Plant-microbe Interactions Research Articles

Benefits of symbiotic ectomycorrhizal fungi to plant water relations depend on plant genotype in pinyon pine

Rhizosphere microbes, such as root-associated fungi, can improve plant access to soil resources, affecting plant health, productivity, and stress tolerance. While mycorrhizal associations are ubiquitous, plant–microbe interactions can be species specific. Here we show that the specificity of the effects of microbial symbionts on plant function can go beyond species level: colonization of roots by ectomycorrhizal fungi (EMF) of the genus Geopora has opposite effects on water uptake, and stomatal control of desiccation in drought tolerant and intolerant genotypes of pinyon pine (Pinus edulis Engelm.). These results demonstrate, for the first time, that microorganisms can have significant and opposite effects on important plant functional traits like stomatal control of desiccation that are associated with differential mortality and growth in nature. They also highlight that appropriate pairing of plant genotypes and microbial associates will be important for mitigating climate change impacts on vegetation.

Plant-microbe interactions: mechanisms and applications for improving crop yield and quality

In light of the dual challenges posed by climate change and the burgeoning global population, which are putting food security at risk, there is an urgent need to develop sustainable agricultural innovations. These innovations must be capable of increasing crop productivity and maintaining soil health, reducing our dependence on synthetic agrochemical inputs, and preserving the nutritional quality of our food crops. It is crucial to delve into the biological and physiological processes that underlie plant-microbe interactions. Such knowledge is paramount in harnessing the advantages of these interactions for sustainable agriculture. This review delves into the intricate mechanisms through which beneficial rhizosphere and soil bacteria, known as plant growth-promoting bacteria (PGPB), contribute to enhancing crop yields, bolstering stress resilience, and improving the nutritional quality of crops. We explore the vital capabilities of PGPB, encompassing nitrogen fixation, phosphorus solubilization, iron chelation through microbial siderophores, and modulation of hormonal signaling pathways. The PGPB taxa in focus include rhizobial diazotrophs (genera Rhizobium, Bradyrhizobium) and diverse heterotrophic genera (Azotobacter, Bacillus, Pseudomonas). Recent studies have provided compelling evidence of the effectiveness of PGPB in biofortification interventions, which involve enriching essential micronutrients in crops through microbial enhancement of nutrient mobilization, uptake, translocation, and acquisition. Understanding the genomic and metabolic mechanisms that govern plant growth promotion, abiotic stress tolerance, pathogen inhibition, and biofortification by PGPR is pivotal. Such insights can inform endeavors to optimize, formulate, and apply tailored PGPR inoculants. Adopting a systems perspective that acknowledges the intricate interactions among plants, microbes, and soil in this context is essential. Furthermore, we advocate for continued research in various domains, including microbiota recruitment, PGPR screening, the cumulative effects of various approaches, developing effective delivery systems, field testing, and integrating these findings with breeding programs. Interdisciplinary collaboration among microbial ecologists, plant physiologists, crop scientists, and farmers will be instrumental in unlocking the full potential of plant-microbe associations to ensure sustainable agriculture and food crop quality. In summary, more profound insights into PGPB biology and their interactions with plants offer a promising path toward enhancing productivity and sustainability in the face of escalating demands.

Assembly, diversity and coexistence of bacteria communities in various rhizocompartment niches in Sorghum Cultivars

Root-associated microbial communities play a vital role in plant health, but the assembly processes in sorghum and associated soil factors remain unclear. We conducted 16S rDNA sequencing on bulk soils and rhizocompartments (rhizosphere, rhizoplane, and endosphere) of three sorghum cultivars. Physicochemical properties were measured in bulk and rhizosphere soils. Alpha-diversity decreased from bulk soil to endosphere, and beta-diversity showed compartmental separation. Relative abundances of 16 dominant genera varied among compartments and cultivars. Dispersal limitation increased from (17.0%) to endosphere (35.8%), with homogenous selection dominating rhizocompartment assembly (51.1%–83.0%). Certain soil factors mediated community assembly and shaped phylogenetic structures. Rhizosphere displayed the most complex network, followed by bulk soil, rhizoplane, and endosphere. Differentially abundant taxa were more important in maintaining network stability and connectivity in the endosphere (47.0%–68.4%) compared to the other rhizocompartments. This study provides insights into the factors influencing the assembly of root-associated bacterial communities in sorghum, highlighting the roles of compartment niches, sorghum cultivars, and soil properties. These findings contribute to our understanding of plant-microbe interactions and have implications for agricultural management and ecological restoration efforts. Furthermore, the identification of key soil factors that mediate community assembly processes and shape phylogenetic structures offers potential targets for manipulating microbial communities in agricultural systems, leading to improved plant health and productivity.

