Identification of tomato F-box proteins functioning in phenylpropanoid metabolism.
Solanum lycopersicum
CHS
F-box
KFB
PAL
Phenylpropanoids
Journal
Plant molecular biology
ISSN: 1573-5028
Titre abrégé: Plant Mol Biol
Pays: Netherlands
ID NLM: 9106343
Informations de publication
Date de publication:
12 Jul 2024
12 Jul 2024
Historique:
received:
07
04
2024
accepted:
26
06
2024
medline:
12
7
2024
pubmed:
12
7
2024
entrez:
12
7
2024
Statut:
epublish
Résumé
Phenylpropanoids, a class of specialized metabolites, play crucial roles in plant growth and stress adaptation and include diverse phenolic compounds such as flavonoids. Phenylalanine ammonia-lyase (PAL) and chalcone synthase (CHS) are essential enzymes functioning at the entry points of general phenylpropanoid biosynthesis and flavonoid biosynthesis, respectively. In Arabidopsis, PAL and CHS are turned over through ubiquitination-dependent proteasomal degradation. Specific kelch domain-containing F-Box (KFB) proteins as components of ubiquitin E3 ligase directly interact with PAL or CHS, leading to polyubiquitinated PAL and CHS, which in turn influences phenylpropanoid and flavonoid production. Although phenylpropanoids are vital for tomato nutritional value and stress responses, the post-translational regulation of PAL and CHS in tomato remains unknown. We identified 31 putative KFB-encoding genes in the tomato genome. Our homology analysis and phylogenetic study predicted four PAL-interacting SlKFBs, while SlKFB18 was identified as the sole candidate for the CHS-interacting KFB. Consistent with their homolog function, the predicted four PAL-interacting SlKFBs function in PAL degradation. Surprisingly, SlKFB18 did not interact with tomato CHS and the overexpression or knocking out of SlKFB18 did not affect phenylpropanoid contents in tomato transgenic lines, suggesting its irreverence with flavonoid metabolism. Our study successfully discovered the post-translational regulatory machinery of PALs in tomato while highlighting the limitation of relying solely on a homology-based approach to predict interacting partners of F-box proteins.
Identifiants
pubmed: 38995464
doi: 10.1007/s11103-024-01483-4
pii: 10.1007/s11103-024-01483-4
doi:
Substances chimiques
F-Box Proteins
0
Plant Proteins
0
Phenylalanine Ammonia-Lyase
EC 4.3.1.24
Acyltransferases
EC 2.3.-
flavanone synthetase
EC 2.3.1.74
Flavonoids
0
Propanols
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
85Subventions
Organisme : National Science Foundation
ID : IOS-2142898
Organisme : National Institute of Food and Agriculture
ID : HATCH-7004334
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Nature B.V.
