Soil Origin and Plant Genotype Modulate Switchgrass Aboveground Productivity and Root Microbiome Assembly

Costa, Pedro Beschoren da; Benucci, Gian Niccolò; Chou, Ming-Yi; Wyk, Judson Van; Chretien, Morgane; Bonito, Gregory

doi:10.1128/mbio.00079-22

Cited by 15 publications

(18 citation statements)

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“…However, a few species were also found to be pathogenic to plants (Munkvold and White, 2016; Pfordt et al ., 2020). Linnemannia , formerly classified as Mortierella , is closely associated with switchgrass roots (Vandepol et al ., 2020; Beschoren da Costa et al ., 2022). Isolates of the species promoted growth of Arabidopsis and economically important crops such as Citrullus lanatus, Zea mays, Solanum lycopersicum, Cucurbita and Calibrachoa through inducing IAA production and facilitating P and Fe acquisition (Li et al ., 2018; Becker and Cubeta, 2020; Zhang et al ., 2020; Ozimek and Hanaka, 2021; Vandepol et al ., 2022).…”

Section: Discussionmentioning

confidence: 99%

“…Manipulation of microbiomes was demonstrated to be a viable approach for plant disease control via microbe-mediated pathogen suppression (Fierer, 2017) or plant immune system priming (Raaijmakers and Mazzola, 2016). Rhizosphere microbial compositions and functions are influenced by multiple factors, such as abiotic conditions (Edwards et al ., 2015; Simonin et al ., 2020), plant species (Berg and Smalla, 2009; Fitzpatrick et al ., 2018) and plant genotypes (Wagner et al, 2016; Morella et al, 2020; Brown et al, 2021; Beschoren da Costa et al, 2022). Among these, variations in metabolites of plant above- and below-ground tissues as well as root exudates have been implicated in microbiome function (Jones et al, 2009; Venturi & Keel, 2016; Korenblum et al, 2020; VanWallendael et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

“…For example, secretion of coumarin and benzoxazinoid specialized metabolites from the root shape the maize rhizosphere microbiomes (Stringlis et al, 2018; Cotton et al, 2019). There is increasing evidence suggesting that switchgrass genotype influences the rhizosphere microbiome (Beschoren da Costa et al ., 2022; Ulbrich et al ., 2022). Our working hypothesis is that genotype-specific differences in specialized metabolite accumulation influences rhizosphere microbial assembly.…”

Section: Introductionmentioning

confidence: 99%

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Identification of anti-fungal bioactive terpenoids from the bioenergy crop switchgrass (Panicum virgatum)

Chou

Bonito

et al. 2023

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Plant derived bioactive small molecules have attracted attention of scientists across fundamental and applied scientific disciplines. We seek to understand the influence of these phytochemicals on functional phytobiomes. Increased knowledge of specialized metabolite bioactivities could inform strategies for sustainable crop production. Our recent investigations of metabolomes of the upland and lowland ecotypes of the bioenergy crop switchgrass revealed large differences in types and abundances of terpenoid specialized metabolites. We hypothesized that - consistent with accumulating evidence that switchgrass genotype impacts microbiome assembly - differential terpenoid accumulation contributes to switchgrass ecotype-specific microbiome composition. An initial plate-based disc diffusion screen of 18 switchgrass root derived fungal isolates revealed differential responses to upland- and lowland-isolated metabolites. To identify specific fungal growth-modulating metabolites, we tested fractions from root extracts on three ecologically important fungal isolates - Linnemania elongata, Trichoderma sp. and Fusarium sp. Saponins and diterpenoids were identified as the most prominent antifungal metabolites. Finally, analysis of liquid chromatography-purified terpenoids revealed fungal inhibition structure - activity relationships (SAR). Saponin antifungal activity was primarily determined by the number of sugar moieties - saponins glycosylated at a single core position were inhibitory whereas saponins glycosylated at two core positions were inactive. Saponin core hydroxylation and acetylation were also associated with reduced activity. Diterpenoid activity required the presence of an intact furan ring for strong fungal growth inhibition. This study demonstrates that switchgrass genotype-specific metabolites differentially inhibit fungal isolates from the root and rhizosphere, supporting the hypothesis that these molecules contribute to microbiome assembly and function.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Identification of anti-fungal bioactive terpenoids from the bioenergy crop switchgrass (Panicum virgatum)