Nodulation number tempers the relative importance of stochastic processes in the assembly of soybean root-associated communities

Identifying the ecological forces that structure root-associated microbial communities is an essential step toward more sustainable agriculture. Legumes are widely utilized as model plants to study selective forces and their functioning in plant-microbial interactions owing to their ability to establish mutualism with rhizobia. Root nodules act as symbiotic organs to optimize the cost-benefit balance in this mutualistic relationship by modulating the number of nodules. However, it is not known whether the number of nodules is related to the structure of root-associated bacterial communities. Here, the root-associated bacterial communities of soybean grown in native soil by means of soybean cultivars with super- or normal nodulation were investigated across four developmental stages. We compared ecological processes between communities and found decreased relative importance of neutral processes for super-nodulating soybean, although the overall structures resembled those of normal-nodulating soybean. We identified the generalist core bacterial populations in each root-associated compartment, that are shared across root-associated niches, and persist through developmental stages. Within core bacterial species, the relative abundances of bacterial species in the rhizosphere microbiome were linked to host-plant functional traits and can be used to predict these traits from microbes using machine learning algorithms. These findings broaden the comprehensive understanding of the ecological forces and associations of microbiotas in various root-associated compartments and provide novel insights to integrate beneficial plant microbiomes into agricultural production to enhance plant performance.

The CAP superfamily protein PsCAP1 secreted by Phytophthora triggers immune responses in Nicotiana benthamiana through a leucine-rich repeat receptor-like protein.

The role of cysteine-rich secretory proteins, antigen 5, and pathogenesis-related 1 (CAP) superfamily proteins in the innate immune responses of mammals is well characterized. However, the biological function of CAP superfamily proteins in plant-microbe interactions is poorly understood. We used proteomics and transcriptome analyses to dissect the apoplastic effectors secreted by the oomycete Phytophthora sojae during early infection of soybean leaves. By transiently expressing these effectors in Nicotiana benthamiana, we identified PsCAP1, a novel type of secreted CAP protein that triggers immune responses in multiple solanaceous plants including N. benthamiana. This secreted CAP protein is conserved among oomycetes, and multiple PsCAP1 homologs can be recognized by N. benthamiana. PsCAP1-triggered immune responses depend on the N-terminal immunogenic fragment (aa 27-151). Pretreatment of N. benthamiana with PsCAP1 or the immunogenic fragment increases plant resistance against Phytophthora. The recognition of PsCAP1 and different homologs requires the leucine-rich repeat receptor-like protein RCAP1, which associates with two central receptor-like kinases BRI1-associated receptor kinase 1 (BAK1) and suppressor of BIR1-1 (SOBIR1) in planta. These findings suggest that the CAP-type apoplastic effectors act as an important player in plant-microbe interactions that can be perceived by plant membrane-localized receptor to activate plant resistance.

Microbe-plant interaction in phyllosphere and development of biostimulant

Microbe-plant interaction in phyllosphere and development of biostimulant

The Legacy of Plant Invasion: Impacts on Soil Nitrification and Management Implications.

Plant invasions can have long-lasting impacts on soil nitrification, which plays a critical role in nutrient cycling and plant growth. This review examines the legacy effects of plant invasion on soil nitrification, focusing on the underlying mechanisms, context dependence, and implications for management. We synthesize literature on the positive, negative and neutral legacy effects of plant invasion on soil nitrification, highlighting the complexity of these effects and the need for further research to fully understand them. Positive legacy effects include increased soil microbial biomass or activity, potentially enhancing nutrient availability for plants. However, negative legacy effects, like reduced nitrifier abundance, can result in decreased soil nitrification rates and nutrient availability. In some cases, changes to nitrification during active invasion appear transitory after the removal of invasive plants, indicating neutral short-term legacies. We discuss the context dependence of legacy effects considering factors, including location, specific invasive plant species, and other environmental conditions. Furthermore, we discuss the implications of these legacy effects for management and restoration strategies, such as the removal or control of invasive plants, and potential approaches for restoring ecosystems with legacy effects on soil nitrification. Finally, we highlight future research directions, including further investigation into the mechanisms and context dependence of legacy effects, and the role of plant-microbe interactions. Overall, this review provides insights into the legacy effects of plant invasion on soil nitrification and their implications for ecosystems.