Références
Agati G, Brunetti C, Fini A et al (2020) Are flavonoids effective antioxidants in plants? twenty years of our investigation. Antioxidants. https://doi.org/10.3390/antiox9111098
doi: 10.3390/antiox9111098
pubmed: 33182252
pmcid: 7695271
Anwar R, Fatima T, Mattoo A (2019) Tomatoes: a model crop of solanaceous plants. Environ Sci. https://doi.org/10.1093/acrefore/9780199389414.013.223
doi: 10.1093/acrefore/9780199389414.013.223
Berger A, Latimer S, Stutts LR et al (2022) Kaempferol as a precursor for ubiquinone (coenzyme Q) biosynthesis: an atypical node between specialized metabolism and primary metabolism. Curr Opin Plant Biol 66:102165. https://doi.org/10.1016/j.pbi.2021.102165
doi: 10.1016/j.pbi.2021.102165
pubmed: 35026487
Bondonno NP, Dalgaard F, Kyrø C et al (2019) Flavonoid intake is associated with lower mortality in the danish diet cancer and health cohort. Nat Commun 10:3651. https://doi.org/10.1038/s41467-019-11622-x
doi: 10.1038/s41467-019-11622-x
pubmed: 31409784
pmcid: 6692395
Brown DE, Rashotte AM, Murphy AS et al (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol 126:524–535. https://doi.org/10.1104/pp.126.2.524
doi: 10.1104/pp.126.2.524
pubmed: 11402184
pmcid: 111146
Chandra HM, Shanmugaraj BM, Srinivasan B, Ramalingam S (2012) Influence of genotypic variations on antioxidant properties in different fractions of tomato. J Food Sci 77:C1174–C1178. https://doi.org/10.1111/j.1750-3841.2012.02962.x
doi: 10.1111/j.1750-3841.2012.02962.x
pubmed: 23106237
Chapman JM, Muday GK (2021) Flavonols modulate lateral root emergence by scavenging reactive oxygen species in Arabidopsis thaliana. J Biol Chem 296:100222. https://doi.org/10.1074/jbc.RA120.014543
doi: 10.1074/jbc.RA120.014543
pubmed: 33839683
Chen W, Xiao Z, Wang Y et al (2021) Competition between anthocyanin and kaempferol glycosides biosynthesis affects pollen tube growth and seed set of Malus. Hortic Res 8:173. https://doi.org/10.1038/s41438-021-00609-9
doi: 10.1038/s41438-021-00609-9
pubmed: 34333541
pmcid: 8325685
Deng Y, Lu S (2017) Biosynthesis and regulation of phenylpropanoids in plants. CRC Crit Rev Plant Sci 36:257–290. https://doi.org/10.1080/07352689.2017.1402852
doi: 10.1080/07352689.2017.1402852
Dixon RA, Paiva NL (1995) Stress-Induced Phenylpropanoid Metabolism. Plant Cell 7:1085–1097. https://doi.org/10.1105/tpc.7.7.1085
doi: 10.1105/tpc.7.7.1085
pubmed: 12242399
pmcid: 160915
Dong N-Q, Lin H-X (2021) Contribution of phenylpropanoid metabolism to plant development and plant-environment interactions. J Integr Plant Biol 63:180–209. https://doi.org/10.1111/jipb.13054
doi: 10.1111/jipb.13054
pubmed: 33325112
Edwards K, Cramer CL, Bolwell GP et al (1985) Rapid transient induction of phenylalanine ammonia-lyase mRNA in elicitor-treated bean cells. Proc Natl Acad Sci 82:6731–6735. https://doi.org/10.1073/pnas.82.20.6731
doi: 10.1073/pnas.82.20.6731
pubmed: 16593613
pmcid: 390760
España L, Heredia-Guerrero JA, Reina-Pinto JJ et al (2014) Transient silencing of CHALCONE SYNTHASE during fruit ripening modifies tomato epidermal cells and cuticle properties. Plant Physiol 166:1371–1386. https://doi.org/10.1104/pp.114.246405
doi: 10.1104/pp.114.246405
pubmed: 25277718
