Next Frontier: A Decade of Progress in Unraveling the Complexity of Plant-Microbe Interactions (2015-2025)

Received 19 Oct, 2025

Accepted 07 Feb, 2026

Published 31 Mar, 2026

Over the past decade, research on plant-microbe interactions has undergone a significant paradigm shift, moving from a focus on individual relationships to a comprehensive understanding of the “plant holobiont”. This review synthesizes key advancements from 2015 to the present, highlighting how a plant’s health and productivity are inextricably linked to its associated microbial communities. Major discoveries include the elucidation of a sophisticated, bidirectional molecular dialogue involving root exudates, quorum sensing, and signaling peptides that orchestrate a wide spectrum of interactions from mutualism to pathogenesis. This progress has been enabled by a technological revolution, particularly the widespread application of “omics” approaches like metagenomics and multi-omics, which have allowed for the high-resolution analysis of previously unculturable microorganisms and their functional roles. These insights are being directly applied to address global challenges, leading to the development of Plant Growth-Promoting Rhizobacteria (PGPRs), microbial biocontrol agents, and strategies to aid plant resilience to abiotic stresses. While the question of the precise mechanisms by which plants differentiate between beneficial and pathogenic microbes continues to linger, the field is transitioning from a descriptive science to a predictive one. Future research directions are focused on intentional “microbiome engineering” and leveraging computational tools to create more resilient and sustainable agricultural systems.

INTRODUCTION

The period from 2015 to the present has ushered in a fundamental paradigm shift in plant biology, moving the scientific community away from viewing plants as solitary organisms to embracing the concept of the plant holobiont¹. This perspective recognizes the plant as a complex, co-evolved ecosystem comprising the interaction of the host plant in relation to its microbial communities². This complex assemblage of microorganisms, referred to as the plant microbiome, is now understood to be crucial to plant fitness, influencing everything from growth and nutrient acquisition to disease resistance and adaptation to environmental stressors². The rapid evolution of high-throughput technologies has been instrumental in this transformation, enabling researchers to move beyond traditional, culture-dependent methods and analyze these complex microbial communities at a granular, molecular level².

The plant microbiome is not a monolithic entity; rather, it is structured into distinct ecological domains, each with a unique set of microbial inhabitants and functions. The three primary domains are the rhizosphere, the phyllosphere, and the endosphere². The rhizosphere is the subsoil layer surrounding the plant's root system, a zone teeming with microorganisms that are significantly influenced by substances released by the roots³. The important roles played by microbes in this domain in nutrient uptake, coupled with resistance to stress and diseases, cannot be overlooked³. The phyllosphere encompasses the entire above-ground surface of the plant, including the leaves, stems, and flowers⁴. This habitat is more dynamic and nutrient-poor compared to the rhizosphere and is subject to significant environmental fluctuations, such as variations in temperature, moisture, and radiation. Finally, the endosphere refers to the microbial communities that reside within the plant’s tissues, living inside or between the host cells. The recognition of the plant holobiont as a unified system has profoundly altered the direction of research. A plant’s ability to grow, thrive, and reproduce is now understood to be a direct result of its interactions with its microbiome, rather than the plant’s genetics alone⁴. This interconnectedness extends beyond a simple binary relationship. For instance, some soil bacteria are now known to participate in the symbiosis between arbuscular mycorrhizal (AM) fungi and plants, forming a “plant-AM fungus-bacterium continuum”⁴. In this tripartite relationship, AM fungi provide a habitat for soil bacteria via their vast network of extraradical hyphae, which grow through the soil and connect plant roots to soil microbial communities. In turn, these bacteria mineralize organic compounds, compensating for the limited saprophytic capacity of the fungi and making nutrients available for the plant-fungus symbiosis⁴. This shift to a multi-organismal network approach, enabled by modern analytical tools, represents a major conceptual advance that underpins much of the research detailed in this review.

SPECTRUM OF INTERACTIONS: FROM SYMBIOSIS TO SICKNESS

The relationships between plants and microbes encompass a wide and dynamic spectrum, ranging from beneficial mutualism to detrimental pathogenesis⁷. Over the past decade, research has significantly deepened the understanding of the specific molecular and genetic mechanisms that govern these interactions.

