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Investigation of flavonoid expression and metabolite content patterns during seed formation of Artemisia sphaerocephala Krasch.

Published online by Cambridge University Press:  02 July 2021

Chengshuai Li
Affiliation:
State Key Laboratory of Grassland Agro-ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou730020, China
Lijing Zhang*
Affiliation:
State Key Laboratory of Grassland Agro-ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou730020, China
Decao Niu
Affiliation:
State Key Laboratory of Grassland Agro-ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou730020, China
Shuzhen Nan
Affiliation:
State Key Laboratory of Grassland Agro-ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou730020, China
Xiumei Miao
Affiliation:
State Key Laboratory of Grassland Agro-ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou730020, China
Xiaowei Hu
Affiliation:
State Key Laboratory of Grassland Agro-ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou730020, China
Hua Fu
Affiliation:
State Key Laboratory of Grassland Agro-ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs; Engineering Research Center of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou730020, China
*
*Correspondence: Lijing Zhang, E-mail: [email protected]

Abstract

Flavonoids are a group of phenolic secondary metabolites in plants that have important physiological, ecological and economic value. In this study, using the desert plant Artemisia sphaerocephala Krasch. as the sample material, the content and components of the total flavonoids in its seeds at seven different developmental stages were determined. In addition, the genes involved in flavonoid metabolism were identified by full-length transcriptome sequencing (third-generation sequencing technology based on PacBio RS II). Their expression levels were analysed by RNA-seq short reading sequencing, to reveal the patterns and regulation mechanisms of flavonoid accumulation during seed development. The key results were as follows: the content of total flavonoids in mature seeds was 15.05 mg g−1, including five subclasses: flavonols, chalcones, flavones, flavanones and proanthocyanidins, among which flavonols accounted for 45.78%. The period of rapid accumulation of flavonoids was 40–70 d following anthesis. The high expression of phenylalanine ammonia-lyase (PAL), 4-coumarate-CoA ligase (4CL) and UDP-glucose:flavonoids 3-o-glucosyltransferase (UF3GT) promoted the accumulation of total flavonoids, while the high expression of flavonoids 3′-hydroxylase (F3′H) and flavonols synthase (FLS) made flavanols the main component. Transcription factors such as the MYB-bHLH-WDR (MBW) complex and Selenium-binding protein (SBP) directly regulated the structural genes of flavonoid metabolism, while C2H2-type zinc finger (C2H2), Zinc-finger transcription factor (GATA), Dehydration-responsive element binding (DREB), Global Transcription factor Group E protein (GTE), Trihelix DNA-binding factors (Trihelix) and Phytochrome-interacting factor (PIF) indirectly promoted the synthesis of flavonoids through hormones such as brassinoidsteroids (BRs) and abscisic acid (ABA). These results provided valuable resources for the application of related genes in genetics and breeding.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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Footnotes

Chengshuai Li and Lijing Zhang contributed equally to this work.

References

Arlotta, C, Puglia, GD, Genovese, C, Toscano, V, Karlova, R, Beekwilder, J, De Vos, RCH and Raccuia, SA (2020) MYB5-like and bHLH influence flavonoid composition in pomegranate. Plant Science 298, 110563.CrossRefGoogle ScholarPubMed
