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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.
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MGEs as the MVPs of Partner Quality Variation in Legume-Rhizobium Symbiosis
ABSTRACT Despite decades of research, we are only just beginning to understand the forces maintaining variation in the nitrogen-fixing symbiosis between rhizobial bacteria and leguminous plants. In their recent work, Alexandra Weisberg and colleagues use genomics to document the breadth of mobile element diversity that carries the symbiosis genes of Bradyrhizobium in natural populations. Studying rhizobia from the perspective of their mobile genetic elements, which have their own transmission modes and fitness interests, reveals novel mechanisms for the generation and maintenance of diversity in natural populations of these ecologically and economically important mutualisms.
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- Award ID(s):
- 2022049
- PAR ID:
- 10414712
- Date Published:
- Journal Name:
- mBio
- Volume:
- 13
- Issue:
- 4
- ISSN:
- 2150-7511
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1128/mbio.00888-22
