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Title: Home-field advantage affects the local adaptive interaction between Andropogon gerardii ecotypes and root-associated bacterial communities
ABSTRACT
Due to climate change, drought frequencies and severities are predicted to increase across the United States. Plant responses and adaptation to stresses depend on plant genetic and environmental factors. Understanding the effect of those factors on plant performance is required to predict species’ responses to environmental change. We used reciprocal gardens planted with distinct regional ecotypes of the perennial grassAndropogon gerardiiadapted to dry, mesic, and wet environments to characterize their rhizosphere communities using 16S rRNA metabarcode sequencing. Even though the local microbial pool was the main driver of these rhizosphere communities, the significant plant ecotypic effect highlighted active microbial recruitment in the rhizosphere, driven by ecotype or plant genetic background. Our data also suggest that ecotypes planted at their homesites were more successful in recruiting rhizosphere community members that were unique to the location. The link between the plants’ homesite and the specific local microbes supported the “home field advantage” hypothesis. The unique homesite microbes may represent microbial specialists that are linked to plant stress responses. Furthermore, our data support ecotypic variation in the recruitment of congeneric but distinct bacterial variants, highlighting the nuanced plant ecotype effects on rhizosphere microbiome recruitment. These results improve our understanding of the complex plant host–soil microbe interactions and should facilitate further studies focused on exploring the functional potential of recruited microbes. Our study has the potential to aid in predicting grassland ecosystem responses to climate change and impact restoration management practices to promote grassland sustainability.
IMPORTANCE
In this study, we used reciprocal gardens located across a steep precipitation gradient to characterize rhizosphere communities of distinct dry, mesic, and wet regional ecotypes of the perennial grassAndropogon gerardii. We used 16S rRNA amplicon sequencing and focused oligotyping analysis and showed that even though location was the main driver of the microbial communities, ecotypes could potentially recruit distinct bacterial populations. We showed that differentA. gerardiiecotypes were more successful in overall community recruitment and recruitment of microbes unique to the “home” environment, when growing at their “home site.” We found evidence for “home-field advantage” interactions between the host and host–root-associated bacterial communities, and the capability of ecotypes to recruit specialized microbes that were potentially linked to plant stress responses. Our study aids in a better understanding of the factors that affect plant adaptation, improve management strategies, and predict grassland function under the changing climate.
Climate change will result in more frequent droughts that can impact soil-inhabiting microbiomes (rhizobiomes) in the agriculturally vital North American perennial grasslands. Rhizobiomes have contributed to enhancing drought resilience and stress resistance properties in plant hosts. In the predicted events of more future droughts, how the changing rhizobiome under environmental stress can impact the plant host resilience needs to be deciphered. There is also an urgent need to identify and recover candidate microorganisms along with their functions, involved in enhancing plant resilience, enabling the successful development of synthetic communities.
Results
In this study, we used the combination of cultivation and high-resolution genomic sequencing of bacterial communities recovered from the rhizosphere of a tallgrass prairie foundation grass,Andropogon gerardii. We cultivated the plant host-associated microbes under artificial drought-induced conditions and identified the microbe(s) that might play a significant role in the rhizobiome ofAndropogon gerardiiunder drought conditions. Phylogenetic analysis of the non-redundant metagenome-assembled genomes (MAGs) identified a bacterial genome of interest – MAG-Pseudomonas. Further metabolic pathway and pangenome analyses recovered genes and pathways related to stress responses including ACC deaminase; nitrogen transformation including assimilatory nitrate reductase in MAG-Pseudomonas,which might be associated with enhanced drought tolerance and growth forAndropogon gerardii.
Conclusions
Our data indicated that the metagenome-assembled MAG-Pseudomonashas the functional potential to contribute to the plant host’s growth during stressful conditions. Our study also suggested the nitrogen transformation potential ofMAG-Pseudomonasthat could impactAndropogon gerardiigrowth in a positive way. The cultivation of MAG-Pseudomonassets the foundation to construct a successful synthetic community forAndropogon gerardii. To conclude, stress resilience mediated through genes ACC deaminase, nitrogen transformation potential through assimilatory nitrate reductase in MAG-Pseudomonascould place this microorganism as an important candidate of the rhizobiome aiding the plant host resilience under environmental stress. This study, therefore, provided insights into the MAG-Pseudomonasand its potential to optimize plant productivity under ever-changing climatic patterns, especially in frequent drought conditions.
