Editorial: Plant Microbiome: Interactions, Mechanisms of Action, and Applications, Volume III

Alok Kumar Srivastava¹Prem Lal Kashyap²Gustavo Santoyo^3*George Newcombe⁴

• ¹ICAR - National Bureau of Agriculturally Important Microorganisms, Mau, India
• ²ICAR - Indian Institute of Wheat and Barley Research, Panipat Refinery Township, India
• ³Instituto de Investigaciones Químico-Biológicas, Universidad Michoacana de San Nicolás de Hidalgo, Morelia, Mexico
• ⁴University of Idaho Department of Forest Rangeland and Fire Sciences, Moscow, United States

Editorial of the research topic: Plant Microbiome: Interactions, Mechanisms of Action, and Applications, Volume III Terrestrial plants are of unique evolutionary and ecological importance (Margulis and Sagan, 1997). At present, approximately 400,000 plant species comprise nearly 80% of the world's living biomass (Bar-On et al., 2018). Their symbionts are equally remarkable, including representatives of fungi, bacteria and other microorganisms (Gray, 2017). Microbes inhabit nearly all plant tissues, both inside and out (Barnes et al, 2025); collectively, they are referred to as the plant microbiome. Interactions within and among these microbes, and between microbes and plants, are central to terrestrial life, shaping individual plant phenotypes and driving the functioning of entire ecosystems (Barnes et al, 2025). The interactions of plants with fungi and bacteria are the focus of this special issue. Fungi vary in their interactions with plants, from obligate parasites (e.g., rust fungi, order Uredinales) to obligate mutualists without which certain plants can not survive (e.g., some mycorrhizal interactions). Some fungi are even parasitized by plants (Bidartondo, 2005). The functional diversity of plant-fungal interactions is striking. Fungi, themselves, "probably evolved from a line of fungus-like protists that absorbs food directly from the living or dead bodies of algae, plants, and animals; and fungi seems to have coevolved with plants in the move to the land" (Margulis and Sagan, 1997). The latter authors argue that without their symbionts, plants might never have emerged and evolved on land: "dry land was as hostile an environment for plants as the moon is for us". Today, drought and salinity represent major constraints on crop yields (Verma et al, 2021). The papers of this issue primarily address research with microbes that improve growth and yield of economically important plants affected by drought and salinity (Delaux and Schornack, 2021). Knowledge of endophyte applications to crops is more advanced than any other sector of agriculture. However, even with crop plants the most effective endophytes may never be selected, and even when identified, their performance in a given crop system may fall short of optimal outcomes in the near future. The growth of the frontier of plant–microbe research reveals the critical nature of the microbiomes in maintaining plant health, productivity, and resilience across both ecological and agricultural environments. A central theme across the articles in Plant Microbiome: Interactions, Mechanisms of Action, and Applications, Volume III, is that plants and their microbiomes are integrated holobionts and their interactions are the key to solving problems of food security, environmental stress, loss of biodiversity, and sustainable use of bioresources. Together, the articles cover staple cereals, legumes, fruit trees, medicinal herbs, forest ecosystems, and desert shrubs, painting a tapestry of how microbiomes influence plant function, environmental tolerance, and even the integrity of medicinal compounds. One overlying theme throughout this collection of work is the untapped microbial richness contained within medicinally and endangered plants. Research on Elephantorrhiza elephantina, a tradition-valued but declining medicinally significant herb of southern Africa, illustrates how combination of both next generation sequencing and culturing strategies can uncover the concealed microbial symbionts in plant tissues. Predominant taxa like Pseudomonas, Microbacterium oxydans, and Stenotrophomonas maltophilia were not only detected but also found to be bioactive metabolite producers, with high antimicrobial activity against a wide array of bacterial pathogens (Tlou et al.). Their demonstrated production of antimicrobial metabolites reveals the unexploited potential for endophytes as sustainable bioactive compound resources. This is important as it gives room for sustainable alternatives to plants' overharvesting for therapeutic use, placing endophytes themselves on the spot as new reservoirs of pharmacological agents. Likewise, in Polygonatum cyrtonema, a medicinal plant used in traditional Chinese medicine, microbial structure was directly correlated with the storage of polysaccharides and saponins, the key compounds to its activity and commercial value (Yang et al.). Endophytic and rhizosphere