The Gma-miR4359b/GmFBX193 module is involved in the response of soybean to salt stress

MicroRNAs (miRNAs) are key regulators of F-box-mediated signal transduction in plants and play important roles in the stress response. The ways in which miRNAs target F-box genes in soybeans under salt stress are currently unknown. In this study, the functional role of GmFBX193, the gene target of gma-miR4359b, under salt stress was investigated. The length, surface area ratio, survival rate, proline content, superoxide dismutase (SOD) activity and peroxidase (POD) activity of soybean hairy roots with inhibited GmFBX193 expression were greater than those of the K599 reference root samples. In contrast, the root length, seed germination rate, number of green cotyledons, chlorophyll content, catalase activity, SOD activity and POD activity of transgenic Arabidopsis plants overexpressing GmFBX193 were lower than those of wild-type (WT) Arabidopsis plants. Under salt stress, compared with WT Arabidopsis control plants, GmFBX193 transgenic Arabidopsis plants presented 239 differentially expressed genes, including several known salt stress-related genes. Dual-luciferase assays and cotransformation of soybean hairy roots revealed that gma-miR4359b participates in salt tolerance regulation by cleaving GmFBX193. Yeast two-hybrid, bimolecular fluorescence complementation and coimmunoprecipitation assays revealed that the GmFBX193 protein interacted with two proteins, GmSK12 and GmSK15, which are encoded by soybean SKP1 family genes. In summary, gma-miR4359b can target the gene expression of GmFBX193 and respond to salt stress. The inhibition of GmFBX193 can improve the salt tolerance of plants.