Bains, S, Thakur, V, Kaur, J, Singh, K and Kaur, R (2019) Elucidating genes involved in sesquiterpenoid and flavonoid biosynthetic pathways in Saussurea lappa by de novo leaf transcriptome analysis. Genomics 111, 14741482.CrossRefGoogle ScholarPubMed
Balakhnina, TI, Gavrilov, AB, Wlodarczyk, TM, Borkowska, A, Nosalewicz, M and Fomina, IR (2009) Dihydroquercetin protects barley seeds against mold and increases seedling adaptive potential under soil flooding. Plant Growth Regulation 57, 127135.CrossRefGoogle Scholar
Chen, J, Tang, XH, Ren, CX, Wei, B, Wu, YY, Wu, QH and Pei, J (2018) Full-length transcriptome sequences and the identification of putative genes for flavonoid biosynthesis in safflower. BMC Genomics 19, 548.CrossRefGoogle ScholarPubMed
De Palma, M, Fratianni, F, Nazzaro, F and Tucci, M (2014) Isolation and functional characterization of a novel gene coding for flavonoid 3′-hydroxylase from globe artichoke. Biologia Plantarum 58, 445455.CrossRefGoogle Scholar
de Rijke, E, Out, P, Niessen, WM, Ariese, F, Gooijer, C and Brinkman, UA (2006) Analytical separation and detection methods for flavonoids. Journal of Chromatography A 1112, 3163.CrossRefGoogle ScholarPubMed
Diaz-Tielas, C, Grana, E, Reigosa, MJ and Sanchez-Moreiras, AM (2016) Biological activities and novel applications of chalcones. Planta Daninha 34, 607616.CrossRefGoogle Scholar
Dixon, RA and Pasinetti, GM (2010) Flavonoids and isoflavonoids: from plant biology to agriculture and neuroscience. Plant Physiology 154, 453457.CrossRefGoogle ScholarPubMed
Dong, C, Hu, HG, Hu, YL and Xie, JH (2016) Metabolism of flavonoids in novel banana germplasm during fruit development. Frontiers in Plant Science 7, 1291.CrossRefGoogle ScholarPubMed
Doughty, J, Aljabri, M and Scott, RJ (2014) Flavonoids and the regulation of seed size in Arabidopsis. Biochemical Society Transactions 42, 364369.CrossRefGoogle ScholarPubMed
Dyduch-SiemiNska, M, Najda, A, Dyduch, J, Gantner, M and Klimek, K (2015) The content of secondary metabolites and antioxidant activity of wild strawberry fruit (Fragaria vesca L.). Journal of Analytical Methods in Chemistry 2015, 831238.CrossRefGoogle Scholar
Gao, MJ, Li, X, Huang, J, Gropp, GM, Gjetvaj, B, Lindsay, DL, Wei, S, Coutu, C, Chen, Z, Wan, XC, Hannoufa, A, Lydiate, DJ, Gruber, MY, Chen, ZJ and Hegedus, DD (2015) SCARECROW-LIKE15 interacts with HISTONE DEACETYLASE19 and is essential for repressing the seed maturation programme. Nature Communications 6, 7243.CrossRefGoogle ScholarPubMed
Gao, F, Huang, G and Xiao, JQ (2020) Chalcone hybrids as potential anticancer agents: current development, mechanism of action, and structure-activity relationship. Medicinal Research Reviews 40, 20492084.CrossRefGoogle ScholarPubMed
Georgieva, Y, Кatsarova, М, Gercheva, K, Bozov, P and Dimitrova, S (2019) HPLC analysis of flavonoids from Scutellaria altissima. Bulgarian Chemical Communications 51, 119123.Google Scholar
Han, J, Liu, HT, Wang, SC, Wang, CR and Miao, GP (2020a) A class I TGA transcription factor from Tripterygium wilfordii Hook.f. modulates the biosynthesis of secondary metabolites in both native and heterologous hosts. Plant Science 290, 110293.CrossRefGoogle Scholar
Han, XX, Zhang, LJ, Miao, XM, Hu, XW, Nan, SZ and Fu, H (2020b) Transcriptome analysis reveals the molecular mechanisms of mucilage biosynthesis during Artemisia sphaerocephala seed development. Industrial Crops and Products 145, 111991.CrossRefGoogle Scholar
