Prediction of C-glycosylated apigenin (vitexin) biosynthesis in <i>Ficus deltoidea</i> based on plant proteins identified by LC-MS/MS

doi:10.1007/s11515-017-1472-0

Front. Biol.

2017, Vol. 12

Issue (6) : 448-458 https://doi.org/10.1007/s11515-017-1472-0

RESEARCH ARTICLE

Prediction of C-glycosylated apigenin (vitexin) biosynthesis in Ficus deltoidea based on plant proteins identified by LC-MS/MS

Farah Izana Abdullah^1,², Lee Suan Chua^1,²(

), Zaidah Rahmat³

¹. Metabolites Profiling Laboratory, Institute of Bioproduct Development, Universiti Teknologi Malaysia, 81310 UTM Skudai, Johor Bahru, Johor, Malaysia
². Department of Bioprocess and Polymer Engineering, Faculty of Chemical and Energy Engineering, Universiti Teknologi Malaysia, 81310 UTM Skudai, Johor Bahru, Johor, Malaysia
³. Department of Biotechnology and Medical Engineering, Faculty of Biosciences & Medical Engineering, Universiti Teknologi Malaysia, 81310 UTM Skudai, Johor Bahru, Johor, Malaysia

Download: PDF(552 KB) HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks

Abstract

BACKGROUND: Plant secondary metabolites act as defence molecules to protect plants from biotic and abiotic stresses. In particular, C-glycosylated flavonoids are more stable and reactive than their O-glycosylated counterparts. Therefore, vitexin (apigenin 8-C glucoside) present in Ficus deltoidea is well-known for its antioxidant, anti-inflammatory, and antidiabetic properties.

METHODS: Phenol based extraction was used to extract proteins (0.05% yield) with less plant pigments. This can be seen from clear protein bands in gel electrophoresis. In-gel trypsin digestion was subsequently carried out and analysed for the presence of peptides by LC-MS/MS.

RESULTS: Thirteen intact proteins are identified on a 12% polyacrylamide gel. The mass spectra matching was found to have 229 proteins, and 11.4% of these were involved in secondary metabolism. Proteins closely related to vitexin biosynthesis are listed and their functions are explained mechanistically. Vitexin synthesis is predicted to involve plant polyketide chalcone synthase, isomerization by chalcone isomerase, oxidation by cytochrome P450 to convert flavanone to flavone, and transfer of sugar moiety by C-glycosyltransferase, followed by dehydration to produce flavone-8-C-glucosides.

CONCLUSIONS: Phenol based extraction, followed by gel electrophoresis and LC-MS/MS could identify proteome explaining vitexin biosynthesis in F. deltoidea. Many transferases including β-1,3-galactosyltransferase 2 and glycosyl hydrolase family 10 protein were detected in this study. This explains the importance of transferase family proteins in C-glycosylated apigenin biosynthesis in medicinal plant.

Keywords C-glycosylation vitexin apigenin 8-C glucoside proteins peptides LC-MS/MS

Corresponding Author(s): Lee Suan Chua

Online First Date: 18 December 2017 Issue Date: 10 January 2018

Cite this article:

Farah Izana Abdullah,Lee Suan Chua,Zaidah Rahmat. Prediction of C-glycosylated apigenin (vitexin) biosynthesis in Ficus deltoidea based on plant proteins identified by LC-MS/MS[J]. Front. Biol., 2017, 12(6): 448-458.

URL:

https://academic.hep.com.cn/fib/EN/10.1007/s11515-017-1472-0
https://academic.hep.com.cn/fib/EN/Y2017/V12/I6/448

Fig.1 Electrophoretic gel imageof proteins extracted from Ficus deltoidea leaves.

