Title: Evolution of manipulative microbial behaviors in the rhizosphere
Abstract
The rhizosphere has been called “one of the most complex ecosystems on earth” because it is a hotspot for interactions among millions of microbial cells. Many of these are microbes are also participating in a dynamic interplay with host plant tissues, signaling pathways, and metabolites. Historically, breeders have employed aplant‐centric perspective when trying to harness the potential of microbiome‐derived benefits to improve productivity and resilience of economically important plants. This is potentially problematic because: (i) the evolution of the microbes themselves is often ignored, and (ii) it assumes that the fitness of interacting plants and microbes is strictly aligned. In contrast, amicrobe‐centric perspective recognizes that putatively beneficial microbes are still under selection to increase their own fitness, even if there are costs to the host. This can lead to the evolution of sophisticated, potentially subtle, ways for microbes to manipulate the phenotype of their hosts, as well as other microbes in the rhizosphere. We illustrate this idea with a review of cases where rhizosphere microbes have been demonstrated to directly manipulate host root growth, architecture and exudation, host nutrient uptake systems, and host immunity and defense. We also discuss indirect effects, whereby fitness outcomes for the plant are a consequence of ecological interactions between rhizosphere microbes. If these consequences are positive for the plant, they can potentially be misconstrued as traits that have evolved to promote host growth, even if they are a result of selection for unrelated functions. The ubiquity of both direct microbial manipulation of hosts and context‐dependent, variable indirect effects leads us to argue that an evolutionary perspective on rhizosphere microbial ecology will become increasingly important as we continue to engineer microbial communities for crop production.
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.
Francis, Jacob S.; Mueller, Tobias G.; Vannette, Rachel L.(
, New Phytologist)
Summary
Epiphytic microbes frequently affect plant phenotype and fitness, but their effects depend on microbe abundance and community composition. Filtering by plant traits and deterministic dispersal‐mediated processes can affect microbiome assembly, yet their relative contribution to predictable variation in microbiome is poorly understood.
We compared the effects of host‐plant filtering and dispersal on nectar microbiome presence, abundance, and composition. We inoculated representative bacteria and yeast into 30 plants across four phenotypically distinct cultivars ofEpilobium canum. We compared the growth of inoculated communities to openly visited flowers from a subset of the same plants.
There was clear evidence of host selection when we inoculated flowers with synthetic communities. However, plants with the highest microbial densities when inoculated did not have the highest microbial densities when openly visited. Instead, plants predictably varied in the presence of bacteria, which was correlated with pollen receipt and floral traits, suggesting a role for deterministic dispersal.
These findings suggest that host filtering could drive plant microbiome assembly in tissues where species pools are large and dispersal is high. However, deterministic differences in microbial dispersal to hosts may be equally or more important when microbes rely on an animal vector, dispersal is low, or arrival order is important.
DeWolf, Ella; Brock, Marcus T.; Calder, William John; Kliebenstein, Daniel J.; Katz, Ella; Li, Baohua; Morrison, Hilary G.; Maïgnien, Lois; Weinig, Cynthia(
, Molecular Ecology)
Abstract
The rhizosphere microbiome influences many aspects of plant fitness, including production of secondary compounds and defence against insect herbivores. Plants also modulate the composition of the microbial community in the rhizosphere via secretion of root exudates. We tested both the effect of the rhizosphere microbiome on plant traits, and host plant effects on rhizosphere microbes using recombinant inbred lines (RILs) ofBrassica rapathat differ in production of glucosinolates (GLS), secondary metabolites that contribute to defence against insect herbivores. First, we investigated the effect of genetic variation in GLS production on the composition of the rhizosphere microbiome. Using a Bayesian Dirichlet‐multinomial regression model (DMBVS), we identified both negative and positive associations between bacteria from six genera and the concentration of five GLS compounds produced in plant roots. Additionally, we tested the effects of microbial inoculation (an intact vs. disrupted soil microbiome) on GLS production and insect damage in these RILs. We found a significant microbial treatment × genotype interaction, in which total GLS was higher in the intact relative to the disrupted microbiome treatment in some RILs. However, despite differences in GLS production between microbial treatments, we observed no difference in insect damage between treatments. Together, these results provide evidence for a full feedback cycle of plant–microbe interactions mediated by GLS; that is, GLS compounds produced by the host plant “feed‐down” to influence rhizosphere microbial community and rhizosphere microbes “feed‐up” to influence GLS production.
Heath, Katy D.; Podowski, Justin C.; Heniff, Stephanie; Klinger, Christie R.; Burke, Patricia V.; Weese, Dylan J.; Yang, Wendy H.; Lau, Jennifer A.(
, American Journal of Botany)
Premise
Nutrients, 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.
