Current perspectives on the beneficial effects of soybean isoflavones and their metabolites on plants

Abstract

Soybeans have traditionally been a staple part of the human diet being highly rich in protein and lipid content. In an addition to the high nutritional components, soybeans have several functional components, like isoflavones, saponins, lecithin, and oligosaccharides. Soybeans emerge as a healthy functional food option. Isoflavones are most notable functional component of soybeans, exhibiting antioxidant activity while preventing plant-related diseases (e.g., antimicrobial and antiherbivore activities) and having positive effects on the life quality of plants. Isoflavones are thus sometimes referred to as phytochemicals. The latest research trends evince substantial interest in the biological efficacy of isoflavones in the human body as well as in plants and their related mechanisms. However, there is little information on the relationship between isoflavones and plants than beneficial human effects. This review discusses what is known about the physiological communication (transport and secretion) between isoflavones and plants, especially in soybeans.

Keywords: Environmental adaptation; Plant; Rhizobium; Soybean-derived isoflavone; Symbiotic interaction.

Fig. 1

Schematic representation of the phenylpropanoid pathway depicting the key intermediates and enzymes for isoflavone biosynthesis, as well as partial regulation pathway. Isoflavones are biosynthesized via a phenylalanine-dependent pathway. GmMYB29 activates CHS expression, and GmMYB176 inhibits CHS expression. In addition, Gma-miRNA26, Gma-miRNA269, and Gma-miRNA28 suppress the gene expression or enzymatic activity of 4CL, IFS, and glucosyltransferase (GT), respectively. The dotted lines indicate the unclear role of miRNA in the pathway (Gupta et al., ; Yu et al., 2000). This isoflavone biosynthetic pathway is adapted from the USDA Database for the Isoflavone Content of Selected Foods Release 2.1 (http://www.ars.usda.gov/nutrientdata). ANS anthocyanidin synthase, AT acetyltransferase, 4CL 4-coumarate:CoA ligase, C4H cinnamic acid 4-hydroxylae, CHI chalcone isomerase, CHR chalcone reductase, CHS chalcone synthase, DFR dihydroflavonol reductase, F3H flavanone 3-hydroxylase, FNS flavone synthase, FLS flavonol synthase, GT glycosyltransferase, 12´H isoflavone hydroxylase, HI4´OMT 2,7,4´-trihydroxyisoflavanone 4´-O-methyltransferase, HID 2-hydroxyisoflavone dehydratase, 2-HIS 2-hydroxyisoflavone synthase, IFH isoflavone hydroxylase, IFS isoflavone synthase, IFR isoflavone reductase, IMT isoflavone malonyl transferase, LAR flavan-3,4-diol reductase, MT malonyltransferase, PAL phenylalanine ammonia lyase, PTS pterocarpan synthase, PTS pterocarpan synthase

Fig. 2

Chemical structures for the major classes of isoflavones and their metabolites. Structures have been drawn using ChemSpider

Fig. 3

Isoflavone transport mechanism dependent on vesicular or multidrug and toxin extrusion (MATE)/ATP-binding cassette (ABC) proteins and the effect of inhibitors. Genistein and daidzein synthesized from l-phenylalanine in the presence of endoplasmic reticulum (ER)-coupled isoflavone biosynthetic enzyme complex in the cytosol are released to apoplasts by ABC. Furthermore, metabolites processed via the isoflavone-7-O-glucosyltransferase (IF7GT) and isoflavone-7-O-glucoside-6′′-O-malonyltransferase (IF7MaT) are transported to vacuoles by MATE proteins. Accumulated metabolites in vacuoles, such as genistin, daidzin, 6′′-O-malonylgenistin, and 6′′-O-malonyldaidzin, are released to apoplasts by ABC transporters and converted to genistein and daidzein in the presence of isoflavone conjugate-hydrolyzing β-glucosidase (ICHG) expressed in the apoplast and cell wall. The biosynthesized genistein and daidzein are involved in defense mechanisms against abiotic and biotic stress in soybean plant cells and exhibit a wide range of biological effects, including normal cell growth development and defense against abiotic and biotic stress, through symbiotic mechanisms within the rhizosphere in the soil. They eventually lead to improved soybean life quality (Ku et al., ; Sugiyama, ; Taneja et al., 2016)

Fig. 4

Inhibitors affecting plasma-membrane transport mechanism (vesicular or multidrug and toxin extrusion [MATE]/ATP-binding cassette [ABC] pathways) of genistein, daidzein, and genistin in soybean plant cells. Inhibitors indicated in bold significantly affect isoflavone contents in both the nutrient medium and the dry mass of seedling plants (Kubes et al., 2019). AC ammonium chloride (NH₄Cl), GR gramicidin, BA brefeldin A, SO sodium orthovanadate (Na₃VO₄), VE verapamil, PR probenecid, GI glibenclamide

Fig. 5

Relationship between isoflavone products and antimicrobial activity. Phenylalanine-derived biosynthetic isoflavone products, including 6″-O-malonylgenistein, glyceollins (I–III), coumestan, isoflavan, and pterocarpan, have antimicrobial and antiherbivore activities (Dixon, ; Olanrewaju et al., ; Singh et al., 2021). CHI chalcone isomerase, CHR chalcone reductase, CHS chalcone synthase, DMID 7,2'-dihydroxy-4'-methoxy-isoflavanol dehydratase, G2´DT glycinol 2-dimethylallyltransferase, G4´DT glycinol 4-dimethylallyltransferase, GLS glyceollin synthase, 2-HIS 2-hydroxyisoflavanone synthase, H4´OMT 2,7,4′-trihydroxyisoflavanone 4′-O-methyltransferase, I2´H isoflavone 2-hydroxylase, IFR isoflavone reductase, IFS isoflavone synthase, VR vestitone reductase