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1. Interspecific conflict and the evolution of ineffective rhizobia

   https://doi.org/10.1111/ele.13247  

   Gano‐Cohen, Kelsey A. ; Wendlandt, Camille E. ; Stokes, Peter J. ; Blanton, Mia A. ; Quides, Kenjiro W. ; Zomorrodian, Avissa ; Adinata, Eunice S. ; Sachs, Joel L. ; Johnson, ed., Nancy ( March 2019 , Ecology Letters)

   Microbial symbionts exhibit broad genotypic variation in their fitness effects on hosts, leaving hosts vulnerable to costly partnerships. Interspecific conflict and partner‐maladaptation are frameworks to explain this variation, with different implications for mutualism stability. We investigated the mutualist service of nitrogen fixation in a metapopulation of root‐nodule formingBradyrhizobiumsymbionts inAcmisponhosts. We uncoveredBradyrhizobiumgenotypes that provide negligible mutualist services to hosts and had superiorin plantafitness during clonal infections, consistent with cheater strains that destabilise mutualisms. Interspecific conflict was also confirmed at the metapopulation level – by a significant negative association between the fitness benefits provided byBradyrhizobiumgenotypes and their local genotype frequencies – indicating that selection favours cheating rhizobia. Legumes have mechanisms to defend against rhizobia that fail to fix sufficient nitrogen, but these data support predictions that rhizobia can subvert plant defenses and evolve to exploit hosts.
2. Host-Associated Rhizobial Fitness: Dependence on Nitrogen, Density, Community Complexity, and Legume Genotype

   https://doi.org/10.1128/aem.00526-22  

   Burghardt, Liana T. ; Epstein, Brendan ; Hoge, Michelle ; Trujillo, Diana I. ; Tiffin, Peter ( August 2022 , Applied and Environmental Microbiology)

   Glass, Jennifer B. (Ed.)

   ABSTRACT The environmental context of the nitrogen-fixing mutualism between leguminous plants and rhizobial bacteria varies over space and time. Variation in resource availability, population density, and composition likely affect the ecology and evolution of rhizobia and their symbiotic interactions with hosts. We examined how host genotype, nitrogen addition, rhizobial density, and community complexity affected selection on 68 rhizobial strains in the Sinorhizobium meliloti – Medicago truncatula mutualism. As expected, host genotype had a substantial effect on the size, number, and strain composition of root nodules (the symbiotic organ). The understudied environmental variable of rhizobial density had a stronger effect on nodule strain frequency than the addition of low nitrogen levels. Higher inoculum density resulted in a nodule community that was less diverse and more beneficial but only in the context of the more selective host genotype. Higher density resulted in more diverse and less beneficial nodule communities with the less selective host. Density effects on strain composition deserve additional scrutiny as they can create feedback between ecological and evolutionary processes. Finally, we found that relative strain rankings were stable across increasing community complexity (2, 3, 8, or 68 strains). This unexpected result suggests that higher-order interactions between strains are raremore »in the context of nodule formation and development. Our work highlights the importance of examining mechanisms of density-dependent strain fitness and developing theoretical predictions that incorporate density dependence. Furthermore, our results have translational relevance for overcoming establishment barriers in bioinoculants and motivating breeding programs that maintain beneficial plant-microbe interactions across diverse agroecological contexts. IMPORTANCE Legume crops establish beneficial associations with rhizobial bacteria that perform biological nitrogen fixation, providing nitrogen to plants without the economic and greenhouse gas emission costs of chemical nitrogen inputs. Here, we examine the influence of three environmental factors that vary in agricultural fields on strain relative fitness in nodules. In addition to manipulating nitrogen, we also use two biotic variables that have rarely been examined: the rhizobial community's density and complexity. Taken together, our results suggest that (i) breeding legume varieties that select beneficial strains despite environmental variation is possible, (ii) changes in rhizobial population densities that occur routinely in agricultural fields could drive evolutionary changes in rhizobial populations, and (iii) the lack of higher-order interactions between strains will allow the high-throughput assessments of rhizobia winners and losers during plant interactions.« less
3. Experimental evolution can enhance benefits of rhizobia to novel legume hosts

   https://doi.org/10.1098/rspb.2021.0812  

   Quides, Kenjiro W. ; Weisberg, Alexandra J. ; Trinh, Jerry ; Salaheldine, Fathi ; Cardenas, Paola ; Lee, Hsu-Han ; Jariwala, Ruchi ; Chang, Jeff H. ; Sachs, Joel L. ( May 2021 , Proceedings of the Royal Society B: Biological Sciences)

   null (Ed.)