Category	Protein name	Accession number	Mass (Da)	MOWSE score	Sequence
Transcription factors	Putative WRKY transcription factor2	NP_200438.1	74562	155	CTAPGCTVR; DSSQSNVFR; TNTDFSIDSNLR;FPFLPGVNGNALSSEK
	Putative c-myb-like transcriptionfactor MYB3R-4	BAD94312.1	90420	71.6	MPEETMHIR; VDQICMEANVR; TDVQCLHRWQK;NDPLHDYSPLGIR
	Ethylene-responsive factor 2 (ERF2)	NP_193820.1	45668	211	EMQTIRDVMFK; NNKNNKAQTETR; VLSPPPPHMSLQR;KEMQTIRDVMFK; RNNVYFEIIEEPR; VFAIGLTLSWCLILR
	Ethylene-responsive factor 10 (ERF10)	NP_171876.1	26393	123	MEPDLDLNASP; LRMEPDLDLNASP; ENVTTAVAVKDGGEK
	Auxin response factor 10 (ARF 10)	AAF04627.1	77795	103	WPNSPWR; HHHYQAR; IGDEPFSDFMK; VEAVAGSGGACSXVDK
	ABRE binding factor 4	NP_001154626.1	44845	22.6	DGNMEGSSGGGGESNVPPGR
Jasmonic acid	12-oxophytodienoate reductase 1 (OPR1)	NP_177794.1	41168	26.7	TMGEVHACPHTLMPMR; SYGNVPQPHAAIYYSQR
Cysteine	Serine O-acetyltransferase (Transferase)	NP_175988.1	34251	108	TGNTQDDDSR; VSESFAVDIHPGAK; DVPARTTAVGNPARLIGGK
Transferase	O-methyltransferase family protein	NP_177877.1	42327	169	ENGQTGK; AMSESSTMVM; AMSESSTMVMK;AMSESSTMVMKK
	Putative protein kinase	NP_001154651.1	47141	23.3	SDVYSFGVVLLEILTGR; DTGCAESGSSTPLMSGELK
	Putative β-1,3-galactosyltransferase2 (glycosyltransferase)	Q8L7F9	45758	548	YHEPEYWK; GEYSSRSFVSR; GMSHPSVTEAER;SVQESLQNGAPLSDDMGK
	Putative glycosyl hydrolase family10 protein	NP_192556.2	74402	9383	IVPLSGKVFAAATQR; NTNTNHTSDDNNDK;TQTWMGPAQMITDK; QTYNSFPVGTCINR; QLNKTDLMNAVQKR; IVPLSGKVFAAATQRK;REQYIVIANVQATDK; TQTWMGPAQMITDKIK; TDLMNAVQKRLTDLLTR
	β-galactosidase 5	NP_175127.1	81444	3404	GLGPAGHSYVNWAAK; LGNYEEAHVFTAGK;FSFSSQVNLRGGANK; GNLLVLFEELGGDISK; ENRKFSFSSQVNLR; QPLTWYKAYFDAPR;GSLAKQNKQPLTWYK; SAMQGFTEKIVQMMK; DTTDYLWYTTSVDIK; GSCVAFLTNYHMNAPAK
	O-fucosyltransferase family protein	NP_176423.3	73297	31.8	AELDAYR; MPTIRPNK; EAKPGFYMK; IQETGAILVR;MLNATLVIPK
	Sucrose synthase 6 (glycosyltransferase)	NP_177480.1	106877	69.9	QSRYHMK; DGQEQHDVK; EHLMNEIEK; MSSSSQAMLQK;DNAEHMGYLADR
Polyketide	Polyketide cyclase/dehydrase andlipid transport superfamily protein	NP_850574.1	46265	217	MENALR; GIWSYVCK; FYLCDGSPMK; GAQLSQTSQNAGI;DFYMDNEYRK
Flavonol	Flavonol synthase 5	NP_201165.1	36964	32.2	ETFTQSIGGDTAEYVL; NYLGGINNWDEHLFHR
Miscellaneous	Putative cytochrome P450 71A28	P58047.2	58217	133	FNWR; TNEFELER; VVQEHVDEGENK; FPLIAFPSLASFTI
	cytochrome P450, family 87, subfamilyA, polypeptide 2	NP_001184974.1	55058	131	NDVDMCR; HFMAFGGGMR; LQMAAFLHSLVTK;LQMAAFLHSLVTK; RLTEEHETILRNR
	Cytochrome P450, family 706, subfamilyA, polypeptide 7	NP_192970.1	58774	144	DEDENMSMNHVK;
	LACERATA	ACO87292.1	7506	126	MHDWISDNLR;
	Cytochrome b5 isoform B	NP_180831.1	15016	88.3	MGDEAKIFTL; SEVSEHNQAHD; CWIVINGKVYN;VTKFLEDHPGGD;DVLLSSTGKD; ATDDFEDVG; MMEQYYVGEI; TPPKQPHYNQ; DKTSEFIIK; LLQFLVPLAI;LGLAVGIR

Tab.1 Identified proteinsrelated to secondary metabolites production

Fig.2 Flavone biosynthesis pathwayCHS: chalcone synthase; STS: stilbene synthase; CHI: chalcone isomerase;FNS: flavone synthase; CGT: C-glycosyltransferase.