microbiota differed between Sichuan and Guangxi provinces, with Burkholderia, Caballeronia, Paraburkholderia and Amycolatopsis being negatively correlated with levels of bioactive compounds and Enterobacter having a positive correlation with accumulation of polysaccharides. These observations place microbial ecology in the context not just of agronomy, but also that of the consistency and authenticity of medicinal plant products. In these contexts, the microbiome is no longer a silent background associate and becomes an active driver of cultural, economic, and pharmacological value. The articles also emphasize the manner in which plant-associated microbiomes support stress tolerance in main staple crops. Repeated monocropping of peanuts, a key legume, was found to significantly reorganize rhizosphere microbial communities, reducing taxa with beneficial functions in nutrient cycling and disease suppression and increasing potential pathogens. This microbial imbalance, commonly referred to as "continuous cropping obstacles," contributes to the gradual decrease in peanut yields under prolonged monoculture. Control over microbiome structure thus becomes a viable option to restore soil equilibrium and maintain productivity in high-input cropping systems. The same was found with rice crops in saline–alkaline soils, where the salt-tolerant cultivar 'Jida177' assembled a more diverse and stress-acclimatized microbiome compared to the susceptible 'Tongxi933', also showing positive correlation with improved yield and grain quality (Zhong et al.). Functional pathways involving stress tolerance, nutrient cycling, and hormone modulation were enriched in Jida177-associated communities, illustrating how crop breeding and microbiome engineering are complementary levers for resilience. Casting the net wider to encompass nutrient limitation, phosphate solubilizing rhizobacteria were found to mobilize phosphorus present in insoluble forms, enhancing rice P status and increasing field yields by as much as 15% (Rasul et al.). The multi-trait functions carried out by Acinetobacter MR5 and Pseudomonas R7 provide stress-relief, suggesting the practical value of well-characterized microbial inocula. All of these studies show that plant productivity from monocultures under salinity and nutrient limitation is associated with the host's ability to recruit, host, and work with beneficial microbes. A study on Bacillus sp. SW7 derived from mangroves highlights an underutilized opportunity for exploring the potential of extremophilic microbes adapted to saline and heat-stressed systems. Isolated from mangrove sediments in the U.A.E., the bacterium exhibited remarkable tolerances to high salinity (11% NaCl) and temperature (50°C), and expressed multiple traits typically associated with plant growth-promoting (PGP) characteristics including: solubilization of phosphate and potassium, production of indole acetic acid and ammonia, and catalase/oxidase activities (Afridi et al.). In a shade-house trial using tomato (Solanum lycopersicum), the addition of SW7 to tomato seeds greatly increased seed germination, leaf density and plant biomass. Harvested plants had only slight to no effects on the levels of photosynthetic pigments, indicating that beneficial nutritive substances and stress-tolerance (not photosynthetic efficiency) are responsible for growth-promoting effects. Together the results of this study demonstrate the potential of extremophilic PGP bacteria as bioinoculants for improving agroecological performance in arid and marginal soils, which can allow agriculture to become less reliant on chemical fertilizers and increase resilience to climate stressors. In addition to co-inoculation of PGP bacteria, there are increasing consortia of fungi and bacteria for consideration in synergistic roles. Zeng et al. reported that co-inoculation of the arbuscular mycorrhizal fungus (Funneliformis mosseae) with a PGP bacterium (Pseudomanas sp. SG29) and PGP rhizobacteria (Bacillus sp. SG42) resulted in greater improvements in tobacco seedling growth. Among the treatments tested, A_SG29, a co-inoculation of F. mosseae and Pseudomonas SG29, produced the greatest changes with regard to biomass, nutrient uptake (N, P, K), leaf area, chlorophyll content and root morphology. Using rhizosphere sequencing, they found evidence of increased beneficial microbial taxa, increased arbuscular mycorrhizal fungi (AMF) root colonisation, and upregulation of metabolic pathways related to nutrient cycling and supporting plant growth. These results illustrate the ecological benefits of microbial co-culture: the ability to create targeted combinations of AMF and plant growth-promoting rhizobacteria (PGPR) that shaped the microbiome of the rhizosphere enough to enhance early seedling development, while decreasing reliance on agrochemicals. Soil type itself is a central parameter affecting plant–microbe interactions and their ultimate influence on