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Gfeller, V.

Publications and source records attributed to Gfeller, V..

10 recordsLinked to original sources

Soil iron drives beneficial maize microbiome feedbacks inrotations with wheat

BackgroundPlants change their surrounding soil microbiome by root exudates and such conditioned microbiomes impact the performance of the present as well as the next plant generation as for example in crop rotations. The big challenge is that such microbiome feedbacks are highly context-dependent, i.e. they vary in strength and direction dependent on the local soil environment - of which the driving factor(s) remain unknown. Including maize in crop rotations involves benzoxazinoids (BXs), which are exuded from roots and alter the soil microbiome, which in turn affects growth and defence of the following crop. ResultsHere, we grew wild-type and BX-depleted maize in the field to differentially condition their soil microbiome and we found varying feedbacks on wheat performance dependent on the local physicochemical soil parameters. Using multivariate, correlation and modelling approaches and including additional data from two previous field experiments, we identified plant-available (PA) iron to explain BX-dependent microbiome feedbacks on wheat. The BX-conditioned soil microbiome caused wheat to grow taller at low levels of soil PA-iron but smaller at high levels. This finding was generalized testing these maize microbiome feedbacks on the model plant Arabidopsis thaliana using soil batches containing different levels of iron. Consistent with wheat, a significant inverse relationship between soil PA-iron levels and plant growth was found. This relationship was experimentally validated with Arabidopsis grown at low levels of soil iron where iron supplementation abolished the beneficial feedback of the BX-conditioned soil microbiome. ConclusionTogether these findings revealed that beneficial microbiome feedbacks occur at low levels of plant-available iron, i.e. when plants grow in a suboptimal soil, but they are lost when plants are nutritionally well supported. These results underscore the importance of iron availability in soil for beneficial microbial feedbacks on plant growth and predict agronomic benefits of incorporating maize in crop rotations on low iron soils.

microbiology↗

Crop genotype modulates root rot resistance-associated microbial community composition and abundance of key taxa

Plants are constantly challenged by pathogens, which can cause substantial yield losses. The aggressiveness of and damage by pathogens depends on the host-associated microbiome, which might be shaped by plant genetics to improve resistance. How different crop genotypes modulate their microbiota when challenged by a complex of pathogens is largely unknown. Here, we investigate if and how pea (Pisum sativum L.) genotypes shape their root microbiota upon challenge by soil-borne pathogens and how this relates to a genotypes resistance. Building on the phenotyping efforts of 252 pea genotypes grown in naturally infested soil, we characterized root fungi and bacteria by ITS region and 16S rRNA gene amplicon sequencing, respectively. Pea genotype markedly affected both fungal and bacterial community composition, and these genotype-specific microbiota were associated with root rot resistance. For example, genotype resistance was correlated (R2 = 19%) with root fungal community composition. Further, several key microbes, showing a high relative abundance, heritability, connectedness with other microbes, and correlation with plant resistance, were identified. Our findings highlight the importance of crop genotype-specific root microbiota under root rot stress and the potential of the plant to shape its associated microbiota as a second line of defense.

plant biology↗

The lactonase BxdA mediates metabolic adaptation of maize root bacteria to benzoxazinoids

Root exudates contain secondary metabolites that affect the plants root microbiome. How microbes cope with these bioactive compounds, and how this ability shapes root microbiomes remain largely unknown. We investigated how maize root bacteria metabolise benzoxazinoids, the main specialised metabolites of maize. Diverse and abundant bacteria metabolised the major compound (6-methoxy-benzoxazolin-2-one, MBOA) in the maize rhizosphere to 2-amino-7-methoxyphenoxazin-3-one (AMPO). By contrast, bacteria isolated from Arabidopsis, which does not produce benzoxazinoids, were unable to metabolise MBOA. Among Microbacteria strains, this differential metabolisation allowed to identify a conserved gene cluster containing the lactonase bxdA. BxdA converts MBOA to AMPO in vitro and we show that this capacity provided bacteria a growth benefit under carbon-limiting conditions. Together these results reveal that maize root bacteria - through BxdA - are metabolically adapted to the benzoxazinoids of their host. We propose that metabolic adaptation to plant-specialised compounds shapes root bacterial communities across the plant kingdom.

microbiology↗

Bacterial tolerance to host-exuded specialized metabolites structures the maize root microbiome

