Differential light-dependent regulation of soybean nodulation by papilionoid-specific HY5 homologs

Legumes have evolved photosynthesis and symbiotic nitrogen fixation for the acquisition of energy and nitrogen nutrients. During the transition from heterotrophic to autotrophic growth, blue light primarily triggers photosynthesis and low soil nitrogen induces symbiotic nodulation. Whether and how darkness and blue light influence root symbiotic nodulation during this transition is unknown. Here, we show that short-term darkness promotes nodulation and that blue light inhibits nodulation through two soybean TGACG-motif-binding factors (STF1 and STF2), which are Papilionoideae-specific transcription factors and divergent orthologs of Arabidopsis ELONGATED HYPOCOTYL 5 (HY5). STF1 and STF2 negatively regulate soybean nodulation by repressing the transcription of nodule inception a (GmNINa), which is a central regulator of nodulation, in response to darkness and blue light. STF1 and STF2 are not capable of moving from the shoots to roots, and they act both locally and systemically to mediate darkness- and blue-light-regulated nodulation. We further show that cryptochromes GmCRY1s are required for nodulation in the dark and partially contribute to the blue light inhibition of nodulation. In addition, root GmCRY1s mediate blue-light-induced transcription of STF1 and STF2, and intriguingly, GmCRY1b can interact with STF1 and STF2 to stabilize the protein stability of STF1 and STF2. Our results establish that the blue light receptor GmCRY1s-STF1/2 module plays a pivotal role in integrating darkness/blue light and nodulation signals. Furthermore, our findings reveal a molecular basis by which photosensory pathways modulate nodulation and autotrophic growth through an intricate interplay facilitating seedling establishment in response to low nitrogen and light signals.