Abstract
Here, we identified sequence variations of CYP72A69 and UGT73F4 genes from the Sojeongja and Haepum cultivars, and revealed that accumulation patterns of soyasaponin Aa and Ab were different in the Sojeongja and Haepum cultivars. Several genes related in soyasaponin biosynthetic pathway showed significant changes in their expression patterns in two soybean cultivars and soyasaponin contents were also altered under several abiotic stress conditions, albeit no significant correlations between soyasaponin contents and biosynthetic gene expression were observed. We also demonstrated that UGT73F4 gene could be responsible for biosynthesis of soyasaponin Aa in the Socheongja by investigating gene expression and soyasaponin accumulations. Our results provide a molecular basis to improve the commercial properties of soyasaponin in Korean domestic soybean cultivars.
This is a preview of subscription content, log in via an institution to check access.
References
Abe I, Rohmer M, Prestwich GD (1993) Enzymatic cyclization of squalene and oxidosqualene to sterols and triterpenes. Chem Rev 93:2189–2206
Bowles D, Isayenkova J, Lim EK, Poppenberger B (2005) Glycosyltransferases: managers of small molecules. Curr Opin Plant Biol 8:254–263
Choi CW, Choi SW, Kim HJ, Lee KS, Kim SH, Kim SL, Do SH, Seo WD (2018) Germinated soy germ with increased soyasaponin Ab improves BMP-2-induced bone formation and protects against in vivo bone loss in osteoporosis. Scientific Reports 8:12970
De Geyter N, Gholami A, Goormachtig S, Goossens A (2012) Transcriptional machineries in jasmonate-elicited plant secondary metabolism. Trends Plant Sci 17:349–359
Ebizuka Y, Shibuya M, Wakita E (2011) C-22 Hydroxylase. United States Patent Appl Publ 2011(0171698):A1
Ellington AA, Berhow M, Singletary KW (2005) Induction of macroautophagy in human colon cancer cells by soybean B-group triterpenoid saponins. Carcinogenesis 26:159–167
Ellington AA, Berhow MA, Singletary KW (2006) Inhibition of Akt signaling and enhanced ERK1/2 activity are involved in induction of macroautophagy by triterpenoid B-group soyasaponins in colon cancer cells. Carcinogenesis 27:298–306
Eum HL, Park Y, Yi TG, Lee JW, Ha KS, Choi IY, Park NI (2020) Effect of germination environment on the biochemical compounds and anti-inflammatory properties of soybean cultivars. PLoS ONE 15:e0232159
Guang CE, Chen J, Sang SY, Cheng SY (2014) Biological functionality of soyasaponins and soyasapogenols. J Agric and Food Chem 62:8247–8255
Huang X, Cai W, Xu B (2014) Kinetic changes of nutrients and antioxidant capacities of germinated soybean (Glycine max L.) and mung bean (Vigna radiata L.) with germination time. Food Chem 143:268–276
Huang GC, Cai WX, Xu BJ (2017) Improvement in beta-carotene, vitamin B-2, GABA, free amino acids and isoflavones in yellow and black soybeans upon germination. Lwt-Food Science and Technology 75:488–496
Im JY, Kim S-C, Kim SH, Choi Y, Yang M, Cho IH, Kim HR (2016) Protein and amino-acid contents in backtae, seoritae, huktae, and seomoktae soybeans with different cooking methods. Korean J Food Cook Sci 32:567–574
Kim SL, Lee JE, Kwon YU, Kim WH, Jung GH, Kim DW, Lee CK, Lee YY, Kim MJ, Kim YH, Hwang TY, Chung IM (2013) Introduction and nutritional evaluation of germinated soy germ. Food Chem 136:491–500
Kim HJ, Choi EJ, Kim HS, Choi CW, Choi SW, Kim SL, Seo WD, Do SH (2019) Soyasaponin Ab alleviates postmenopausal obesity through browning of white adipose tissue. J Funct Foods 57:453–464
Kim YC, Cha A, Hussain M, Lee K, Lee S (2020) Impact of Agrobacterium-infiltration and transient overexpression of BroMYB28 on glucoraphanin biosynthesis in broccoli leaves. Plant Biotechnology Reports 14:373–380
Lee JH, Han JH, Kim YC, Lee YH, Hong JK, Lee S (2019) Transgenic Arabidopsis plants expressing CsBCATs affect seed germination under abiotic stress conditions. Plant Biotechnol Rep 13:95–101
Ma M, Wang P, Yang RQ, Gu ZX (2018) Effects of UV-B radiation on the isoflavone accumulation and physiological-biochemical changes of soybean during germination Physiological-biochemical change of germinated soybean induced by UV-B. Food Chem 250:259–267
Matsuda H, Nakayasu M, Aoki Y, Yamazaki S, Nagano AJ, Yazaki K, Sugiyama A (2020) Diurnal metabolic regulation of isoflavones and soyasaponins in soybean roots. Plant Direct 4:e00286
Messina MJ, Persky V, Setchell KD, Barnes S (1994) Soy intake and cancer risk: a review of the in vitro and in vivo data. Nutr Cancer 21:113–131
Mora-Escobedo R, Robles-Ramirez Mdel C, Ramon-Gallegos E, Reza-Aleman R (2009) Effect of protein hydrolysates from germinated soybean on cancerous cells of the human cervix: an in vitro study. Plant Foods Hum Nutr 64:271–278
Moses T, Papadopoulou KK, Osbourn A (2014) Metabolic and functional diversity of saponins, biosynthetic intermediates and semi-synthetic derivatives. Crit Rev Biochem Mol Biol 49:439–462
