Shoot‐to‐root communication via GmUVR8‐GmSTF3 photosignaling and flavonoid biosynthesis fine‐tunes soybean nodulation under UV‐B light

Abstract

Summary Legume nodulation requires light perception by plant shoots and precise long‐distance communication between shoot and root. Recent studies have revealed that TGACG‐motif binding factors (GmSTFs) integrate light signals to promote root nodulation; however, the regulatory mechanisms underlying nodule formation in changing light conditions remain elusive. Here, we applied genetic engineering, metabolite measurement, and transcriptional analysis to study soybean (Glycine max) nodules. We clarify a fine‐tuning mechanism in response to ultraviolet B (UV‐B) irradiation and rhizobia infection, involving GmUVR8‐dependent UV‐B perception and GmSTF3/4‐GmMYB12‐GmCHS‐mediated (iso)flavonoid biosynthesis for soybean nodule formation. GmUVR8 receptor‐perceived UV‐B signal triggered R2R3‐MYB transcription factors GmMYB12‐dependent flavonoid biosynthesis separately in shoot and root. In shoot, UV‐B‐triggered flavonoid biosynthesis relied on GmUVR8a, b, c receptor‐dependent activation of GmMYB12L‐GmCHS8 (chalcone synthase) module. In root, UV‐B signaling distinctly promotes the accumulation of the isoflavones, daidzein, and its derivative coumestrol, via GmMYB12B2‐GmCHS9 module, resulting in hypernodulation. The mobile transcription factors, GmSTF3/4, bind to cis‐regulatory elements in the GmMYB12L, GmMYB12B2, and GmCHS9 promoters, to coordinate UV‐B light perception in shoot and (iso)flavonoid biosynthesis in root. Our findings establish a novel shoot‐to‐root communication module involved in soybean nodulation and reveal an adaptive strategy employed by soybean roots in response to UV‐B light.