA, Pineros MA, Shaff JE, Klein PE, Carneiro NP, Coelho CM, Trick HN, Kochian LV., Nat. Genet. 39(9), 2007
PMID: 17721535
The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+ -antiporter active in proanthocyanidin-accumulating cells of the seed coat.
Marinova K, Pourcel L, Weder B, Schwarz M, Barron D, Routaboul JM, Debeaujon I, Klein M., Plant Cell 19(6), 2007
PMID: 17601828
Activation tagging in tomato identifies a transcriptional regulator of anthocyanin biosynthesis, modification, and transport.
Mathews H, Clendennen SK, Caldwell CG, Liu XL, Connors K, Matheis N, Schuster DK, Menasco DJ, Wagoner W, Lightner J, Wagner DR., Plant Cell 15(8), 2003
PMID: 12897245
The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis.
Mehrtens F, Kranz H, Bednarek P, Weisshaar B., Plant Physiol. 138(2), 2005
PMID: 15923334

Ohno, 1970
Characterization of flavonol synthase and leucoanthocyanidin dioxygenase genes in Arabidopsis. Further evidence for differential regulation of "early" and "late" genes.
Pelletier MK, Murrell JR, Shirley BW., Plant Physiol. 113(4), 1997
PMID: 9112784
Concentrations and characteristics of procyanidins and other phenolics in apples during fruit growth.
Renard CM, Dupont N, Guillermin P., Phytochemistry 68(8), 2007
PMID: 17400262
Rates of intron loss and gain: implications for early eukaryotic evolution
Roy, Proceedings of the National Academy of Sciences USA 102(), 2005
Patterns of intron loss and gain in plants: intron loss-dominated evolution and genome-wide comparison of O. sativa and A. thaliana.
Roy SW, Penny D., Mol. Biol. Evol. 24(1), 2006
PMID: 17065597
Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples.
Takos AM, Jaffe FW, Jacob SR, Bogs J, Robinson SP, Walker AR., Plant Physiol. 142(3), 2006
PMID: 17012405
Condensed tannin biosynthesis genes are regulated separately from other flavonoid biosynthesis genes in apple fruit skin
Takos AM, Ubi BE, Robinson SP, Walker AR., Plant Sci. 170(3), 2006
PMID: IND43813218
Biosynthesis of phenolic compounds and its regulation in apple
Treutter, Plant Growth Regulation 34(), 2001
OCTOPUS: improving topology prediction by two-track ANN-based preference scores and an extended topological grammar.
Viklund H, Elofsson A., Bioinformatics 24(15), 2008
PMID: 18474507
The origins of genomic duplications in Arabidopsis.
Vision TJ, Brown DG, Tanksley SD., Science 290(5499), 2000
PMID: 11118139
Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis.
Xie DY, Sharma SB, Paiva NL, Ferreira D, Dixon RA., Science 299(5605), 2003
PMID: 12532018
Secondary transport as an efficient membrane transport mechanism for plant secondary metabolites
Yazaki, Phytochemistry Reviews 7(), 2008
InterProScan--an integration platform for the signature-recognition methods in InterPro.
Zdobnov EM, Apweiler R., Bioinformatics 17(9), 2001
PMID: 11590104
MATE transporters facilitate vacuolar uptake of epicatechin 3'-O-glucoside for proanthocyanidin biosynthesis in Medicago truncatula and Arabidopsis.
Zhao J, Dixon RA., Plant Cell 21(8), 2009
PMID: 19684242
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