Methods
We 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.
Results
Light availability and rhizobium inoculum interactively determined plant growth, and variation in rhizobium partner quality was more apparent in ambient light.
Conclusions
Our 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.
Flowers, L.(
, International Journal of Science and Research Archive)
The sustainability of plant life is intimately connected to its evolution with microbial life. Based on experimental evidence, microbial assemblages benefit plants on molecular, cellular, and ecological levels. The plant microbiome or phytomicrobiome are the microbes closely associated with a particular plant species. Distinct plant microbial ecosystems are in the phyllosphere, rhizosphere, soil, and endosphere. Plant-associated microbes affect plants in numerous ways and participate in various physiological functions essential for the plant, including nutrient recycling, the breakdown and synthesis of critical molecules, and other phytoprotective functions. While studying plant-microbe interactions is not new, recent developments in metagenomic sequencing and high-throughput pathway identification techniques have allowed scientists to explore unculturable microbes associated with plants. This review primarily focuses on the significant role of the phytomicrobiome and describes the prevalent taxonomic units found in association
with plants. Plants are suitable tractable model systems to study plant-microbe interactions and can be grown under different experimental conditions to examine other characteristics of the phytomicrobiome. This article also provides a systematic review of the current research on the phytomicrobiome. It explores the extent to which the
phytomicrobiome participates in an essential process that promotes plant fitness and sustainabilityand reviews research that focuses on microbiome community shifts in response to abiotic and biotic stress. Genetic engineering of plant-associated microbes to enhance plant growth and protection is addressed. The use of nanofertilizers and
phytomicrobiome transplantation to restore plant health and improve the success of agriculturally beneficial crops is also discussed.
Klein, Malin, Stewart, Justin D., Porter, Stephanie S., Weedon, James T., and Kiers, E. Toby. Evolution of manipulative microbial behaviors in the rhizosphere. Evolutionary Applications 15.10 Web. doi:10.1111/eva.13333.
Klein, Malin, Stewart, Justin D., Porter, Stephanie S., Weedon, James T., & Kiers, E. Toby. Evolution of manipulative microbial behaviors in the rhizosphere. Evolutionary Applications, 15 (10). https://doi.org/10.1111/eva.13333
Klein, Malin, Stewart, Justin D., Porter, Stephanie S., Weedon, James T., and Kiers, E. Toby.
"Evolution of manipulative microbial behaviors in the rhizosphere". Evolutionary Applications 15 (10). Country unknown/Code not available: Wiley-Blackwell. https://doi.org/10.1111/eva.13333.https://par.nsf.gov/biblio/10378190.
@article{osti_10378190,
place = {Country unknown/Code not available},
title = {Evolution of manipulative microbial behaviors in the rhizosphere},
url = {https://par.nsf.gov/biblio/10378190},
DOI = {10.1111/eva.13333},
abstractNote = {Abstract The rhizosphere has been called “one of the most complex ecosystems on earth” because it is a hotspot for interactions among millions of microbial cells. Many of these are microbes are also participating in a dynamic interplay with host plant tissues, signaling pathways, and metabolites. Historically, breeders have employed aplant‐centric perspective when trying to harness the potential of microbiome‐derived benefits to improve productivity and resilience of economically important plants. This is potentially problematic because: (i) the evolution of the microbes themselves is often ignored, and (ii) it assumes that the fitness of interacting plants and microbes is strictly aligned. In contrast, amicrobe‐centric perspective recognizes that putatively beneficial microbes are still under selection to increase their own fitness, even if there are costs to the host. This can lead to the evolution of sophisticated, potentially subtle, ways for microbes to manipulate the phenotype of their hosts, as well as other microbes in the rhizosphere. We illustrate this idea with a review of cases where rhizosphere microbes have been demonstrated to directly manipulate host root growth, architecture and exudation, host nutrient uptake systems, and host immunity and defense. We also discuss indirect effects, whereby fitness outcomes for the plant are a consequence of ecological interactions between rhizosphere microbes. If these consequences are positive for the plant, they can potentially be misconstrued as traits that have evolved to promote host growth, even if they are a result of selection for unrelated functions. The ubiquity of both direct microbial manipulation of hosts and context‐dependent, variable indirect effects leads us to argue that an evolutionary perspective on rhizosphere microbial ecology will become increasingly important as we continue to engineer microbial communities for crop production.},
journal = {Evolutionary Applications},
volume = {15},
number = {10},
publisher = {Wiley-Blackwell},
author = {Klein, Malin and Stewart, Justin D. and Porter, Stephanie S. and Weedon, James T. and Kiers, E. Toby},
}
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