Mobile gene clusters and coexpressed plant-rhizobium pathways drive partner quality variation in symbiosis

• 成果类型: Article
• 署名作者: Riaz, Muhammad Rizwan; Marquez, Ivan Sosa; Lindgren, Hanna; Levin, Garrett; Doyle, Rebecca; Romero, Mario Ceron; Paoli, Julia C.; Drnevich, Jenny; Fields, Christopher J.; Geddes, Barney A.; Marshall-Colon, Amy; Heath, Katy D.
• 署名单位: University of Illinois System; University of Illinois Urbana-Champaign; University of Illinois System; University of Illinois Urbana-Champaign; University of Illinois System; University of Illinois Urbana-Champaign; North Dakota State University Fargo; McMaster University; University of Illinois System; University of Illinois Urbana-Champaign
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-14996
• DOI: 10.1073/pnas.2411831122
• 发表日期: 2025-07-29
• 关键词: root-nodules; legume; genome; expression; EVOLUTION; host; SANCTIONS; specificity; COOPERATION; metabolism

摘要

Plant-microbe symbioses such as the legume-rhizobium mutualism are vital in the web of ecological relationships within both natural and managed ecosystems, influencing primary productivity, crop yield, and ecosystem services. The outcome of these interactions for plant hosts varies quantitatively and can range from highly beneficial to even detrimental depending on natural genetic variation in microbial symbionts. Here, we take a systems genetics approach, harnessing the genetic diversity present in wild rhizobial populations to predict genes and molecular pathways crucial in determining partner quality, i.e., the benefits of symbiosis for legume hosts. We combine traits, dual-RNAseq of both partners from active nodules, pangenomics/pantranscriptomics, and Weighted Gene Co-expression Network Analysis (WGCNA) for a panel of 20 Sinorhizobium meliloti strains that vary in symbiotic partner quality. We find that genetic variation in the nodule transcriptome predicts host plant biomass, and WGCNA reveals networks of genes in plants and rhizobia that are coexpressed and associated with high-quality symbiosis. Presence-absence variation of gene clusters on the symbiosis plasmid (pSymA), validated in planta, is associated with high or low-quality symbiosis and is found within important coexpression modules. Functionally our results point to management of oxidative stress, amino acid and carbohydrate transport, and NCR peptide signaling mechanisms in driving symbiotic outcomes. Our integrative approach highlights the complex genetic architecture of microbial partner quality and raises hypotheses about the genetic mechanisms and evolutionary dynamics of symbiosis.