The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms

Essential oils are well‐known for their antimicrobial activity against different plant and human pathogenic microorganisms. The results of the most commonly used antimicrobial assays are very different; sometimes their reliability is questionable, therefore standardized methods need to be used to solve this problem. The present study aims at the phytochemical characterization of some essential oils (thyme, lavender, eucalyptus, spearmint and cinnamon) that are important from the therapeutic and economic aspects and the optimized microbiological investigation of the effect of essential oils on human and plant pathogenic microorganisms. The chemical composition of the essential oils was analysed with thin‐layer chromatography (TLC) and their composition was controlled by gas chromatography (GC). The antibacterial effect was investigated using the TLC‐bioautographic method. The solvents applied in TLC developing systems were also tested. Our results showed that toluene, ethyl acetate, ethanol and chloroform as solvents used in the assay had no inhibiting effect on the test bacteria. The antibacterial activity of thyme, lavender and cinnamon oils and their main components (thymol, carvacrol, linalool, eugenol) was observed in the case of two plant pathogenic bacteria (Xanthomonas campestris pv. vesicatoria and Pseudomonas syringae pv. phaseolicola) and some human pathogens (Staphylococcus epidermidis, S. saprophyticus and two strains of S. aureus, including one methicillin‐resistant strain). On the whole, the antibacterial activity of essential oils can be related to their most abundant components, but the effect of the minor components should also be taken into consideration. Direct bioautography is more cost‐effective and compares better with traditional microbiological laboratory methods (e.g. disc‐diffusion, agar‐plate technique). Copyright © 2010 John Wiley & Sons, Ltd.

Sustainable agriculture is highly dependent on a diverse soil microbiome that facilitates ecosystem services such as nutrient cycling and organic matter degradation. These transformations are mediated by microorganisms together with fauna. Nematodes, as important microbial gazers, play a key role in these processes, e.g. nutrient mineralisation. Due to their central position in the soil food web, nematodes provide an essential link for carbon and energy flow from microorganisms to higher trophic levels. These multiple functions of nematodes have made them as useful indicators of soil condition and plant health. However, plant parasites are severe pests that control plant carbon allocation and, in turn, the rhizosphere microbiome. Another aspect is their vector potential for both plant and human pathogenic microorganisms within microbial hotspots. Overall, nematodes have a major impact on agricultural soils, and sustainable management requires consideration of their diverse interactions with the soil microbiome.

Harnessing microbial multitrophic interactions for rhizosphere microbiome engineering

The interplay between the inoculation of plant growth-promoting rhizobacteria and the rhizosphere microbiome and their impact on plant phenotype

Sustainable agriculture demands the balanced use of inorganic, organic, and microbial biofertilizers for enhanced plant productivity and soil fertility. Plant growth-enhancing rhizospheric bacteria can be an excellent biotechnological tool to augment plant productivity in different agricultural setups. We present an overview of microbial mechanisms which directly or indirectly contribute to plant growth, health, and development under highly variable environmental conditions. The rhizosphere microbiomes promote plant growth, suppress pathogens and nematodes, prime plants immunity, and alleviate abiotic stress. The prospective of beneficial rhizobacteria to facilitate plant growth is of primary importance, particularly under abiotic and biotic stresses. Such microbe can promote plant health, tolerate stress, even remediate soil pollutants, and suppress phytopathogens. Providing extra facts and a superior understanding of microbial traits underlying plant growth promotion can stir the development of microbial-based innovative solutions for the betterment of agriculture. Furthermore, the application of novel scientific approaches for facilitating the design of crop-specific microbial biofertilizers is discussed. In this context, we have highlighted the exercise of "multi-omics" methods for assessing the microbiome's impact on plant growth, health, and overall fitness via analyzing biochemical, physiological, and molecular facets. Furthermore, the role of clustered regularly interspaced short palindromic repeats (CRISPR) based genome alteration and nanotechnology for improving the agronomic performance and rhizosphere microbiome is also briefed. In a nutshell, the paper summarizes the recent vital molecular processes that underlie the different beneficial plant-microbe interactions imperative for enhancing plant fitness and resilience under-challenged agriculture.

