Isolation, sequencing of the HvnHID gene and its role in the purple-grain colour development in Tibetan hulless barley
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2-hydroxyisoflavanone dehydratase (HID) plays an important role in isoflavone biosynthesis. In this study, HID was isolated from the seeds of the purple-grained Tibetan hulless barley variety Nerumuzha and the white-grained variety Kunlun 10. The HvnHID gene includes the 981 bp open reading frame and encodes a protein of 327 amino acids. It has a typical Abhydrolase_3 domain (78–306) and belongs to the carboxylesterase (CXE) family of the Abhydrolase_3 (α/β hydrolase) superfamily. There are eight nucleotide differences in the HvnHID coding sequence and two amino acid differences (one in the Abhydrolase_3 domain) between Nerumuzha and Kunlun 10. The HvnHID of hulless barley has the closest relationship with the HID in Hordeum vulgare, and the most distant relationship in Panicum hallii. At the early-mid stage of the seed colour development, the HvnHID expression levels in the purple and black seeds were significantly higher than in the white and blue ones (P < 0.01). During the seed colour development of purple-grained hulless barley, the expression of the key genes (HvnF3'H, HvnDRF, HvnANT1, and HvnGT) in the anthocyanidin biosynthetic pathway increased significantly, while the HvnHID expression decreased significantly (P < 0.01). Thus, it is likely that HvnHID negatively regulates the anthocyanidin biosynthesis. This result provides an important basis for further study of the biological functions of HvnHID in the anthocyanidin biosynthetic pathway.

Akashi T., Aoki T., Ayabe S.I. (1999): Cloning and functional expression of a cytochrome P450 cDNA encoding 2-hydroxyisoflavanone synthase involved in biosynthesis of the isoflavonoid skeleton in licorice. Plant Physiology, 121: 821−828.
Akashi T., Aoki T., Ayabe S.I. (2005): Molecular and biochemical characterization of 2-hydroxyisoflavanone dehydratase. involvement of carboxylesterase-like proteins in leguminous isoflavone 9biosynthesis. Plant Physiology, 137: 882–891.
Ayabe S. (2007): Polynucleotide encoding 2-hydorxyisoflavanone dehydratase and application of the same. US20070050865.
Clark S.T., Verwoerd W.S. (2011): A systems approach to identifying correlated gene targets for the loss of colour pigmentation in plants. BMC Bioinformatics, 12: 343.
Dai F., Wang X., Zhang X., Chen Z., Zhang G. (2018): Assembly and analysis of a qingke reference genome demonstrates its close genetic relation to modern cultivated barley. Plant Biotechnology Journal, 16: 760–770.
Deavours B.E., Dixon R.A. (2005): Metabolic engineering of isoflavonoid biosynthesis in Alfalfa. Plant Physiology, 138: 2245–2259.
Du H., Huang Y.B., Tang Y.X. (2010): Genetic and metabolic engineering of isoflavonoid biosynthesis. Applied Microbiology and Biotechnology, 86: 1293–1312.
Eulgem T., Rushton P.J., Robatzek S., Somssich I.E. (2000): The WRKY superfamily of plant transcription factors. Trends in Plant Science, 5: 199–206.
Ferreira L.L., Silva T.R., Maturana M.A., Spritzer P.M. (2019): Dietary intake of isoflavones is associated with a lower prevalence of subclinical cardiovascular disease in postmenopausal women: cross-sectional study. Journal of Human Nutrition and Dietetics, 32: 810–818.
Gershater M.C., Cummins I., Edwards R. (2007): Role of a carboxylesterase in herbicide bioactivation in Arabidopsis thaliana. Journal of Biological Chemistry, 282: 21460−21466.
Gordeeva E.I., Glagoleva A.Y., Kukoeva T.V., Khlestkina E.K., Shoeva O.Y. (2019): Purple-grained barley (Hordeum vulgare L.): marker-assisted development of NILs for investigating peculiarities of the anthocyanin biosynthesis regulatory network. BMC Plant Biology, 19 (S1): 52.
Hakamatsuka T., Mori K., Ishida S., Ebizuka Y., Sankawa U. (1998): Purification of 2-hydroxyisoflavanone dehydratase from the cell cultures of Pueraria lobata in honour of Professor G.H. Neil Towers 75th birthday. Phytochemistry, 49: 497–505.
Hu M., Lu Z., Guo J., Luo Y., Li H., Li L., Gao F. (2016): Cloning and characterization of the cDNA and promoter of UDP-glucose: flavonoid 3-O-glucosyltransferase gene from a purple-fleshed sweet potato. South African Journal of Botany, 106: 211–220.
Jayakodi M., Padmarasu S., Haberer G., Bonthala V.S., Stein N. (2020): The barley pan-genome reveals the hidden legacy of mutation breeding. Nature, 588: 284–289.
Jia Y., Selva C., Zhang Y., Li B., Mcfawn L.A., Li C.D. (2020): Uncovering the evolutionary origin of blue anthocyanins in cereal grains. The Plant Journal, 101: 1057–1074.
