Abstract
Chalcone Isomerase (CHI) catalyzes the biosynthesis of flavonoids and secondary metabolism in plants. Currently, there is no systematic analysis of CHIs gene family in Fagaceae which is available. In this study, twenty-two CHI proteins were identified in five species of the Fagaceae family. The CHI superfamily in Fagaceae can be classified into three subfamilies and five groups using phylogenetic analysis, analysis of physicochemical properties, and structural prediction. Results indicated that serine (Ser) and isoleucine (Ile) residues determine the substrate preferred by active Type I Fagaceae CHI, and the chalcone isomerase-like (CHIL) of Fagaceae had active site residues. Adaptive analysis of CHIs showed that CHIs are subject to selection pressure. The active CHI gene of Fagaceae was located in the cytoplasm, and it had the typical gene structure of CHI and contains four exons. All the twenty-two identified CHIs had the conserved domain motif 3, and the different groups had their own structural characteristics. In the process of fatty acid binding protein (FAP) evolution to CHIL and CHI, the physical and chemical properties of proteins also had significant differences in addition to changes in protein functions.
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References
Ban ZN, Qin H, Mitchell AJ, Liu BX, Zhang FX, Weng JK et al (2018) Noncatalytic chalcone isomerase-fold proteins in Humulus lupulus are auxiliary components in prenylated flavonoid biosynthesis. Proc Natl Acad Sci U S A 115:E5223–E5232. https://doi.org/10.1073/pnas.1802223115
Chen J, Wang J, Wang R, Xian B, Ren CX, Liu QQ et al. (2020) Integrated metabolomics and transcriptome analysis on flavonoid biosynthesis in safflower (Carthamus tinctorius L.) under MeJA treatment. BMC Plant Biology 20:1–12. https://doi.org/https://doi.org/10.1186/s12870-020-02554-6
Chen C, Xia R, Chen H, He Y (2018) TBtools, a Toolkit for Biologists integrating various HTS-data handling tools with a user-friendly interface.bioRxiv:289660 Doi: https://doi.org/10.1101/289660
Chen M, Zhu WJ, You X, Liu YD, Kaleri GM, Yang Q (2015) Isolation and characterization of a chalcone isomerase gene promoter from potato cultivars. Genet Mol Res 14:18872–18885. https://doi.org/10.4238/2015.December.28.37
Cheng CY, Krishnakumar V, Chan AP, Thibaud-Nissen F, Schobel S, Town CD (2017) Araport11: a complete reannotation of the Arabidopsis thaliana reference genome. Plant J 89:789–804. https://doi.org/10.1111/tpj.13415
Chung MS, Lee GW, Jeong YS, Kuk YI, Lee SS, Chung BY, Lee S (2019) Functional and genomic characterization of a wound- and methyl jasmonate-inducible chalcone isomerase in Eremochloa ophiuroides [Munro] Hack. Plant Physiol Biochem 144:355–364. https://doi.org/10.1016/j.plaphy.2019.10.008
Dastmalchi M, Dhaubhadel S (2015) Soybean chalcone isomerase: evolution of the fold, and the differential expression and localization of the gene family. Planta 241:507–523. https://doi.org/10.1007/s00425-014-2200-5
El A-D, Rafieian-Kopaei M, Amini-Khoei H, Abbasi S (2019) In Vitro Evaluation of Antioxidant Activity and Antibacterial Effects and Measurement of Total Phenolic and Flavonoid Contents of Quercus brantii L. Fruit Extract J Diet Suppl 16:408–416. https://doi.org/10.1080/19390211.2018.1470126