Johnson, Loretta C.; Galliart, Matthew B.; Alsdurf, Jacob D.; Maricle, Brian R.; Baer, Sara G.; Bello, Nora M.; Gibson, David J.; Smith, Adam B.(
, Journal of Ecology)
Abstract
Local adaptation is a fundamental phenomenon in evolutionary biology, with relevance to formation of ecotypes, and ultimately new species, and application to restoration and species’ response to climate change. Reciprocal transplant gardens, a common garden in which ecotypes are planted among home and away habitats, are the gold standard to detect local adaptation in populations.
This review focuses on reciprocal transplant gardens to detect local adaptation, especially in grassland species beginning with early seminal studies of grass ecotypes. Fast forward more than half a century, reciprocal gardens have moved into the genomic era, in which the genetic underpinnings of ecotypic variation can now be uncovered. Opportunities to combine genomic and reciprocal garden approaches offer great potential to shed light on genetic and environmental control of phenotypic variation. Our decadal study of adaptation in a dominant grass across the precipitation gradient of the US Great Plains combined genomic approaches and realistic community settings to shed light on controls over phenotype.
Common gardens are not without limitations and challenges. A survey of recent studies indicated the modal study uses a tree species, three source sites and one growing site, focuses on one species growing in a monoculture, lasts 3 years, and does not use other experimental manipulations and rarely employs population genetic tools. Reciprocal transplant gardens are even more uncommon, accounting for only 39% of the studies in the literature survey with the rest occurring at a single common site. Reciprocal transplant gardens offer powerful windows into local adaptation when (a) placed across wide environmental gradients to encompass the species’ range; (b) conducted across timespans adequate for detecting responses; (c) employing selection studies among competing ecotypes in community settings and (d) combined with measurements of form and function which ultimately determine success in home and away environments.
Synthesis. Reciprocal transplant gardens have been one of the foundations in evolutionary biology for the study of adaptation for the last century, and even longer in Europe. Moving forward, reciprocal gardens of foundational non‐model species, combined with genomic analyses and incorporation of biotic factors, have the potential to further revolutionize evolutionary biology. These field experiments will help to predict and model response to climate change and inform restoration practices.
Gibson, David J.; Donatelli, Juliette M.; AbuGhazaleh, Amer; Baer, Sara G.; Johnson, Loretta C.(
, Grassland Science)
Abstract
Ecotypic variation in forage nutrient value of a dominant grassland species,Andropogon gerardiiVitman (big bluestem), was quantified across a longitudinal precipitation gradient of theUSGreat Plains. Ecotypic variation ofA. gerardiihas been documented across this gradient, but the extent to which forage nutrient value differs among ecotypes is poorly known. Seven indicators of forage nutrient value (neutral detergent fiber [NDF], acid detergent fiber [ADF],in‐vitrodry matter digestibility [IVDMD], crude protein [CP], crude fat [CF], ash content) and relative feed value [RFV] were examined in 12 populations representing four ecotypes corresponding with distinct climate regions: eastern Colorado, central Kansas, eastern Kansas and southern Illinois. Vegetative material ofA. gerardiiwas collected from each population in July 2010. A greenhouse study tested the effect of watering regime on seedlings of the ecotypes from three of the precipitation regions grown under controlled conditions. Forage nutrient value indicators nitrogen andCPincreased, andADFdecreased east to west, whileIVDMDdecreased across the gradient corresponding with less annual precipitation. The greenhouse experiment showed that sampling before and after water treatment affected forage nutrient value measurements, with the exception ofNDFandCF. Nutrient value was most related to soil moisture and phenology, with smaller differences among ecotypes. Nutrient value of populations from the southern Illinois ecotype changed the least in response to variation in soil moisture. The southern Illinois ecotype will likely maintain forge nutrient value under variable precipitation projected to occur with climate change better than the ecotypes from more westerly parts of the range ofA. gerardii.