The rhizosphere microbiome plays a vital role in plant growth, health, and nutrient acquisition. One of the key factors that shape the composition and function of the rhizosphere microbiome is root exudates, the complex mixture of organic compounds released by plant roots. Root exudates serve as a source of energy and nutrients for the rhizosphere microbiome, as well as a means of communication between plants and microbes. The dynamic interplay between root exudates and rhizosphere microbiome is a complex and highly regulated process that involves multiple feedback loops and interactions. Recent studies have revealed that the composition and quantity of root exudates are modulated by a range of biotic and abiotic factors, including plant genotype, soil type, nutrient availability, and microbial community structure. In turn, the rhizosphere microbiome can influence the production and composition of root exudates, through processes such as nutrient cycling, plant hormone synthesis, and modulation of plant defense responses. Understanding the dynamics of root exudates and rhizosphere microbiomes is crucial for developing effective strategies for microbiome engineering, plant-microbe symbiosis, and sustainable agriculture. This review provides an overview of the current state of knowledge on the dynamic interplay between root exudates and rhizosphere microbiomes, highlighting the key factors and mechanisms that govern this complex relationship.

Soil salinization adversely impacts plant and soil health. While amendment with chemicals is not sustainable, the application of bioinoculants suffers from competition with indigenous microbes. Hence, microbiome-based rhizosphere engineering, focussing on acclimatization of rhizosphere microbiome under selection pressure to facilitate plant growth, exhibits promise. This study aimed to acclimatize a salt-susceptible tomato cultivar to high salt concentration through a microbiome-based top-down approach of rhizosphere engineering. Multiple passaging of the rhizosphere microbiome of the cultivar was performed for twelve plant growth cycles in the presence of increasing salt stress. The rhizosphere microbiome of the phenotypically best-grown plant under stress was transferred as inoculum to the next plant growth cycle. Plant growth attributes and stress marker levels were assessed, expression levels of plant salt stress-responsive genes were examined, and the bacterial community composition in the initial and final plant growth cycles was analysed. Rhizosphere microbiome inoculation promoted plant growth under increasing salt concentrations. Stress markers were reduced in plants inoculated with an acclimatized microbiome, while the root architecture was enhanced, indicating salt tolerance. The salt stress-responsive genes were downregulated in salt-treated plants, whereas upregulation of these genes was observed upon microbiome inoculation. The relative abundance of Exiguobacterium, Arthrobacter, and Lysobacter was higher in microbiome-treated plants under salt stress compared to the salt-treated plants without microbiome inoculation. The strategy of acclimatizing the rhizosphere microbiome of a salt-susceptible tomato cultivar was successfully implemented for stress amelioration and plant growth promotion, thereby offering a sustainable means with immense potential for application in other crops.

Seed-associated microbiomes can impact the later colonization of a plant rhizosphere microbiome. However, there remains little insight into the underlying mechanisms concerning how alterations in the composition of the seed microbiome may intervene in the assembly of a rhizosphere microbiome. In this study, the fungus Trichoderma guizhouense NJAU4742 was introduced to both maize and watermelon seed microbiomes by seed coating. Application was found to significantly promote seed germination and improve plant growth and rhizosphere soil quality. The activities of acid phosphatase, cellulase, peroxidase, sucrase, and α-glucosidase increased significantly in two crops. The introduction of Trichoderma guizhouense NJAU4742 also led to a decrease in the occurrence of disease. Coating with T. guizhouense NJAU4742 did not alter the alpha diversities of the bacterial and fungal communities but formed a key network module that contained both Trichoderma and Mortierella. This key network module comprised of these potentially beneficial microorganisms was positively linked with the belowground biomass and activities of rhizosphere soil enzymes but negatively correlated with disease incidence. Overall, this study provides insights into plant growth promotion and plant health maintenance via seed coating in order to influence the rhizosphere microbiome. IMPORTANCE Seed-associated microbiomes can impact the rhizosphere microbiome assembly and function display. However, there remains little insight into the underlying mechanisms concerning how alterations in the composition of the seed microbiome with the beneficial microbes may intervene in the assembly of a rhizosphere microbiome. Here, we introduced T. guizhouense NJAU4742 to the seed microbiome by seed coating. This introduction led to a decrease in the occurrence of disease and an increase in plant growth; furthermore, it formed a key network module that contained both Trichoderma and Mortierella. Our study provides insights into plant growth promotion and plant health maintenance via seed coating in order to influence the rhizosphere microbiome.

