Plant-microbiome Interactions Research Articles

Root exudate-mediated plant–microbiome interactions determine plant health during disease infection

Understanding the interactions between plants and microbes during pathogen infection is crucial for plant health improvement. However, the integrated role of soil nutrients, root exudates, and plant microbiomes in plant health during disease outbreaks remains unclear. In this study, we hypothesized that root exudate-mediated healthy microbiomes (HealthyBiome) would facilitate the escape of soil-borne pathogen infection, whereas a root exudate-mediated disease-conductive microbiome (PathoBiome) would induce disease occurrence. Using watermelon wilt disease caused by Fusarium oxysporum as a model, we investigated these interactions and their implications in plant disease. We examined the pathogen load across plant compartments during the pathogen accumulation (AH) and disease outbreak periods. We analyzed the plant microbiomes and root exudates during the outbreak, which was associated with the emergence in both healthy (BH) and diseased (BD) plants. Compared with AH and BD plants, BH plants had the lowest F. oxysporum density in the root–soil system (0.74–0.84 times that of AH and BD plants). BD plants showed an elevated amino acid metabolism (2.84–3.38 times that of healthy plants), whereas BH plants showed a higher metabolism of phenolic compounds (1.73 times that of diseased plants). BH plants secreted more palmitic acid (1.53 times that of diseased plants) and recruited more nitrogen (N)-fixing bacteria (e.g., Paenarthrobacter, Sphingomonas), which potentially alleviated N scarcity in the soil, promoted plant growth, and improved the plant defense. Structural equation modeling highlighted the interactions among soil nutrients, root metabolites, and plant nutrients in recruiting pro-growth bacteria to the rhizosphere and roots for healthy plant growth. Our findings provide novel evidence of how root exudates influence plant–microbiome interactions during pathogen infections, highlighting the importance of a balanced root exudate profile and its associated “HealthyBiome” in promoting plant health and growth.

Phyllosphere fungal diversity generates pervasive nonadditive effects on plant performance.

Plants naturally harbor diverse microbiomes that can dramatically impact their health and productivity. However, it remains unclear how fungal microbiome diversity, especially in the phyllosphere, impacts intermicrobial interactions and consequent nonadditive effects on plant productivity. Combining manipulative experiments, field collections, culturing, microbiome sequencing, and synthetic consortia, we experimentally tested for the first time how foliar fungal community diversity impacts plant productivity. We inoculated morning glories (Ipomoea hederifolia L.) with 32 phyllosphere consortia of either low or high diversity or with single fungal taxa, and measured effects on plant productivity and allocation. We found the following: (1) nonadditive effects were pervasive with 56% of fungal consortia interacting synergistically or antagonistically to impact plant productivity, including some consortia capable of generating acute synergism (e.g. > 1000% increase in productivity above the additive expectation), (2) interactions among 'commensal' fungi were responsible for this nonadditivity in diverse consortia, (3) synergistic interactions were approximately four times stronger than antagonistic effects, (4) fungal diversity affected the magnitude but not frequency or direction of nonadditivity, and (5) diversity affected plant performance nonlinearly with the highest performance in low-diversity treatments. These findings highlight the importance of interpreting plant-microbiome interactions under a framework that incorporates intermicrobial interactions and nonadditive outcomes to understand natural complexity.