Divergent sequences of tetraspanins enable plants to specifically recognize microbe-derived extracellular vesicles

Extracellular vesicles (EVs) are important for cell-to-cell communication in animals. EVs also play important roles in plant–microbe interactions, but the underlying mechanisms remain elusive. Here, proteomic analyses of EVs from the soybean (Glycine max) root rot pathogen Phytophthora sojae identify the tetraspanin family proteins PsTET1 and PsTET3, which are recognized by Nicotiana benthamiana to trigger plant immune responses. Both proteins are required for the full virulence of P. sojae. The large extracellular loop (EC2) of PsTET3 is the key region recognized by N. benthamiana and soybean cells in a plant receptor-like kinase NbSERK3a/b dependent manner. TET proteins from oomycete and fungal plant pathogens are recognized by N. benthamiana thus inducing immune responses, whereas plant-derived TET proteins are not due to the sequence divergence of sixteen amino acids at the C-terminal of EC2. This feature allows plants to distinguish self and non-self EVs to trigger active defense responses against pathogenic eukaryotes.

Illuminating plant–microbe interaction: How photoperiod affects rhizosphere and pollutant removal in constructed wetland?

Rhizosphere is a crucial area in comprehending the interaction between plants and microorganisms in constructed wetlands (CWs). However, influence of photoperiod, a key factor that regulates photosynthesis and rhizosphere microbial activity, remains largely unknown. This study investigated the effect of photoperiod (9, 12, 15 h/day) on pollutant removal and underlying mechanisms. Results showed that 15-hour photoperiod treatment exhibited the highest removal efficiencies for COD (87.26%), TN (63.32%), and NO3–-N (97.79%). This treatment enhanced photosynthetic pigmentation and root activity, which increased transport of oxygen and soluble organic carbon to rhizosphere, thus promoting microbial nitrification and denitrification. Microbial community analysis revealed a more stable co-occurrence network due to increased complexity and aggregation in the 15-hour photoperiod treatment. Phaselicystis was identified as a key connector, which was responsible for transferring necessary carbon sources, ATP, and electron donors that supported and optimized nitrogen metabolism in the CWs. Structural equation model analysis emphasized the importance of plant–microbe interactions in pollutant removal through increased substance, information, and energy exchange. These findings offer valuable insights for CWs design and operation in various latitudes and rural areas for small-scale decentralized systems.

Drought conditioning of rhizosphere microbiome influences maize water use traits

Background and AimsBeneficial plant–microbe interactions can improve plant performance under drought; however, we know less about how drought-induced shifts in microbial communities affect plant traits.MethodsWe cultivated Zea mays in fritted clay with soil microbiomes originating from contrasting environments (agriculture or forest) under two irrigation treatments (well-watered or water limited). Using this design, we investigated whether water conditioning was carried forward through the microbiome to affect a subsequent plant cohort that was subjected to either a well-watered or water limited treatment.ResultsRegardless of the microbiome-origin, plants inoculated with a microbiome from a water limited legacy had traits that allowed them to avoid stress but conserve water. They produced longer roots to explore soil, generated greater soil dissolved organic carbon, potentially stimulating the microbiome, and slower soil water content loss during drought. A well-watered legacy resulted in plants that delayed permanent stomatal closure and higher photosynthetic nitrogen use efficiency. In plants with a forest-originated microbiome, a well-watered legacy and water treatment also resulted in higher rates of photosynthesis and stomatal conductance.ConclusionThese results demonstrate that soil microbiomes can be developed to influence plant drought performance, impacting crop resilience, using short-term microbial conditioning.

Application of Multi-Perspectives in Tea Breeding and the Main Directions.