Harris, NN, Luczo, JM, Robinson, SP and Walker, AR (2013) Transcriptional regulation of the three grapevine chalcone synthase genes and their role in flavonoid synthesis in Shiraz. Australian Journal of Grape and Wine Research 19, 221229.CrossRefGoogle Scholar
Hostetler, GL, Ralston, RA and Schwartz, SJ (2017) Flavones: food sources, bioavailability, metabolism, and bioactivity. Advances in Nutrition 8, 423435.CrossRefGoogle ScholarPubMed
Hu, XW, Zhang, LJ, Nan, SZ, Miao, XM, Yang, PF, Duan, GQ and Fu, H (2018) Selection and validation of reference genes for quantitative real-time PCR in Artemisia sphaerocephala based on transcriptome sequence data. Gene 657, 3949.CrossRefGoogle ScholarPubMed
Huang, ZY, Gutterman, Y and Osborne, DJ (2004) Value of the mucilaginous pellicle to seeds of the sand-stabilizing desert woody shrub Artemisia sphaerocephala (Asteraceae). Trees – Structure and Function 18, 669676.CrossRefGoogle Scholar
Ibrahim, RK (2005) A forty-year journey in plant research: original contributions to flavonoid biochemistry. Canadian Journal of Botany – Revue Canadienne De Botanique 83, 433450.Google Scholar
Jagetia, GC and Reddy, TK (2011) Alleviation of iron induced oxidative stress by the grape fruit flavanone naringin in vitro. Chemico-Biological Interactions 190, 121128.CrossRefGoogle ScholarPubMed
Jiang, J, Shao, Y, Li, A, Lu, C, Zhang, Y and Wang, Y (2013) Phenolic composition analysis and gene expression in developing seeds of yellow- and black-seeded Brassica napus. Journal of Integrative Plant Biology 55, 537551.CrossRefGoogle ScholarPubMed
Koes, RE, Quattrocchio, F and Mol, JNM (1994) The flavonoid biosynthetic-pathway in plants – function and evolution. Bioessays 16, 123132.CrossRefGoogle Scholar
Kruger, MJ, Davies, N, Myburgh, KH and Lecour, S (2014) Proanthocyanidins, anthocyanins and cardiovascular diseases. Food Research International 59, 4152.CrossRefGoogle Scholar
Kuhn, BM, Geisler, M, Bigler, L and Ringli, C (2011) Flavonols accumulate asymmetrically and affect auxin transport in Arabidopsis. Plant Physiology 156, 585595.CrossRefGoogle ScholarPubMed
Kurepa, J, Shull, TE and Smalle, JA (2016) Quercetin feeding protects plants against oxidative stress. F1000Research 5, 2430.CrossRefGoogle Scholar
Langdon, WB (2015) Performance of genetic programming optimised Bowtie2 on genome comparison and analytic testing (GCAT) benchmarks. BioData Mining 8, 1.CrossRefGoogle ScholarPubMed
Lepiniec, L, Debeaujon, I, Routaboul, JM, Baudry, A, Pourcel, L, Nesi, N and Caboche, M (2006) Genetics and biochemistry of seed flavonoids. Annual Review of Plant Biology 57, 405430.CrossRefGoogle ScholarPubMed
Li, CL, Bai, YC, Li, SJ, Chen, H, Han, XY, Zhao, HX, Shao, JR, Park, SU and Wu, Q (2012) Cloning, characterization, and activity analysis of a flavonol synthase gene FtFLS1 and its association with flavonoid content in tartary buckwheat. Journal of Agricultural and Food Chemistry 60, 51615168.CrossRefGoogle ScholarPubMed
Li, JE, Fan, ST, Qiu, ZH, Li, C and Nie, SP (2015) Total flavonoids content, antioxidant and antimicrobial activities of extracts from Mosla chinensis Maxim. cv. Jiangxiangru. LWT – Food Science and Technology 64, 10221027.CrossRefGoogle Scholar
Li, Q, Yu, HM, Meng, XF, Lin, JS, Li, YJ and Hou, BK (2018) Ectopic expression of glycosyltransferase UGT76E11 increases flavonoid accumulation and enhances abiotic stress tolerance in Arabidopsis. Plant Biology (Stuttgart, Germany) 20, 1019.CrossRefGoogle ScholarPubMed
Li, H, Li, D, Yang, Z, Zeng, QW, Luo, YW and He, NJ (2020) Flavones produced by mulberry flavone synthase type I constitute a defense line against the ultraviolet-B stress. Plants (Basel) 9, 215.CrossRefGoogle ScholarPubMed
