Spatially distributed metabolites SWEETen the root for microbes.

Limited understanding exists on the spatial configuration of underground plant-microbe interactions. In this issue of Cell Host & Microbe, Loo et al. illustrate the sugar transporter-involved interdependent interaction between root metabolites and microbial spatial colonization, providing insights into metabolic-associated organization of plant-microbe interactions.

Streptomyces-triggered coordination between rhizosphere microbiomes and plant transcriptome enables watermelon Fusarium wilt resistance.

The use of microbial inoculant is a promising strategy to improve plant health, but their efficiency often faces challenges due to difficulties in successful microbial colonization in soil environments. To this end, the application of biostimulation products derived from microbes is expected to resolve these barriers via direct interactions with plants or soil pathogens. However, their effectiveness and mechanisms for promoting plant growth and disease resistance remain elusive. In this study, we showed that root irrigation with the extracts of Streptomyces ahygroscopicus strain 769 (S769) solid fermentation products significantly reduced watermelon Fusarium wilt disease incidence by 30% and increased the plant biomass by 150% at a fruiting stage in a continuous cropping field. S769 treatment led to substantial changes in both bacterial and fungal community compositions, and induced a highly interconnected microbial association network in the rhizosphere. The root transcriptome analysis further suggested that S769 treatment significantly improved the expression of the MAPK signalling pathway, plant hormone signal transduction and plant-pathogen interactions, particular those genes related to PR-1 and ethylene, as well as genes associated with auxin production and reception. Together, our study provides mechanistic and empirical evidences for the biostimulation products benefiting plant health through coordinating plant and rhizosphere microbiome interaction.

Microbial species pool-mediated diazotrophic community assembly in crop microbiomes during plant development.

Plant-associated diazotrophs strongly relate to plant nitrogen (N) supply and growth. However, our knowledge of diazotrophic community assembly and microbial N metabolism in plant microbiomes is largely limited. Here we examined the assembly and temporal dynamics of diazotrophic communities across multiple compartments (soils, epiphytic and endophytic niches of root and leaf, and grain) of three cereal crops (maize, wheat, and barley) and identified the potential N-cycling pathways in phylloplane microbiomes. Our results demonstrated that the microbial species pool, influenced by site-specific environmental factors (e.g., edaphic factors), had a stronger effect than host selection (i.e., plant species and developmental stage) in shaping diazotrophic communities across the soil-plant continuum. Crop diazotrophic communities were dominated by a few taxa (~0.7% of diazotrophic phylotypes) which were mainly affiliated with Methylobacterium, Azospirillum, Bradyrhizobium, and Rhizobium. Furthermore, eight dominant taxa belonging to Azospirillum and Methylobacterium were identified as keystone diazotrophic taxa for three crops and were potentially associated with microbial network stability and crop yields. Metagenomic binning recovered 58 metagenome-assembled genomes (MAGs) from the phylloplane, and the majority of them were identified as novel species (37 MAGs) and harbored genes potentially related to multiple N metabolism processes (e.g., nitrate reduction). Notably, for the first time, a high-quality MAG harboring genes involved in the complete denitrification process was recovered in the phylloplane and showed high identity to Pseudomonas mendocina. Overall, these findings significantly expand our understanding of ecological drivers of crop diazotrophs and provide new insights into the potential microbial N metabolism in the phyllosphere.IMPORTANCEPlants harbor diverse nitrogen-fixing microorganisms (i.e., diazotrophic communities) in both belowground and aboveground tissues, which play a vital role in plant nitrogen supply and growth promotion. Understanding the assembly and temporal dynamics of crop diazotrophic communities is a prerequisite for harnessing them to promote plant growth. In this study, we show that the site-specific microbial species pool largely shapes the structure of diazotrophic communities in the leaves and roots of three cereal crops. We further identify keystone diazotrophic taxa in crop microbiomes and characterize potential microbial N metabolism pathways in the phyllosphere, which provides essential information for developing microbiome-based tools in future sustainable agricultural production.

Dynamic root microbiome sustains soybean productivity under unbalanced fertilization.