Murata M, Houdai T, Yamamoto H, Matsumori M, Oishi T (2006) Membrane interaction of soyasaponins in association with their antioxidation effect analysis of biomembrane interaction. Soy Protein Res 8:81–85
Sayama T, Ono E, Takagi K, Takada Y, Horikawa M, Nakamoto Y, Hirose A, Sasama H, Ohashi M, Hasegawa H, Terakawa T, Kikuchi A, Kato S, Tatsuzaki N, Tsukamoto C, Ishimoto M (2012) The Sg-1 glycosyltransferase locus regulates structural diversity of triterpenoid saponins of soybean. Plant Cell 24:2123–2138
Shi H, Nam PK, Ma Y (2010) Comprehensive profiling of isoflavones, phytosterols, tocopherols, minerals, crude protein, lipid, and sugar during soybean (Glycine max) germination. J Agric Food Chem 58:4970–4976
Shibuya M, Hoshino M, Katsube Y, Hayashi H, Kushiro T, Ebizuka Y (2006) Identification of beta-amyrin and sophoradiol 24-hydroxylase by expressed sequence tag mining and functional expression assay. FEBS J 273:948–959
Shibuya M, Nishimura K, Yasuyama N, Ebizuka Y (2010) Identification and characterization of glycosyltransferases involved in the biosynthesis of soyasaponin I in Glycine max. FEBS Lett 584:2258–2264
Sundaramoorthy J, Park GT, Komagamine K, Tsukamoto C, Chang JH, Lee JD, Kim JH, Seo HS, Song JT (2019) Biosynthesis of DDMP saponins in soybean is regulated by a distinct UDP-glycosyltransferase. New Phytol 222:261–274
Takagi K, Nishizawa K, Hirose A, Kita A, Ishimoto M (2011) Manipulation of saponin biosynthesis by RNA interference-mediated silencing of beta-amyrin synthase gene expression in soybean. Plant Cell Rep 30:1835–1846
Thimmappa R, Geisler K, Louveau T, O’Maille P, Osbourn A (2014) Triterpene biosynthesis in plants. Annu Rev Plant Biol 65(65):225–257
Wan Q, Chen SL, Shan ZH, Yang ZL, Chen LM, Zhang CJ, Yuan SL, Hao QN, Zhang XJ, Qiu DZ, Chen HF, Zhou XA (2017) Stability evaluation of reference genes for gene expression analysis by RT-qPCR in soybean under different conditions. PLoS ONE 12:e0189405
Wang FZ, Wang HF, Wang DH, Fang F, Lai JX, Wu T, Tsao R (2015) Isoflavone, gamma-aminobutyric acid contents and antioxidant activities are significantly increased during germination of three Chinese soybean cultivars. J Funct Foods 14:596–604
Wang FB, Ren XQ, Zhang F, Qi MY, Zhao HY, Chen XH, Ye YX, Yang JY, Li SG, Zhang Y, Niu Y, Zhou Q (2019) A R2R3-type MYB transcription factor gene from soybean, GmMYB12, is involved in flavonoids accumulation and abiotic stress tolerance in transgenic Arabidopsis. Plant Biotechnol Rep 13:219–233
Yang SH, Ahn EK, Lee JA, Shin TS, Tsukamoto C, Suh JW, Mei I, Chung G (2015) Soyasaponins Aa and Ab exert an anti-obesity effect in 3T3-L1 adipocytes through downregulation of PPAR gamma. Phytother Res 29:281–287
Yano R, Takagi K, Takada Y, Mukaiyama K, Tsukamoto C, Sayama T, Kaga A, Anai T, Sawai S, Ohyama K, Saito K, Ishimoto M (2017) Metabolic switching of astringent and beneficial triterpenoid saponins in soybean is achieved by a loss-of-function mutation in cytochrome P450 72A69. Plant Journal 89:527–539
Yano R, Takagi K, Tochigi S, Fujisawa Y, Nomura Y, Tsuchinaga H, Takahashi Y, Takada Y, Kaga A, Anai T, Tsukamoto C, Seki H, Muranaka T, Ishimoto M (2018) Isolation and characterization of the soybean Sg-3 gene that is involved in genetic variation in sugar chain composition at the C-3 position in soyasaponins. Plant Cell Physiol 59:797–810
Yim JH, Lee OH, Choi UK, Kim YC (2009) Antinociceptive and anti-inflammatory effects of ethanolic extracts of Glycine max (L.) Merr and Rhynchosia nulubilis seeds. Int J Mol Sci 10:4742–4753
Acknowledgements
This work was supported by various grants from: (1) the New Breeding Technologies Development Program of the Republic of Korea’s Rural Development Administration (RDA) (Project No. PJ01532503 to J.H.Lee), (2) the Basic Science Research Program of the National Research Foundation (NRF) funded by the Republic of Korea’s Ministry of Education (Grant No. 2020R1I1A1A01072914 to Y.-C.Kim), (3) the RDA’s “Cooperative Research Program for Agriculture Science & Technology Development” (Project title: ‘Study on the identification of useful metabolites derived from crop sprout and standardization,’ Project No. PJ01421201 to W.D.Seo), and (4) the Medical Research Center Program (NRF-2017R1A5A2015061 to D.J.Yoo) through the NRF funded by the Republic of Korea’s MSIP. We wish to express our gratitude towards Jae-Hyeok Park for his assistance.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yun, Y.J., Lee, H., Yoo, D.J. et al. Molecular analysis of soyasaponin biosynthetic genes in two soybean (Glycine max L. Merr.) cultivars. Plant Biotechnol Rep 15, 117–124 (2021). https://doi.org/10.1007/s11816-021-00661-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11816-021-00661-w