Liang, WX, Ni, L, Carballar-Lejarazu, R, Zou, XX, Sun, WH, Wu, LJ, Yuan, XY, Mao, YL, Huang, W and Zou, SQ (2019) Comparative transcriptome among Euscaphis konishii Hayata tissues and analysis of genes involved in flavonoid biosynthesis and accumulation. BMC Genomics 20, 24.CrossRefGoogle ScholarPubMed
Liu, RR, Xu, SH, Li, JL, Hu, YL and Lin, ZP (2006) Expression profile of a PAL gene from Astragalus membranaceus var. Mongholicus and its crucial role in flux into flavonoid biosynthesis. Plant Cell Reports 25, 705710.CrossRefGoogle ScholarPubMed
Liu, XJ, An, XH, Liu, X, Hu, DG, Wang, XF, You, CX and Hao, YJ (2017) MdSnRK1.1 interacts with MdJAZ18 to regulate sucrose-induced anthocyanin and proanthocyanidin accumulation in apple. Journal of Experimental Botany 68, 29772990.CrossRefGoogle ScholarPubMed
Liu, XY, Si, Y, Jiao, YF, Zhang, QH, Li, YP, Liu, JP and Wang, ZY (2020) Research progress on flavonoids from Artemisia and their pharmacological activities. Special Wild Economic Animal and Plant Research 42, 8094.Google Scholar
Luo, XM, Lin, WH, Zhu, S, Zhu, JY, Sun, Y, Fan, XY, Cheng, M, Hao, Y, Oh, E, Tian, M, Liu, L, Zhang, M, Xie, Q, Chong, K and Wang, ZY (2010) Integration of light- and brassinosteroid-signaling pathways by a GATA transcription factor in Arabidopsis. Developmental Cell 19, 872883.CrossRefGoogle ScholarPubMed
Luo, JL, Tang, SH, Mei, FL, Peng, XJ, Li, J, Li, XF, Yan, XH, Zeng, XH, Liu, F, Wu, YH and Wu, G (2017) BnSIP1-1, a trihelix family gene, mediates abiotic stress tolerance and ABA signaling in Brassica napus. Frontiers in Plant Science 8, 44.CrossRefGoogle ScholarPubMed
Matus, JT, Poupin, MJ, Canon, P, Bordeu, E, Alcalde, JA and Arce-Johnson, P (2010) Isolation of WDR and bHLH genes related to flavonoid synthesis in grapevine (Vitis vinifera L.). Plant Molecular Biology 72, 607620.CrossRefGoogle Scholar
Mbatchou, VC, Ghafa, V and Khan, EM (2019) Assessment of piper guineense seed crude flavonoids for attractant activity using Prostephanus truncatus (larger grain borer). Journal of Agriculture and Ecology Research International 16, 15.CrossRefGoogle Scholar
Mesquita, E and Monteiro, M (2018) Simultaneous HPLC determination of flavonoids and phenolic acids profile in Pera-Rio orange juice. Food Research International 106, 5463.CrossRefGoogle ScholarPubMed
Messina, M (2010) Brief historical overview of the past two decades of soy and isoflavone research. Journal of Nutrition 140, 1350S1354S.CrossRefGoogle ScholarPubMed
Misra, A, McKnight, TD and Mandadi, KK (2018) Bromodomain proteins GTE9 and GTE11 are essential for specific BT2-mediated sugar and ABA responses in Arabidopsis thaliana. Plant Molecular Biology 96, 393402.CrossRefGoogle ScholarPubMed
Mlcek, J and Rop, O (2011) Fresh edible flowers of ornamental plants – a new source of nutraceutical foods. Trends in Food Science & Technology 22, 561569.CrossRefGoogle Scholar
Mou, WS, Li, DD, Luo, ZS, Mao, LC and Ying, TJ (2015) Transcriptomic analysis reveals possible influences of ABA on secondary metabolism of pigments, flavonoids and antioxidants in tomato fruit during ripening. PLoS One 10, e0129598.CrossRefGoogle ScholarPubMed
Mphahlele, RR, Stander, MA, Fawole, OA and Opara, UL (2014) Effect of fruit maturity and growing location on the postharvest contents of flavonoids, phenolic acids, vitamin C and antioxidant activity of pomegranate juice (cv. Wonderful). Scientia Horticulturae 179, 3645.CrossRefGoogle Scholar
Oh, E, Zhu, JY and Wang, ZY (2012) Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nature Cell Biology 14, 802809.CrossRefGoogle ScholarPubMed