Root-associated microbiomes contribute to plant growth and health, and are dynamically affected by plant development and changes in the soil environment. However, how different fertilizer regimes affect quantitative changes in microbial assembly to effect plant growth remains obscure. Here, we explore the temporal dynamics of the root-associated bacteria of soybean using quantitative microbiome profiling (QMP) to examine its response to unbalanced fertilizer treatments (i.e., lacking either N, P or K) and its role in sustaining plant growth after four decades of unbalanced fertilization. We show that the root-associated bacteria exhibit strong succession during plant development, and bacterial loads largely increase at later stages, particularly for Bacteroidetes. Unbalanced fertilization has a significant effect on the assembly of the soybean rhizosphere bacteria, and in the absence of N fertilizer the bacterial community diverges from that of fertilized plants, while lacking P fertilizer impedes the total load and turnover of rhizosphere bacteria. Importantly, a SynCom derived from the low-nitrogen-enriched cluster is capable of stimulating plant growth, corresponding with the stabilized soybean productivity in the absence of N fertilizer. These findings provide new insights in the quantitative dynamics of the root-associated microbiome and highlight a key ecological cluster with prospects for sustainable agricultural management.

Salinity-dependent potential soil fungal decomposers under straw amendment.

Soil salinization is a severe environmental problem that restricts plant productivity and ecosystem functioning. Straw amendment could increase the fertility of saline soils by improving microbial activity and carbon sequestration, however, the adaptation and ecological preference of potential fungal decomposers after straw addition under varied soil salinities remains elusive. Here, a soil microcosm study was conducted by incorporating wheat and maize straws into soils with a range of salinities, respectively. We showed that the amendment of straws increased MBC, SOC, DOC and NH4+-N contents by 75.0 %, 17.2 %, 88.3 % and 230.9 %, respectively, but decreased NO3--N content by 79.0 %, irrespective of soil salinity, with intensified connections among these parameters after straw addition. Although soil salinity had a more profound effect on both fungal α- and ß-diversity, straw amendment also significantly reduced fungal Shannon diversity and changed community composition, especially for severe saline soil. Complexity of the fungal co-occurrence network was specifically strengthened after straw addition, with average degree increasing from 11.9 in the control to 22.0 and 22.7 in wheat and maize straw treatments, respectively. Intriguingly, there was very little overlap among the straw-enriched ASVs (Amplicon Sequence Variants) in each saline soil, indicating the soil-specific involvement of potential fungal decomposers. Particularly, fungal species belonging to Cephalotrichum and unclassified Sordariales were the most responsive to straw addition in severe saline soil, whereas light saline soil supported the enrichment of Coprinus and Schizothecium species after straw addition. Together, our study provides a new insight on the common and specific responses of soil chemical and biological characteristics at different salinity levels under straw management, which will help guide precise microbial-based strategies to boost straw decomposition in future agricultural practice and environmental management of saline-alkali lands.

Harnessing biological nitrogen fixation in plant leaves.

The importance of biological nitrogen fixation (BNF) in securing food production for the growing world population with minimal environmental cost has been increasingly acknowledged. Leaf surfaces are one of the biggest microbial habitats on Earth, harboring diverse free-living N2-fixers. These microbes inhabit the epiphytic and endophytic phyllosphere and contribute significantly to plant N supply and growth. Here, we summarize the contribution of phyllosphere-BNF to global N cycling, evaluate the diversity of leaf-associated N2-fixers across plant hosts and ecosystems, illustrate the ecological adaptation of N2-fixers to the phyllosphere, and identify the environmental factors driving BNF. Finally, we discuss potential BNF engineering strategies to improve the nitrogen uptake in plant leaves and thus sustainable food production.

Reclamation effects of distinct volumes and concentrations of CaCl2-amended brackish ice in different saline-sodic soils.

The proper usage of marginal soil and water resources has major implications for the sustainability of agriculture, such as brackish water and saline-sodic soils. The saline soils can be ameliorated though melting process of calcium-containing brackish ice, however, the optimum concentration and volume of brackish ice (water) for the reclamation of different saline-sodic soils remain to be determined. In this study, 108 soil columns representing four Ice salinity levels (16, 26, 36, 46 mmolc L-1) and three Pore Volumes (2/3, 1.5, 2.5 PV) of calcium-amended brackish ice were tested to reveal the reclaiming effect on a range of saline-sodic soils. The linear mixed model (LMM), multiple regression equation, and principal coordinate analysis (PCoA) were applied to calculate the amelioration effect in terms of three factors: Ice volume, Ice salinity and Column depth. Our results showed that the soil salinity and sodicity generally decreased with increasing Ice volume and Ice salinity, and the saline-sodic soils with low exchangeable sodium percentages (i.e. ESP 20) were more sensitive to Ice salinity, with high salinity (26-46 mmolc L-1) and large volume (2.5 PV) of brackish ice reaching a better amelioration effect. The effect of Ice volume became more dominant in medium and high ESP soils (ESP 40 and ESP 70), whereas the high salinity combined with low volume of brackish ice would lead to worse soil properties, especially at the bottom layers. Meanwhile, the Column depth factor had a considerable effect on the soil chemical properties, with the variance explained ranging from 18.6% to 36.0%. These results provide theoretical guidance in the rational use of calcium-amended brackish ice and highlight the necessity to take layer effect into consideration for reclaiming saline-sodic soils.

