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

## TL;DR

This study maps RNA activity in soybean during nitrogen fixation, showing how long noncoding RNAs help control the balance between plant growth and nodulation.

## Contribution

The work provides a comprehensive transcriptome atlas and identifies specific lncRNAs that regulate nodulation through ceRNA networks.

## Key findings

- Roots show the highest abundance of nodulation-regulated ncRNAs and dynamic lncRNA-miRNA interactions.
- lnc-NNR6788 and lnc-NNR7059 promote nodulation by regulating target genes.
- lnc-NNR4481 inhibits nodulation via miR172c in a ceRNA network.

## Abstract

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.

Symbiotic nitrogen fixation promotes soybean growth, but maintaining energy balance is challenging. RNA‐seq of three organs of inoculated soybean identifies 88,814 mRNAs and 6,156 ncRNAs. Roots exhibit the most NR‐ncRNAs and dynamic crosstalk controlled by GmNARK. Lnc‐NNR6788 and lnc‐NNR7059 boost nodulation, whereas lnc‐NNR4481 inhibits it in a ceRNA network. This atlas facilitates the understanding of balancing nodulation and growth.