crop yield responses. For example, in a comprehensive study of ratoon sugarcane (Saccharum officinarum) on sandy, loam and clay soils, Wang et al. determined that soil microbiological functions (which included respiration and catalase activity) were highly correlated with the theoretical sugar yield that could be obtained from the crop. Also, loam soils had the most balanced environment which supported the greatest rhizosphere function and yield potential compared to sandy or clay soils. As well, bacterial abundance in the rhizosphere was negatively correlated with soil biochemical function, while fungal abundance was positively correlated. This indicates the distinct functional roles of fungi and bacteria in sugarcane rhizospheres, where fungi performed more of the biochemical function associated with yield. The structure of root-associated endophyte communities also differed between soil types, demonstrating direct effects on plant growth. These findings provide a basis for soil-specific management approaches, which highlights that improving microbial community structure of different soils is important for improving sugarcane yield in ratoon systems. While much of the focus has been on crop systems, insights from forest ecosystems can also provide valuable lessons for plant-microbe-soil interactions. Guo et al. examined the soil microbiome for the shiro, the distinct mycelial zone for the ectomycorrhizal fungus Tricholoma bakamatsutake, in association with Quercus mongolica. Shiro soils had higher availability of potassium and nitrogen, but a lower availability of phosphorus and organic matter, when compared to non-mycorrhizal rhizosphere soils. Fungal community diversity was lower in shiro soils than in non-mycorrhizal rhizosphere soils, and the community was dominated by T. bakamatsutake, which suppressed potential competitors such as Russula and Penicillium. In contrast, the bacterial community showed more diversity, with enriching communities of mycorrhization-helper taxa (such as Paenibacillus and Bacillus) and associated plant growth-promoting genera (Solirubrobacter, Streptomyces). Functional predictions showed upregulation of pathways for sugar and fat catabolism, enrichment for genes involved in gibberellin biosynthesis and activity for carboxylesterase. Microbiomes also emerge as key players in plant adaptations to environmental contamination. Alongside ecological evidence, experimental work using ectomycorrhizal fungi with Pinus tabulaeformis with added lead stress, showed how fungal partners increased host growth, photosynthesis, and antioxidant defense while immobilizing lead in lead pyromorphite minerals through biomineralization (Cheng et al.). This novel dual mechanism of physiological tolerance on behalf of the host and geochemical stabilization in the rhizosphere is a potential model for sustainable remediation of contaminated soils. All of these studies suggest that microbes are not passive residents in contaminated ecological zones but instead are highly active participants. Beyond the well-studied bacteria–fungi consortia, other cross-kingdom microbial associations, such as those involving microalgae and bacteria, are emerging as important ecological inputs. An integrated review of microalgae–microbe interactions in saline– alkaline agriculture shows that algal photosynthesis and bacterial respiration constitute metabolic cycles exchanging carbon, oxygen, vitamins, and siderophores and generating extracellular polysaccharides enhancing soil aggregation and water relations (Ren et al.). These consortia have proven to promote enhanced plant antioxidant responses and perform better than individual inoculants in soil and foliar treatments. By connecting autotrophic and heterotrophic metabolisms, algal-microbial systems open up new ranges of bioformulations for dealing with salinity stress. Notably, it also suggests the future of microbial interventions in agriculture, beyond single-strain inoculants to multi-kingdom consortia that reflect the complexity of natural ecosystems. The shrub and tree microbiomes add a new perspective, emphasizing drought resilience and long life. The hybrid buffaloberry (Shepherdia utahensis 'Torrey') study showed how the communities of soil, rhizosphere, and nodular organisms, dominated by Proteobacteria, Actinobacteriota, and Frankia nitrogen-fixers, support plant survival in droughty habitats (Devkota et al.). Interestingly, some individual strains had a combination of plant growth promoting characteristics, including some that had all seven functions that were tested. These multipurpose microbes could be advantageous for designing inoculants for low water-use horticulture and dryland restoration, safe from potential isolation of microbes. An example of this would be the global citrus root study which identified a conserved core microbiome from 9 countries and 6 continents associated with fruit perennial systems, that comprised