1	Adam Z, Khamis S, Ismail A , Hamid M (2012). Ficus deltoidea: A potential alternative medicine for diabetes mellitus. Evid Based Complement Alternat Med, 2012: 632763 https://doi.org/10.1155/2012/632763 pmid: 22701507
2	Afrin S, Huang J J, Luo Z Y (2015). JA-mediated transcriptional regulation of secondary metabolism in medicinal plants. Sci Bull, 60(12): 1062–1072 https://doi.org/10.1007/s11434-015-0813-0
3	Akashi T, Aoki T, Ayabe S (2005). Molecular and biochemical characterization of 2-hydroxyisoflavanone dehydratase. Involvement of carboxylesterase-like proteins in leguminous isoflavone biosynthesis. Plant Physiol, 137(3): 882–891 https://doi.org/10.1104/pp.104.056747 pmid: 15734910
4	Akashi T, Fukuchi-Mizutani M, Aoki T , Ueyama Y , Yonekura-Sakakibara K , Tanaka Y , Kusumi T , Ayabe S (1999). Molecular cloning and biochemical characterization of a novel cytochrome P450, flavone synthase II, that catalyzes direct conversion of flavanones to flavones. Plant Cell Physiol, 40(11): 1182–1186 https://doi.org/10.1093/oxfordjournals.pcp.a029505 pmid: 10635120
5	Akey D L, Razelun J R, Tehranisa J, Sherman D H , Gerwick W H , Smith J L (2010). Crystal structures of dehydratase domains from the curacin polyketide biosynthetic pathway. Structure, 18(1): 94–105 https://doi.org/10.1016/j.str.2009.10.018 pmid: 20152156
6	Alejandro S, Lee Y, Tohge T , Sudre D , Osorio S , Park J, Bovet L, Lee Y , Geldner N , Fernie A R , Martinoia E (2012). AtABCG29 is a monolignol transporter involved in lignin biosynthesis. Curr Biol, 22(13): 1207–1212 https://doi.org/10.1016/j.cub.2012.04.064 pmid: 22704988
7	Austin M B, Noel J P (2003). The chalcone synthase superfamily of type III polyketide synthases. Nat Prod Rep, 20(1): 79–110 https://doi.org/10.1039/b100917f pmid: 12636085
8	Azemin A, Dharmaraj S, Hamdan M R , Mat N, Ismail Z, Khamsah S M (2014). Discriminating Ficus deltoidea var. bornensis from Different Localities by HPTLC and FTIR Fingerprinting. J Appl Pharm Sci, 4: 69–75
9	Bak S, Beisson F, Bishop G , Hamberger B , Höfer R , Paquette S (2011). Cytochromes P450. Arab B, e0144 https://doi.org/10.1199/tab.0144
10	Bednar R A, Hadcock J R (1988). Purification and characterization of chalcone isomerase from soybeans. J Biol Chem, 263(20): 9582–9588 pmid: 3384815
11	Bernhoft A, Siem H, Bjertness E , Meltzer M , Flaten T , Holmsen E (2010). Bioactive compounds in plants–benefits and risks for man and animals. in Proceedings from a Symposium Held at The Norwegian Academy of Science and Letters, Novus forlag, Oslo
12	Bradford M M (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem, 72(1-2): 248–254 https://doi.org/10.1016/0003-2697(76)90527-3 pmid: 942051
13	Brazier-Hicks M, Edwards R (2013). Metabolic engineering of the flavone-C-glycoside pathway using polyprotein technology. Metab Eng, 16: 11–20 https://doi.org/10.1016/j.ymben.2012.11.004 pmid: 23246521
14	Brazier-Hicks M, Evans K M, Cunningham O D, Hodgson D R W, Steel P G, Edwards R (2008). Catabolism of glutathione conjugates in Arabidopsis thaliana. Role in metabolic reactivation of the herbicide safener fenclorim. J Biol Chem, 283(30): 21102–21112 https://doi.org/10.1074/jbc.M801998200 pmid: 18522943
15	Brazier-Hicks M, Evans K M, Gershater M C, Puschmann H, Steel P G , Edwards R (2009). The C-glycosylation of flavonoids in cereals. J Biol Chem, 284(27): 17926–17934 https://doi.org/10.1074/jbc.M109.009258 pmid: 19411659
16	Bungaruang L, Gutmann A, Nidetzky B (2013). Leloir glycosyltransferases and natural product glycosylation: Biocatalytic synthesis of the C-glucoside nothofagin, a major antioxidant of redbush herbal tea. Adv Synth Catal, 355(14-15): 2757–2763 https://doi.org/10.1002/adsc.201300251 pmid: 24415961