Fumigation practice combined with organic fertilizer increase antibiotic resistance in watermelon rhizosphere soil.

Chemical fumigants and organic fertilizer are commonly used in facility agriculture to control soil-borne diseases and promote soil health. However, there is a lack of evidence for the effect of non-antibiotic fumigants on the distribution of antibiotic resistance genes (ARGs) in plant rhizosphere soils. Here, the response of a wide spectrum of ARGs and mobile genetic elements (MGEs) to dazomet fumigation practice in the rhizosphere soil of watermelon was investigated along its branching, flowering and fruiting growth stages in plastic shelters using high-throughput quantitative PCR approach. Our results indicated that soil fumigation combined with organic fertilizer application significantly increased the relative abundance of ARGs and MGEs in the rhizosphere soil of watermelon plant. The positive correlations between the relative abundance of ARGs and MGEs suggested that soil fumigation might increase the horizontal gene transfer (HGT) potential of ARGs. This result was further confirmed by the enhanced associations between ARG and MGE subtypes in the networks of fumigation treatments. Moreover, bipartite associations between ARGs/MGEs and microbial communities (bacteria and fungi) revealed a higher percentage of linkage between MGEs and microbial taxa in the fumigated soils. Structural equation model analysis further suggested that the increases in antibiotic resistance after fumigation and organic fertilizer application were mainly driven by MGEs and fungal community. Together, our results provide vital evidence that dazomet fumigation process combined with organic fertilizer in plastic shelters has the great potential to promote ARGs' dissemination in the rhizosphere, and raise cautions of the acquired resistance by soil-borne fungal pathogen and the potential spreading of ARGs along soil-plant continuum.

Plant developmental stage drives the differentiation in ecological role of the maize microbiome.

BACKGROUND: Plants live with diverse microbial communities which profoundly affect multiple facets of host performance, but if and how host development impacts the assembly, functions and microbial interactions of crop microbiomes are poorly understood. Here we examined both bacterial and fungal communities across soils, epiphytic and endophytic niches of leaf and root, and plastic leaf of fake plant (representing environment-originating microbes) at three developmental stages of maize at two contrasting sites, and further explored the potential function of phylloplane microbiomes based on metagenomics. RESULTS: Our results suggested that plant developmental stage had a much stronger influence on the microbial diversity, composition and interkingdom networks in plant compartments than in soils, with the strongest effect in the phylloplane. Phylloplane microbiomes were co-shaped by both plant growth and seasonal environmental factors, with the air (represented by fake plants) as its important source. Further, we found that bacterial communities in plant compartments were more strongly driven by deterministic processes at the early stage but a similar pattern was for fungal communities at the late stage. Moreover, bacterial taxa played a more important role in microbial interkingdom network and crop yield prediction at the early stage, while fungal taxa did so at the late stage. Metagenomic analyses further indicated that phylloplane microbiomes possessed higher functional diversity at the early stage than the late stage, with functional genes related to nutrient provision enriched at the early stage and N assimilation and C degradation enriched at the late stage. Coincidently, more abundant beneficial bacterial taxa like Actinobacteria, Burkholderiaceae and Rhizobiaceae in plant microbiomes were observed at the early stage, but more saprophytic fungi at the late stage. CONCLUSIONS: Our results suggest that host developmental stage profoundly influences plant microbiome assembly and functions, and the bacterial and fungal microbiomes take a differentiated ecological role at different stages of plant development. This study provides empirical evidence for host exerting strong effect on plant microbiomes by deterministic selection during plant growth and development. These findings have implications for the development of future tools to manipulate microbiome for sustainable increase in primary productivity. Video Abstract.

