A review of endophytic Bacillus as a model for understanding how metabolically versatile and genomically plastic bacteria establish functional, but context-dependent, associations with plants extends the discussion beyond agricultural systems to consider the use of endophytic Bacillus in wild plant systems and ecological restoration.
Abstract
The genus Bacillus, particularly endophytic species, has been widely studied as a source of plant growth-promoting bacteria in agricultural systems. These microorganisms contribute to plant performance through nutrient acquisition, phytohormone production, pathogen suppression, microbiome modulation, and enhanced tolerance to biotic and abiotic stresses. However, their ecological roles, functional plasticity, and genomic diversity remain poorly integrated into conceptual frameworks that extend beyond crop-based applications. Functional plasticity is reflected in their ability to colonize diverse plant hosts and tissues and to promote similar plant responses through distinct molecular mechanisms. Likewise, genomic diversity is evidenced by variation in accessory genomes, biosynthetic gene clusters, and regulatory networks that shape ecological functions and metabolite production. This review examines endophytic Bacillus as a model for understanding how metabolically versatile and genomically plastic bacteria establish functional, but context-dependent, associations with plants. Drawing on evidence from functional genomics, pangenomics, metabolomics, and microbial ecology, we discuss mechanisms associated with plant growth promotion and emphasize their dependence on host identity, environmental conditions, and microbial interactions. We address functional convergence arising from distinct genetic and metabolic routes, the contribution of accessory genomes and regulatory variation, and the ecological consequences of microbial inoculation in resident plant-associated microbiomes. We also highlight the limitations of in vitro screening approaches and the need for experimental validation across multiple biological scales to establish robust genotype-phenotype relationships. Finally, we extend the discussion beyond agricultural systems to consider the use of endophytic Bacillus in wild plant systems and ecological restoration, emphasizing the importance of evaluating both functional outcomes and ecological impacts.
Abstract Plant root microbial symbioses influence plant performance and ecosystem processes. Among these, dark septate endophyte (DSE) fungi are ubiquitous, non-mycorrhizal root endophytes with broad host ranges that facilitate nutrient acquisition, mitigate biotic and abiotic stress, and elicit positive, neutral, or negative plant growth responses depending on host and environmental context. Comparative genomic and transcriptomic analyses provide a robust framework for evaluating DSE lifestyles. Beyond their direct effects on plants, fungal endophytes contribute to soil microbiome networks, soil health, regenerative agriculture, and One Health. Integrating comparative genomics, transcriptomics, microbiome ecology, soil health, and agricultural studies, we present a systems-level synthesis of DSE biology that identifies key knowledge gaps and advances our understanding of DSE ecology and function. Comparative genomic, transcriptomic, and ecological evidence indicates that DSE share molecular and functional characteristics with ericoid mycorrhizal fungi, consistent with a hypothesized transition from saprotrophic toward specialized root-associated lifestyles. Their melanin production, extensive CAZyme repertoires, and broad ecological distribution suggest important roles in microbiome assembly, nutrient cycling, carbon dynamics, soil aggregation, and plant stress tolerance. We conclude by presenting an integrated framework linking plant–soil–fungus–environment interactions that defines core DSE competencies and highlights their importance for ecosystem functioning and sustainable agriculture.
K. Mandyam, A. Jumpponen· FEMS Microbiology Reviews· 0 citations
Endophytes are diverse microorganisms inhabiting plant tissues that can promote plant growth, enhance stress tolerance, or suppress pathogens. However, the ecological roles of endophytes after host senescence and death remain poorly understood. This review examines how a subset of endophytes helps maintain ecosystem function in living plants, senescent tissues, litter, and associated microbial environments. Mechanisms of endophyte-mediated plant protection in living plants include pathogen inhibition, host regulation, nutrient acquisition, and abiotic stress tolerance. We also investigate post-senescence persistence and potential roles in litter decomposition and nutrient cycling via microbial and functional legacies, priority effects, extracellular enzyme activities, and community reassembly. Vertical transmission and horizontal dispersal can move microorganisms among stages, whereas host filtering acts after arrival to determine which microorganisms establish within host tissues. However, a full same-strain life-history loop has not been established. We propose an open, non-linear ecological continuum for selected endophytes that connects endophytic colonisation, saprotrophic persistence, and potential new-host establishment. In the future, longitudinal, strain-resolved, multi-omics, and synthetic-community studies will be conducted to verify the cross-stage connections and offer a microbial framework for plant protection, litter management, and ecological restoration.