17	Cheng H, Li L, Cheng S , Cao F, Wang Y, Yuan H (2011). Molecular cloning and function assay of a chalcone isomerase gene (GbCHI) from Ginkgo biloba. Plant Cell Rep, 30(1): 49–62 https://doi.org/10.1007/s00299-010-0943-4 pmid: 21046109
18	Choo C Y, Sulong N Y, Man F, Wong T W (2012). Vitexin and isovitexin from the Leaves of Ficus deltoidea with in-vivo α-glucosidase inhibition. J Ethnopharmacol, 142(3): 776–781 https://doi.org/10.1016/j.jep.2012.05.062 pmid: 22683902
19	Courts F L, Williamson G (2015). Critical Reviews in Food Science and Nutrition The occurrence, fate and biological activities of C- glycosyl flavonoids in the human diet. Crit Rev Food Sci Nutr, 55(10): 1352–1367 https://doi.org/10.1080/10408398.2012.694497 pmid: 24915338
20	Crosby K C, Pietraszewska-Bogiel A, Gadella T W J Jr, Winkel B S J (2011). Förster resonance energy transfer demonstrates a flavonoid metabolon in living plant cells that displays competitive interactions between enzymes. FEBS Lett, 585(14): 2193–2198 https://doi.org/10.1016/j.febslet.2011.05.066 pmid: 21669202
21	Crozier A, Jaganath I B, Clifford M N (2009). Dietary phenolics: chemistry, bioavailability and effects on health. Nat Prod Rep, 26(8): 1001–1043 https://doi.org/10.1039/b802662a pmid: 19636448
22	Day A J, Gee J M, DuPont M S, Johnson I T, Williamson G (2003). Absorption of quercetin-3-glucoside and quercetin-4′-glucoside in the rat small intestine: the role of lactase phlorizin hydrolase and the sodium-dependent glucose transporter. Biochem Pharmacol, 65(7): 1199–1206 https://doi.org/10.1016/S0006-2952(03)00039-X pmid: 12663055
23	Dey S, Corina Vlot A (2015). Ethylene responsive factors in the orchestration of stress responses in monocotyledonous plants. Front Plant Sci, 6: 640 https://doi.org/10.3389/fpls.2015.00640 pmid: 26379679
24	Dixon D P, Hawkins T, Hussey P J , Edwards R (2009). Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily. J Exp Bot, 60(4): 1207–1218 https://doi.org/10.1093/jxb/ern365 pmid: 19174456
25	Du Y, Chu H, Chu I K , Lo C (2010a). CYP93G2 is a flavanone 2-hydroxylase required for C-glycosyl-flavone biosynthesis in rice. Plant Physiol, 154(1):324–33
26	Du Y, Chu H, Wang M , Chu I K , Lo C (2010b). Identification of flavone phytoalexins and a pathogen-inducible flavone synthase II gene (SbFNSII) in sorghum. J Exp Bot, 61(4): 983–994 https://doi.org/10.1093/jxb/erp364 pmid: 20007684
27	Dürr C, Hoffmeister D, Wohlert S E , Ichinose K , Weber M , Von Mulert U , Thorson J S , Bechthold A (2004). The glycosyltransferase UrdGT2 catalyzes both C- and O-glycosidic sugar transfers. Angew Chem Int Ed Engl, 43(22): 2962–2965 https://doi.org/10.1002/anie.200453758 pmid: 15170316
28	Dzolin S, Ahmad R, Zain M M , Ismail M I (2015). Flavonoid distribution in four varieties of Ficus deltoidea (Jack). J Med Plant Herb Ther Res, 3: 1–9
29	El Amrani A, Barakate A, Askari B M , Li X, Roberts A G, Ryan M D, Halpin C (2004). Coordinate expression and independent subcellular targeting of multiple proteins from a single transgene. Plant Physiol, 135(1): 16–24 https://doi.org/10.1104/pp.103.032649 pmid: 15141063
30	Falcone Ferreyra M L , Rodriguez E , Casas M I , Labadie G , Grotewold E , Casati P (2013). Identification of a bifunctional maize C- and O-glucosyltransferase. J Biol Chem, 288(44): 31678–31688 https://doi.org/10.1074/jbc.M113.510040 pmid: 24045947
31	Farsi E, Shafaei A, Hor S Y , Ahamed M B K , Fei M, Attitalla I H (2011). Correlation between enzymes inhibitory effects and antioxidant activities of standardized fractions of methanolic extract obtained from Ficus deltoidea leaves. Afr J Biotechnol, 10(67): 15184–15194 https://doi.org/10.5897/AJB11.1365