Fertilizer regime and cultivar affect barley growth and rhizobiome composition

To combat climate change and environmental pollution, agriculture must reduce mineral fertilizer use and adopt sustainable, low-input, and organic practices. In such systems, plants depend on the soil microbiome for nutrient acquisition and growth. Thus, enhancing plant-microbiome interactions is vital for maintaining or even increasing production sustainably. Modern plant breeding has led to barley cultivars that yield high under substantial mineral fertilizer application. However, this selective breeding may have diminished traits essential for plant-microbiome interactions, making these cultivars less suitable for sustainable agriculture. In contrast, older cultivars might have preserved traits from their common wild ancestor, enabling them to prosper under low nutrient conditions. This study evaluated four modern elite barley cultivars and three older (pre-1980). Grown under various fertilizer regimes, we assessed their root microbiome using 16S rRNA amplicon sequencing. Our objectives were: i) to determine the impact of nutrient availability on plant nutrient uptake and biomass production, and ii) to understand how the time since domestication (domestication age), individual cultivar, and fertilizer regime influence the root microbiome. We found that without fertilizer, old cultivars had superior biomass production and higher leaf concentrations of nitrogen, potassium, sulfur, iron, zinc, and copper than modern cultivars. This indicates that older barley cultivars may have retained their wild ancestors' capability to synergize with the soil microbiome, enhancing nutrient acquisition in low-input systems. Notably, the diversity of the rhizo-microbiome was not significantly affected by domestication age but varied with individual cultivar and fertilizer treatment.

Harnessing root exudates for plant microbiome engineering and stress resistance in plants

A wide range of abiotic and biotic stresses adversely affect plant's growth and production. Under stress, one of the main responses of plants is the modulation of exudates excreted in the rhizosphere, which consequently leads to alterations in the resident microbiota. Thus, the exudates discharged into the rhizospheric environment play a preponderant role in the association and formation of plant-microbe interactions. In this review, we aimed to provide a synthesis of the latest and most pertinent literature on the diverse biochemical and structural compositions of plant root exudates. Also, this work investigates into their multifaceted role in microbial nutrition and intricate signaling processes within the rhizosphere, which includes quorum-sensing molecules. Specifically, it explores the contributions of low molecular weight compounds, such as carbohydrates, phenolics, organic acids, amino acids, and secondary metabolites, as well as the significance of high molecular weight compounds, including proteins and polysaccharides. It also discusses the state-of-the-art omics strategies that unveil the vital role of root exudates in plant-microbiome interactions, including defense against pathogens like nematodes and fungi. We propose multiple challenges and perspectives, including exploiting plant root exudates for host-mediated microbiome engineering. In this discourse, root exudates and their derived interactions with the rhizospheric microbiota should receive greater attention due to their positive influence on plant health and stress mitigation.

Diversity and plant growth promoting ability of rice root-associated bacteria in Burkina-Faso and cross-comparison with metabarcoding data.

Plant-associated bacteria are essential partners in plant health and development. In addition to taking advantage of the rapid advances recently achieved in high-throughput sequencing approaches, studies on plant-microbiome interactions require experiments with culturable bacteria. A study on the rice root microbiome was recently initiated in Burkina Faso. As a follow up, the aim of the present study was to develop a collection of corresponding rice root-associated bacteria covering maximum diversity, to assess the diversity of the obtained isolates based on the culture medium used, and to describe the taxonomy, phenotype and abundance of selected isolates in the rice microbiome. More than 3,000 isolates were obtained using five culture media (TSA, NGN, NFb, PCAT, Baz). The 16S rRNA fragment sequencing of 1,013 selected isolates showed that our working collection covered four bacterial phyla (Proteobacteria, Firmicutes, Actinobacteria and Bacteroidetes) and represented 33% of the previously described diversity of the rice root microbiome at the order level. Phenotypic in vitro analysis of the plant growth promoting capacity of the isolates revealed an overall ammonium production and auxin biosynthesis capacity, while siderophore production and phosphate solubilisation were enriched in Burkholderia, Ralstonia, Acinetobacter and Pseudomonas species. Of 45 representative isolates screened for growth promotion on seedlings of two rice cultivars, five showed an ability to improve the growth of both cultivars, while five others were effective on only one cultivar. The best results were obtained with Pseudomonas taiwanensis ABIP 2315 and Azorhizobium caulinodans ABIP 1219, which increased seedling growth by 158% and 47%, respectively. Among the 14 best performing isolates, eight appeared to be abundant in the rice root microbiome dataset from previous study. The findings of this research contribute to the in vitro and in planta PGP capacities description of rice root-associated bacteria and their potential importance for plants by providing, for the first time, insight into their prevalence in the rice root microbiome.