pmcid: 4226350
Feder A, Burger J, Gao S et al (2015) A kelch domain-containing F-Box coding gene negatively regulates Flavonoid accumulation in muskmelon. Plant Physiol 169:1714–1726. https://doi.org/10.1104/pp.15.01008
doi: 10.1104/pp.15.01008
pubmed: 26358418
pmcid: 4634078
Fernández-Del-Río L, Soubeyrand E, Basset GJ, Clarke CF (2020) Metabolism of the flavonol kaempferol in kidney cells liberates the B-ring to enter coenzyme Q biosynthesis. Molecules. https://doi.org/10.3390/molecules25132955
doi: 10.3390/molecules25132955
pubmed: 32605010
pmcid: 7412559
Fernandez-Pozo N, Menda N, Edwards JD et al (2015) The sol genomics network (SGN)–from genotype to phenotype to breeding. Nucleic Acids Res 43:D1036–D1041. https://doi.org/10.1093/nar/gku1195
doi: 10.1093/nar/gku1195
pubmed: 25428362
Garibay-Hernández A, Kessler N, Józefowicz AM et al (2021) Untargeted metabotyping to study phenylpropanoid diversity in crop plants. Physiol Plant 173:680–697. https://doi.org/10.1111/ppl.13458
doi: 10.1111/ppl.13458
pubmed: 33963574
Gietz RD, Woods RA (2002) Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Meth Enzymol 350:87–96. https://doi.org/10.1016/S0076-6879(02)50957-5
Gray WM, Estelle I (2000) Function of the ubiquitin-proteasome pathway in auxin response. Trends Biochem Sci 25:133–138. https://doi.org/10.1016/s0968-0004(00)01544-9
doi: 10.1016/s0968-0004(00)01544-9
pubmed: 10694884
Grotewold E (2006) The genetics and biochemistry of floral pigments. Annu Rev Plant Biol 57:761–780. https://doi.org/10.1146/annurev.arplant.57.032905.105248
doi: 10.1146/annurev.arplant.57.032905.105248
pubmed: 16669781
Gu Z, Men S, Zhu J et al (2019) Chalcone synthase is ubiquitinated and degraded via interactions with a RING-H2 protein in petals of Paeonia “He Xie.” J Exp Bot 70:4749–4762. https://doi.org/10.1093/jxb/erz245
doi: 10.1093/jxb/erz245
pubmed: 31106836
pmcid: 6760318
Guo J, Wang M-H (2009) Characterization of the phenylalanine ammonia-lyase gene (SlPAL5) from tomato (Solanum lycopersicum L.). Mol Biol Rep 36:1579–1585. https://doi.org/10.1007/s11033-008-9354-9
doi: 10.1007/s11033-008-9354-9
pubmed: 18791854
Gupta S, Van Eck J (2016) Modification of plant regeneration medium decreases the time for recovery of Solanum lycopersicum cultivar M82 stable transgenic lines. Plant Cell Tissue Organ Cult 127:417–423. https://doi.org/10.1007/s11240-016-1063-9
doi: 10.1007/s11240-016-1063-9
Han J, Ma K, Li H et al (2022) All-in-one: a robust fluorescent fusion protein vector toolbox for protein localization and BiFC analyses in plants. Plant Biotechnol J 20:1098–1109. https://doi.org/10.1111/pbi.13790
doi: 10.1111/pbi.13790
pubmed: 35179286
pmcid: 9129086
Hristova V, Sun S, Zhang H, Chan DW (2020) Proteomic analysis of degradation ubiquitin signaling by ubiquitin occupancy changes responding to 26S proteasome inhibition. Clin Proteomics 17:2. https://doi.org/10.1186/s12014-020-9265-x
doi: 10.1186/s12014-020-9265-x
pubmed: 31997977
pmcid: 6982382
Huang J, Gu M, Lai Z et al (2010) Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiol 153:1526–1538. https://doi.org/10.1104/pp.110.157370
doi: 10.1104/pp.110.157370
pubmed: 20566705
pmcid: 2923909