BackgroundSoil microbiomes are considered a cornerstone of the next green revolution, and plant growth-promoting bacteria (PGPB) are critical for microbiome engineering. However, taking plant-beneficial microorganisms from discovery to agricultural application remains challenging, as the mechanisms underlying the interactions between beneficial strains and plants in native soils are still largely unknown. Increasing numbers of studies have indicated that strains introduced to manipulate microbiomes are usually eliminated in soils, while others have reported that application of PGPB as inocula significantly improves plant growth. This contradiction suggests the need for a deeper understanding of the mechanisms underlying microbe-induced growth promotion.ResultsWe showed PGPB-induced long-term plant growth promotion after elimination of the PGPB inoculum in soils and explored the three-way interactions among the exogenous inoculum, indigenous microbiome, and plant, which were key elements of the plant growth-promoting process. We found the rhizosphere microbiome assembly was mainly driven by plant development and root recruitments greatly attenuated the influence of inocula on the rhizosphere microbiome. Neither changes in the rhizosphere microbiome nor colonization of inocula in roots was necessary for plant growth promotion. In roots, modification of DNA methylation in response to inoculation affects gene expression related to PGPB-induced growth promotion, and disruptions of the inoculation-induced DNA methylation patterns greatly weakened the plant growth promotion. Together, our results showed PGPB-induced DNA methylation modifications in roots mediated the promotion process and these modifications remained functional after elimination of the inoculum from the microbiome.ConclusionThis study suggests a new mechanism in which PGPB affect DNA methylation in roots to promote plant growth, which provides important insights into microbiome–plant interactions and offers new strategies for plant microbiome engineering beyond the perspective of maintaining inoculum persistence in soils.4DAt-NxeARCpvmCXo93oLmVideo abstractGraphical abstract

The rhizosphere provides a home to numerous (micro)organisms that in turn may affect plant growth, development, and tolerance to abiotic and biotic stresses. How plants shape the rhizosphere microbiome has been subject of many past and present studies with the ultimate goal to identify plant genetic traits that select and support beneficial microorganisms. Novel ‘omics technologies have provided more in-depth knowledge of the diversity and functioning of the rhizosphere microbiome and significant advances are being made to uncover mechanisms, genes and metabolites involved in the multitrophic interactions in the rhizosphere. To better understand this intriguing complexity, both reductionists’ and systems ecology approaches are needed to identify the biotic and abiotic factors involved in microbiome assembly. Here, different strategies are discussed to re-shape the rhizosphere microbiome in favour of microbial consortia that promote root development and plant growth, and that prevent the proliferation of pests and diseases.

Plant-parasitic nematodes cause considerable damage to crop plants. The rhizosphere microbiome can affect invasion and reproductive success of plant-parasitic nematodes, thus affecting plant damage. In this study, we investigated how the transplanted rhizosphere microbiome from different crops affect plant-parasitic nematodes on soybean or tomato, and whether the plant’s own microbiome from the rhizosphere protects it better than the microbiome from fallow soil. Soybean plants growing in sterilized substrate were inoculated with the microbiome extracted from the rhizosphere of soybean, maize, or tomato. Controls were inoculated with extracts from bulk soil, or not inoculated. After the microbiome was established, the root lesion nematode Pratylenchus penetrans was added. Root invasion of P. penetrans was significantly reduced on soybean plants inoculated with the microbiome from maize or soybean compared to tomato or bulk soil, or the uninoculated control. In the analogous experiment with tomato plants inoculated with either P. penetrans or the root knot nematode Meloidogyne incognita, the rhizosphere microbiomes of maize and tomato reduced root invasion by P. penetrans and M. incognita compared to microbiomes from soybean or bulk soil. Reproduction of M. incognita on tomato followed the same trend, and it was best suppressed by the tomato rhizosphere microbiome. In split-root experiments with soybean and tomato plants, a systemic effect of the inoculated rhizosphere microbiomes on root invasion of P. penetrans was shown. Furthermore, some transplanted microbiomes slightly enhanced plant growth compared to uninoculated plants. The microbiomes from maize rhizosphere and bulk soil increased the fresh weights of roots and shoots of soybean plants, and microbiomes from soybean rhizosphere and bulk soil increased the fresh weights of roots and shoots of tomato plants. Nematode invasion did not affect plant growth in these short-term experiments. In conclusion, this study highlights the importance of the rhizosphere microbiome in protecting crops against plant-parasitic nematodes. An effect of pre-crops on the rhizosphere microbiome might be harnessed to enhance the resistance of crops towards plant-parasitic nematodes. However, nematode-suppressive effects of a particular microbiome may not necessarily coincide with improvement of plant growth in the absence of plant-parasitic nematodes.