32	François I E J A , Van Hemelrijck W , Aerts A M , Wouters P F J , Proost P , Broekaert W F , Cammue B P A (2004). Processing in Arabidopsis thaliana of a heterologous polyprotein resulting in differential targeting of the individual plant defensins. Plant Sci, 166(1): 113–121 https://doi.org/10.1016/j.plantsci.2003.09.001
33	Ha S H, Liang Y S, Jung H, Ahn M J , Suh S C , Kweon S J , Kim D H , Kim Y M , Kim J K (2010). Application of two bicistronic systems involving 2A and IRES sequences to the biosynthesis of carotenoids in rice endosperm. Plant Biotechnol J, 8(8): 928–938 https://doi.org/10.1111/j.1467-7652.2010.00543.x pmid: 20649940
34	Hakamatsuka T, Mori K, Ishida S , Ebizuka Y , Sankawa U (1998). Purification of 2-hydroxyisoflavanone dehydratase from the Cell Cultures of Pueraria lobata. Phytochemistry, 49(2): 497–505 https://doi.org/10.1016/S0031-9422(98)00266-0
35	Halpin C, Cooke S E, Barakate A, El Amrani A , Ryan M D (1999). Self-processing 2A-polyproteins--a system for co-ordinate expression of multiple proteins in transgenic plants. Plant J, 17(4): 453–459 https://doi.org/10.1046/j.1365-313X.1999.00394.x pmid: 10205902
36	Hasegawa K, Cowan A B, Nakatsuji N, Suemori H (2007). Efficient multicistronic expression of a transgene in human embryonic stem cells. Stem Cells, 25(7): 1707–1712 https://doi.org/10.1634/stemcells.2006-0813 pmid: 17395772
37	He M, Min J W, Kong W L, He X H, Li J X, Peng B W (2016). A review on the pharmacological effects of vitexin and isovitexin. Fitoterapia, 115: 74–85 https://doi.org/10.1016/j.fitote.2016.09.011 pmid: 27693342
38	Hicks M A, Barber A E 2nd, Giddings L A, Caldwell J, O’Connor S E , Babbitt P C (2011). The evolution of function in strictosidine synthase-like proteins. Proteins, 79(11): 3082–3098 https://doi.org/10.1002/prot.23135 pmid: 21948213
39	Isaacson T, Damasceno C M B, Saravanan R S, He Y, Catalá C , Saladié M , Rose J K (2006). Sample extraction techniques for enhanced proteomic analysis of plant tissues. Nat Protoc, 1(2): 769–774 https://doi.org/10.1038/nprot.2006.102 pmid: 17406306
40	Ishihara A, Ogura Y, Tebayashi S , Iwamura H (2002). Jasmonate-induced changes in flavonoid metabolism in barley (Hordeum vulgare) leaves. Biosci Biotechnol Biochem, 66(10): 2176–2182 https://doi.org/10.1271/bbb.66.2176 pmid: 12450129
41	Ishikawa F, Haushalter R W, Burkart M D (2012). Dehydratase-specific probes for fatty acid and polyketide synthases. J Am Chem Soc, 134(2): 769–772 https://doi.org/10.1021/ja2082334 pmid: 22188524
42	Jiménez C R , Huang L , Qiu Y, Burlingame A L (2001). Searching sequence databases over the internet: protein identification using MS-Fit. Curr Protoc Protein Sci, Chapter 16: 5 pmid: 18429132
43	Kaltenbach M, Schröder G, Schmelzer E , Lutz V, Schröder J (1999). Flavonoid hydroxylase from Catharanthus roseus: cDNA, heterologous expression, enzyme properties and cell-type specific expression in plants. Plant J, 19(2): 183–193 https://doi.org/10.1046/j.1365-313X.1999.00524.x pmid: 10476065
44	Kašparová M , Siatka T (2014). Production of flavonoids and isoflavonoids in jasmonic acid-induced red clover suspension cultures. Ceska Slov Farm, 63(1): 17–21 pmid: 24568333
45	Kerscher F, Franz G (1987). Biosynthesis of Vitexin and Isovitexin : Enzymatic Synthesis of the C-Glucosylflavones Vitexin and Isovitexin with an Enzyme Preparation from Fagopyrum esculentum M. Seedlings. Z Naturforsch C, 42: 519–524
46	Kramell R, Miersch O, Atzorn R , Parthier B , Wasternack C (2000). Octadecanoid-derived alteration of gene expression and the “oxylipin signature” in stressed barley leaves. Implications for different signaling pathways. Plant Physiol, 123(1): 177–188 https://doi.org/10.1104/pp.123.1.177 pmid: 10806235
