Differential symbiotic compatibilities between rhizobium strains and cultivated and wild soybeans revealed by anatomical and transcriptome analyses

Authors: BAHRAMI ZADEGAN, SOBHAN - University Of Tennessee; KIM, WONSEOK - University Of Missouri; ABBAS, HAFIZ MUHAMMAD - University Of Tennessee; KIM, SUNHYUNG - University Of Missouri; Krishnan, Hari; HEWEZI, TAREK - University Of Tennessee

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/9/2024
Publication Date: 9/3/2024
Citation: Bahrami Zadegan, S., Kim, W., Abbas, H.K., Kim, S., Krishnan, H.B., Hewezi, T. 2024. Differential symbiotic compatibilities between rhizobium strains and cultivated and wild soybeans revealed by anatomical and transcriptome analyses. Frontiers in Plant Science. 15. https://doi.org/10.3389/fpls.2024.1435632.
DOI: https://doi.org/10.3389/fpls.2024.1435632

Interpretive Summary: Soybean plants have the unique ability to form nodules on the roots by 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. However, the formation of nodules is highly influenced by different strains of rhizobia. Only certain strains of rhizobia can form functional nitrogen-fixing nodules, while other strains will elicit non-functional nodules. Despite the differential compatibility between rhizobium strains and soybeans, host transcriptome responses that determine the outcome of the symbiotic interactions leading to the formation of functional or non-functional nodules remain poorly understood. In this study, we have examined the anatomical features and changes in gene expression in functional and non-functional soybean nodules. Our study has identified genes associated with cell wall biogenesis and organization and defense responses together with downregulation of genes involved in the biosynthesis of isoprenoids and antioxidant stress are associated with the formation of non-functional soybean root nodules. Information obtained from this study will help scientists to better understand the factors that limit the formation of nitrogen-fixing functional nodules on soybean. Such an understanding should enable scientists to manipulate biological nitrogen fixation so that US farmers can increase yields without the use of nitrogen fertilizers.

Technical Abstract: Various species of rhizobium establish compatible symbiotic relationships with soybean (Glycinemax) leading to the formation of nitrogen-fixing nodules in roots. The formation of functional nodules is mediated through complex developmental and transcriptional reprogramming that involves the activity of thousands of plant genes. However, host transcriptome that differentiate between functional or nonfunctional nodules remain largely unexplored. In this study, we investigated differential compatibilities between rhizobium strains (Bradyrhizobium diazoefficiens USDA110 Bradyrhizobium sp. strain LVM105) and cultivated and wild soybeans. The nodulation assays revealed that both USDA110 and LVM105 strains effectively nodulate G. soja but only USDA110 can form symbiotic relationships with Williams 82. LVM105 formed pseudonodules on Williams 82 that consist of a central nodule-like mass that are devoid of any rhizobia. RNA-seq data revealed that USDA110 and LVM105 induce distinct transcriptome programing in functional mature nodules formed on G. soja roots, where genes involved in nucleosome assembly, DNA replication, regulation of cell cycle, and defense responses play key roles. Transcriptome comparison also suggested that activation of genes associated with cell wall biogenesis and organization and defense responses together with downregulation of genes involved in the biosynthesis of isoprenoids and antioxidant stress are associated with the formation of non-functional nodules on Williams 82 roots. Moreover, our analysis implies that increased activity of genes involved in oxygen binding, amino acid transport, and nitrate transport differentiates between fully-developed nodules in cultivated versus wild soybeans.