Peng, ZH, Han, CY, Yuan, LB, Zhang, K, Huang, HM and Ren, CM (2011) Brassinosteroid enhances jasmonate-induced anthocyanin accumulation in Arabidopsis seedlings. Journal of Integrative Plant Biology 53, 632640.CrossRefGoogle ScholarPubMed
Petrussa, E, Braidot, E, Zancani, M, Peresson, C, Bertolini, A, Patui, S and Vianello, A (2013) Plant flavonoids – biosynthesis, transport and involvement in stress responses. International Journal of Molecular Sciences 14, 1495014973.CrossRefGoogle ScholarPubMed
Prati, S, Baravelli, V, Fabbri, D, Schwarzinger, C, Brandolini, V, Maietti, A, Tedeschi, P, Benvenuti, S, Macchia, M, Marotti, I, Bonetti, A, Catizone, P and Dinelli, G (2007) Composition and content of seed flavonoids in forage and grain legume crops. Journal of Separation Science 30, 491501.CrossRefGoogle ScholarPubMed
Saito, K, Yonekura-Sakakibara, K, Nakabayashi, R, Higashi, Y, Yamazaki, M, Tohge, T and Fernie, AR (2013) The flavonoid biosynthetic pathway in Arabidopsis: structural and genetic diversity. Plant Physiology and Biochemistry 72, 2134.CrossRefGoogle ScholarPubMed
Sikdar, S and Datta, S (2017) A novel statistical approach for identification of the master regulator transcription factor. BMC Bioinformatics 18, 79.CrossRefGoogle ScholarPubMed
Singh, M, Kaur, M and Silakari, O (2014) Flavones: an important scaffold for medicinal chemistry. European Journal of Medicinal Chemistry 84, 206239.CrossRefGoogle ScholarPubMed
Sosa, T, Chaves, N, Alias, JC, Escudero, JC, Henao, F and Gutierrez-Merino, C (2004) Inhibition of mouth skeletal muscle relaxation by flavonoids of Cistus ladanifer L.: a plant defense mechanism against herbivores. Journal of Chemical Ecology 30, 10871101.CrossRefGoogle ScholarPubMed
Su, H, Jiang, H and Li, YP (2015) Effects of PAL and ICS on the production of total flavonoids, daidzein and puerarin in Pueraria thomsonii Benth. Suspension cultures under low light stress. Journal of Plant Biochemistry and Biotechnology 24, 3441.CrossRefGoogle Scholar
Upadhyay, RK, Gupta, A, Soni, D, Garg, R, Pathre, UV, Nath, P and Sane, AP (2017) Ectopic expression of a tomato DREB gene affects several ABA processes and influences plant growth and root architecture in an age-dependent manner. Journal of Plant Physiology 214, 97107.CrossRefGoogle Scholar
Wang, LK, Feng, ZX, Wang, X, Wang, XW and Zhang, XG (2010a) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26, 136138.CrossRefGoogle Scholar
Wang, Y, Li, J and Xia, RX (2010b) Expression of chalcone synthase and chalcone isomerase genes and accumulation of corresponding flavonoids during fruit maturation of Guoqing No. 4 satsuma mandarin (Citrus unshiu Marcow). Scientia Horticulturae 125, 110116.CrossRefGoogle Scholar
Wang, Y, Hua, WP, Wang, J, Hannoufa, A, Xu, ZQ and Wang, ZZ (2013) Deep sequencing of Lotus corniculatus L. reveals key enzymes and potential transcription factors related to the flavonoid biosynthesis pathway. Molecular Genetics and Genomics 288, 131139.CrossRefGoogle Scholar
Wang, CH, Yu, J, Cai, YX, Zhu, PP, Liu, CY, Zhao, AC, Lu, RH, Li, MJ, Xu, FX and Yu, MD (2016) Characterization and functional analysis of 4-coumarate: CoA ligase genes in mulberry. PLoS One 11, e0157414.Google ScholarPubMed
Wang, N, Xu, HF, Jiang, SH, Zhang, ZY, Lu, NL, Qiu, HR, Qu, CZ, Wang, YC, Wu, SJ and Chen, XS (2017) MYB12 and MYB22 play essential roles in proanthocyanidin and flavonol synthesis in red-fleshed apple (Malus sieversii f. niedzwetzkyana). Plant Journal 90, 276292.CrossRefGoogle Scholar
