Summary Many plant species simultaneously interact with multiple symbionts, which can, but do not always, generate synergistic benefits for their host. We ask if plant life history (i.e. annual vs perennial) can play an important role in the outcomes of the tripartite symbiosis of legumes, arbuscular mycorrhizal fungi (AMF), and rhizobia.We performed a meta‐analysis of 88 studies examining outcomes of legume–AMF–rhizobia interactions on plant and microbial growth.Perennial legumes associating with AMF and rhizobia grew larger than expected based on their response to either symbiont alone (i.e. their response to co‐inoculation was synergistic). By contrast, annual legume growth with co‐inoculation did not differ from additive expectations. AMF and rhizobia differentially increased phosphorus (P) and nitrogen (N) tissue concentration. Rhizobium nodulation increased with mycorrhizal fungi inoculation, but mycorrhizal fungi colonization did not increase with rhizobium inoculation. Microbial responses to co‐infection were significantly correlated with synergisms in plant growth.Our work supports a balanced plant stoichiometry mechanism for synergistic benefits. We find that synergisms are in part driven by reinvestment in complementary symbionts, and that time‐lags in realizing benefits of reinvestment may limit synergisms in annuals. Optimization of microbiome composition to maximize synergisms may be critical to productivity, particularly for perennial legumes.
more »
« less
Mycorrhizal and rhizobial interactions influence model grassland plant community structure and productivity
Arbuscular mycorrhizal (AM) fungi and rhizobium are likely important drivers of plant coexistence and grassland productivity due to complementary roles in supplying limiting nutrients. However, the interactive effects of mycorrhizal and rhizobial associations on plant community productivity and competitive dynamics remain unclear. To address this, we conducted a greenhouse experiment to determine the influences of these key microbial functional groups on communities comprising three plant species by comparing plant communities grown with or without each symbiont. We also utilized N-fertilization and clipping treatments to explore potential shifts in mycorrhizal and rhizobial benefits across abiotic and biotic conditions. Our research suggests AM fungi and rhizobium co-inoculation was strongly facilitative for plant community productivity and legume (Medicago sativa) growth and nodulation. Plant competitiveness shifted in the presence of AM fungi and rhizobium, favoring M. sativa over a neighboring C4 grass (Andropogon gerardii) and C 3 forb (Ratibida pinnata). This may be due to rhizobial symbiosis as well as the relatively greater mycorrhizal growth response of M. sativa, compared to the other model plants. Clipping and N-fertilization altered relative costs and benefits of both symbioses, presumably by altering host-plant nitrogen and carbon dynamics, leading to a relative decrease in mycorrhizal responsiveness and proportional biomass of M. sativa relative to the total biomass of the entire plant community, with a concomitant relative increase in A. gerardii and R. pinnata proportional biomass. Our results demonstrate a strong influence of both microbial symbioses on host-plant competitiveness and community dynamics across clipping and N-fertilization treatments, suggesting the symbiotic rhizosphere community is critical for legume establishment in grasslands.