47	Laemmli U K (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227(5259): 680–685 https://doi.org/10.1038/227680a0 pmid: 5432063
48	Le Roy J, Huss B, Creach A , Hawkins S , Neutelings G (2016). Glycosylation Is a Major Regulator of Phenylpropanoid Availability and Biological Activity in Plants. Front Plant Sci, 7: 735 https://doi.org/10.3389/fpls.2016.00735 pmid: 27303427
49	Li Y, Dodge G J, Fiers W D, Fecik R A, Smith J L, Aldrich C C (2015). Functional Characterization of a Dehydratase Domain from the Pikromycin Polyketide Synthase. J Am Chem Soc, 137(22): 7003–7006 https://doi.org/10.1021/jacs.5b02325 pmid: 26027428
50	Luley-Goedl C, Nidetzky B (2011). Glycosides as compatible solutes: biosynthesis and applications. Nat Prod Rep, 28(5): 875–896 https://doi.org/10.1039/c0np00067a pmid: 21390397
51	Lussier F X, Colatriano D, Wiltshire Z , Page J E , Martin V J J (2013). Engineering microbes for plant polyketide biosynthesis. Comput Struct Biotechnol J, 3(4): e201210020 https://doi.org/10.5936/csbj.201210020 pmid: 24688680
52	Martens S, Mithöfer A (2005). Flavones and flavone synthases. Phytochemistry, 66(20): 2399–2407 https://doi.org/10.1016/j.phytochem.2005.07.013 pmid: 16137727
53	Mierziak J, Kostyn K, Kulma A (2014). Flavonoids as important molecules of plant interactions with the environment. Molecules, 19(10): 16240–16265 https://doi.org/10.3390/molecules191016240 pmid: 25310150
54	Misbah H, Aziz A A, Aminudin N (2013). Antidiabetic and antioxidant properties of Ficus deltoidea fruit extracts and fractions. BMC Complement Altern Med, 13(1): 118 https://doi.org/10.1186/1472-6882-13-118 pmid: 23718315
55	Mizutani M, Sato F (2011). Unusual P450 reactions in plant secondary metabolism. Arch Biochem Biophys, 507(1): 194–203 https://doi.org/10.1016/j.abb.2010.09.026 pmid: 20920462
56	Mohd K S, Rosli A S, Azemin A, Mat N , Zakaria A J (2016). Comprehensive Biological Activities Evaluation and Quantification of Marker Compounds of Ficus deltoiea Jack Varieties. Int J Pharmacogn Phytochem Res, 8: 1698–1708
57	Morant M, Bak S, Møller B L , Werck-Reichhart D (2003). Plant cytochromes P450: tools for pharmacology, plant protection and phytoremediation. Curr Opin Biotechnol, 14(2): 151–162 https://doi.org/10.1016/S0958-1669(03)00024-7 pmid: 12732316
58	Nagatomo Y, Usui S, Ito T , Kato A, Shimosaka M, Taguchi G (2014). Purification, molecular cloning and functional characterization of flavonoid C-glucosyltransferases from Fagopyrum esculentum M. (buckwheat) cotyledon. Plant J, 80(3): 437–448 https://doi.org/10.1111/tpj.12645 pmid: 25142187
59	Pauwels L, Inzé D, Goossens A (2009). Jasmonate-inducible gene: What does it mean? Trends Plant Sci, 14(2): 87–91 https://doi.org/10.1016/j.tplants.2008.11.005 pmid: 19162528
60	Praveena R, Sadasivam K, Kumaresan R , Deepha V , Sivakumar R (2013). Experimental and DFT studies on the antioxidant activity of a C-glycoside from Rhynchosia capitata. Spectrochim Acta A Mol Biomol Spectrosc, 103: 442–452 https://doi.org/10.1016/j.saa.2012.11.001 pmid: 23246319
61	Rawat P, Kumar M, Sharan K , Chattopadhyay N , Maurya R (2009). Ulmosides A and B: flavonoid 6-C-glycosides from Ulmus wallichiana, stimulating osteoblast differentiation assessed by alkaline phosphatase. Bioorg Med Chem Lett, 19(16): 4684–4687 https://doi.org/10.1016/j.bmcl.2009.06.074 pmid: 19596573
62	Saito K, Yonekura-Sakakibara K, Nakabayashi R , Higashi Y , Yamazaki M , Tohge T , Fernie A R (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 pmid: 23473981