Soil bacterial microbiota predetermines rice yield in reclaiming saline-sodic soils leached with brackish ice.

BACKGROUND: Saline-sodic lands threaten the food supply and ecological security in the western Songnen Plain of northeast China, and the gypsum is commonly adopted for restoration. However, the dynamics of soil bacterial community and the correlation with crop yield during restoring processes remain poorly understood. Here, we elucidated the soil chemical properties and bacterial communities and their associations with rice yield under different flue gas desulphurization gypsum (FGDG) application rates combined with brackish ice leaching. RESULTS: The increased application rate of FGDG generally improved soil reclamation effects, as indicated by soil chemical properties, bacterial diversity, and rice yield. Compared with fresh ice irrigation, the rice yield in brackish ice treatment increased by 15.84%, and the soil alkalinity and sodium adsorption ratio (SAR) decreased by 35.19% and 10.30%, respectively. The bacterial alpha diversity significantly correlated and predicted rice yield as early as brackish ice melt, suggesting the bacterial diversity was a sensitive indicator in predicting rice yield. Meanwhile, the bacterial communities in the control possessed a high abundance of oligotrophic Firmicutes, while eutrophic bacterial taxa (e.g. Proteobacteria) were enriched after brackish water irrigation and FGDG application. Moreover, we also established a Random Forest model and identified a bacterial consortium that explained an 80.0% variance of rice yield. CONCLUSION: Together, our results highlight the reclaiming effect of brackish ice in the saline-sodic field and demonstrate the sensitivity and importance of the soil bacterial community in predicting crop yield, which would provide essential knowledge on the soil quality indication and bio-fertilizer development for soil reclamation. © 2021 Society of Chemical Industry.

Rare taxa maintain the stability of crop mycobiomes and ecosystem functions.

Plants harbour highly diverse mycobiomes which sustain essential functions for host health and productivity. However, ecological processes that govern the plant-mycobiome assembly, interactions and their impact on ecosystem functions remain poorly known. Here we characterized the ecological role and community assembly of both abundant and rare fungal taxa along the soil-plant continuums (rhizosphere, phyllosphere and endosphere) in the maize-wheat/barley rotation system under different fertilization practices at two contrasting sites. Our results indicate that mycobiome assembly is shaped predominantly by compartment niche and host species rather than by environmental factors. Moreover, crop-associated fungal communities are dominated by few abundant taxa mainly belonging to Sordariomycetes and Dothideomycetes, while the majority of diversity within mycobiomes are represented by rare taxa. For plant compartments, the abundant sub-community is mainly determined by stochastic processes. In contrast, the rare sub-community is more sensitive to host selection and mainly governed by deterministic processes. Furthermore, our results demonstrate that rare taxa play an important role in fungal co-occurrence network and ecosystem functioning like crop yield and soil enzyme activities. These results significantly advance our understanding of crop mycobiome assembly and highlight the key role of rare taxa in sustaining the stability of crop mycobiomes and ecosystem functions.

Host selection shapes crop microbiome assembly and network complexity.

Plant microbiomes are essential to host health and productivity but the ecological processes that govern crop microbiome assembly are not fully known. Here we examined bacterial communities across 684 samples from soils (rhizosphere and bulk soil) and multiple compartment niches (rhizoplane, root endosphere, phylloplane, and leaf endosphere) in maize (Zea mays)-wheat (Triticum aestivum)/barley (Hordeum vulgare) rotation system under different fertilization practices at two contrasting sites. Our results demonstrate that microbiome assembly along the soil-plant continuum is shaped predominantly by compartment niche and host species rather than by site or fertilization practice. From soils to epiphytes to endophytes, host selection pressure sequentially increased and bacterial diversity and network complexity consequently reduced, with the strongest host effect in leaf endosphere. Source tracking indicates that crop microbiome is mainly derived from soils and gradually enriched and filtered at different plant compartment niches. Moreover, crop microbiomes were dominated by a few dominant taxa (c. 0.5% of bacterial phylotypes), with bacilli identified as the important biomarker taxa for wheat and barley and Methylobacteriaceae for maize. Our work provides comprehensive empirical evidence on host selection, potential sources and enrichment processes for crop microbiome assembly, and has important implications for future crop management and manipulation of crop microbiome for sustainable agriculture.