Tea plants are an economically important crop and conducting research on tea breeding contributes to enhancing the yield and quality of tea leaves as well as breeding traits that satisfy the requirements of the public. This study reviews the current status of tea plants germplasm resources and their utilization, which has provided genetic material for the application of multi-omics, including genomics and transcriptomics in breeding. Various molecular markers for breeding were designed based on multi-omics, and available approaches in the direction of high yield, quality and resistance in tea plants breeding are proposed. Additionally, future breeding of tea plants based on single-cellomics, pangenomics, plant-microbe interactions and epigenetics are proposed and provided as references. This study aims to provide inspiration and guidance for advancing the development of genetic breeding in tea plants, as well as providing implications for breeding research in other crops.

Purification of archetypal soybean root suberin mostly comprising alka(e)noic acids using an ionic liquid catalyst.

Soybean (Glycine max) is an increasingly relevant crop due to its economic importance and also a model plant for the study of root symbiotic associations with nodule forming rhizobia. Plant polyesters mediate plant-microbe interactions with both pathogenic and beneficial microbes; suberin has been hypothesized to play a key role during the early steps of rhizobia attachment to the root. The downside is that suberin chemistry in soybean root is still scarcely studied. This study addresses this outstanding question by reporting a straightforward workflow for a speedy purification of suberin from soybean root and for its subsequent detailed chemical analysis. To purify suberin, cholinium hexanoate (an ionic liquid) was used as the catalyst. The ensuing suberin is highly esterified as observed by a precise Nuclear Magnetic Resonance quantification of each ester type, discriminating between primary and acylglycerol esters. Moreover, the composing hydrolysable monomers detected through GC-MS revealed that hexadecanoic acid is the most abundant monomer, similar to that reported before by others. Overall, this study highlights the adequacy of the ionic liquid catalyst for the isolation of suberin from soybean roots, where the polymer natural abundance is low, and builds new knowledge on the specificities of its chemistry; essential to better understand the biological roles of suberin in roots.

Durum wheat-lentil relay intercropping enhances soil mycorrhizal activity but does not alter structure of arbuscular mycorrhizal fungal community within roots

In intercropping systems, crop species select host-adapted microorganisms and influence the associated plant-microbial interactions like in the case of arbuscular mycorrhizal fungi (AMF). Attempts to assess the impact of intercropping on the activity, diversity, and community composition of AMF remain inconclusive, more so in intercropping systems involving traditional Mediterranean crops such as durum wheat and lentils. We carried out field experiments in Central Italy to assess the impact of relay intercropping durum wheat (Triticum durum Desf. cv. Minosse) and lentil (Lens culinaris Medik. cv. Elsa) on soil mycorrhizal inoculum potential (MIP) (2019 and 2020), AMF root colonization (2019, 2020, and 2021), and root AMF diversity and community composition (2020 and 2021), compared to the respective sole crops. Results showed that relay intercropping enhanced lentil grain yield and durum wheat grain protein concentration but marginally reduced durum wheat grain yield and lentil grain protein concentration. In addition, relay intercropping enhanced soil mycorrhizal activity but differentially influenced mycorrhizal root colonization compared to sole cropping. Sequencing analyses generated a total of 234 amplicon sequence variants belonging to Glomeromycota, which were assigned to 31 virtual taxa using the MaarjAM reference database. Glomeraceae and Claroideoglomeraceae were the most abundant taxa but had contrasting abundances in 2020 and 2021. The overall changes in AMF species diversity and community structure were affected by the interaction between crop species and year, and not by intercropping. Claroideoglomus and Septoglomus showed a strong association with lentil roots while Rhizophagus and Paraglomus were associated with durum wheat roots in 2020, affirming host genotype-AMF preferences. The principal component analysis showed that grain protein concentration was associated with selected mycorrhizal parameters such as community richness and AMF root colonization. Further studies on the functional analysis of the different AMF communities selected by the crop genotype and year may reveal the importance of intercropping in maintaining soil functionality and productivity under low-input systems.

Mass Spectral Imaging to Map Plant-Microbe Interactions.