Forkmann G, Dangelmayr B (1980) Genetic control of chalcone isomerase activity in flowers of Dianthus caryophyllus. Biochem Genet 18:519–527. https://doi.org/10.1007/BF00484399
Hou SZ, Xu SJ, Jiang DX, Chen SX, Wang LL, Huang S, Lai XP (2012) Effect of the flavonoid fraction of Lithocarpus polystachyus Rehd. on spontaneously hypertensive and normotensive rats. J Ethnopharmacol 143:441–447. https://doi.org/10.1016/j.jep.2012.06.016
Jiang N, Doseff AI, Grotewold E (2016) Flavones From Biosynthesis to Health Benefits. Plants (Basel). https://doi.org/10.3390/plants5020027
Kaltenbach M, Burke JR, Dindo M, Pabis A, Munsberg FS, Rabin A et al (2018) Evolution of chalcone isomerase from a noncatalytic ancestor. Nat Chem Biol 14:548–555. https://doi.org/10.1038/s41589-018-0042-3
Kang JH, McRoberts J, Shi F, Moreno JE, Jones AD, Howe GA (2014) The flavonoid biosynthetic enzyme chalcone isomerase modulates terpenoid production in glandular trichomes of tomato. Plant Physiol 164:1161–1174. https://doi.org/10.1104/pp.113.233395
Karabin M, Hudcova T, Jelinek L, Dostalek P (2015) Biotransformations and biological activities of hop flavonoids. Biotechnol Adv 33:1063–1090. https://doi.org/10.1016/j.biotechadv.2015.02.009
Kheirandish F, Delfan B, Mahmoudvand H, Moradi N, Ezatpour B, Ebrahimzadeh F, Rashidipour M (2016) Antileishmanial, antioxidant, and cytotoxic activities of Quercus infectoria Olivier extract. Biomed Pharmacother 82:208–215. https://doi.org/10.1016/j.biopha.2016.04.040
Liu XM, Ahmad N, Yang LY, Fu TY, Kong J, Yao N et al (2019) Molecular cloning and functional characterization of chalcone isomerase from Carthamus tinctorius. AMB Express 9:132. https://doi.org/10.1186/s13568-019-0854-x
Liu Y, Zhao SZ, Wang JS, Zhao CZ, Guan HS, Hou L et al (2015) Molecular cloning, expression, and evolution analysis of type II CHI gene from peanut (Arachis hypogaea L.). Dev Genes Evol 225:1–10. https://doi.org/10.1007/s00427-015-0489-0
Mishra B, Gupta DK, Pfenninger M, Hickler T, Langer E, Nam B et al (2018) A reference genome of the European beech (Fagus sylvatica L). Gigascience. https://doi.org/10.1093/gigascience/giy063
Ngaki MN, Louie GV, Philippe RN, Manning G, Pojer F, Bowman ME et al (2012) Evolution of the chalcone-isomerase fold from fatty-acid binding to stereospecific catalysis. Nature 485:530–533. https://doi.org/10.1038/nature11009
Ni R, Zhu TT, Zhang XS, Wang PY, Sun CJ, Qiao YN et al (2019) Identification and evolutionary analysis of chalcone isomerase-fold proteins in ferns. J Exp Bot 71:290–304. https://doi.org/10.1093/jxb/erz425
Park SH, Lee CW, Cho SM, Lee H, Park H, Lee J, Lee JH (2018) Crystal structure and enzymatic properties of chalcone isomerase from the Antarctic vascular plant Deschampsia antarctica Desv. PLoS ONE 13:e0192415. https://doi.org/10.1371/journal.pone.0192415
Plomion C, Aury JM, Amselem J, Leroy T, Murat F, Duplessis S et al (2018) Oak genome reveals facets of long lifespan. Nat Plants 4:440–452. https://doi.org/10.1038/s41477-018-0172-3
Przysiecka L, Ksiazkiewicz M, Wolko B, Naganowska B (2015) Structure, expression profile and phylogenetic inference of chalcone isomerase-like genes from the narrow-leafed lupin (Lupinus angustifolius L.) genome. Front Plant Sci 6:268. https://doi.org/10.3389/fpls.2015.00268