Exploration of rhizosphere and rhizosphere microbiome has been the research focus for last many decades. The rhizosphere is a junction for intercommunication among plants, insects, and microorganisms. It serves as diverse habitat with a nutrient-rich niche by providing a platform interaction among plants-soil-microorganism trio along with energy and matter trade-off. The rhizosphere microbiome also influences plant vigour, health, and defence against stresses by interfering with nutrient uptake, chemical signalling, and enzyme activity. Interaction among the microbiome, the environment, and the genetic makeup of host is well-known to contribute towards host health. The present chapter summarises the major effects of microbial communities present in rhizosphere on plant health and diseases.

Physiological and metagenomic strategies uncover the rhizosphere bacterial microbiome succession underlying three common environmental stresses in cassava

BackgroundPlant health is intimately influenced by the rhizosphere microbiome, a complex assembly of organisms that changes markedly across plant growth. However, most rhizosphere microbiome research has focused on fractions of this microbiome, particularly bacteria and fungi. It remains unknown how other microbial components, especially key microbiome predators—protists—are linked to plant health. Here, we investigated the holistic rhizosphere microbiome including bacteria, microbial eukaryotes (fungi and protists), as well as functional microbial metabolism genes. We investigated these communities and functional genes throughout the growth of tomato plants that either developed disease symptoms or remained healthy under field conditions.ResultsWe found that pathogen dynamics across plant growth is best predicted by protists. More specifically, communities of microbial-feeding phagotrophic protists differed between later healthy and diseased plants at plant establishment. The relative abundance of these phagotrophs negatively correlated with pathogen abundance across plant growth, suggesting that predator-prey interactions influence pathogen performance. Furthermore, phagotrophic protists likely shifted bacterial functioning by enhancing pathogen-suppressing secondary metabolite genes involved in mitigating pathogen success.ConclusionsWe illustrate the importance of protists as top-down controllers of microbiome functioning linked to plant health. We propose that a holistic microbiome perspective, including bacteria and protists, provides the optimal next step in predicting plant performance.4pRGo2biPz35arE7pbprXhVideo

The rhizosphere microbiome plays an important role in plant growth, nutrient acquisition, and overall health. In this study, we investigated the relationship between the rhizosphere microbiome and the health status of strawberries (Fragaria × ananassa) under identical soil and environmental conditions. Strawberry plants were categorized into a healthy group (H) and an unhealthy group (UH) based on morphological characteristics, and the soil microbial community was analyzed using 16S rRNA gene sequencing. The H group exhibited significantly higher nitrogen concentrations, whereas the UH group showed excessive accumulation of iron, manganese, zinc, and copper. Microbiota analysis revealed distinct structural differences between the H and UH groups, with several bacterial taxa displaying significant differences in relative abundance. Notably, Microvirga and JG30-KF-CM45 emerged as key bacterial taxa associated with plant nutrient status. Microvirga was positively correlated with nitrogen levels but negatively associated with micronutrient accumulation, while JG30-KF-CM45 showed the opposite trend. Furthermore, co-occurrence network analysis indicated that microbial communities in the UH group were characterized by intensified competitive interactions, which may contribute to rhizosphere microbiome destabilization and impaired plant growth. These findings indicate that microbial interactions within the rhizosphere influence nutrient homeostasis and plant health. The observed microbial imbalances in UH plants suggest the importance of maintaining a stable microbial community for improved crop productivity. This study provides valuable insights into the role of rhizosphere microbiome in sustainable strawberry cultivation and underscores the potential of microbiome-based strategies to improve plant health and productivity.