more »
« less
- Award ID(s):
- 1946093
- PAR ID:
- 10495361
- Publisher / Repository:
- Springer Nature
- Date Published:
- Journal Name:
- Mycorrhiza
- Volume:
- 32
- Issue:
- 1
- ISSN:
- 0940-6360
- Page Range / eLocation ID:
- 15 to 32
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
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.more » « less
-
Hui, Dafeng (Ed.)Abstract While the relationship between genetic diversity and plant productivity has been established for many species, it is unclear whether environmental conditions and biotic associations alter the nature of the relationship. To address this, we investigated the interactive effects of genotypic diversity, drought and mycorrhizal association on plant productivity and plant traits. Our mesocosm study was set up at the Konza Prairie Biological Research Station, located in the south of Manhattan, Kansas. Andropogon gerardii, the focal species for our study, was planted in two levels of genotypic richness treatment: monoculture or three-genotype polyculture. A rainout shelter was constructed over half of the experimental area to impose a drought and Thiophanate-methyl fungicide was used to suppress arbuscular mycorrhizal fungi in selected pots within each genotypic richness and drought treatment. Genotypic richness and mycorrhizal association did not affect above-ground biomass of A. gerardii. Drought differentially affected the above-ground biomass, the number of flowers and bolts of A. gerardii genotypes, and the biomass and the functional traits also differed for monoculture versus polyculture. Our results suggest that drought and genotypic richness can have variable outcomes for different genotypes of a plant species.more » « less
-
Abstract Restoration of soil microbial communities, and microbial mutualists in particular, is increasingly recognized as critical for the successful restoration of grassland plant communities. Although the positive effects of restoring arbuscular mycorrhizal fungi during the restoration of these systems have been well documented, less is known about the potential importance of nitrogen‐fixing rhizobium bacteria, which associate with legume plant species that comprise an essential part of grassland plant communities, to restoration outcomes. In a series of greenhouse and field experiments, we examined the effects of disturbance on rhizobium communities, how plant interactions with these mutualists changed with disturbance, and whether rhizobia can be used to enhance the establishment of desirable native legume species in degraded grasslands. We found that agricultural disturbance alters rhizobium communities in ways that affect the growth and survival of legume species. Native legume species derived more benefit from interacting with rhizobia than did non‐native species, regardless of rhizobia disturbance history. Additionally, slow‐growing, long‐lived legume species received more benefits from associating with rhizobia from undisturbed native grasslands than from associating with rhizobia from more disturbed sites. Together, this suggests that native rhizobia may be key to enhancing the restoration success of legumes in disturbed habitats.more » « less
-
Druzhinina, Irina S. (Ed.)ABSTRACT Trees associating with different mycorrhizas often differ in their effects on litter decomposition, nutrient cycling, soil organic matter (SOM) dynamics, and plant-soil interactions. For example, due to differences between arbuscular mycorrhizal (AM) and ectomycorrhizal (ECM) tree leaf and root traits, ECM-associated soil has lower rates of C and N cycling and lower N availability than AM-associated soil. These observations suggest that many groups of nonmycorrhizal fungi should be affected by the mycorrhizal associations of dominant trees through controls on nutrient availability. To test this overarching hypothesis, we explored the influence of predominant forest mycorrhizal type and mineral N availability on soil fungal communities using next-generation amplicon sequencing. Soils from four temperate hardwood forests in southern Indiana, United States, were studied; three forests formed a natural gradient of mycorrhizal dominance (100% AM tree basal area to 100% ECM basal area), while the fourth forest contained a factorial experiment testing long-term N addition in both dominant mycorrhizal types. We found that overall fungal diversity, as well as the diversity and relative abundance of plant pathogenic and saprotrophic fungi, increased with greater AM tree dominance. Additionally, tree community mycorrhizal associations explained more variation in fungal community composition than abiotic variables, including soil depth, SOM content, nitrification rate, and mineral N availability. Our findings suggest that tree mycorrhizal associations may be good predictors of the diversity, composition, and functional potential of soil fungal communities in temperate hardwood forests. These observations help explain differing biogeochemistry and community dynamics found in forest stands dominated by differing mycorrhizal types. IMPORTANCE Our work explores how differing mycorrhizal associations of temperate hardwood trees (i.e., arbuscular [AM] versus ectomycorrhizal [ECM] associations) affect soil fungal communities by altering the diversity and relative abundance of saprotrophic and plant-pathogenic fungi along natural gradients of mycorrhizal dominance. Because temperate hardwood forests are predicted to become more AM dominant with climate change, studies examining soil communities along mycorrhizal gradients are necessary to understand how these global changes may alter future soil fungal communities and their functional potential. Ours, along with other recent studies, identify possible global trends in the frequency of specific fungal functional groups responsible for nutrient cycling and plant-soil interactions as they relate to mycorrhizal associations.more » « less
An official website of the United States government