Plants exude specialized metabolites from their roots and these compounds are known to structure the root microbiome. However, the underlying mechanisms are poorly understood. We established a representative collection of maize root bacteria and tested their tolerance against benzoxazinoids, the dominant specialized and bioactive metabolites in the root exudates of maize plants. In vitro experiments revealed that benzoxazinoids inhibited bacterial growth in a strain- and compound-dependent manner. Tolerance against these selective antimicrobial compounds depended on bacterial cell wall structure. Further, we found that native root bacteria isolated from maize tolerated the benzoxazinoids better compared to non-host Arabidopsis bacteria. This finding suggests the adaptation of the root bacteria to the specialized metabolites of their host plant. Bacterial tolerance to 6-methoxy-benzoxazolin-2-one (MBOA), the most abundant and selective antimicrobial metabolite in the maize rhizosphere, correlated significantly with the abundance of these bacteria on benzoxazinoid-exuding maize roots. Thus, strain-dependent tolerance to benzoxazinoids largely explained the abundance pattern of bacteria on maize roots. Abundant bacteria generally tolerated MBOA, while low abundant root microbiome members were sensitive to this compound. Our findings reveal that tolerance to plant specialized metabolites is an important competence determinant for root colonization. We propose that bacterial tolerance to plant-secreted antimicrobial compounds is an underlying mechanism determining the structure of host-specific microbial communities. Significance StatementDiverse microbial communities colonize plant roots. They feed on carbon rich root exudates which contain a diverse mix of chemicals including primary and specialized metabolites. Here we show that specialized metabolites act as selective antibiotics to shape the root bacterial communities. By growing single isolates of maize root bacteria in the presence of benzoxazinoids in vitro, we find that the strains differ greatly in their tolerance to benzoxazinoids. Their different levels of tolerance largely explained their abundance on benzoxazinoid-exuding roots. Our work shows how plant specialized metabolites act to shape the maize root microbial community and thus deepened our mechanistic understanding of how plants shape their microbiome.

microbiology↗

Soil chemical and microbial gradients determine accumulation of root exuded secondary metabolites and plant-soil feedbacks in the field

IntroductionHarnessing positive plant-soil feedbacks via crop rotations is a promising strategy for sustainable agriculture. Plants can influence soil properties including microbes by exuding specialized metabolites. However, the effects are often context dependent and variable. If and how local soil heterogeneity may explain this variation is unknown. Benzoxazinoids are specialized metabolites that are released in high quantities by cereals such as wheat and maize. Benzoxazinoids can alter rhizosphere microbiota and the performance of plants subsequently growing in the exposed soils and are thus an excellent model to study agriculturally relevant plant-soil feedbacks in the field, and to assess how soil factors affect their outcome. Materials & methodsTo understand the importance of local variation in soil properties on benzoxazinoid-mediated plant-soil feedbacks, we conditioned plots with wild-type maize and benzoxazinoid-deficient bx1 mutant plants in a grid pattern across an arable field. We then grew winter wheat across the entire field in the following season. We determined accumulation of benzoxazinoids, root-associated microbial communities, abiotic soil properties and wheat performance in each plot. We also determined benzoxazinoid conversion dynamics in a labelling experiment under controlled conditions, and then assessed associations between soil chemical variation and benzoxazinoid-mediated plant-soil feedbacks. ResultsAcross the field, we detected a marked gradient in soil chemical and microbial community composition. This gradient resulted in significant differences in benzoxazinoid accumulation. These differences were explained by differential benzoxazinoid degradation rather than exudation. Benzoxazinoid exudation modulated alpha diversity of root and rhizosphere bacteria and fungi during maize growth, but not during subsequent wheat growth, while the chemical fingerprint of benzoxazinoid accumulation persisted. Averaged across the field, we detected no significant feedback effects of benzoxazinoid conditioning on wheat performance and defence, apart from a transient decrease in biomass during vegetative growth. Closer analysis however, revealed pronounced feedback effects along the chemical and microbial gradient of the field, with effects gradually changing from negative to positive along the gradient. ConclusionOverall, this study revealed that plant-soil feedbacks differ in strength and direction within a field, and that this variation can be explained by standing chemical and microbial gradients, which strongly affect benzoxazinoid accumulation in the soil. Understanding within-field soil heterogeneity is crucial for the future exploitation of plant-soil feedbacks in sustainable precision agriculture.

plant biology↗

Root-exuded secondary metabolites can alleviate negative plant-soil feedbacks

Plants can suppress the growth of other plants by modifying soil properties. These negative plant-soil feedbacks are often species-specific, suggesting that some plants possess resistance strategies. However, the underlying mechanisms remain largely unknown. Here, we investigated if and how benzoxazinoids, a class of dominant secondary metabolites that are exuded into the soil by maize and other cereals, help plants to resist negative plant-soil feedbacks. We find that three out of five tested crop species suppress maize performance relative to the mean across species. This effect is partially alleviated by the plants capacity to produce benzoxazinoids. Soil complementation of benzoxazinoid-deficient mutants with purified benzoxazinoids is sufficient to restore the protective effect. Sterilization and reinoculation experiments suggest that benzoxazinoid-mediated protection acts via changes in soil microbes. Substantial variation of the protective effect between experiments and soil types illustrates that the magnitude of the protective effect of benzoxazinoids against negative plant-soil feedbacks is context dependent. In summary, our study demonstrates that plant secondary metabolites can confer resistance to negative plant-soil feedbacks. These findings expand the functional repertoire of plant secondary metabolites, reveal a mechanism by which plants can resist suppressive soils, and may represent a promising avenue to stabilize plant performance in crop rotations in the future.

plant biology↗

Plant secondary metabolite-dependent plant-soil feedbacks can improve crop yield in the field