Chou

Bonito

et al. 2023

Preprint

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“…We subjected genetically variable individuals to identical rearing conditions, truly co-housed and with replication, allowing the disentanglement of host genotypic from environmental effects on the gut microbiome. This degree of experimental control has been implemented more commonly for plant microbiome studies [56][57][58][59] , but it is logistically difficult for studies of free-living animal species. Because animal experiments with unrestricted co-housing require the tracking of individuals via marking or genotyping, a more convenient alternative has been to keep subjects with different genotypes physically separated but generally exposed to similar conditions 28,29,[60][61][62][63] .…”

Section: Controlled Common Garden Experiments Are Essential For Under...mentioning

confidence: 99%

Host genomic variation shapes gut microbiome diversity in threespine stickleback fish

Small¹,

Beck²,

Currey³

et al. 2022

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Variation among host-associated microbiomes is well documented across species, populations, and individuals. Understanding relationships between host-genetic and microbial variation is important for predicting coevolutionary dynamics between hosts and their microbiota and is also biomedically relevant to understanding why some humans are more susceptible to chronic disorders like Inflammatory Bowel Diseases (IBD). Unfortunately, the relative contributions of host genetics and the environment to microbiome variation have been difficult to study. Human research shows that genetic variation influences microbiome differences but confounding environmental effects cannot be controlled experimentally. Isogenic laboratory models can be used in controlled environments but often focus on large-effect mutations and do not recapitulate genetic variation observed in nature. Thus, although important factors impacting the microbiome have been identified, few studies have tested for the direct influence of natural host-genetic variation on microbiome differences within a controlled environment. To address this, we performed a common garden experiment using laboratory lines of genetically divergent populations of threespine stickleback fish - an outbred model organism commonly used for determining the genetic basis of complex traits in the context of natural genetic variation. Using germ-free derivation of divergent lines and hybrids between them in this experimental framework, we detected a clear, positive association between stickleback genetic dissimilarity and microbiome dissimilarity. With RAD-seq data we identified regions of the genome that contributed most significantly to this relationship. Importantly, we also highlight that heritable morphological traits like body size -when correlated with microbiome composition - need consideration in future host-associated microbiome studies.

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Section: Controlled Common Garden Experiments Are Essential For Under...mentioning

confidence: 99%

Host genomic variation shapes gut microbiome diversity in threespine stickleback fish

Small

Beck

Currey

et al. 2022

Preprint

View full text Add to dashboard Cite

Variation among host-associated microbiomes is well documented across species, populations, and individuals. However, the relative importance of host genetic differences for microbiome variation has been difficult to study. While research in humans has shown that genetic variation influences microbiome differences, confounding environmental effects have been very difficult to control. Isogenic laboratory models help isolate host genetic variants to test for influences of the environment or large- effect mutations on the microbiome, but such studies seldom incorporate natural genetic variation. Thus, although many important factors potentially impacting the microbiome have been identified, most studies have failed to test for the direct influence of natural host-genetic variation on microbiome differences within a controlled environment. Understanding the relationship between host-genetic and microbial variation also has biomedical implications, such as understanding why some humans are more susceptible to chronic inflammatory disorders like Crohn's Disease and Ulcerative Colitis. To directly assess the relationship between host-genetic variation and microbiome variation, we performed a common garden experiment using laboratory lines of genetically divergent populations of threespine stickleback fish - a species that is an outbred model organism commonly used for determining the genetic basis of complex traits in the context of natural genetic variation. Using germ-free derivation and the powerful common garden design with these divergent lines, as well as hybrids between them, we detected clear associations between stickleback genetic dissimilarity and microbiome dissimilarity. Using genome-wide RAD-seq data we also identified regions of the genome underlying differences in microbiome composition. Importantly, we highlight that heritable morphological traits such as body size that are correlated with microbiome dissimilarity also need consideration in future microbiome studies.

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Soil Origin and Plant Genotype Modulate Switchgrass Aboveground Productivity and Root Microbiome Assembly

Abstract: Greenhouse gas reduction, carbon sequestration, and environmental remediation are top research themes within the U.S. Department of Energy funded bioenergy research centers.

Cited by 15 publications

References 75 publications

Identification of anti-fungal bioactive terpenoids from the bioenergy crop switchgrass (Panicum virgatum)

Identification of anti-fungal bioactive terpenoids from the bioenergy crop switchgrass (Panicum virgatum)

Host genomic variation shapes gut microbiome diversity in threespine stickleback fish

Host genomic variation shapes gut microbiome diversity in threespine stickleback fish

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