63	Schaller F (2001). Enzymes of the biosynthesis of octadecanoid-derived signalling molecules. J Exp Bot, 52(354): 11–23 https://doi.org/10.1093/jexbot/52.354.11 pmid: 11181709
64	Shafaei A, Farsi E, Ismail Z , Asmawi M Z (2012). Quantitative High Performance Thin-Layer Chromatography Method for Analysis of Vitexin and Isovitexin in Extracts of Leaves of Ficus deltoidea. Asian J Chem, 24: 2286
65	Shevchenko A, Tomas H, Havlis J , Olsen J V , Mann M (2006). In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc, 1(6): 2856–2860 https://doi.org/10.1038/nprot.2006.468 pmid: 17406544
66	Stafford H A (1991). Flavonoid evolution: an enzymic approach. Plant Physiol, 96(3): 680–685 https://doi.org/10.1104/pp.96.3.680 pmid: 16668242
67	University of California (2017). Ms-Fit. Available at: .
68	Väisänen E E , Smeds A I , Fagerstedt K V , Teeri T H , Willför S M , Kärkönen A (2015). Coniferyl alcohol hinders the growth of tobacco BY-2 cells and Nicotiana benthamiana seedlings. Planta, 242(3): 747–760 https://doi.org/10.1007/s00425-015-2348-7 pmid: 26108783
69	Wu J, Zaleski T J, Valenzano C, Khosla C , Cane D E (2005). Polyketide double bond biosynthesis. Mechanistic analysis of the dehydratase-containing module 2 of the picromycin/methymycin polyketide synthase. J Am Chem Soc, 127(49): 17393–17404 https://doi.org/10.1021/ja055672+ pmid: 16332089
70	Xiao J, Capanoglu E, Jassbi A R , Miron A (2016). Advance on the flavonoid C-glycosides and health benefits. Crit Rev Food Sci Nutr, 56(sup1 Suppl 1): S29–S45 https://doi.org/10.1080/10408398.2015.1067595 pmid: 26462718
71	Xiao J, Chen T, Cao H (2015). Flavonoid glycosylation and biological benefits. Biotechnol Adv, https://doi.org/10.1016/j.biotechadv.2014.05.004 pmid: 24858477
72	Xu F, Li L, Zhang W , Cheng H , Sun N, Cheng S, Wang Y (2012). Isolation, characterization, and function analysis of a flavonol synthase gene from Ginkgo biloba. Mol Biol Rep, 39(3): 2285–2296 https://doi.org/10.1007/s11033-011-0978-9 pmid: 21643949
73	Yang C Q, Fang X, Wu X M , Mao Y B , Wang L J , Chen X Y (2012). Transcriptional regulation of plant secondary metabolism. J Integr Plant Biol, 54(10): 703–712 https://doi.org/10.1111/j.1744-7909.2012.01161.x pmid: 22947222
74	Yonekura-Sakakibara K , Hanada K (2011). An evolutionary view of functional diversity in family 1 glycosyltransferases. Plant J, 66(1): 182–193 https://doi.org/10.1111/j.1365-313X.2011.04493.x pmid: 21443631
75	Yonekura-Sakakibara K , Tohge T , Matsuda F , Nakabayashi R , Takayama H , Niida R , Watanabe-Takahashi A , Inoue E , Saito K (2008). Comprehensive flavonol profiling and transcriptome coexpression analysis leading to decoding gene-metabolite correlations in Arabidopsis. Plant Cell, 20(8): 2160–2176 https://doi.org/10.1105/tpc.108.058040 pmid: 18757557
76	Zhai R, Wang Z, Zhang S , Meng G, Song L, Wang Z , Li P, Ma F, Xu L (2016). Two MYB transcription factors regulate flavonoid biosynthesis in pear fruit (Pyrus bretschneideri Rehd.). J Exp Bot, 67(5): 1275–1284 https://doi.org/10.1093/jxb/erv524 pmid: 26687179
77	Zhang X, Abrahan C, Colquhoun T A , Liu C and Sciences A (2017). A proteolytic regulator controlling chalcone synthase stability and flavonoid biosynthesis in Arabidopsis. Plant Cell Online, tpc-00855 https://doi.org/10.1105/tpc.16.00855.
78	Zhao J, Davis L C, Verpoorte R (2005). Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv, 23(4): 283–333 https://doi.org/10.1016/j.biotechadv.2005.01.003 pmid: 15848039
79	Zunoliza A, Khalid H, Zhari I , Rasadah M A (2009). Anti-inflammatory activity of standardised extracts of leaves of three varieties of Ficus deltoidea. Int J Pharm Clin Res, 1: 100–105