Plant secondary metabolites that are released into the rhizosphere alter biotic and abiotic soil properties, which in turn affect the performance of other plants. How such plant-soil feedbacks affect agricultural productivity and food quality in crop rotations is unknown. Here, we assessed the impact of maize benzoxazinoids on the performance, yield and food quality of three winter wheat varieties in a two-year field experiment. Following maize cultivation, we detected benzoxazinoid-dependent chemical and microbial fingerprints in the soil. The chemical fingerprint was still visible during wheat growth, while the microbial fingerprint was no longer detected. Benzoxazinoid soil conditioning by wild-type maize led to increased wheat emergence, tillering, growth and biomass compared to soil conditioning by bx1 mutant plants. Weed cover remained unaffected, while insect damage decreased in a subset of varieties. Wheat yield was increased by over 4% without a reduction in grain quality across varieties. This improvement was directly associated with increased germination and tillering. Taken together, our experiments demonstrate that plant secondary metabolites can increase yield via plant-soil feedbacks under agronomically realistic conditions. If this phenomenon holds across different soils and environmental conditions, optimizing plant root exudation could be a powerful, genetically tractable strategy to enhance crop yields without additional inputs.

plant biology↗

Soil composition and plant genotype determine benzoxazinoid-mediated plant-soil feedbacks in cereals

Plant-soil feedbacks refer to effects on plants that are mediated by soil modifications caused by the previous plant generation. Maize conditions the surrounding soil by secretion of root exudates including benzoxazinoids (BXs), a class of bioactive secondary metabolites. Previous work found that a BX- conditioned soil microbiota enhances insect resistance while reducing biomass in the next generation of maize plants. Whether these BX-mediated and microbially driven feedbacks are conserved across different soils and response species is unknown. We found the BX-feedbacks on maize growth and insect resistance conserved between two arable soils, but absent in a more fertile grassland soil, suggesting a soil-type dependence of BX feedbacks. We demonstrated that wheat also responded to BX-feedbacks. While the negative growth response to BX-conditioning was conserved in both cereals, insect resistance showed opposite patterns, with an increase in maize and a decrease in wheat. Wheat pathogen resistance was not affected. Finally and consistent with maize, we found the BX-feedbacks to be cultivar specific. Taken together, BX- feedbacks affected cereal growth and resistance in a soil and genotype dependent manner. Cultivar-specificity of BX-feedbacks is a key finding, as it hides the potential to optimize crops that avoid negative plant-soil feedbacks in rotations.

plant biology↗

Root volatiles in plant-plant interactions I: Characterization of root sesquiterpene emissions from Centaurea stoebe and their effects on other plants

Volatile organic compounds (VOCs) emitted by plant leaves can influence the physiology of neighboring plants. In contrast to interactions above ground, little is known about the role of VOCs in belowground plant-plant interactions. Here, we characterize constitutive root volatile emissions of the spotted knapweed (Centaurea stoebe) and explore the impact of these volatiles on the germination and growth of different sympatric plant species. We show that C. stoebe roots emit high amounts of sesquiterpenes, with estimated release rates of (E)-{beta}-caryophyllene above 3 g g-1 dw h-1. Sesquiterpene emissions show little variation between different C. stoebe populations, but vary substantially between different Centaurea species. Through root transcriptome sequencing, we identify six root-expressed sesquiterpene synthases (TPSs). Two root-specific TPSs, CsTPS4 and CsTPS5, are sufficient to produce the full blend of emitted root sesquiterpenes. Volatile exposure experiments demonstrate that C. stoebe root volatiles have neutral to positive effects on the germination and growth of different sympatric neighbors. Thus, constitutive root sesquiterpenes produced by two C. stoebe TPSs are associated with facilitation of sympatric neighboring plants. The release of root VOCs may thus influence C. stoebe abundance and plant community structure in nature.

plant biology↗

Root volatiles in plant-plant interactions II: Root terpenes from Centaurea stoebe modify Taraxacum officinale root chemistry and root herbivore growth

Volatile organic compounds (VOCs) emitted by plant roots can influence the germination and growth of neighboring plants. However, little is known about the effects of root VOCs on plant-herbivore interactions. The spotted knapeed (Centaurea stoebe) constitutively releases high amounts of sesquiterpenes into the rhizosphere. Here, we examine the impact of C. stoebe root VOCs on primary and secondary metabolites of sympatric Taraxacum officinale plants and the resulting plant-mediated effects on a generalist root herbivore, the white grub Melolontha melolontha. We show that exposure of T. officinale to C. stoebe root VOCs does not affect the accumulation of defensive secondary metabolites, but modulates carbohydrate and total protein levels in T. officinale roots. Furthermore, VOC exposure increases M. melolontha growth on T. officinale plants. Exposure of T. officinale to a major C. stoebe root VOC, the sesquiterpene (E)-{beta}-caryophyllene, partially mimics the effect of the full root VOC blend on M. melolontha growth. Thus, releasing root VOCs can modify plant-herbivore interactions of neighboring plants. The release of VOCs to increase the susceptibility of other plants may be a form of plant offense.

plant biology↗