Soybean gene co-expression network analysis identifies two co-regulated gene modules associated with nodule formation and development

Authors: PIYA, SARBOTTAM - University Of Tennessee; PANTALONE, VINCE - University Of Tennessee; ZADEGAN, SOBHAN - University Of Tennessee; SHIPP, SARAH - Southern Illinois University; LAKHSSASSI, NAOUFAL - Southern Illinois University; KNIZIA, DOUNYA - Southern Illinois University; Krishnan, Hari; MEKSEM, KHALID - Southern Illinois State University; HEWEZI, TAREK - University Of Tennessee

Submitted to: Molecular Plant Pathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/6/2023
Publication Date: 6/1/2023
Citation: Piya, S., Pantalone, V., Zadegan, S.B., Shipp, S., Lakhssassi, N., Knizia, D., Krishnan, H.B., Meksem, K., Hewezi, T. 2023. Soybean gene co-expression network analysis identifies two co-regulated gene modules associated with nodule formation and development. Molecular Plant Pathology. 24(6):628-636. https://doi.org/10.1111/mpp.13327.
DOI: https://doi.org/10.1111/mpp.13327

Interpretive Summary: Soybean plants have the unique ability to form nodules on the roots by symbiotically interacting with soil bacteria collectively known as rhizobia. Nodules are a specialized plant organ where atmospheric nitrogen is reduced to ammonia which can be utilized by soybean plants for its growth and development. This process is termed as biological nitrogen fixation. Due to this process, application of nitrogen fertilizer is not required for soybean fields. Nodule formation is a complex genetic process and involves changes in the expression of significant number of plant genes. In this study, we conducted gene co-expression network analysis to identify clusters of functionally related genes. We have identified two nodule-specific modules and have established the involvement of unsaturated fatty acid biosynthesis and folate metabolism in nodule formation and development. Information obtained from this study will help scientists to better understand the factors that limit the formation of nitrogen-fixing nodules on soybean. Such an understanding should enable scientists to manipulate biological nitrogen fixation so that US farmers can increase yields with minimal use of nitrogen fertilizers.

Technical Abstract: Gene co-expression network analysis is an efficient systems biology approach for the discovery of novel gene functions and trait-associated gene modules. To identify clusters of functionally related genes involved in soybean nodule formation and development, we performed a weighted gene co-expression network analysis. Two nodule-specific modules (NSM-1 and NSM-2, containing 304 and 203 genes, respectively) were identified. The NSM-1 gene promoters were significantly enriched in cis-binding elements for ERF, MYB, and C2H2-type zinc transcription factors, whereas NSM-2 gene promoters were enriched in cis-binding elements for TCP, bZIP, and bHLH transcription factors, suggesting a role of these regulatory factors in the transcriptional activation of nodule co-expressed genes. The co-expressed gene modules included genes with potential novel roles in nodulation, including those involved in xylem development, transmembrane transport, the ethylene signalling pathway, cytoskeleton organization, cytokinesis and regulation of the cell cycle, regulation of meristem initiation and growth, transcriptional regulation, DNA methylation, and histone modifications. Functional analysis of two co-expressed genes using TILLING mutants provided novel insight into the involvement of unsaturated fatty acid biosynthesis and folate metabolism in nodule formation and development. The identified gene co-expression modules provide valuable resources for further functional genomics studies to dissect the genetic basis of nodule formation and development in soybean.