Mutualistic partnerships: The pillars of plant health: The most widely studied mutualistic relationships involve nutrient exchange, a process crucial to agricultural productivity. The interaction between leguminous plants and nitrogen-fixing bacteria, such as rhizobia, is a well-known example⁷. In this symbiosis, the bacteria colonize the plant’s roots and induce the morphology of root modified for a special function called nodules. Within these nodules, the bacteria do the conversion of atmospheric nitrogen gas into ammonia or ammonium for plant usage, while the plant gives the bacteria carbohydrates produced during photosynthesis. This partnership reduces the plant’s reliance on synthetic nitrogen fertilizers, making it a critical area of focus for sustainable agriculture⁸. Since 2015, genetic studies using model legumes have identified over 150 genes required for various stages of the legume-rhizobia symbiosis, revealing the complexity of this molecular dialogue⁹.

Another key mutualistic interaction involves mycorrhizal fungi, which form a mutualistic relationship with the many roots of land plants⁹. These fungi, particularly arbuscular mycorrhizal (AM), aid the extension of the root system of a plant through the mycelium, dramatically enhancing the absorption of nutrients by increasing the surface area (Table 1). This is especially beneficial for the uptake of less mobile nutrients like phosphorus⁹. In exchange, the plant provides the fungi with photosynthetically derived carbohydrates¹⁰. The molecular mechanisms of this relationship have been a subject of extensive research, revealing that genes involved in nutrient transfer, such as the phosphate (H₃PO₃-) transporter 1 and ammonium (NH₄ transporter 2 gene families, are consistently induced during AM symbiosis across diverse plant families¹¹.

Table 1:

Plant microbiome: Domains and functions

Domain	Location	Key microbial groups	Primary functions
Rhizosphere	Soil surrounding the root system4	Rhizobacteria (Bacillus, Azospirillum), Mycorrhizal fungi, Archaea5	Influences nutrient uptake, aids instress resistance (e.g., drought), and protects from disease
Phyllosphere	Aerial plant surfaces (leaves, stems, flowers)4	Bacteria (Methylobacterium), Fungi, Archaea, Viruses5	Can influence host physiology and metabolism; subject to dynamic environmental stress5
Endosphere	Inside plant tissues (between or within cells)4	Endophytic bacteria (Azoarcus), Fungi5	Often mutualistic, aiding in plant growth and conferring stress tolerance6

Pathogenic encounters: A constant arms race: In contrast to mutualism, pathogenic interactions are characterized by a microbe causing injury that can lead to disease, thereby having a significant negative impact on the survival of the plant and the yield¹¹. The pathogens, such as bacteria, fungi, and viruses, strategically position themselves to infest and colonize the tissues of plants, thereby producing toxins, cell wall-degrading enzymes, or proteins to affect the plant’s immune response.

The plant immune system, in turn, has evolved a sophisticated two-layered defense system, elegantly conceptualized by the “zigzag model” of plant immunity¹¹. The first layer is pathogen-associated molecular pattern (PAMP), and the second layer is pathogen-triggered immunity (PTI)¹². In PTI, plants recognize broadly conserved microbial or PAMPs, such as bacterial flagellum or fungal chitin, through cell-surface pattern recognition receptors (PRRs). This recognition activates a basal defense response that is believed to be a principal component of resistance against a wide range of microbes¹². For example, upon sensing PAMPs, plants like Arabidopsis can trigger stomatal closure to reduce bacterial entry into the leaf interior. The pathogen would have to release an effector protein into the host cell to overcome PTI¹². The second layer of plant defense, effector-triggered immunity (ETI), is a more violent and robust response that is activated when a plant recognizes these specific effector proteins through intracellular nucleotide-binding leucine-rich repeat (NLR) immune receptors¹². The ETI often culminates in a localized programmed cell death, known as the hypersensitive response (HR), at the infection site to contain the pathogen¹³.

