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. This work demonstrates molecular links underlying key pleiotropic agronomic traits associated with soybean yield potential, adaptability, and environmental resilience such as drought tolerance, which are reshaped by spatiotemporal expression of a gene with a gain-of-function mutation, Dt2, which occurred after the domestication of soybeans.