   Legumes preferentially associate with and reward beneficial rhizobia in root nodules, but the processes by which rhizobia evolve to provide benefits to novel hosts remain poorly understood. Using cycles of in planta and in vitro evolution, we experimentally simulated lifestyles where rhizobia repeatedly interact with novel plant genotypes with which they initially provide negligible benefits. Using a full-factorial replicated design, we independently evolved two rhizobia strains in associations with each of two Lotus japonicus genotypes that vary in regulation of nodule formation. We evaluated phenotypic evolution of rhizobia by quantifying fitness, growth effects and histological features on hosts, and molecular evolution via genome resequencing. Rhizobia evolved enhanced host benefits and caused changes in nodule development in one of the four host–symbiont combinations, that appeared to be driven by reduced costs during symbiosis, rather than increased nitrogen fixation. Descendant populations included genetic changes that could alter rhizobial infection or proliferation in host tissues, but lack of evidence for fixation of these mutations weakens the results. Evolution of enhanced rhizobial benefits occurred only in a subset of experiments, suggesting a role for host–symbiont genotype interactions in mediating the evolution of enhanced benefits from symbionts.
4. Autopolyploidy alters nodule‐level interactions in the legume – rhizobium mutualism

   https://doi.org/10.1002/ajb2.1375  

   Forrester, Nicole J. ; Ashman, Tia‐Lynn ( November 2019 , American Journal of Botany)

   Polyploidy is a major genetic driver of ecological and evolutionary processes in plants, yet its effects on plant interactions with mutualistic microbes remain unresolved. The legume–rhizobium symbiosis regulates global nutrient cycles and plays a role in the diversification of legume species. In this mutualism, rhizobia bacteria fix nitrogen in exchange for carbon provided by legume hosts. This exchange occurs inside root nodules, which house bacterial cells and represent the interface of legume–rhizobium interactions. Although polyploidy may directly impact the legume–rhizobium mutualism, no studies have explored how it alters the internal structure of nodules.

   We created synthetic autotetraploids usingMedicago sativasubsp.caerulea. Neotetraploid plants and their diploid progenitors were singly inoculated with two strains of rhizobia,Sinorhizobium melilotiandS. medicae. Confocal microscopy was used to quantify internal traits of nodules produced by diploid and neotetraploid plants.

   Autotetraploid plants produced larger nodules with larger nitrogen fixation zones than diploids for both strains of rhizobia, although the significance of these differences was limited by power. NeotetraploidM. sativasubsp.caeruleaplants also produced symbiosomes that were significantly larger, nearly twice the size, than those present in diploids.

   This study sheds light on how polyploidy directly affects a plant–bacterium mutualism and uncovers novel mechanisms. Changes in plant–microbe interactions that directly result frommore »polyploidy likely contribute to the increased ability of polyploid legumes to establish in diverse environments.

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5. Sinorhizobium medicae WSM419 Genes That Improve Symbiosis between Sinorhizobium meliloti Rm1021 and Medicago truncatula Jemalong A17 and in Other Symbiosis Systems

   https://doi.org/10.1128/AEM.03004-20  

   Ghosh, Prithwi ; Adolphsen, Katie N. ; Yurgel, Svetlana N. ; Kahn, Michael L. ( July 2021 , Applied and Environmental Microbiology)

   Stabb, Eric V. (Ed.)

   ABSTRACT Some soil bacteria, called rhizobia, can interact symbiotically with legumes, in which they form nodules on the plant roots, where they can reduce atmospheric dinitrogen to ammonia, a form of nitrogen that can be used by growing plants. Rhizobium-plant combinations can differ in how successful this symbiosis is: for example, Sinorhizobium meliloti Rm1021 forms a relatively ineffective symbiosis with Medicago truncatula Jemalong A17, but Sinorhizobium medicae WSM419 is able to support more vigorous plant growth. Using proteomic data from free-living and symbiotic S. medicae WSM419, we previously identified a subset of proteins that were not closely related to any S. meliloti Rm1021 proteins and speculated that adding one or more of these proteins to S. meliloti Rm1021 would increase its effectiveness on M. truncatula A17. Three genes, Smed_3503, Smed_5985, and Smed_6456, were cloned into S. meliloti Rm1021 downstream of the E. coli lacZ promoter. Strains with these genes increased nodulation and improved plant growth, individually and in combination with one another. Smed_3503, renamed iseA ( i ncreased s ymbiotic e ffectiveness), had the largest impact, increasing M. truncatula biomass by 61%. iseA homologs were present in all currently sequenced S. medicae strains but were infrequent in other Sinorhizobium isolates.more »Rhizobium leguminosarum bv. viciae 3841 containing iseA led to more nodules on pea and lentil. Split-root experiments with M. truncatula A17 indicated that S. meliloti Rm1021 carrying the S. medicae iseA is less sensitive to plant-induced resistance to rhizobial infection, suggesting an interaction with the plant’s regulation of nodule formation. IMPORTANCE Legume symbiosis with rhizobia is highly specific. Rhizobia that can nodulate and fix nitrogen on one legume species are often unable to associate with a different species. The interaction can be more subtle. Symbiotically enhanced growth of the host plant can differ substantially when nodules are formed by different rhizobial isolates of a species, much like disease severity can differ when conspecific isolates of pathogenic bacteria infect different cultivars. Much is known about bacterial genes essential for a productive symbiosis, but less is understood about genes that marginally improve performance. We used a proteomic strategy to identify Sinorhizobium genes that contribute to plant growth differences that are seen when two different strains nodulate M. truncatula A17. These genes could also alter the symbiosis between R. leguminosarum bv. viciae 3841 and pea or lentil, suggesting that this approach identifies new genes that may more generally contribute to symbiotic productivity.« less