Johnson E.T., Ryu S., Yi H., Shin B., Cheong H., Choi G. (2001): Alteration of a single amino acid changes the substrate specificity of dihydroflavonol 4-reductase. Plant Journal, 25: 325–333.
Jung W., Yu O., Lau S.-M.C., O’Keefe D.P., Odell J., Fader G., McGonigle B. (2000): Identification and expression of isoflavone synthase, the key enzyme for biosynthesis of isoflavones in legumes. Nature Biotechnology, 18: 208–220.
Kaur R., Aslam L., Kapoor N., Mahajan R. (2020): Identification and comparative expression analysis of chalcone synthase, flavanone 3-hydroxylase and dihydroflavonol 4-reductase genes in wild pomegranate (Punica granatum L.) organs. Brazilian Journal of Botany, 43: 1–14.
Lee Y., Yoon H.R., Yong S.P., Liu J.R., Choi G. (2005): Reciprocal regulation of arabidopsis ugt78d2 and banyuls is critical for regulation of the metabolic flux of anthocyanidins to condensed tannins in developing seed coats. Journal of Plant Biology, 48: 356–370.
Lenfant N., Hotelier T., Velluet E., Bourne Y., Marchot P., Chatonnet A. (2012): ESTHER, the database of the α/β-hydrolase fold superfamily of proteins: tools to explore diversity of functions. Nucleic Acids Research, 41: D423–D429.
Li Y.L., Long C.L., Kato K.J., Yang C.Y., Sato K. (2011): Indigenous knowledge and traditional conservation of hulless barley (Hordeum vulgare) germplasm resources in the Tibetan communities of Shangri-la, Yunnan, SW China. Genetic Resources and Crop Evolution, 58: 645–655.
Liang J.J., Deng G.D., Long H., Pan Z.F., Wang C.P., Cai P., Xu D.L., Nimaand Z.X., Yu M.Q. (2012): Virus-induced silencing of genes encoding LEA protein in Tibetan hulless barley (Hordeum vulgare ssp. vulgare) and their relationship to drought tolerance. Molecular Breeding, 30: 441–451.
Liu C.J., Blount J.W., Steele C.L., Dixon R.A. (2002): Bottlenecks for metabolic engineering of isoflavone glycoconjugates in Arabidopsis. Proceedings of the National Academy of Sciences, 99: 14578–14583.
Livingstone J.M., Zolotarov Y., StröMvik M.V. (2011): Transcripts of soybean isoflavone 7-O-glucosyltransferase and hydroxyisoflavanone dehydratase gene homologues are at least as abundant as transcripts of their well known counterparts. Plant Physiology and Biochemistry, 49: 1071–1075.
Lou Q., Liu Y., Qi Y., Jiao S., Tian F., Jiang L., Wang Y. (2014): Transcriptome sequencing and metabolite analysis reveals the role of delphinidin metabolism in flower colour in grape hyacinth. Journal of Experimental Botany, 65: 3157–3164.
Ma D., Constabel C.P. (2019): MYB repressors as regulators of phenylpropanoid metabolism in plants. Trends in Plant Science, 24: 275–289.
Nomura T., Murase T., Ogita S., Kato Y. (2015): Molecular identification of tuliposide B-converting enzyme: a lactone-forming carboxylesterase from the pollen of tulip. The Plant Journal, 83: 252–262.
Ollis D.L., Cheah E., Cygler M., Dijkstra B., Frolow F., Franken S.M., Harel M., Remington S.J., Silman I., Schrag J. (1992): The α/β hydrolase fold. Protein Engineering Design & Selection, 5: 197−211.
Petroni K., Tonelli C. (2011): Recent advances on the regulation of anthocyanin synthesis in reproductive organs. Plant Science, 181: 219–229.
Rodas F.R., Rodriguez T.O., Murai Y., Iwashina T., Sugawara S., Suzuki M., Nakabayashi R., Yonekura-Sakakibara K., Saito K., Kitajima J., Toda K., Takahashi R. (2014): Linkage mapping, molecular cloning and functional analysis of soybean gene Fg2 encoding flavonol 3-O-glucoside (16) rhamnosyltransferase. Plant Molecular Biology, 84: 287–300.
Sawada Y., Kinoshita K., Akashi T., Aoki T., Ayabe S.I. (2002): Key amino acid residues required for aryl migration catalysed by the cytochrome p450 2-hydroxyisoflavanone synthase. Plant Journal, 31: 555−564.
Shimamura M., Akashi T., Sakurai N., Suzuki H., Saito K., Shibata D., Ayabe S., Aoki T. (2007): 2-Hydroxyisoflavanone dehydratase is a critical determinant of isoflavone productivity in hairy root cultures of Lotus japonicus. Plant and Cell Physiology, 48: 1652–1657.
Shoeva O.Y., Mock H.P., Kukoeva T.V., Börner A., Khlestkina E.K. (2016): Regulation of the flavonoid biosynthesis pathway genes in purple and black grains of Hordeum vulgare. PLoS ONE, 11: e0163782.