While the zigzag model has been a powerful explanatory framework for plant-pathogen co-evolution, recent research has highlighted its limitations¹⁴. The model is primarily based on interactions with biotrophic pathogens that depend on a living host and does not fully account for the complex interplay with necrotrophs, which thrive on dead tissue, or with beneficial symbionts¹⁴. A critical, unresolved question in the field is how plants can effectively differentiate between mutualistic and pathogenic microorganisms, and how they modulate their immune responses to accommodate beneficial partners while restricting harmful ones¹⁵. For instance, studies have shown that during interactions with beneficial microbes, plants may repress the expression of certain defense-related genes, a molecular response that supports the accommodation of the symbiont without entirely suppressing immunity¹⁵. This suggests that the plant's immune system is not a simple "on/off" switch but rather a finely tuned regulatory network that is integrated with symbiotic pathways, a concept that challenges the original, more simplified interpretation of the zigzag model.

LANGUAGE OF THE ECOSYSTEM: MOLECULAR COMMUNICATION

The complex interactions between plants and their associated microbes are not random but are orchestrated by a sophisticated and bidirectional molecular dialogue¹⁵. This cross-kingdom communication involves a diverse array of chemical signals produced by both partners. The past decade has seen significant advances in identifying these signals and understanding their regulatory roles.

Table 2:

Key molecular signals in plant-microbe communication

Signal type	Origin	Example molecule	Role in interaction
Plant-derived	Root Exudates	Flavonoids	Act as chemoattractant and induce nodulation genes in16
Plant-derived	Signaling Peptides	Peptides (5-50 amino acids)	Transmit signals systemically to coordinate plant defense and symbiotic responses16
Microbe-derived	Quorum Sensing	Autoinducers (QSMs)	Coordinate microbial group behaviors like virulence, biofilm formation, and symbiosis16
Microbe-derived	Effector Proteins	Effectors	Secreted by pathogens to interfere with plant immunity and enable infection17

Cross-kingdom dialogue: Plant-derived signals: Plants actively shape their microbial communities by releasing a vast array of allelopathic substances, particularly from their roots¹⁶. These root exudates, which include sugars, organic acids, and secondary metabolites, act as chemoattractant (Table 2) that recruit particular beneficial microbes to the rhizosphere. Flavonoids are a key example of these signaling compounds. In legume-rhizobia symbiosis, flavonoids released by the plant roots attract rhizobia and influence the appearance of their morphological modification for specialized functions, which is the nod genes, which are essential for nodule formation¹⁶. Similarly, flavonoids play an ecological role in enhancing the germination of AM fungal spores and directing hyphal growth toward the plant roots. The flavonoid pattern in roots is known to change dramatically as the AM symbiosis develops, suggesting a dynamic regulatory role throughout the interaction¹⁶.

Furthermore, to small molecules, plants also use secreted signaling peptides, which are short proteins (5-50 amino acids)¹⁶. Plants are allowed to make a coordinated, systemic response to microbial partners or threats, provided the peptides transmit information between different cells or organs. This internal signaling is crucial for regulating cellular programs to either host a mutualist or activate defense responses against a pathogen¹⁶.

Microbial communication: Quorum sensing and beyond: Microbes are not passive recipients of plant signals; they also possess sophisticated communication systems to coordinate their behavior. A key mechanism is quorum sensing (QS), a cell-to-cell communication system (Table 2) that permits microbes to coordinate group activities based on population density¹⁶. Bacteria produce and release small, diffusible chemical signals called autoinducers or quorum signaling molecules (QSMs)¹⁶. As the population density of the microbe increases to a certain level, these QSMs accumulate and trigger coordinated gene expression programs that regulate group behaviors, including the production of virulence factors, antibiotic synthesis, and the establishment of biofilms¹⁶.

The dense, nutrient-rich environment of the rhizosphere, nourished by plant root exudates, provides an ideal setting for bacteria to multiply to high densities, thus enabling QS to control beneficial traits¹⁶. This molecular dialogue is not one-way. Research has revealed that microbes does secrete peptide signals that are detected by plant receptors, a strategy some pathogens use to “hijack endogenous plant signaling pathways” and evade the host immune system. In a remarkable example of co-evolutionary adaptation, plants have also developed countermeasures to this microbial communication¹⁶. They can “decipher or even sabotage” QS signals by producing their own “QS mimic molecules” and enzymes, which disrupt microbial communication and can reduce pathogen virulence¹⁶. This bidirectional communication is a critical element of the plant-microbe battlefield and represents a dynamic interplay of co-evolved signaling and counter-signaling systems.