Plant-microbe interactions are of rising interest in plant sustainability, biomass production, plant biology, and systems biology. These interactions have been a challenge to detect until recent advancements in mass spectrometry imaging. Plants and microbes interact in four main regions within the plant, the rhizosphere, endosphere, phyllosphere, and spermosphere. This mini review covers the challenges within investigations of plant and microbe interactions. We highlight the importance of sample preparation and comparisons among time-of-flight secondary ion mass spectroscopy (ToF-SIMS), matrix-assisted laser desorption/ionization (MALDI), laser desorption ionization (LDI/LDPI), and desorption electrospray ionization (DESI) techniques used for the analysis of these interactions. Using mass spectral imaging (MSI) to study plants and microbes offers advantages in understanding microbe and host interactions at the molecular level with single-cell and community communication information. More research utilizing MSI has emerged in the past several years. We first introduce the principles of major MSI techniques that have been employed in the research of microorganisms. An overview of proper sample preparation methods is offered as a prerequisite for successful MSI analysis. Traditionally, dried or cryogenically prepared, frozen samples have been used; however, they do not provide a true representation of the bacterial biofilms compared to living cell analysis and chemical imaging. New developments such as microfluidic devices that can be used under a vacuum are highly desirable for the application of MSI techniques, such as ToF-SIMS, because they have a subcellular spatial resolution to map and image plant and microbe interactions, including the potential to elucidate metabolic pathways and cell-to-cell interactions. Promising results due to recent MSI advancements in the past five years are selected and highlighted. The latest developments utilizing machine learning are captured as an important outlook for maximal output using MSI to study microorganisms.

Organic Contaminants are Degraded by Rhizospheric Microorganisms: A Review

Organic pollutants have grown to be a serious global problem because of their massive creation, widespread application, and eventual discharge. Due to biomagnification, accumulation, and their harmful acute and chronic impacts on all living things, these substances significantly increased the load on the ecosystem and its potential threats. Reducing the risk factors associated with organic contaminantsthrough rhizospheric microfilms is crucial. Rhizoremediation is phytoremediation that removes toxins from the soil using plant roots and the rhizospheric microorganisms living on them. Research has shown that one of the best techniques is bioremediation utilizing plants. Utilizing bacteria from plants offers a lot of potential for rhizoremediation. Dangerous environmental contaminants include toxic industry byproducts, polychlorinated biphenyls (PCBs), polycyclic aromatic hydrocarbons (PAHs), organochlorine insecticides, and polychlorinated biphenyls (PCBs). These substances are categorized as global concern chemicals due to their propensity to travel long distances, remain in the environment, and potential for bio-accumulation and bio-magnification through the food chain. Organic pollutants can be broken down from the soil by soil microflora, which can also promote plant development in stressful environments. Plant-microbe interaction is essential for removing contaminants from the soil. Cleaning up these and harmful pollutants is therefore essential together with microbes; phytoremediation is an economical way to remove the pollutants from the soil, air, and water that is also environmentally acceptable.

First insights into diversity and potential metabolic pathways of bacterial and fungal communities in the rhizosphere of Argemonemexicana L. (Papaveraceae) from the water-level-fluctuation zone of Wudongde Reservoir of the upper Yangtze river, China.

The water-level fluctuation zone (WLFZ) of Wudongde reservoir of the upper Yangtze river is a completely new aquatic-terrestrial transitional zone, and its plant degenerate issue is attracting global concerns. Uncovering the unknown rhizosphere microbiome of dominant plants of this zone is helpful in understanding the plant-microbe interactions and their growth under the largely varying environment. Here, a first exploration of the rhizosphere bacterial and fungal communities of wilted (JB) and unwilted (JA) Argemonemexicana L. individuals from the WLFZ of Wudongde reservoir was carried out using high-throughput sequencing and MetaCyc metabolic pathway analyses. The results showed that rhizosphere of wilted A.mexicana L individuals exhibited a higher microbial richness and diversity than the unwilted ones, irrespective of the bacterial and fungal communities. It was noted that 837 common bacterial amplicon sequence variants (ASV) and 92 common fungal ASV were presented in both JA and JB with 3108 bacteria and 212 fungi unique to JA, and 3569 bacteria and 693 fungi unique to JB. Linear discriminant analysis effect Size (LEfSe) analyses indicated that the taxa that had the most contribution to observed differences between both JA and JB was Proteobacteria, Actinobacteria and Ascomycota for JA, and Bacteroidetes, Firmicutes, Verrucomicrobia, Basidiomycota and Ascomycota for JB. Organic compound conversion pathway (degradation/reduction/oxidation) was consistently highly represented in the rhizosphere microbiomes of both JA and JB. Overall, this study provides insights into the rhizosphere microbiome composition, diversity and metabolic pathways of both wilted and unwilted A.mexicana L. individuals in the WLFZ of Wudongde reservoir, and the results give valuable clues for manipulating microbes to support plant growth in such a recently-formed WLFZ under a dry-hot valley environment.

