A Comprehensive Transcriptome Atlas Reveals the Crucial Role of LncRNAs in Maintaining Nodulation Homeostasis in Soybean

Symbiotic nitrogen fixation (SNF) provides nitrogen for soybean. A primary challenge in enhancing yield through efficient SNF lies in striking a balance between its high energy consumption and plant growth. However, the systemic transcriptional reprogramming during nodulation remains limited. Here, this work conducts a comprehensive RNA-seq of the roots, cotyledons and leaves of inoculated-soybean. This work finds 88,814 mRNAs and 6,156 noncoding RNAs (ncRNAs) across various organs. Notably, this work identifies 6,679 nodulation-regulated mRNAs (NR-mRNAs), 1,681 long noncoding RNAs (lncRNAs) (NR-lncRNAs), and 59 miRNAs (NR-miRNAs). The majority of these NR-RNAs are associated with plant-microbial interaction and exhibit high organ specificity. Roots display the highest abundance of NR-ncRNAs and the most dynamic crosstalk between NR-lncRNAs and NR-miRNAs in a GmNARK-dependent manner. This indicates that while each tissue responds uniquely, GmNARK serves as a primary regulator of the transcriptional control of nodulated-plants. Furthermore, this work proves that lnc-NNR6788 and lnc-NNR7059 promote nodulation by regulating their target genes. This work also shows that the nodulation- and GmNARK-regulated (NNR) lnc-NNR4481 negatively regulates nodulation through miR172c within a competing endogenous RNA (ceRNA) network. The spatial organ-type transcriptomic atlas establishes a benchmark and provides a valuable resource for integrative analyses of the mechanism underlying of nodulation and plant growth balance.