Exploring the connectivity between rhizosphere microbiomes and the plant genes: A way forward for sustainable increase in primary productivity

AbstractThe plant genome and its microbiome act together to enhance survival and promote host growth under various stresses. Plant microbiome plays an important role in plant productivity via a multitude of mechanisms including provision of nutrients and resistance against different biotic and abiotic factors. However, the molecular mechanisms responsible for plant microbiome interactions remain largely unknown. Nevertheless, gaining a deeper understanding of the plant genetic traits driving microbiome recruitments and assembly holds the potential to greatly enhance our capacity to utilize the microbiome effectively, leading to sustainable improvements in agricultural productivity and produce quality. This article explores the mutual influence of specific plant genes in modulating the rhizosphere (area around plant roots) microbiome, and how this rhizosphere microbiome impacts the plant genes, ultimately enhancing plant health and productivity. It further examines the effects of various rhizosphere microbiota, including Bacillus, Pseudomonas, Azospirillum, Trichoderma spp., on plant development, immunology and the expression of host functional genes. We conclude that the adoption of a hologenomics approach (i.e., considering both the plant genome and the genomes of all microorganisms colonizing the plant) can significantly advance our understanding of plant resistance and resilience to biotic and abiotic stresses. This approach can offer improved solutions for agronomic challenges in the future. Furthermore, within this context, we identify key knowledge gaps within the discipline and propose frameworks that may be employed in the future to harness plant–microbial interactions effectively, leading to a sustainable increase in farm productivity.

Plant-associated microorganisms during the reproductive period best predict sorghum yield and quality

ContextCrop plants are intimately associated with an enormous diversity of microbiota that profoundly influence their productivity, but the contribution of plant-microbiome interactions to grain yield and quality of sorghum during different developmental stages remains unclear. ObjectivesThe aim of this study was to evaluate the relative importance of sorghum-associated bacterial and fungal communities in different compartments in predicting sorghum grain yield and quality. MethodsWe collected soil and sorghum plant samples from various compartments during the vegetative (jointing and heading stages) and reproductive (filling and maturity stages) periods of a long-term field experiment with multiple fertilization regimes. The sorghum-microbiomes in different compartments, including phyllosphere, leaf endosphere, stem endosphere, root endosphere and rhizosphere, were characterized using bacterial 16 S rRNA gene and fungal ITS region sequencing. ResultsMicrobial diversity at the filling and maturity stages was higher than that at the heading and jointing stages. Microbial community composition during the reproductive period was distinct from that during the vegetative period, and the microbial co-occurrence network was more stable and complex during the reproductive period. Random forest analysis revealed that the microbiome during the reproductive period had a greater impact on grain yield and protein content than during the vegetative period. In predicting sorghum grain yield and protein content, the microbiomes in the root endosphere and rhizosphere were more important than other compartments. Both bacterial and fungal community in these compartments played an equal role. ConclusionsThese findings highlight the importance of bacterial and fungal communities during the reproductive period for grain yield and quality formation in sorghum, with profound implications for developing new microbiome-based strategies to promote plant performance and sustainable agriculture.

Rice bacterial leaf blight drives rhizosphere microbial assembly and function adaptation.