TECHNOLOGICAL REVOLUTION: ILLUMINATING THE UNSEEN

The profound discoveries in plant-microbe interactions over the last decade have been driven by a technological revolution, particularly in the field of "omics”¹⁸. These high-throughput techniques have provided the means to analyze the community of microbes in relation to their potential functions at an unprecedented scale, moving the field beyond the inherent limitations of traditional culture-based methods, which fail to capture the vast majority of unculturable microorganisms¹⁸.

Table 3:

Omics toolkit for plant-microbe research

Omics technology	Type of data	Application in plant-microbe research
Metagenomics	Genomic and Transcriptomic DNA/RNA from entire communities	Reveals unculturable microbial diversity, functional potential (e.g., nutrient cycling, disease suppression)18
Transcriptomics	mRNA expression patterns	Shows the dynamic changes in gene expression during interactions
Proteomics	Protein profiles and post-translational modifications	Identifies essential proteins involved in symbiosis and immunity20
Metabolomics	Small molecule profiles (e.g., phytohormones, antioxidants)	Unravels communication signals and plant defense mechanisms20

Power of omics: A holistic view: Metagenomics has been a particularly transformative tool. By directly sequencing microbial DNA and RNA from environmental samples like soil and plant tissues, researchers can now comprehensively analyze the entire microbial community without the need for cultivation¹⁸ Meragenomics provides a high-resolution view of the diversity of microbes, functions, and ecological roles, revealing previously uncharacterized species and their contributions to plant health¹⁸.

However, the full power of modern research lies in the integration of multiple omics approaches, a technique known as multi-omics¹⁸. While individual omics techniques provide valuable information genomics for genes, transcriptomics for gene expression, proteomics for proteins, and metabolomics for small molecules their integration provides a holistic, systems-level understanding of the complex biological networks at play¹⁸. This integrated approach is crucial because, as studies have shown (Table 3), there can be a poor correlation between messenger RNA (mRNA) and protein expression (biological control 2025). Therefore, a joint analysis is necessary to gain a complete picture of the molecular events that govern plant-microbe interactions (biological control 2025).

Case studies in omics-driven discovery: Multi-omics has provided concrete insights into how plants and microbes interact. For example, the integration of multi-omics and bioinformatics has shown that plant-microbe symbiosis in contaminated rhizospheres influences the release of antioxidants and phytohormones, which activate the defense mechanisms in plant¹⁹. Similarly, metabolomic analysis of a pathogen-host interaction revealed that the microbe triggered the hyperaccumulation of a specific metabolite, which was found to be responsible for restricting the pathogen’s growth²⁰.

This technological shift has enabled the field to transition from a descriptive science cataloging what is present to a more functional and ultimately predictive discipline. By revealing the intricate biochemical, physiological, and molecular aspects of these interactions, omics approaches are allowing researchers to understand how the plant-microbe ecosystem²⁰. The ultimate goal, supported by the growing use of computational tools like Artificial Intelligence (AI) and machine learning, is to move toward predictive modeling of microbial functions, which is a critical step in translating foundational knowledge into practical agricultural solutions²⁰.

PRACTICAL APPLICATIONS FOR A SUSTAINABLE FUTURE

A key driver of plant-microbe research is the immense potential for its application in sustainable agriculture²¹. The last decade has focused on harnessing beneficial microorganisms to reduce fertilizer and chemical application to tackle challenges globally, which include climate change and food security²¹.