Yu-Meng Sun, Xing-bing He, Yong-hui Lin et al.· Plants· 0 citations
The rhizosphere is a narrow and dynamic soil zone where bacteria and fungi establish symbiotic and synergistic relationships with each other and with plants, collectively influencing nutrient cycling, soil health, and overall ecosystem functioning. Mycorrhiza Helper Bacteria (MHB) are a diverse group of bacterial taxa that promote mycorrhiza establishment, together with those that positively influence already established symbiotic associations. MHB have been largely described from the perspectives of interaction mechanisms, ecological functions, or agricultural applications, treating them as generalized fungal growth-promoters or biofertilizers. However, how their effects change throughout fungal development has received little attention. This review addresses this knowledge gap by reframing MHB not as generic growth promoters, but as stage-specific regulators of the fungal development program. We integrate current evidence on transcriptional responses, metabolite-mediated signaling, and emerging small RNA regulatory networks across five sequential phases of the fungal life cycle: spore germination, presymbiotic hyphal growth, mycelial expansion, root colonization, and nutrient uptake. Elucidating these stage-specific regulatory mechanisms may provide the basis for the rational, stage-targeted design of MHB-based innovative strategies for sustainable agriculture.
A. Pennesi, Antonietta Mello, M. Acquaviva et al.· Frontiers in Plant Science· 0 citations
: This review focuses on the synergistic roles of plant growth-promoting rhizobacteria (PGPR) and plant growth-promoting fungi (PGPF) in horticultural systems, highlighting their mechanisms from physiological functions to molecular regulation and community-level synergy. PGPR and PGPF enhance nutrient acquisition, modulate phytohormones, induce systemic resistance, and alleviate abiotic stresses through complementary pathways. At the molecular level, microbial signals trigger downstream signaling cascades, leading to transcriptional reprogramming and epigenetic priming for long-lasting stress memory. The coexistence of PGPR and PGPF can generate synergistic benefits that may outperform single strains under suitable host, microbial, and environmental conditions; however, challenges remain in strain antagonism, host genotype specificity, environmental dependence, formulation instability, and regulatory hurdles. This review provides a conceptual roadmap for precision microbiome management, shifting from empirical application toward predictive, mechanism-guided consortium design. Finally, leveraging advanced technologies (multi-omics, synthetic biology, and AI-driven modeling) together with the synergistic actions of PGPR and PGPF offers directions for achieving sustainable and climate-resilient horticulture.
Yu-Meng Zhao, J. Tao, Yue-Qi Tang· Phyton· 0 citations
Abstract Rhizobacteria play a central role in supporting plant growth, contributing to nutrient acquisition, stress tolerance and disease suppression. Harnessing and improving rhizosphere microbial communities therefore represents a promising avenue towards more sustainable agriculture. Recent advances in microbiome ecology and synthetic biology have enabled the rational design of microbial consortia. Synthetic communities are widely used as tractable models to study ecological interactions and are increasingly explored as biofertilizers and biocontrol agents. Here, we define engineered microbial communities (EngComs) as microbial consortia augmented with strains carrying synthetic genetic circuits. These systems extend SynCom approaches by enabling programmable functions, such as intercellular communication, division of labour, biosensing and controlled nutrient mobilization, ultimately improving functional stability in complex environments. Beyond bacteria–bacteria interactions, we highlight emerging strategies to engineer plant–microbe interfaces through synthetic signalling pathways and multi-input genetic circuits that enable context-dependent responses. Despite this progress, the engineering of rhizobacteria for real soil environments remains at an early stage. Most systems are still characterized in simplified or artificial conditions, and key challenges persist, including environmental complexity, genetic stability, biocontainment and regulatory constraints. Addressing these limitations will be essential to translate engineered functions from laboratory settings to the field. Overall, continued integration of synthetic biology with ecological and biophysical understanding of the rhizosphere will pave the way for programmable plant–microbe systems, offering new opportunities to enhance crop productivity while reducing environmental impact.
Elena Garcia-Perez, Louis Perrin, Jacob G. Malone et al.· Microbiology· 0 citations
This mini-review examines the role of rhizosphere microbiomes associated with cereal crops as functional models for extraterrestrial agriculture within closed ecological systems. The rhizosphere microbiome, conceptualized as a plant’s “second genome,” plays a central role in nutrient acquisition, stress resilience, and disease suppression through complex plant–microbe interactions. The review synthesizes current knowledge on microbiome assembly, emphasizing the contributions of soil-derived, seed-borne, and host genotype-dependent microbial communities. Particular attention is given to biological nitrogen fixation and other nutrient-mobilizing processes mediated by plant growth-promoting microorganisms, which are critical in environments where synthetic inputs are limited. Furthermore, the paper explores microbiome-mediated mechanisms of abiotic stress tolerance, including hormonal regulation and metabolic adaptation under extreme conditions. Advances in microbiome engineering - such as synthetic microbial consortia, host-mediated selection, and microbiome transplantation - are discussed as strategies to enhance plant productivity in controlled and resource-constrained environments, including space-based greenhouses. Finally, key translational challenges are identified, including context-dependent inoculant performance, ecological compatibility, and the gap between laboratory findings and field application. The review highlights the necessity of integrating multi-omics approaches, precision breeding, and genome editing technologies to fully exploit microbiome-assisted agriculture for sustainable extraterrestrial food production.