Rice bacterial leaf blight (BLB) is the most destructive phyllosphere bacterial disease caused by Xanthomonas oryzae pv. oryzae. The effect of soil-borne diseases on the rhizosphere microbiome has been extensively investigated. However, the regulatory role of the phyllosphere disease BLB on the rhizosphere microbiome remains unclear. Here, we observed that BLB significantly altered the composition of the bacterial-fungal community in the rhizosphere, decreasing bacterial diversity but not fungal diversity. The scale of inter-kingdom networks in the rhizosphere microbiome of BLB-infected plants was more complex and broader than in healthy plants, while the bacterial community was more vulnerable to BLB than the fungal community. Indeed, the relative abundance of Streptomyces, Chitinophaga, Sphingomonas, and Bacillus was higher in the BLB rhizosphere, which can be explained by their keystone hub taxa status in the rhizosphere co-occurrence network. Null model analysis showed that the deterministic assembly of bacterial communities increased while that of fungi decreased. Additionally, the assembly of bacterial and fungal communities was significantly related to variations in BLB and soil nutrients, especially pH and available phosphorus. Random forest model results showed that the bacterial community in the rhizosphere had a strong potential for predicting BLB. Metagenomic analysis revealed that BLB had a considerable impact on the functional adaptation of the rhizosphere microbiome. Interestingly, the abundance of some functional genes involved in carbon, phosphorus, and methane metabolism increased drastically.IMPORTANCEOur results suggest that rhizosphere bacteria are more sensitive to bacterial leaf blight (BLB) than fungi. BLB infection decreased the diversity of the rhizosphere bacterial community but increased the complexity and size of the rhizosphere microbial community co-occurrence networks. In addition, the relative abundance of the genera Streptomyces, Chitinophaga, Sphingomonas, and Bacillus increased significantly. Finally, these findings contribute to the understanding of plant-microbiome interactions by providing critical insight into the ecological mechanisms by which rhizosphere microbes respond to phyllosphere diseases. In addition, it also lays the foundation and provides data to support the use of plant microbes to promote plant health in sustainable agriculture, providing critical insight into ecological mechanisms.

Plant beneficial microbiome a boon for improving multiple stress tolerance in plants.

Beneficial microbes or their products have been key drivers for improving adaptive and growth features in plants under biotic and abiotic stress conditions. However, the majority of these studies so far have been utilized against individual stressors. In comparison to individual stressors, the combination of many environmental stresses that plants experience has a greater detrimental effect on them and poses a threat to their existence. Therefore, there is a need to explore the beneficial microbiota against combined stressors or multiple stressors, as this will offer new possibilities for improving plant growth and multiple adaptive traits. However, recognition of the multifaceted core beneficial microbiota from plant microbiome under stress combinations will require a thorough understanding of the functional and mechanistic facets of plant microbiome interactions under different environmental conditions in addition to agronomic management practices. Also, the development of tailored beneficial multiple stress tolerant microbiota in sustainable agriculture necessitates new model systems and prioritizes agricultural microbiome research. In this review, we provided an update on the effect of combined stressors on plants and their microbiome structure. Next, we discussed the role of beneficial microbes in plant growth promotion and stress adaptation. We also discussed how plant-beneficial microbes can be utilized for mitigating multiple stresses in plants. Finally, we have highlighted some key points that warrant future investigation for exploring plant microbiome interactions under multiple stressors.

Impact of conservation tillage on wheat performance and its microbiome.

Winter wheat is an important cereal consumed worldwide. However, current management practices involving chemical fertilizers, irrigation, and intensive tillage may have negative impacts on the environment. Conservation agriculture is often presented as a sustainable alternative to maintain wheat production, favoring the beneficial microbiome. Here, we evaluated the impact of different water regimes (rainfed and irrigated), fertilization levels (half and full fertilization), and tillage practices (occasional tillage and no-tillage) on wheat performance, microbial activity, and rhizosphere- and root-associated microbial communities of four winter wheat genotypes (Antequera, Allez-y, Apache, and Cellule) grown in a field experiment. Wheat performance (i.e., yield, plant nitrogen concentrations, and total nitrogen uptake) was mainly affected by irrigation, fertilization, and genotype, whereas microbial activity (i.e., protease and alkaline phosphatase activities) was affected by irrigation. Amplicon sequencing data revealed that habitat (rhizosphere vs. root) was the main factor shaping microbial communities and confirmed that the selection of endophytic microbial communities takes place thanks to specific plant-microbiome interactions. Among the experimental factors applied, the interaction of irrigation and tillage influenced rhizosphere- and root-associated microbiomes. The findings presented in this work make it possible to link agricultural practices to microbial communities, paving the way for better monitoring of these microorganisms in the context of agroecosystem sustainability.