Keskin O, Gursoy A, Ma B, Nussinov R (2008) Principles of protein-protein interactions: what are the preferred ways for proteins to interact? Chem Rev 108:1225–1244. https://doi.org/10.1021/cr040409x
doi: 10.1021/cr040409x
pubmed: 18355092
Kim HJ, Chiang Y-H, Kieber JJ, Schaller GE (2013) SCF(KMD) controls cytokinin signaling by regulating the degradation of type-B response regulators. Proc Natl Acad Sci USA 110:10028–10033. https://doi.org/10.1073/pnas.1300403110
doi: 10.1073/pnas.1300403110
pubmed: 23720308
pmcid: 3683760
Kim JI, Dolan WL, Anderson NA, Chapple C (2015) Indole glucosinolate Biosynthesis Limits phenylpropanoid Accumulation in Arabidopsis thaliana. Plant Cell 27:1529–1546. https://doi.org/10.1105/tpc.15.00127
doi: 10.1105/tpc.15.00127
pubmed: 25944103
pmcid: 4456644
Kim JI, Zhang X, Pascuzzi PE et al (2020) Glucosinolate and phenylpropanoid biosynthesis are linked by proteasome-dependent degradation of PAL. New Phytol 225:154–168. https://doi.org/10.1111/nph.16108
doi: 10.1111/nph.16108
pubmed: 31408530
Kong D, Li S, Smolke CD (2020) Discovery of a previously unknown biosynthetic capacity of naringenin chalcone synthase by heterologous expression of a tomato gene cluster in yeast. Sci Adv. https://doi.org/10.1126/sciadv.abd1143
doi: 10.1126/sciadv.abd1143
pubmed: 33277260
pmcid: 7821898
Li Y, Kim JI, Pysh L, Chapple C (2015) Four isoforms of arabidopsis 4-coumarate: CoA ligase Have overlapping yet distinct roles in phenylpropanoid metabolism. Plant Physiol 169:2409–2421. https://doi.org/10.1104/pp.15.00838
doi: 10.1104/pp.15.00838
pubmed: 26491147
pmcid: 4677886
Liang XW, Dron M, Cramer CL et al (1989) Differential regulation of phenylalanine ammonia-lyase genes during plant development and by environmental cues. J Biol Chem 264:14486–14492
doi: 10.1016/S0021-9258(18)71704-3
pubmed: 2760071
Liddington RC (2004) Structural basis of protein–protein interactions. Methods Mol Biol 261:3–14. https://doi.org/10.1385/1-59259-762-9:003
doi: 10.1385/1-59259-762-9:003
pubmed: 15064446
Liu J, Osbourn A, Ma P (2015) MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Mol Plant 8:689–708. https://doi.org/10.1016/j.molp.2015.03.012
doi: 10.1016/j.molp.2015.03.012
pubmed: 25840349
Løvdal T, Olsen KM, Slimestad R et al (2010) Synergetic effects of nitrogen depletion, temperature, and light on the content of phenolic compounds and gene expression in leaves of tomato. Phytochemistry 71:605–613. https://doi.org/10.1016/j.phytochem.2009.12.014
doi: 10.1016/j.phytochem.2009.12.014
pubmed: 20096428
Mao W, Han Y, Chen Y et al (2022) Low temperature inhibits anthocyanin accumulation in strawberry fruit by activating FvMAPK3-induced phosphorylation of FvMYB10 and degradation of chalcone synthase 1. Plant Cell 34:1226–1249. https://doi.org/10.1093/plcell/koac006
doi: 10.1093/plcell/koac006
pubmed: 35018459
pmcid: 8972286
Micek A, Godos J, Del Rio D et al (2021) Dietary flavonoids and cardiovascular disease: a comprehensive dose-response meta-analysis. Mol Nutr Food Res 65:e2001019. https://doi.org/10.1002/mnfr.202001019
doi: 10.1002/mnfr.202001019
pubmed: 33559970