taxa such as Bradyrhizobium, Pseudomonas, Streptomyces, Cladosporium and Mortierella (Lombardo et al.). Despite the obvious environmental heterogeneity, consistency of plants and the associations with microbes indicate that perennial fruit trees may have a functional template that could be exploited to create universal inoculants. This provides the opportunity for scaling, and by virtue of not needing to adapt to each and every local environment, suggests that microbiome management is about optimizing conserved cores. Endophytic microorganisms are part of the plant microbiome, fulfilling important functions such as promoting plant growth and protecting against potential pathogens (Ghosh et al., 2020). The mechanisms can be diverse but have been divided into two categories for study: direct and indirect. Direct mechanisms include functions such as the production of phytohormones and facilitation of nutrient uptake from the soil. On the other hand, indirect mechanisms include the production of antimicrobial compounds that inhibit pathogen growth, as well as stimulation of the plant's defense systems (Glick and Gamalero, 2021). By providing these microbial services to their plant host, the plant exhibits better growth and can improve its overall fitness even under biotic or abiotic stress conditions (e.g., drought or salinity) (Kumar and Nautiyal, 2022). Two microbial groups reported as endophytes include fungi of the genus Trichoderma and bacteria of the genus Bacillus. In the work by Santoyo et al., they analyze the multitrait characteristics of both microbial groups, although not exclusively focusing on endophytes, but they do emphasize the importance of these groups in performing synergistic tasks that help plants tolerate salt stress. Salt stress in agriculture is a global problem affecting a large portion of arable land, about 40%, and is more severe in underdeveloped regions. Another problem in arable lands is the presence of heavy metals and metalloids such as arsenic (Zhou et al., 2018). However, it has been highlighted that endophytic fungi can increase tolerance and even aid in the phytoremediation of contaminated soils. Such is the case of the endophytic fungus Serendipita indica, which in a synergistic interaction with the actinobacterium Zhihengliuella sp. ISTPL4, improved rice tolerance to arsenic presence and toxicity. Both microorganisms improved plant growth parameters such as shoot length, root length, shoot dry weight, and root dry weight, as well as biochemical parameters such as chlorophyll content, protein content, and antioxidant enzymatic activities. These improvements were seen compared to uninoculated control plants. Additionally, plants managed to resist arsenic stress due to the active production of phytohormones in the presence of microbial mixtures (Sharma et al.). The study of beneficial microorganisms can be approached via two strategies: culture-based and non-culture-based. The first represents an opportunity to study or manipulate them in interaction with various agricultural crops, and also offers the possibility of generating bioinoculants applicable in different production systems. For example, the work of Safaie et al. isolated over one thousand strains of endophytic fungi from plant tissues such as roots and shoots (from Ferula ovina, F. galbaniflua, and F. persica), which were assigned to different species across the orders Eurotiales, Pleosporales, Botryosphaeriales, Cladosporiales, Helotiales, Hypocreales, Sordariales, Glomerellales, and Polyporales. It was interesting to highlight that root tissues harbored greater diversity than aerial tissues, given their closer contact with the rhizosphere. Using techniques such as high-throughput 16S rRNA gene sequencing, the diversity of endophytic bacterial populations was determined in three Sichuan bamboo species: Phyllostachys edulis, Bambusa rigida, and Pleioblastus amarus. Out of a total of 1,159 operational taxonomic units (OTUs) possibly belonging to 811 species, the most abundant phyla were Proteobacteria, Actinobacteria, and Myxococcota. According to functional analysis with PICRUSt, the endophytic bacteria from bamboo leaves are mainly associated with six biological pathways: human diseases, metabolism, cellular processes, environmental and genetic information processing, and organ systems. This indicates that their metabolic functions jointly influence the genetics, environment, and community structure of bamboo (Yan et al.). Microbial diversity associated with a plant can be influenced by various factors, including biotic stress—particularly pathogen attacks—which can lead to the recruitment of beneficial microbes (Liu et al., 2021). Thus, Wang et al. evaluated the endophytic microbiome in walnut (Juglans regia) and how it changes in interaction with two pathogens: Colletotrichum gloeosporioides and Fusarium proliferatum. The results showed that despite changes in relative abundances, the