Zinc accumulation in Atriplex lentiformis is driven by plant genes and the soil microbiome

Successful phytoremediation of acidic metal-contaminated mine tailings requires amendments to condition tailings properties prior to plant establishment. This conditioning process is complex and includes multiple changes in tailings bio-physico-chemical properties. The objective of this project is to identify relationships between tailings properties, the soil microbiome, and plant stress response genes during growth of Atriplex lentiformis in compost-amended (10 %, 15 %, 20 % w/w) mine tailings. Analyses include RNA-Seq for plant root gene expression, 16S rRNA amplicon sequencing for bacterial/archaeal communities, metal concentrations in both tailings and plant organs, and phenotypic measures of plant stress. Zn accumulation in A. lentiformis leaves varied with compost levels and was the highest in the intermediate treatment (15 %, TC15). Microbial analysis identified Alicyclobacillus, Hydrotalea, and Pseudolabrys taxa with the highest relative abundance in TC15, and these taxa were strongly associated with Zn accumulation. Furthermore, we identified 190 root genes with significant gene expression changes. These root genes were associated with different pathways including, abscisic acid and auxin signaling, defense responses, ion channels, metal ion binding, oxidative stress, transcription regulation, and transmembrane transport. However, root gene expression changes were not driven by the increasing levels of compost. For example, there were 15 genes that were up-regulated in TC15, whereas 106 genes were down-regulated in TC15. The variables analyzed explained 86 % of the variance in Zn accumulation in A. lentiformis leaves. Importantly, Zn accumulation was driven by Zn shoot concentrations, leaf stress symptoms, plant root genes, and microbial taxa. Therefore, our results suggest there are strong plant-microbiome associations that drive Zn accumulation in A. lentiformis and different plant gene pathways are involved in alleviating varying levels of metal stress. Future work is needed to gain a mechanistic understanding of these plant-microbiome interactions to optimize phytoremediation strategies as they will govern the success or failure of the revegetation process.

Pioneer Arabidopsis thaliana spans the succession gradient revealing a diverse root-associated microbiome

BackgroundSoil microbiomes are increasingly acknowledged to affect plant functioning. Research in molecular model species Arabidopsis thaliana has given detailed insights of such plant-microbiome interactions. However, the circumstances under which natural A. thaliana plants have been studied so far might represent only a subset of A. thaliana’s full ecological context and potential biotic diversity of its root-associated microbiome.ResultsWe collected A. thaliana root-associated soils from a secondary succession gradient covering 40 years of land abandonment. All field sites were situated on the same parent soil material and in the same climatic region. By sequencing the bacterial and fungal communities and soil abiotic analysis we discovered differences in both the biotic and abiotic composition of the root-associated soil of A. thaliana and these differences are in accordance with the successional class of the field sites. As the studied sites all have been under (former) agricultural use, and a climatic cline is absent, we were able to reveal a more complete variety of ecological contexts A. thaliana can appear and sustain in.ConclusionsOur findings lead to the conclusion that although A. thaliana is considered a pioneer plant species and previously almost exclusively studied in early succession and disturbed sites, plants can successfully establish in soils which have experienced years of ecological development. Thereby, A. thaliana can be exposed to a much wider variation in soil ecological context than is currently presumed. This knowledge opens up new opportunities to enhance our understanding of causal plant-microbiome interactions as A. thaliana cannot only grow in contrasting soil biotic and abiotic conditions along a latitudinal gradient, but also when those conditions vary along a secondary succession gradient. Future research could give insights in important plant factors to grow in more ecologically complex later-secondary succession soils, which is an impending direction of our current agricultural systems.

