Modeling the Flowering Activation Motif during Vernalization in Legumes: A Case Study of M. trancatula

In many plant species, flowering is promoted by the cold treatment or vernalization. The mechanism of vernalization-induced flowering has been extensively studied in Arabidopsis but remains largely unknown in legumes. The orthologs of the FLC gene, a major regulator of vernalization response in Arabidopsis, are absent or non-functional in the vernalization-sensitive legume species. Nevertheless, the legume integrator genes FT and SOC1 are involved in the transition of the vernalization signal to meristem identity genes, including PIM (AP1 ortholog). However, the regulatory contribution of these genes to PIM activation in legumes remains elusive. Here, we presented the theoretical and data-driven analyses of a feed-forward regulatory motif that includes a vernalization-responsive FT gene and several SOC1 genes, which independently activate PIM and thereby mediate floral transition. Our theoretical model showed that the multiple regulatory branches in this regulatory motif facilitated the elimination of no-sense signals and amplified useful signals from the upstream regulator. We further developed and analyzed four data-driven models of PIM activation in Medicago trancatula in vernalized and non-vernalized conditions in wild-type and fta1-1 mutants. The model with FTa1 providing both direct activation and indirect activation via three intermediate activators, SOC1a, SOC1b, and SOC1c, resulted in the most relevant PIM dynamics. In this model, the difference between regulatory inputs of SOC1 genes was nonessential. As a result, in the M. trancatula model, the cumulative action of SOC1a, SOC1b, and SOC1c was favored. Overall, in this study, we first presented the in silico analysis of vernalization-induced flowering in legumes. The considered vernalization network motif can be supplemented with additional regulatory branches as new experimental data become available.