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Drought, bringing the risks of agricultural production losses, is becoming a globally environmental stress. Previous results suggested that legumes with nodules exhibited superior drought tolerance compared with the non-nodule group. To investigate the molecular mechanism of rhizobium symbiosis impacting drought tolerance, transcriptome and sRNAome sequencing were performed to identify the potential mRNA–miRNA–ncRNA dynamic network. Our results revealed that seedlings with active nodules exhibited enhanced drought tolerance by reserving energy, synthesizing N-glycans, and medicating systemic acquired resistance due to the early effects of symbiotic nitrogen fixation (SNF) triggered in contrast to the drought susceptible with inactive nodules. The improved drought tolerance might be involved in the decreased expression levels of miRNA such as mtr_miR169l-5p, mtr_miR398b, and mtr_miR398c and its target genes in seedlings with active nodules. Based on the negative expression pattern between miRNA and its target genes, we constructed an mRNA–miR169l–ncRNA ceRNA network. During severe drought stress, the lncRNA alternative splicings TCONS_00049507 and TCONS_00049510 competitively interacted with mtr_miR169l-5p, which upregulated the expression of NUCLEAR FACTOR-Y (NF-Y) transcription factor subfamily NF-YA genes MtNF-YA2 and MtNF-YA3 to regulate their downstream drought-response genes. Our results emphasized the importance of SNF plants affecting drought tolerance. In conclusion, our work provides insight into ceRNA involvement in rhizobium symbiosis contributing to drought tolerance and provides molecular evidence for future study.

Phosphorus is one of the essential macronutrients required by plant growth and development, but phosphate resources are finite and diminishing rapidly because of the huge need in global agriculture. In this study, 11 genes were found in the Phosphate Transporter 1 (PHT1) family of Medicago truncatula. Seven genes of the PHT1 family were available by qRT-PCR. Most of them were expressed in roots, and almost all genes were induced by low-phosphate stress in the nodule. The expression of MtPT6 was relatively high in nodules and induced by low-phosphate stress. The fusion expression of MtPT6 promoter-GUS gene in M. truncatula suggested that the expression of MtPT6 was induced in roots and nodules by phosphate starvation. In roots, MtPT6 was mainly expressed in vascular tissue and tips, and it was also expressed in cortex under low-phosphate stress; in nodules, it was mainly expressed in vascular bundles, cortical cells, and fixation zone cells. MtPT6 had a close relationship with other PHT1 family members according to amino acid alignment and phylogenetic analysis. Subcellular localization analysis in tobacco revealed that MtPT6 protein was localized to the plasma membrane. The heterologous expression of MtPT6 in Arabidopsis knockout mutants of pht1.1 and pht1.4 made seedlings more susceptible to arsenate treatment, and the phosphate concentrations in pht1.1 were higher in high phosphate condition by expressing MtPT6. We conclude that MtPT6 is a typical phosphate transporter gene and can promote phosphate acquisition efficiency of plants.