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Isoflavones play important roles in rhizosphere plant-microbe interactions. Daidzein and genistein secreted by soybean roots induce the symbiotic interaction with rhizobia and may modulate rhizosphere interactions with microbes. Yet despite their important roles, little is known about the biosynthesis, secretion and fate of isoflavones in field-grown soybeans. Here, we analyzed isoflavone contents and the expression of isoflavone biosynthesis genes in field-grown soybeans. In roots, isoflavone contents and composition did not change with crop growth, but the expression of UGT4, an isoflavone-specific 7-O-glucosyltransferase, and of ICHG (isoflavone conjugates hydrolyzing beta-glucosidase) was decreased during the reproductive stages. Isoflavone contents were higher in rhizosphere soil than in bulk soil during both vegetative and reproductive stages, and were comparable in the rhizosphere soil between these two stages. We analyzed the degradation dynamics of daidzein and its glucosides to develop a model for predicting rhizosphere isoflavone contents from the amount of isoflavones secreted in hydroponic culture. Conjugates of daidzein were degraded much faster than daidzein, with degradation rate constants of 8.51 d-1 for malonyldaidzin and 11.6 d-1 for daidzin, vs. 9.15 × 10-2 d-1 for daidzein. The model suggested that secretion of isoflavones into the rhizosphere is higher during vegetative stages than during reproductive stages in field-grown soybean., (© The Author 2017. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oup.com.)

Isoflavones play important roles in plant-microbe interactions in rhizospheres. Soybean roots secrete daidzein and genistein to attract rhizobia. Despite the importance of isoflavones in plant-microbe interactions, little is known about the developmental and nutritional regulation of isoflavone secretion from soybean roots. In this study, soybeans were grown in hydroponic culture, and isoflavone contents in tissues, isoflavone secretion from the roots, and the expression of isoflavone conjugates hydrolyzing beta-glucosidase (ICHG) were investigated. Isoflavone contents did not show strong growth-dependent changes, while secretion of daidzein from the roots dramatically changed, with higher secretion during vegetative stages. Coordinately, the expression of ICHG also peaked at vegetative stages. Nitrogen deficiency resulted in 8- and 15-fold increases in secretion of daidzein and genistein, respectively, with no induction of ICHG. Taken together, these results suggest that large amounts of isoflavones were secreted during vegetative stages via the hydrolysis of (malonyl)glucosides with ICHG.

Plant specialized metabolites (PSMs) are often stored as glycosides within cells and released from the roots with some chemical modifications. While isoflavones are known to function as symbiotic signals with rhizobia and to modulate the soybean rhizosphere microbiome, the underlying mechanisms of root-to-soil delivery are poorly understood. In addition to transporter-mediated secretion, the hydrolysis of isoflavone glycosides in the apoplast by an isoflavone conjugate–hydrolyzing β-glucosidase (ICHG) has been proposed but not yet verified. To clarify the role of ICHG in isoflavone supply to the rhizosphere, we have isolated two independent mutants defective in ICHG activity from a soybean high-density mutant library. In the root apoplastic fraction of ichg mutants, the isoflavone glycoside contents were significantly increased, while isoflavone aglycone contents were decreased, indicating that ICHG hydrolyzes isoflavone glycosides into aglycones in the root apoplast. When grown in a field, the lack of ICHG activity considerably reduced isoflavone aglycone contents in roots and the rhizosphere soil, although the transcriptomes showed no distinct differences between the ichg mutants and wild-types (WTs). Despite the change in isoflavone contents and composition of the root and rhizosphere of the mutants, root and rhizosphere bacterial communities were not distinctive from those of the WTs. Root bacterial communities and nodulation capacities of the ichg mutants did not differ from the WTs under nitrogen-deficient conditions either. Taken together, these results indicate that ICHG elevates the accumulation of isoflavones in the soybean rhizosphere but is not essential for isoflavone-mediated plant–microbe interactions. [ABSTRACT FROM AUTHOR]