Foliar fungal communities in agroecosystems depend on crop identity and neighboring vegetation

Agricultural intensification causes plant diversity loss and environmental homogenization, which may result in changes to plant-microbiome interactions mediating plant growth and stress tolerance. We hypothesized that foliar fungal microbiomes would depend on plant traits and environmental filters, constrained by neighboring vegetation expected to serve as a fungal source. Thus, we sampled foliar fungi from four crops (three annual and one perennial), four sites per crop, and three varieties per annual crop, across a 500-km expanse in North Carolina, USA and tested the role of host traits, environmental traits, and vegetative landcover on foliar fungal community structure. Crop species and site were major determinants of community structure, primarily due to differences in plant size and growing season. Site consistently explained 10× more variation in community structure than host variety across the annual crops. Finally, reduced natural vegetative cover surrounding farms was correlated with decreased fungal richness and more homogeneous microbiome assembly. Based on these results, we posit that foliar fungal assembly in crops results from host and environmental filters acting on inputs from the nearby vegetation. Future efforts at agricultural microbiome management must therefore consider landscape management and will require an improved understanding of how agricultural intensification alters microbial source pools.

Impact of Two Phosphorus Fertilizer Formulations on Wheat Physiology, Rhizosphere, and Rhizoplane Microbiota.

Phosphorus (P) is the second most important macronutrient for crop growth and a limiting factor in food production. Choosing the right P fertilizer formulation is important for crop production systems because P is not mobile in soils, and placing phosphate fertilizers is a major management decision. In addition, root microorganisms play an important role in helping phosphorus fertilization management by regulating soil properties and fertility through different pathways. Our study evaluated the impact of two phosphorous formulations (polyphosphates and orthophosphates) on physiological traits of wheat related to yield (photosynthetic parameters, biomass, and root morphology) and its associated microbiota. A greenhouse experiment was conducted using agricultural soil deficient in P (1.49%). Phenotyping technologies were used at the tillering, stem elongation, heading, flowering, and grain-filling stages. The evaluation of wheat physiological traits revealed highly significant differences between treated and untreated plants but not between phosphorous fertilizers. High-throughput sequencing technologies were applied to analyse the wheat rhizosphere and rhizoplane microbiota at the tillering and the grain-filling growth stages. The alpha- and beta-diversity analyses of bacterial and fungal microbiota revealed differences between fertilized and non-fertilized wheat, rhizosphere, and rhizoplane, and the tillering and grain-filling growth stages. Our study provides new information on the composition of the wheat microbiota in the rhizosphere and rhizoplane during growth stages (Z39 and Z69) under polyphosphate and orthophosphate fertilization. Hence, a deeper understanding of this interaction could provide better insights into managing microbial communities to promote beneficial plant-microbiome interactions for P uptake.

Presence of microbiome decreases fitness and modifies phenotype in the aquatic plant Lemna minor.

Plants live in close association with microbial organisms that inhabit the environment in which they grow. Much recent work has aimed to characterize these plant-microbiome interactions, identifying those associations that increase growth. Although most work has focused on terrestrial plants, Lemna minor, a floating aquatic angiosperm, is increasingly used as a model in host-microbe interactions and many bacterial associations have been shown to play an important role in supporting plant fitness. However, the ubiquity and stability of these interactions as well as their dependence on specific abiotic environmental conditions remain unclear. Here, we assess the impact of a full L. minor microbiome on plant fitness and phenotype by assaying plants from eight natural sites, with and without their microbiomes, over a range of abiotic environmental conditions. We find that the microbiome systematically suppressed plant fitness, although the magnitude of this effect varied among plant genotypes and depended on the abiotic environment. Presence of the microbiome also resulted in phenotypic changes, with plants forming smaller colonies and producing smaller fronds and shorter roots. Differences in phenotype among plant genotypes were reduced when the microbiome was removed, as were genotype by environment interactions, suggesting that the microbiome plays a role in mediating the plant phenotypic response to the environment.