Muhlemann JK, Younts TLB, Muday GK (2018) Flavonols control pollen tube growth and integrity by regulating ROS homeostasis during high-temperature stress. Proc Natl Acad Sci USA 115:E11188–E11197. https://doi.org/10.1073/pnas.1811492115
doi: 10.1073/pnas.1811492115
pubmed: 30413622
pmcid: 6255205
Muro-Villanueva F, Mao X, Chapple C (2019) Linking phenylpropanoid metabolism, lignin deposition, and plant growth inhibition. Curr Opin Biotechnol 56:202–208. https://doi.org/10.1016/j.copbio.2018.12.008
doi: 10.1016/j.copbio.2018.12.008
pubmed: 30677701
Nakabayashi K, Bartsch M, Ding J, Soppe WJJ (2015) Seed dormancy in arabidopsis requires self-binding ability of DOG1 protein and the presence of multiple isoforms generated by alternative splicing. PLoS Genet 11:e1005737. https://doi.org/10.1371/journal.pgen.1005737
doi: 10.1371/journal.pgen.1005737
pubmed: 26684465
pmcid: 4686169
Novaes E, Kirst M, Chiang V et al (2010) Lignin and biomass: a negative correlation for wood formation and lignin content in trees. Plant Physiol 154:555–561. https://doi.org/10.1104/pp.110.161281
doi: 10.1104/pp.110.161281
pubmed: 20921184
pmcid: 2949025
Ohno S, Hori W, Hosokawa M et al (2018) Post-transcriptional silencing of chalcone synthase is involved in phenotypic lability in petals and leaves of bicolor dahlia (Dahlia variabilis) “Yuino.” Planta 247:413–428. https://doi.org/10.1007/s00425-017-2796-3
doi: 10.1007/s00425-017-2796-3
pubmed: 29063185
Pawlak-Sprada S, Arasimowicz-Jelonek M, Podgórska M, Deckert J (2011) Activation of phenylpropanoid pathway in legume plants exposed to heavy metals. Part I. Effects of cadmium and lead on phenylalanine ammonia-lyase gene expression, enzyme activity and lignin content. Acta Biochim Pol 58:211–216
doi: 10.18388/abp.2011_2267
pubmed: 21503278
Perez VC, Dai R, Bai B et al (2021) Aldoximes are precursors of auxins in arabidopsis and maize. New Phytol 231:1449–1461. https://doi.org/10.1111/nph.17447
doi: 10.1111/nph.17447
pubmed: 33959967
pmcid: 8282758
Potter SC, Luciani A, Eddy SR et al (2018) HMMER web server: 2018 update. Nucleic Acids Res 46:W200–W204. https://doi.org/10.1093/nar/gky448
doi: 10.1093/nar/gky448
pubmed: 29905871
pmcid: 6030962
Prasanna P, Upadhyay A (2021) Flavonoid-based nanomedicines in alzheimer’s disease therapeutics: promises made, a long way to go. ACS Pharmacol Transl Sci 4:74–95. https://doi.org/10.1021/acsptsci.0c00224
doi: 10.1021/acsptsci.0c00224
pubmed: 33615162
pmcid: 7887745
Rohde A, Morreel K, Ralph J et al (2004) Molecular phenotyping of the pal
doi: 10.1105/tpc.104.023705
pubmed: 15377757
pmcid: 520969
Rosa-Martínez E, Bovy A, Plazas M et al (2023) Genetics and breeding of phenolic content in tomato, eggplant and pepper fruits. Front Plant Sci 14:1135237. https://doi.org/10.3389/fpls.2023.1135237
doi: 10.3389/fpls.2023.1135237
pubmed: 37025131
pmcid: 10070870
Ruegger M, Chapple C (2001) Mutations that reduce sinapoylmalate accumulation in arabidopsis thaliana define loci with diverse roles in phenylpropanoid metabolism. Genetics 159:1741–1749. https://doi.org/10.1093/genetics/159.4.1741
doi: 10.1093/genetics/159.4.1741
pubmed: 11779811
pmcid: 1461910
Ruprecht C, Proost S, Hernandez-Coronado M et al (2017) Phylogenomic analysis of gene co-expression networks reveals the evolution of functional modules. Plant J 90:447–465. https://doi.org/10.1111/tpj.13502
