Czech J. Genet. Plant Breed., 2022, 58(1):1-9 | DOI: 10.17221/34/2021-CJGPB

Isolation, sequencing of the HvnHID gene and its role in the purple-grain colour development in Tibetan hulless barleyOriginal Paper

Xiaohua Yao1,2,3,4, Leping Su1,5, Youhua Yao1,2,3,4, Likun An1,2,3,4, Yixiong Bai1,2,3,4, Xin Li1,2,3,4, Kunlun Wu*,1,2,3,4
1 Qinghai University, Xining, P.R. China
2 Qinghai Academy of Agricultural and Forestry Sciences, Xining, P.R. China
3 Qinghai Key Laboratory of Hulless Barley Genetics and Breeding, Xining, P.R. China
4 Qinghai Subcenter of National Hulless Barley Improvement, Xining, P.R. China
5 Yan'an Institute of Agricultural Sciences, Yan'an, P.R. China

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.

Keywords: 2-hydroxyisoflavanone dehydratase; anthocyanidin; isoflavones; purple grain

Published: December 17, 2021  Show citation

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Yao X, Su L, Yao Y, An L, Bai Y, Li X, Wu K. Isolation, sequencing of the HvnHID gene and its role in the purple-grain colour development in Tibetan hulless barley. Czech J. Genet. Plant Breed. 2022;58(1):1-9. doi: 10.17221/34/2021-CJGPB.
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References

  1. 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. Go to original source... Go to PubMed...
  2. 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. Go to original source... Go to PubMed...
  3. Ayabe S. (2007): Polynucleotide encoding 2-hydorxyisoflavanone dehydratase and application of the same. US20070050865.
  4. 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. Go to original source... Go to PubMed...
  5. 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. Go to original source... Go to PubMed...
  6. Deavours B.E., Dixon R.A. (2005): Metabolic engineering of isoflavonoid biosynthesis in Alfalfa. Plant Physiology, 138: 2245-2259. Go to original source... Go to PubMed...
  7. Du H., Huang Y.B., Tang Y.X. (2010): Genetic and metabolic engineering of isoflavonoid biosynthesis. Applied Microbiology and Biotechnology, 86: 1293-1312. Go to original source... Go to PubMed...
  8. 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. Go to original source... Go to PubMed...
  9. 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. Go to original source... Go to PubMed...
  10. 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. Go to original source... Go to PubMed...
  11. 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. Go to original source... Go to PubMed...
  12. 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. Go to original source...
  13. 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. Go to original source...
  14. 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. Go to original source... Go to PubMed...
  15. 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. Go to original source... Go to PubMed...
  16. 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. Go to original source... Go to PubMed...
  17. 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. Go to original source... Go to PubMed...
  18. 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. Go to original source...
  19. 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. Go to original source...
  20. Lenfant N., Hotelier T., Velluet E., Bourne Y., Marchot P., Chatonnet A. (2012): ESTHER, the database of the α/βhydrolase fold superfamily of proteins: tools to explore diversity of functions. Nucleic Acids Research, 41: D423-D429. Go to original source... Go to PubMed...
  21. 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. Go to original source...
  22. 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. Go to original source...
  23. 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. Go to original source... Go to PubMed...
  24. 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. Go to original source... Go to PubMed...
  25. 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. Go to original source... Go to PubMed...
  26. Ma D., Constabel C.P. (2019): MYB repressors as regulators of phenylpropanoid metabolism in plants. Trends in Plant Science, 24: 275-289. Go to original source... Go to PubMed...
  27. 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. Go to original source... Go to PubMed...
  28. 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. Go to original source... Go to PubMed...
  29. Petroni K., Tonelli C. (2011): Recent advances on the regulation of anthocyanin synthesis in reproductive organs. Plant Science, 181: 219-229. Go to original source... Go to PubMed...
  30. 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. Go to original source... Go to PubMed...
  31. 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. Go to original source... Go to PubMed...
  32. 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. Go to original source... Go to PubMed...
  33. 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. Go to original source... Go to PubMed...
  34. 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. Go to original source...
  35. 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.
  36. Tanaka Y., Sasaki N., Ohmiya A. (2008): Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant Journal, 54: 733-749. Go to original source... Go to PubMed...
  37. 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. Go to original source... Go to PubMed...
  38. 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. Go to original source...
  39. 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. Go to original source... Go to PubMed...
  40. 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.
  41. Wang X.Q. (2011): Structure, function, and engineering of enzymes in isoflavonoid biosynthesis. Functional and Integrative Genomics, 11: 13-22. Go to original source... Go to PubMed...
  42. 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. Go to original source...
  43. 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. Go to original source... Go to PubMed...
  44. 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. Go to original source... Go to PubMed...
  45. Yonekura-Sakakibara K., Higashi Y., Nakabayashi R. (2019): The origin and evolution of plant flavonoid metabolism. Frontiers in Plant Science, 10: 943. Go to original source... Go to PubMed...
  46. Zadoks J.C., Chang T.T., Konzak C.F. (1974): A decimal code for the growth stages of cereals. Weed Research, 14: 415-421. Go to original source...
  47. 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. Go to original source... Go to PubMed...
  48. 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. Go to original source... Go to PubMed...
  49. 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. Go to original source... Go to PubMed...
  50. 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. Go to original source...
  51. 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). Go to original source... Go to PubMed...
  52. 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. Go to original source... Go to PubMed...

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