Plant domestication shapes rhizosphere microbiome assembly and metabolic functions

BackgroundThe rhizosphere microbiome, which is shaped by host genotypes, root exudates, and plant domestication, is crucial for sustaining agricultural plant growth. Despite its importance, how plant domestication builds up specific rhizosphere microbiomes and metabolic functions, as well as the importance of these affected rhizobiomes and relevant root exudates in maintaining plant growth, is not well understood. Here, we firstly investigated the rhizosphere bacterial and fungal communities of domestication and wild accessions of tetraploid wheat using amplicon sequencing (16S and ITS) after 9 years of domestication process at the main production sites in China. We then explored the ecological roles of root exudation in shaping rhizosphere microbiome functions by integrating metagenomics and metabolic genomics approaches. Furthermore, we established evident linkages between root morphology traits and keystone taxa based on microbial culture and plant inoculation experiments.ResultsOur results suggested that plant rhizosphere microbiomes were co-shaped by both host genotypes and domestication status. The wheat genomes contributed more variation in the microbial diversity and composition of rhizosphere bacterial communities than fungal communities, whereas plant domestication status exerted much stronger influences on the fungal communities. In terms of microbial interkingdom association networks, domestication destabilized microbial network and depleted the abundance of keystone fungal taxa. Moreover, we found that domestication shifted the rhizosphere microbiome from slow growing and fungi dominated to fast growing and bacteria dominated, thereby resulting in a shift from fungi-dominated membership with enrichment of carbon fixation genes to bacteria-dominated membership with enrichment of carbon degradation genes. Metagenomics analyses further indicated that wild cultivars of wheat possess higher microbial function diversity than domesticated cultivars. Notably, we found that wild cultivar is able to harness rhizosphere microorganism carrying N transformation (i.e., nitrification, denitrification) and P mineralization pathway, whereas rhizobiomes carrying inorganic N fixation, organic N ammonification, and inorganic P solubilization genes are recruited by the releasing of root exudates from domesticated wheat. More importantly, our metabolite-wide association study indicated that the contrasting functional roles of root exudates and the harnessed keystone microbial taxa with different nutrient acquisition strategies jointly determined the aboveground plant phenotypes. Furthermore, we observed that although domesticated and wild wheats recruited distinct microbial taxa and relevant functions, domestication-induced recruitment of keystone taxa led to a consistent growth regulation of root regardless of wheat domestication status.ConclusionsOur results indicate that plant domestication profoundly influences rhizosphere microbiome assembly and metabolic functions and provide evidence that host plants are able to harness a differentiated ecological role of root-associated keystone microbiomes through the release of root exudates to sustain belowground multi-nutrient cycles and plant growth. These findings provide valuable insights into the mechanisms underlying plant-microbiome interactions and how to harness the rhizosphere microbiome for crop improvement in sustainable agriculture.CBzZNC2FEDswGcHctbDosaVideo

Diseased-induced multifaceted variations in community assembly and functions of plant-associated microbiomes.

Plant-associated microorganisms are believed to be part of the so-called extended plant phenotypes, affecting plant growth and health. Understanding how plant-associated microorganisms respond to pathogen invasion is crucial to controlling plant diseases through microbiome manipulation. In this study, healthy and diseased (bacterial wilt disease, BWD) tomato (Solanum lycopersicum L.) plants were harvested, and variations in the rhizosphere and root endosphere microbial communities were subsequently investigated using amplicon and shotgun metagenome sequencing. BWD led to a significant increase in rhizosphere bacterial diversity in the rhizosphere but reduced bacterial diversity in the root endosphere. The ecological null model indicated that BWD enhanced the bacterial deterministic processes in both the rhizosphere and root endosphere. Network analysis showed that microbial co-occurrence complexity was increased in BWD-infected plants. Moreover, higher universal ecological dynamics of microbial communities were observed in the diseased rhizosphere. Metagenomic analysis revealed the enrichment of more functional gene pathways in the infected rhizosphere. More importantly, when tomato plants were infected with BWD, some plant-harmful pathways such as quorum sensing were significantly enriched, while some plant-beneficial pathways such as streptomycin biosynthesis were depleted. These findings broaden the understanding of plant-microbiome interactions and provide new clues to the underlying mechanism behind the interaction between the plant microbiome and BWD.