doi: 10.1111/tpj.13502
pubmed: 28161902
Saito K, Yonekura-Sakakibara K, Nakabayashi R et al (2013) The flavonoid biosynthetic pathway in Arabidopsis: structural and genetic diversity. Plant Physiol Biochem 72:21–34. https://doi.org/10.1016/j.plaphy.2013.02.001
doi: 10.1016/j.plaphy.2013.02.001
pubmed: 23473981
Schijlen EGWM, de Vos CHR, Martens S et al (2007) RNA interference silencing of chalcone synthase, the first step in the flavonoid biosynthesis pathway, leads to parthenocarpic tomato fruits. Plant Physiol 144:1520–1530. https://doi.org/10.1104/pp.107.100305
doi: 10.1104/pp.107.100305
pubmed: 17478633
pmcid: 1914118
Schmelzer E, Jahnen W, Hahlbrock K (1988) In situ localization of light-induced chalcone synthase mRNA, chalcone synthase, and flavonoid end products in epidermal cells of parsley leaves. Proc Natl Acad Sci USA 85:2989–2993. https://doi.org/10.1073/pnas.85.9.2989
doi: 10.1073/pnas.85.9.2989
pubmed: 16578833
pmcid: 280128
Schumann N, Navarro-Quezada A, Ullrich K et al (2011) Molecular evolution and selection patterns of plant F-box proteins with C-terminal kelch repeats. Plant Physiol 155:835–850. https://doi.org/10.1104/pp.110.166579
doi: 10.1104/pp.110.166579
pubmed: 21119043
Shao T, Qian Q, Tang D et al (2012) A novel gene IBF1 is required for the inhibition of brown pigment deposition in rice hull furrows. Theor Appl Genet 125:381–390. https://doi.org/10.1007/s00122-012-1840-8
doi: 10.1007/s00122-012-1840-8
pubmed: 22419106
Shin DH, Cho M, Choi MG et al (2015) Identification of genes that may regulate the expression of the transcription factor production of anthocyanin pigment 1 (PAP1)/MYB75 involved in Arabidopsis anthocyanin biosynthesis. Plant Cell Rep 34:805–815. https://doi.org/10.1007/s00299-015-1743-7
doi: 10.1007/s00299-015-1743-7
pubmed: 25604992
Shin D, Perez VC, Dickinson GK et al (2023) Altered methionine metabolism impacts phenylpropanoid production and plant development in Arabidopsis thaliana. BioRxiv. https://doi.org/10.1101/2023.05.29.542770
doi: 10.1101/2023.05.29.542770
pubmed: 38187698
pmcid: 10769246
Shirley BW, Kubasek WL, Storz G et al (1995) Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. Plant J 8:659–671. https://doi.org/10.1046/j.1365-313x.1995.08050659.x
doi: 10.1046/j.1365-313x.1995.08050659.x
pubmed: 8528278
Shomali A, Das S, Arif N et al (2022) Diverse physiological roles of flavonoids in plant environmental stress responses and tolerance. Plants. https://doi.org/10.3390/plants11223158
doi: 10.3390/plants11223158
pubmed: 36432887
pmcid: 9699315
Slika H, Mansour H, Wehbe N et al (2022) Therapeutic potential of flavonoids in cancer: ROS-mediated mechanisms. Biomed Pharmacother 146:112442. https://doi.org/10.1016/j.biopha.2021.112442
doi: 10.1016/j.biopha.2021.112442
pubmed: 35062053
Soubeyrand E, Johnson TS, Latimer S et al (2018) The peroxidative cleavage of kaempferol contributes to the biosynthesis of the benzenoid moiety of ubiquinone in plants. Plant Cell 30:2910–2921. https://doi.org/10.1105/tpc.18.00688
doi: 10.1105/tpc.18.00688
pubmed: 30429224
pmcid: 6354277