Suantika G., Situmorang M.L., Aditiawati P., Khakim A., Suryanarayan S., Nori S.S., Kumar S. Ferisca P. (2016): Effect of red seaweed on growth, salinity stress tolerance and vibriosis resistance in Shrimp Litopenaeus vannamei Hatchery. Journal of Fisheries and Aquatic Science, 12: 127−133.
Sun M., Wang Y.S., Yang D.Q., Wei C.L., Gao L.P., Xia T., Shan Y., Luo Y. (2010): Reference genes for real-time fluorescence quantitative PCR in Camellia sinensis. Chinese Bulletin of Botany, 45: 579–587.
Tanaka Y., Sasaki N., Ohmiya A. (2008): Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant Journal, 54: 733–749.
Tohge T., de Souza L.P., Fernie A.R. (2017): Current understanding of the pathways of flavonoid biosynthesis in model and crop plants. Journal of Experimental Botany, 68: 4013–4028.
Vadivel A.K.A., Sukumaran A., Li X.Y., Dhaubhadel S. (2016): Soybean isoflavonoids: role of GmMYB176 interactome and 14-3-3 proteins. Phytochemistry Reviews, 15: 391–403.
Waki T., Yoo C.Y., Fujino N., Mameda R., Denessiouk K., Yamashita S., Motohashi R., Akashi T., Aoki T., Ayabe S., Takahashi S., Nakayama T. (2016): Identification of protein-protein interactions of isoflavonoid biosynthetic enzymes with 2-hydroxyisoflavanone synthase in soybean (Glycine max (L.) Merr.). Biochemical and biophysical research communications, 469: 546–551.
Wang H., Li M.F., Yang Y., Jin W.M. (2015): Recent advances on the molecular mechanisms of anthocyanin synthesis in fruits. Plant Physiology Journal, 51: 29–43.
Wang X.Q. (2011): Structure, function, and engineering of enzymes in isoflavonoid biosynthesis. Functional and Integrative Genomics, 11: 13–22.
Wu K.L., Yao X.H., Yao Y.H., Chi D.Z., Feng Z.Y. (2017a): Analysis of the relationship between Wx gene polymorphisms and amylose content in hulless barley. Czech Journal of Genetics and Plant Breeding, 53:144–152.
Wu X.X., Gong Q.H., Ni X.P., Zhou Y., Gao Z.H. (2017b): Ufgt: the key enzyme associated with the petals variegation in japanese apricot. Frontiers in Plant Science, 8: 108.
Yao X.H., Wu K.L., Yao Y.H., Bai Y.X., Ye J.X., Chi D.Z. (2018): Construction of a high-density genetic map: genotyping by sequencing (GBS) to map purple seed coat color (Psc) in hulless barley. Hereditas, 155: 37.
Yonekura-Sakakibara K., Higashi Y., Nakabayashi R. (2019): The origin and evolution of plant flavonoid metabolism. Frontiers in Plant Science, 10: 943.
Zadoks J.C., Chang T.T., Konzak C.F. (1974): A decimal code for the growth stages of cereals. Weed Research, 14: 415–421.
Zeng X., Guo Y., Xu Q., Mascher M., Guo G., Li S., Mao L., Liu Q., Xia Z., Zhou J., Yuan H., Tai S., Wang Y., Wei Z., Song L., Zha S., Li S., Tang Y., Bai L., Zhuang Z., He W., Zhao S., Fang X., Gao Q., Yin Y., Wang J., Yang H., Zhang J., Henry R.J., Stein N., Tashi N. (2018): Origin and evolution of qingke barley in Tibet. Nature Communications, 9: 5433.
Zeng X., Xu T., Ling Z., Wang Y., Li X., Xu S., Xu Q., Zha S., Qimei W., Basang Y., Dunzhu J., Yu M., Yuan H., Nyim T. (2020): An improved high-quality genome assembly and annotation of Tibetan hulless barley. Scientific Data, 7: 139.
Zheng T., Tan W., Yang H., Zhang L.E., Li T.T., Liu B.H., Zhang D.W., Lin H.H. (2019): Regulation of anthocyanin accumulation via MYB75/HAT1/TPL-mediated transcriptional repression. PLoS Genetics, 15: e1007993.
Zheng Y., Li J.H., Xin N., Wang L., Guan B.H., Li S.H. (2013): Anthocyanin profile and gene expression in berry skin of two redvitis viniferagrape cultivars that are sunlight dependent versus sunlight independent. Australian Journal of Grape and Wine Research, 19: 238–248.
Zhou C., Zeng Z., Suo J., Li X., Han N. (2021): Manipulating a single transcription factor, ant1, promotes anthocyanin accumulation in barley grains. Journal of Agricultural and Food Chemistry, 69 (18).
Zhu Y., Bao Y. (2021): Genome-wide mining of myb transcription factors in the anthocyanin biosynthesis pathway of Gossypium Hirsutum. Biochemical Genetics, 59: 678–696.
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