Emerging Pathways for Engineering the Rhizosphere Microbiome for Optimal Plant Health

The increasing impacts of global climate change on crop performance pose a significant threat to global food security. The rhizosphere microbiomes intimately interact with the plant and can largely facilitate plants in growth promotion and stress resistance via multiple mechanisms. This review focuses on approaches for harnessing the rhizosphere microbiomes to produce beneficial effects toward enhanced crop productivity, including the use of organic and inorganic amendments, and microbial inoculants. Emerging methods, such as the utilization of synthetic microbial consortia, host-mediated microbiome engineering, prebiotics made from specific plant root exudates, and crop breeding to promote beneficial plant-microbiome interactions, are highlighted. Updating our knowledge in this field is critical for understanding and improving plant-microbiome interactions, thereby enhancing plant adaptiveness to changing environmental conditions.

Root exudate concentrations of indole-3-acetic acid (IAA) and abscisic acid (ABA) affect maize rhizobacterial communities at specific developmental stages.

Root exudates shape the rhizosphere microbiome, but little is known about the specific compounds in root exudates that are important. Here, we investigated the impacts of the plant-synthesized phytohormones indole-3-acetic acid (IAA) and abscisic acid (ABA) exuded by roots on the maize rhizobacterial communities. To identify maize genotypes that differed in the root exudate concentrations of IAA and ABA, we screened hundreds of inbred lines using a semi-hydroponic system. Twelve genotypes with variable exudate concentrations of IAA and ABA were selected for a replicated field experiment. Bulk soil, rhizosphere, and root endosphere samples were collected at two vegetative and one reproductive maize developmental stage. IAA and ABA concentrations in rhizosphere samples were quantified by liquid chromatography-mass spectrometry. The bacterial communities were analyzed by V4 16S rRNA amplicon sequencing. Results indicated that IAA and ABA concentrations in root exudates significantly affected the rhizobacterial communities at specific developmental stages. ABA impacted the rhizosphere bacterial communities at later developmental stages, whereas IAA affected the rhizobacterial communities at the vegetative stages. This study contributed to our knowledge about the influence that specific root exudate compounds have on the rhizobiome composition, showing that the phytohormones IAA and ABA exuded by roots have a role in the plant-microbiome interactions.

Linking microbial biogeochemical cycling genes to the rhizosphere of pioneering plants in a glacier foreland

Glacier retreat raises global concerns but brings about the moment to study soil and ecosystem development. In nutrient-limited glacier forelands, the adaptability of pioneering plant and microbial species is facilitated by their interactions, including rhizosphere effects, but the details of this adaptability are not yet understood. In the rhizosphere of five pioneering plants, we comprehensively deciphered the microbial taxonomic and functional compositions. Two nitrogen-fixing microbial genera, Bradyrhizobium and Mesorhizobium, were among the most abundant taxa in the rhizomicrobiome. Moreover, several rhizobial genera, including Rhizobium, Pararhizobium, Allohrizobium, and Sinorhizobium, head the list of major modules in microbial co-occurrence networks, highlighting the vital roles of nitrogen-cycling taxa in the rhizomicrobiome of pioneering plants. Microbial genes involved in nitrogen, sulfur, phosphorus, and methane cycles were simultaneously correlated with microbial community dissimilarity, and 12 functional pathways were detected with distinct relative abundances among soils. Zooming in on the nitrogen-cycling genes, nifW, narC, nasA, nasB, and nirA were mainly responsible for the significant differences between soils. Furthermore, soil pH and the carbon/nitrogen ratio were among the topsoil properties interacting with nitrogen and sulfur cycling gene dissimilarity. These results explicitly linked biogeochemical cycling genes to the rhizomicrobiome and soil properties, revealing the roles of these genes as microbial drivers in mediating rhizosphere soil–plant–microbiome interactions.