A Post-domestication Mutation, Dt2, Triggers Systemic Modification of Divergent and Convergent Pathways Modulating Multiple Agronomic Traits in Soybean

The semi-determinate stem growth habit in leguminous crops, similar to the "green revolution" semi-dwarf trait in cereals, is a key plant architecture trait that affects several other traits determining grain yield. In soybean semi-determinacy is modulated by a post-domestication gain-of-function mutation in the gene, Dt2, which encodes an MADS-box transcription factor. However, its role in systemic modification of stem growth and other traits is unknown. In this study, we show that Dt2 functions not only as a direct repressor of Dt1, which prevents terminal flowering, but also as a direct activator of putative floral integrator/identity genes including GmSOC1, GmAP1, and GmFUL, which likely promote flowering. We also demonstrate that Dt2 functions as a direct repressor of the putative drought-responsive transcription factor gene GmDREB1D, and as a direct activator of GmSPCH and GmGRP7, which are potentially associated with asymmetric division of young epidermal cells and stomatal opening, respectively, and may affect the plant's water-use efficiency (WUE). Intriguingly, Dt2 was found to be a direct activator or repressor of the precursors of eight microRNAs targeting genes potentially associated with meristem maintenance, flowering time, stomatal density, WUE, and/or stress responses. This study thus reveals the molecular basis of pleiotropy associated with plant productivity, adaptability, and environmental resilience.