Soubeyrand E, Latimer S, Bernert AC et al (2021) 3-O-glycosylation of kaempferol restricts the supply of the benzenoid precursor of ubiquinone (coenzyme Q) in Arabidopsis thaliana. Phytochemistry 186:112738. https://doi.org/10.1016/j.phytochem.2021.112738
doi: 10.1016/j.phytochem.2021.112738
pubmed: 33756238
Steiner E, Triana MR, Kubasi S et al (2021) KISS ME DEADLY F-box proteins modulate cytokinin responses by targeting the transcription factor TCP14 for degradation. Plant Physiol 185:1495–1499. https://doi.org/10.1093/plphys/kiab033
doi: 10.1093/plphys/kiab033
pubmed: 33580703
pmcid: 8133550
Struk S, Jacobs A, Sánchez Martín-Fontecha E et al (2019) Exploring the protein-protein interaction landscape in plants. Plant Cell Environ 42:387–409. https://doi.org/10.1111/pce.13433
doi: 10.1111/pce.13433
pubmed: 30156707
Sun C, Deng L, Du M et al (2020) A transcriptional network promotes anthocyanin biosynthesis in tomato flesh. Mol Plant 13:42–58. https://doi.org/10.1016/j.molp.2019.10.010
doi: 10.1016/j.molp.2019.10.010
pubmed: 31678614
Tan H, Man C, Xie Y et al (2019) A crucial role of GA-regulated flavonol biosynthesis in root growth of Arabidopsis. Mol Plant 12:521–537. https://doi.org/10.1016/j.molp.2018.12.021
doi: 10.1016/j.molp.2018.12.021
pubmed: 30630075
Teale WD, Pasternak T, Dal Bosco C et al (2021) Flavonol-mediated stabilization of PIN efflux complexes regulates polar auxin transport. EMBO J 40:e104416
doi: 10.15252/embj.2020104416
pubmed: 33185277
Tohge T, de Souza LP, Fernie AR (2017) Current understanding of the pathways of flavonoid biosynthesis in model and crop plants. J Exp Bot 68:4013–4028. https://doi.org/10.1093/jxb/erx177
doi: 10.1093/jxb/erx177
pubmed: 28922752
Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641. https://doi.org/10.1038/nature11119
doi: 10.1038/nature11119
Tu S-H, Chen L-C, Ho Y-S (2017) An apple a day to prevent cancer formation: reducing cancer risk with flavonoids. J Food Drug Anal 25:119–124. https://doi.org/10.1016/j.jfda.2016.10.016
doi: 10.1016/j.jfda.2016.10.016
pubmed: 28911529
Verweij W, Spelt CE, Bliek M et al (2016) Functionally similar WRKY proteins regulate vacuolar acidification in petunia and hair development in arabidopsis. Plant Cell 28:786–803. https://doi.org/10.1105/tpc.15.00608
doi: 10.1105/tpc.15.00608
pubmed: 26977085
pmcid: 4826004
Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3:2–20. https://doi.org/10.1093/mp/ssp106
doi: 10.1093/mp/ssp106
pubmed: 20035037
Wang Y, Liu W, Wang X et al (2020) MiR156 regulates anthocyanin biosynthesis through SPL targets and other microRNAs in poplar. Hortic Res 7:118. https://doi.org/10.1038/s41438-020-00341-w
doi: 10.1038/s41438-020-00341-w
pubmed: 32821401
pmcid: 7395715
Wedick NM, Pan A, Cassidy A et al (2012) Dietary flavonoid intakes and risk of type 2 diabetes in US men and women. Am J Clin Nutr 95:925–933. https://doi.org/10.3945/ajcn.111.028894
doi: 10.3945/ajcn.111.028894
pubmed: 22357723
pmcid: 3302366
Wen W, Alseekh S, Fernie AR (2020) Conservation and diversification of flavonoid metabolism in the plant kingdom. Curr Opin Plant Biol 55:100–108. https://doi.org/10.1016/j.pbi.2020.04.004
doi: 10.1016/j.pbi.2020.04.004
pubmed: 32422532