Ralston L, Subramanian S, Matsuno M, Yu O (2005) Partial reconstruction of flavonoid and isoflavonoid biosynthesis in yeast using soyabean type I and type II chalcone isomerases. Plant Physiology Plant Physiology 137:1375–1388. https://doi.org/10.1104/pp.104.054502
Ramos AM, Usié A, Barbosa P, Barros PM, Capote T, Chaves I et al (2018) The draft genome sequence of cork oak. Scientific Data 5:180069. https://doi.org/10.1038/sdata.2018.69
Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 465:120–120. https://doi.org/10.1038/nature08670
Shimada N, Aoki T, Sato S, Nakamura Y, Tabata S, Ayabe S-i (2003) A cluster of genes encodes the two types of chalcone isomerase involved in the biosynthesis of general flavonoids and legume-specific 5-deoxy(iso)flavonoids in Lotus japonicus. Plant Physiol 131:941–951. https://doi.org/10.1104/pp.004820
Sork VL, Fitz-Gibbon ST, Puiu D, Crepeau M, Gugger PF, Sherman R et al. (2016) First Draft Assembly and Annotation of the Genome of a California Endemic Oak Quercus lobata Nee Fagaceae. G3 Bethesda 6: 3485–3495 Doi: https://doi.org/10.1534/g3.116.030411
Wang HL, Wang W, Zhan JC, Huang WD, Xu HY (2019) Tissue-specific accumulation and subcellular localization of chalcone isomerase (CHI) in grapevine. Plant Cell. Tissue and Organ Culture (PCTOC) 137:125–137. https://doi.org/10.1007/s11240-019-01557-y
Wang RK, Zhan SF, Zhao TJ, Zhou XL, Wang CE (2015) Positive selection sites in tertiary structure of Leguminosae chalcone isomerase 1. Genet Mol Res 14:1957–1967. https://doi.org/10.4238/2015.march.20.5
Xing Y, Liu Y, Zhang Q, Nie XH, Sun YM, Zhang ZZ et al (2019) Hybrid de novo genome assembly of Chinese chestnut (Castanea mollissima). Gigascience. https://doi.org/10.1093/gigascience/giz112
Xu GX, Guo CC, Shan HY, Kong HZ (2012) Divergence of duplicate genes in exon-intron structure. Proc Natl Acad Sci U S A 109:1187–1192. https://doi.org/10.1073/pnas.1109047109
Yang ZH (2006) Computational molecular evolution. . Oxford University Press 259–292.
Yang ZH, Nielsen R (2000) Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 17:32–43. https://doi.org/10.1093/oxfordjournals.molbev.a026236
Yin YC, Zhang XD, Gao ZQ, Hu T, Liu Y (2018) The Research Progress of Chalcone Isomerase (CHI) in Plants. Mol Biotechnol 61:32–52. https://doi.org/10.1007/s12033-018-0130-3
Zhang YT, Lin LM, Long YH, Guo HY, Xing ZB (2019) Comprehensive Transcriptome Analysis Revealed the Effects of the Light Quality, Light Intensity, and Photoperiod on Phlorizin Accumulation in Lithocarpus polystachyus Rehd. Forests 10:995. https://doi.org/10.3390/f10110995
Zu QL, Qu YY, Ni ZY, Zheng K, Chen Q, Chen QJ (2019) The Chalcone Isomerase Family in Cotton: Whole-Genome Bioinformatic and Expression Analyses of the Gossypium barbadense L. Response to Fusarium Wilt Infection Genes (Basel) 1:1006. https://doi.org/10.3390/genes10121006
Funding
The project was supported by grants from the National Natural Science Foundation of China (31760221), Natural Science Foundation of Hebei Province (H2020209033), and Hebei Education Department sponsored scientific research projects (ZD2019075).
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Lin, LM., Guo, HY., Song, X. et al. Adaptive Evolution of Chalcone Isomerase Superfamily in Fagaceae. Biochem Genet 59, 491–505 (2021). https://doi.org/10.1007/s10528-020-10012-z
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DOI: https://doi.org/10.1007/s10528-020-10012-z