dominant bacterial communities remained similar during infection by both pathogens. Interestingly, endophytic fungi were more sensitive to the presence of pathogens. However, both pathogens, C. gloeosporioides and F. proliferatum, promoted enrichment of beneficial bacteria such as Bacillus and Pseudomonas, which are widely reported as antagonists of pathogenic fungi and promoters of plant growth. The study also evaluated the performance of endogenous antagonistic bacteria Pseudomonas psychrotolerans and Bacillus subtilis, which showed inhibitory effects on both pathogenic fungi and participated in the interaction. The role of endophytes in challenging environments has been increasingly documented. Wang et al. provided a comprehensive analysis of dark septate endophytes (DSE) across plant roots inhabiting heavy metal-contaminated ecosystems, identifying 22 distinct DSE species and revealing that colonization patterns are profoundly shaped by environmental variables, including soil nutrient status, organic matter content, and overall fungal community diversity. Their group demonstrated that nutrient-rich soils foster higher DSE abundance, whereas heavy metal stress selects for resilient fungal communities with enhanced tolerance. This research not only elucidates the ecological determinants of DSE distribution but also establishes a theoretical foundation for leveraging these endophytes in the bioremediation of polluted habitats. In a complementary study, Dong et al. explored the contribution of native seed endophytes to tobacco resistance against Ralstonia solanacearum. High-throughput sequencing uncovered a marked enrichment of Paenibacillus in resistant varieties, and the isolated strain Paenibacillusodorifer 6036-R2A-26 demonstrated potent suppression of bacterial wilt while simultaneously promoting plant growth. These results emphasize the dual functional potential of seed-associated microbiomes in enhancing both disease resistance and crop productivity, offering new avenues for microbiome-informed breeding and biocontrol strategies. Understanding the drivers of rhizosphere community assembly is another key research focus. Ma et al. investigated the assembly of rhizosphere microbial communities across 108 plant samples, integrating analysis of root traits, soil chemistry, enzyme activity, and metabolite profiles. Their study revealed that small-molecule metabolites—such as glycerol, sorbitol, phytol, and α-ketoglutaric acid—serve as primary drivers of microbial community composition, exerting greater influence than either soil physicochemical properties or root morphological traits. Rhizobium emerged as a keystone genus shaping community structure, and experimental supplementation with these metabolites successfully steered microbial assemblages toward configurations enriched with beneficial microbes. Their research findings give emphasis to the transformative potential of targeted metabolite interventions to engineer plant-associated microbiomes for improved ecosystem function and crop performance. The integration of natural compounds with beneficial microbes provides innovative solutions. Jiang et al. explored the synergistic effects of osthole and Bacillus amyloliquefaciens on Panax quinquefolius within a forest ecosystem context. Their treatments enhanced photosynthetic efficiency, upregulated antioxidant enzyme activities, and modulated the root microbial community by increasing bacterial diversity while reducing fungal diversity. Crucially, the recruitment of growth-promoting microbes translated into increased biomass and decreased incidence of anthracnose, demonstrating the practical potential of combining natural bioactive compounds with beneficial microbes to elevate plant resilience and productivity under field conditions. Traditional agroecosystems continue to reveal valuable microbial resources. Rivera-Hernández et al. characterized the culturable rhizobacterial communities of tunicate maize grown in traditional Mexican agroecosystems and revealed stage-specific functional roles, with tasseling-stage bacteria enhancing growth and pathogen suppression, and maturity-stage bacteria contributing to organic matter mineralization and nutrient cycling. Importantly, several genera, including Rhizobium, Sphingobium, and Arthrobacter, were identified as previously undescribed plant growth-promoting rhizobacteria (PGPR) in maize landraces. This work highlights the critical importance of conserving native crops and their associated microbial genetic resources as reservoirs for sustainable agriculture and novel biotechnological applications. Conclusion In conclusion, plants and their microbiomes function as integrated holobionts whose interactions are essential for evolution, ecosystem balance, and agricultural resilience. Understanding and harnessing these partnerships offers key solutions to challenges in food security, environmental stress, and sustainable resource use.