Khalil, Mohammed I.; Gibson, David J.; Baer, Sara G.; Jones, ed., Holly(
, Journal of Ecology)
Abstract
Dominant species can act as a biotic filter in structuring plant communities by constraining the establishment and survival of subordinate species. The effect of intraspecific trait variability of dominant species on the functional response of subordinate species, however, is not well understood.
We quantified intraspecific variation in four functional traits of 26 subordinate species in an experimental grassland established with two population sources (i.e. cultivars and local ecotypes) of three dominant grasses (Sorghastrum nutans, Andropogon gerardiiandSchizachyrium scoparium) and three pools of subordinate species (each from one origin) within each of the dominant grass source treatments.
Twenty of the 26 subordinate species exhibited intraspecific trait variability for one trait or more in response to dominant species population source, and variation among population sources of the dominant species was non‐random. Dominant grass population source affected intraspecific variability in functional traits of multiple subordinate species. Cultivar sources of the dominant grasses and some of the subordinate species that established with them had higher and generally more variable functional leaf area and leaf nitrogen content compared to local ecotypes of the dominant grasses and the subordinate species that established with them. Local ecotype sources of the dominant grasses increased leaf area based functional diversity of subordinate species.
Synthesis.This study provides evidence that intraspecific trait variability in dominant species acts as a biotic filter to constrain niche availability and dimensionality affecting trait variation of subordinate species during community assembly.
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.
@article{osti_10477912,
place = {Country unknown/Code not available},
title = {Home-field advantage affects the local adaptive interaction between Andropogon gerardii ecotypes and root-associated bacterial communities},
url = {https://par.nsf.gov/biblio/10477912},
DOI = {10.1128/spectrum.00208-23},
abstractNote = {ABSTRACT Due to climate change, drought frequencies and severities are predicted to increase across the United States. Plant responses and adaptation to stresses depend on plant genetic and environmental factors. Understanding the effect of those factors on plant performance is required to predict species’ responses to environmental change. We used reciprocal gardens planted with distinct regional ecotypes of the perennial grassAndropogon gerardiiadapted to dry, mesic, and wet environments to characterize their rhizosphere communities using 16S rRNA metabarcode sequencing. Even though the local microbial pool was the main driver of these rhizosphere communities, the significant plant ecotypic effect highlighted active microbial recruitment in the rhizosphere, driven by ecotype or plant genetic background. Our data also suggest that ecotypes planted at their homesites were more successful in recruiting rhizosphere community members that were unique to the location. The link between the plants’ homesite and the specific local microbes supported the “home field advantage” hypothesis. The unique homesite microbes may represent microbial specialists that are linked to plant stress responses. Furthermore, our data support ecotypic variation in the recruitment of congeneric but distinct bacterial variants, highlighting the nuanced plant ecotype effects on rhizosphere microbiome recruitment. These results improve our understanding of the complex plant host–soil microbe interactions and should facilitate further studies focused on exploring the functional potential of recruited microbes. Our study has the potential to aid in predicting grassland ecosystem responses to climate change and impact restoration management practices to promote grassland sustainability. IMPORTANCEIn this study, we used reciprocal gardens located across a steep precipitation gradient to characterize rhizosphere communities of distinct dry, mesic, and wet regional ecotypes of the perennial grassAndropogon gerardii. We used 16S rRNA amplicon sequencing and focused oligotyping analysis and showed that even though location was the main driver of the microbial communities, ecotypes could potentially recruit distinct bacterial populations. We showed that differentA. gerardiiecotypes were more successful in overall community recruitment and recruitment of microbes unique to the “home” environment, when growing at their “home site.” We found evidence for “home-field advantage” interactions between the host and host–root-associated bacterial communities, and the capability of ecotypes to recruit specialized microbes that were potentially linked to plant stress responses. Our study aids in a better understanding of the factors that affect plant adaptation, improve management strategies, and predict grassland function under the changing climate.},
journal = {Microbiology Spectrum},
volume = {11},
number = {5},
publisher = {ASM Journals},
author = {Kazarina, Anna and Sarkar, Soumyadev and Thapa, Shiva and Heeren, Leah and Kamke, Abgail and Ward, Kaitlyn and Hartung, Eli and Ran, Qinghong and Galliart, Matthew and Jumpponen, Ari and Johnson, Loretta and Lee, Sonny T.},
editor = {Arias, Renee S.}
}
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