Wen K, Fang X, Yang J et al (2021) Recent research on flavonoids and their biomedical applications. Curr Med Chem 28:1042–1066. https://doi.org/10.2174/0929867327666200713184138
doi: 10.2174/0929867327666200713184138
pubmed: 32660393
Xian D, Guo M, Xu J et al (2021) Current evidence to support the therapeutic potential of flavonoids in oxidative stress-related dermatoses. Redox Rep 26:134–146. https://doi.org/10.1080/13510002.2021.1962094
doi: 10.1080/13510002.2021.1962094
pubmed: 34355664
pmcid: 8354022
Xu W, Dubos C, Lepiniec L (2015) Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends Plant Sci 20:176–185. https://doi.org/10.1016/j.tplants.2014.12.001
doi: 10.1016/j.tplants.2014.12.001
pubmed: 25577424
Yin R, Messner B, Faus-Kessler T et al (2012) Feedback inhibition of the general phenylpropanoid and flavonol biosynthetic pathways upon a compromised flavonol-3-O-glycosylation. J Exp Bot 63:2465–2478. https://doi.org/10.1093/jxb/err416
doi: 10.1093/jxb/err416
pubmed: 22249996
pmcid: 3346215
Yin R, Han K, Heller W et al (2014) Kaempferol 3-O-rhamnoside-7-O-rhamnoside is an endogenous flavonol inhibitor of polar auxin transport in Arabidopsis shoots. New Phytol 201:466–475. https://doi.org/10.1111/nph.12558
doi: 10.1111/nph.12558
pubmed: 24251900
Zhang X, Liu C-J (2015) Multifaceted regulations of gateway enzyme phenylalanine ammonia-lyase in the biosynthesis of phenylpropanoids. Mol Plant 8:17–27. https://doi.org/10.1016/j.molp.2014.11.001
doi: 10.1016/j.molp.2014.11.001
pubmed: 25578269
Zhang X, Henriques R, Lin S-S et al (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat Protoc 1:641–646. https://doi.org/10.1038/nprot.2006.97
doi: 10.1038/nprot.2006.97
pubmed: 17406292
Zhang X, Gou M, Liu C-J (2013) Arabidopsis kelch repeat F-box proteins regulate phenylpropanoid biosynthesis via controlling the turnover of phenylalanine ammonia-lyase. Plant Cell 25:4994–5010. https://doi.org/10.1105/tpc.113.119644
doi: 10.1105/tpc.113.119644
pubmed: 24363316
pmcid: 3904001
Zhang X, Gou M, Guo C et al (2015a) Down-regulation of kelch domain-containing F-box protein in Arabidopsis enhances the production of (poly)phenols and tolerance to ultraviolet radiation. Plant Physiol 167:337–350. https://doi.org/10.1104/pp.114.249136
doi: 10.1104/pp.114.249136
pubmed: 25502410
Zhang Y, Butelli E, Alseekh S et al (2015b) Multi-level engineering facilitates the production of phenylpropanoid compounds in tomato. Nat Commun 6:8635. https://doi.org/10.1038/ncomms9635
doi: 10.1038/ncomms9635
pubmed: 26497596
Zhang X, Abrahan C, Colquhoun TA, Liu C-J (2017) A proteolytic regulator controlling chalcone synthase stability and flavonoid biosynthesis in arabidopsis. Plant Cell 29:1157–1174. https://doi.org/10.1105/tpc.16.00855
doi: 10.1105/tpc.16.00855
pubmed: 28446542
pmcid: 5466025
Zhang D, Song YH, Dai R et al (2020) Aldoxime metabolism is linked to phenylpropanoid production in Camelina sativa. Front Plant Sci 11:17. https://doi.org/10.3389/fpls.2020.00017
Zhao T, Huang C, Li S et al (2023) VviKFB07 F-box E3 ubiquitin ligase promotes stilbene accumulation by ubiquitinating and degrading VviCHSs protein in grape. Plant Sci 331:111687. https://doi.org/10.1016/j.plantsci.2023.111687
doi: 10.1016/j.plantsci.2023.111687
pubmed: 36958599