Seasonal asynchrony in above- and below-ground phenology in a temperate forest: carbon allocation trade-off and plant-microbe interactions

Seasonal asynchrony in above- and below-ground phenology in a temperate forest: carbon allocation trade-off and plant-microbe interactions

Characterization and genomics identification of key genes involved in denitrification-DNRA-nitrification pathway of plant growth-promoting rhizobacteria (Serratia marcescens OK482790)

BackgroundA wide variety of microorganisms, including bacteria, live in the rhizosphere zone of plants and have an impact on plant development both favorably and adversely. The beneficial outcome is due to the presence of rhizobacteria that promote plant growth (PGPR).ResultsIn this study, a bacterial strain was isolated from lupin rhizosphere and identified genetically as Serratia marcescens (OK482790). Several biochemically and genetically characteristics were confirmed in vitro and in vivo to determine the OK482790 strain ability to be PGPR. The in vitro results revealed production of different lytic enzymes (protease, lipase, cellulase, and catalase), antimicrobial compounds (hydrogen cyanide, and siderophores), ammonia, nitrite, and nitrate and its ability to reduce nitrate to nitrite. In silico and in vitro screening proposed possible denitrification-DNRA-nitrification pathway for OK482790 strain. The genome screening indicated the presence of nitrite and nitrate genes encoding Nar membrane bound sensor proteins (NarK, NarQ and NarX). Nitrate and nitrite reductase encoding genes (NarI, NarJ, NarH, NarG and NapC/NirT) and (NirB, NirC, and NirD) are also found in addition to nitroreductases (NTR) and several oxidoreductases. In vivo results on wheat seedlings confirmed that seedlings growth was significantly improved by soil inoculation of OK482790 strain.ConclusionsThis study provides evidence for participation of S. marcescens OK482790 in nitrogen cycling via the denitrification-DNRA-nitrification pathway and for its ability to produce several enzymes and compounds that support the beneficial role of plant-microbe interactions to sustain plant growth and development for a safer environment.

Hidden in the parts: How the cell-type perspective reveals novel insights into plant-microbe interactions

Hidden in the parts: How the cell-type perspective reveals novel insights into plant-microbe interactions

Membrane vesicle engineering with "à la carte" bacterial-immunogenic molecules for organism-free plant vaccination.

The United Nations heralds a world population exponential increase exceeding 9.7 billion by 2050. This poses the challenge of covering the nutritional needs of an overpopulated world by the hand of preserving the environment. Extensive agriculture practices harnessed the employment of fertilizers and pesticides to boost crop productivity and prevent economic and harvest yield losses attributed to plagues and diseases. Unfortunately, the concomitant hazardous effects stemmed from such agriculture techniques are cumbersome, that is, biodiversity loss, soils and waters contaminations, and human and animal poisoning. Hence, the so-called 'green agriculture' research revolves around designing novel biopesticides and plant growth-promoting bio-agents to the end of curbing the detrimental effects. In this field, microbe-plant interactions studies offer multiple possibilities for reshaping the plant holobiont physiology to its benefit. Along these lines, bacterial extracellular membrane vesicles emerge as an appealing molecular tool to capitalize on. These nanoparticles convey a manifold of molecules that mediate intricate bacteria-plant interactions including plant immunomodulation. Herein, we bring into the spotlight bacterial extracellular membrane vesicle engineering to encase immunomodulatory effectors into their cargo for their application as biocontrol agents. The overarching goal is achieving plant priming by deploying its innate immune responses thereby preventing upcoming infections.