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Abstract Microorganisms associated with plants can affect nutrient and water acquisition, plant defenses, and ecological interactions, with effects on plant growth that range from beneficial to antagonistic. In Glycine max (soybean), many studies have examined the soil microbiome and the legume–rhizobium relationship, but little is known about foliar endophytes, their effects on plant biomass and fitness, and how plants respond to their presence. To address these questions, we inoculated Glycine max with field-collected isolates of previously isolated, dominant strains of Methylobacterium and Colletotrichum in either sterile or non-sterile soil. We then used RNAseq to compare the transcriptomic responses of plants to single- and co-inoculation of endophytes. We found that all endophyte treatments increased soybean growth compared to control, but only in sterile soil. These results suggest context-dependency, with endophytes serving as facultative mutualists under stress or nutrient deprivation. Similarly, transcriptomic analyses revealed that soybean defense and stress responses depended on the interaction of endophytes; Methylobacterium elicited the strongest response but was modulated by the presence of Colletotrichum. Our findings highlight the environmentally dependent effects of co-existing endophytes within soybean leaves. 

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 20Sinorhizobium melilotistrains 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. 

PremiseNutrients, light, water, and temperature are key factors limiting the growth of individual plants in nature. Mutualistic interactions between plants and microbes often mediate resource limitation for both partners. In the mutualism between legumes and rhizobia, plants provide rhizobia with carbon in exchange for fixed nitrogen. Because partner quality in mutualisms is genotype‐dependent, within‐species genetic variation is expected to alter the responses of mutualists to changes in the resource environment. Here we ask whether partner quality variation in rhizobia mediates the response of host plants to changing light availability, and conversely, whether light alters the expression of partner quality variation. MethodsWe inoculated clover hosts with 11 strains ofRhizobium leguminosarumthat differed in partner quality, grew plants under either ambient or low light conditions in the greenhouse, and measured plant growth, nodule traits, and foliar nutrient composition. ResultsLight availability and rhizobium inoculum interactively determined plant growth, and variation in rhizobium partner quality was more apparent in ambient light. ConclusionsOur results suggest that variation in the costs and benefits of rhizobium symbionts mediate host responses to light availability and that rhizobium strain variation might more important in higher‐light environments. Our work adds to a growing appreciation for the role of microbial intraspecific and interspecific diversity in mediating extended phenotypes in their hosts and suggests an important role for light availability in the ecology and evolution of legume–rhizobium symbiosis.