Xu, WJ, Grain, D, Bobet, S, Le Gourrierec, J, Thevenin, J, Kelemen, Z, Lepiniec, L and Dubos, C (2014) Complexity and robustness of the flavonoid transcriptional regulatory network revealed by comprehensive analyses of MYB-bHLH-WDR complexes and their targets in Arabidopsis seed. New Phytologist 202, 132144.CrossRefGoogle ScholarPubMed
Xu, WJ, Dubos, C and Lepiniec, L (2015) Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends in Plant Science 20, 176185.CrossRefGoogle ScholarPubMed
Xu, JJ, Zhang, XF and Xue, HW (2016) Rice aleurone layer specific OsNF-YB1 regulates grain filling and endosperm development by interacting with an ERF transcription factor. Journal of Experimental Botany 67, 63996411.CrossRefGoogle ScholarPubMed
Xu, JY, Yu, YL, Shi, RY, Xie, GY, Zhu, Y, Wu, G and Qin, MJ (2018) Organ-specific metabolic shifts of flavonoids in Scutellaria baicalensis at different growth and development stages. Molecules 23, 428.CrossRefGoogle ScholarPubMed
Yang, XJ, Baskin, CC, Baskin, JM, Liu, GZ and Huang, ZY (2012) Seed mucilage improves seedling emergence of a sand desert shrub. PLoS One 7, e34597.Google ScholarPubMed
Yang, N, Zhao, KG, Li, X, Zhao, R, Aslam, MZ, Yu, L and Chen, LQ (2018) Comprehensive analysis of wintersweet flower reveals key structural genes involved in flavonoid biosynthetic pathway. Gene 676, 279289.CrossRefGoogle ScholarPubMed
Zhang, QL, Zhai, JJ, Shao, L and Lin, W (2019) Accumulation of anthocyanins: an adaptation strategy of Mikania micrantha to low temperature in winter. Frontiers in Plant Science 10, 1049.CrossRefGoogle ScholarPubMed
Zhao, J (2015) Flavonoid transport mechanisms: how to go, and with whom. Trends in Plant Science 20, 576585.CrossRefGoogle Scholar
Zhao, DB, Li, LX, Liu, XH, Li, MJ and Wang, WL (2007) Two new phenolic compounds from Artemisia sphaerocephala. Chinese Chemical Letters 18, 551553.CrossRefGoogle Scholar
Zhao, DQ, Tao, J, Han, CX and Ge, JT (2012) Flower color diversity revealed by differential expression of flavonoid biosynthetic genes and flavonoid accumulation in herbaceous peony (Paeonia lactiflora Pall.). Molecular Biology Reports 39, 1126311275.CrossRefGoogle Scholar
Zhao, DQ, Tang, WH, Hao, ZJ and Tao, J (2015) Identification of flavonoids and expression of flavonoid biosynthetic genes in two coloured tree peony flowers. Biochemical and Biophysical Research Communications 459, 450456.CrossRefGoogle ScholarPubMed
Zheng, J, An, YY and Wang, LJ (2018) 24-Epibrassinolide enhances 5-ALA-induced anthocyanin and flavonol accumulation in calli of ‘Fuji’ apple flesh. Plant Cell Tissue and Organ Culture 134, 319330.CrossRefGoogle Scholar
Zheng, JY, Meenu, M and Xu, BJ (2019) A systematic investigation on free phenolic acids and flavonoids profiles of commonly consumed edible flowers in China. Journal of Pharmaceutical and Biomedical Analysis 172, 268277.CrossRefGoogle ScholarPubMed
Zhu, Q, Zhang, JT, Gao, XS, Tong, JH, Xiao, LT, Li, WB and Zhang, HX (2010) The Arabidopsis AP2/ERF transcription factor RAP2.6 participates in ABA, salt and osmotic stress responses. Gene 457, 112.CrossRefGoogle ScholarPubMed
Zhu, JH, Cao, TJ, Dai, HF, Li, HL, Guo, D, Mei, WL and Peng, SQ (2016) De Novo transcriptome characterization of Dracaena cambodiana and analysis of genes involved in flavonoid accumulation during formation of dragon's blood. Scientific Reports 6, 38315.CrossRefGoogle ScholarPubMed
Zong, Y, Li, SM, Xi, XY, Cao, D, Wang, Z, Wang, R and Liu, BL (2019) Comprehensive influences of overexpression of a MYB transcriptor regulating anthocyanin biosynthesis on transcriptome and metabolome of tobacco leaves. International Journal of Molecular Sciences 20, 5123.CrossRefGoogle ScholarPubMed
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