Riaz Muhammad Rizwan, Sosa Marquez Ivan, Lindgren Hanna, Levin Garrett, Doyle Rebecca, Romero Mario Cerón, Paoli Julia C, Drnevich Jenny, Fields Christopher J, Geddes Barney A, Marshall-Colón Amy, Heath Katy D
Department of Plant Biology, University of Illinois Urbana-Champaign, Urbana, IL 61801.
Department of Microbiology, University of Illinois Urbana-Champaign, Urbana, IL 61801.
Proc Natl Acad Sci U S A. 2025 Aug 5;122(31):e2411831122. doi: 10.1073/pnas.2411831122. Epub 2025 Jul 29.
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 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.
植物与微生物的共生关系，如豆科植物与根瘤菌的互利共生，在自然和人工管理的生态系统中的生态关系网络中至关重要，影响着初级生产力、作物产量和生态系统服务。这些植物宿主相互作用的结果在数量上各不相同，根据微生物共生体的自然遗传变异，其范围可以从高度有益到甚至有害。在这里，我们采用系统遗传学方法，利用野生根瘤菌种群中存在的遗传多样性来预测对确定伙伴质量至关重要的基因和分子途径，即共生对豆科植物宿主的益处。我们结合了性状、来自活跃根瘤中双方的双RNA测序、泛基因组学/泛转录组学以及加权基因共表达网络分析（WGCNA），用于一组共生伙伴质量不同的20个菌株。我们发现根瘤转录组中的遗传变异可预测宿主植物生物量，WGCNA揭示了植物和根瘤菌中共同表达且与高质量共生相关的基因网络。共生质粒（pSymA）上基因簇的有无变异在植物体内得到验证，与高质量或低质量共生相关，且存在于重要的共表达模块中。从功能上讲，我们的结果表明氧化应激管理、氨基酸和碳水化合物运输以及NCR肽信号传导机制在驱动共生结果方面发挥作用。我们的综合方法突出了微生物伙伴质量的复杂遗传结构，并提出了关于共生遗传机制和进化动态的假设。