[1]	Clare H. Scott Chialvo, Thomas Werner. **Drosophila, destroying angels, and deathcaps! Oh my! A review of mycotoxin tolerance in the genus Drosophila**[J]. Front. Biol., 2018, 13(2): 91-102.
[2]	Hansa Jain. Cationic antimicrobial peptide: LL-37 and its role in periodontitis[J]. Front. Biol., 2017, 12(2): 116-123.
[3]	Jian Li,Chun Guo,Nickolas Steinauer,Jinsong Zhang. New insights into transcriptional and leukemogenic mechanisms of AML1-ETO and E2A fusion proteins[J]. Front. Biol., 2016, 11(4): 285-304.
[4]	Pijush Basak,Tanay Debnath,Rajat Banerjee,Maitree Bhattacharyya. Selective binding of divalent cations toward heme proteins[J]. Front. Biol., 2016, 11(1): 32-42.
[5]	Leon H. CHEW,Calvin K. YIP. Structural biology of the macroautophagy machinery[J]. Front. Biol., 2014, 9(1): 18-34.
[6]	Lijun WANG, Marit NILSEN-HAMILTON. Biomineralization proteins: from vertebrates to bacteria[J]. Front Biol, 2013, 8(2): 234-246.
[7]	Xin YANG, Fengyang DENG, Katrina M. RAMONELL. Receptor-like kinases and receptor-like proteins: keys to pathogen recognition and defense signaling in plant innate immunity[J]. Front Biol, 2012, 7(2): 155-166.
[8]	Jinbiao MA, Ying HUANG, . Post-transcriptional regulation of miRNA biogenesis and functions[J]. Front. Biol., 2010, 5(1): 32-40.
[9]	Yizhen LIU, Shi-Yan LI. Urokinase-targeted recombinant bacterial protein toxins – a rationally designed and engineered anticancer agent for cancer therapy[J]. Front Biol Chin, 2009, 4(1): 1-6.
[10]	LIU Zhongyuan, WANG Yun, LÜ Guodong, WANG Xianlei, ZHANG Fuchun, MA Ji. Cloning, sequencing and prokaryotic expression of cDNAs for antifreeze protein family from Beetle [J]. Front. Biol., 2008, 3(3): 279-286.
[11]	LU Yiqin, LIU Junfan. Erythrocyte membrane proteins and membrane skeleton[J]. Front. Biol., 2007, 2(3): 247-255.
[12]	LI Dongdong, HE Shaoheng. Analysis of total proteins in pollen of Humulus scandens Lour in Wuhan Region of China by two-dimensional electrophoresis[J]. Front. Biol., 2007, 2(3): 309-313.
[13]	LIU Wenjie, SU Jing, WANG Guizhong, WANG Sanying. Proteomic approach for acute-phase proteins of hemolymph and muscles in Scylla serrata challenged by a pathogenic bacterium[J]. Front. Biol., 2006, 1(3): 254-258.

Viewed

Full text

Abstract

Cited

Shared

Discussed