Coping with extremes: Microbes in harsh environments: Research has also increasingly focused on the role of plant-associated microbes from extreme environments, or extremophiles, in helping plants survive harsh conditions²¹. These microbes, found in habitats with high salinity, extreme temperatures, or low pH, have unique properties that enable them to promote plant growth and confer stress tolerance²¹. For instance, drought-tolerant microbes can protect plants by producing phytohormones like abscisic acid (ABA), which regulates physiological changes to reduce water loss, or by producing bacterial

Table 4:

Field trial data for PGPR-based biofertilizers

Crop	Location	Key conditions	PGPR strain(s)	Results (compared to control)
Maize	Towoomba, South Africa	Dry land conditions; less fertile shortlands soil	UP Strains (T19, T29)	Yield increase of 33% (T19) (T19) and 30% (T29)22
Wheat	Riversdale, South Africa	Severe desiccation stress (drought)	UP Strains, QCM360	Increased plant dry weight22

exopolysaccharides that help retain moisture in the rhizosphere²¹. A study found that drought conditions enrich the abundance of certain microbes, such as the Streptomyces genus of Actinobacteria, which possess thick cell walls and can form spores, making them resilient to water deficit²¹. This area of research holds significant potential for developing strategies to improve crop resilience in the face of global climate change²¹.

Plant Growth-Promoting Rhizobacteria (PGPRs) and biofertilizers: Plant Growth-Promoting Rhizobacteria (PGPRs) are a group of bacteria that are beneficial to plants, colonizing the root of the plant, thereby promoting plant growth through various mechanisms, which may be direct and indirect. These mechanisms include increasing nutrient uptake by mobilizing insoluble nutrients from the soil (Table 4), producing phytohormones (such as indole-3-acetic acid) that stimulate root and shoot growth, and mitigating abiotic stress. PGPRs also provide indirect benefits by acting as biocontrol agents, preventing the growth of phytopathogens through the production of antibiotics or by triggering plant defense programs²¹.

While PGPR-based biofertilizers have shown great promise in controlled laboratory and greenhouse settings, a significant challenge has been the inconsistency of results in real-world field conditions. A central issue is the intense competition that inoculated PGPR strains face from indigenous soil microbes, which can hinder their ability to establish a stable and long-term colonization of plant roots²².

Nevertheless, specific field trials from 2015 onwards provide compelling data on their effectiveness. In a maize field trial conducted in South Africa, specific PGPR strains resulted in yield increases of up to 33% in less fertile soil compared to the untreated control. This demonstrates that the effectiveness of these biofertilizers is often conditional on environmental factors like soil fertility²². Similarly, a wheat trial conducted under severe desiccation stress showed that all inoculated treatments increased the plant's dry weight compared to the control, indicating that the rhizobacterial treatments were able to mitigate drought stress²². These results, while not universally reproducible, show that PGPRs can be a viable tool for enhancing crop resilience.

Microbial biocontrol agents: A natural defense: Microbial biological control agents (MBCAs) are organisms used to inhibit pathogens of plants²³. They represent a natural alternative to conventional chemical pesticides. The MBCAs act through a range of modes of action, which are not mutually exclusive. Some act through direct antagonism, such as hyperparasitism, where the MBCA directly attacks the pathogen, or antibiosis, where it produces allelopathic substances that suppress the growth of pathogens²³. Examples include the fungi Trichoderma, which works against a wide range of pathogens like Fusarium, and the bacterium Bacillus subtilis, which effectively suppresses fungal growth²³.

Other MBCAs operate indirectly by priming the immune system of the plant, which is referred to as induced systemic resistance (ISR). In this mode, the beneficial microbe triggers an enhanced defensive capacity throughout the entire plant, which makes the plant more resistant to a wide range of pathogens. These induced defense mechanisms involve the plant producing reactive oxygen species, phytoalexins, and other pathogenesis-related proteins²³.

UNRESOLVED QUESTIONS AND FUTURE OUTLOOK

Despite the monumental progress of the last decade, fundamental questions persist, which will continue to drive research in the years to come²⁴.

Top unanswered questions: Perhaps the most central and long-standing question in the field is how plants manage to differentiate between beneficial and pathogenic microbes, and subsequently, how they regulate their immunity to accommodate the former while restricting the latter²⁴. This is a particularly puzzling challenge for plants, as a tremendous diversity of microorganisms, both pathogenic and mutualistic, exists in the same environment, and the plant must make a correct and rapid assessment of each²⁴. While dual recognition and other pattern-sensing mechanisms have been proposed, the precise molecular mechanisms behind this discrimination remain largely unexplained²⁴.

Other unresolved issues include fully understanding the intricate interplay between host genetics, microbial community structure, and environmental conditions that ultimately determine the outcome of an interaction whether it results in health or disease²⁴. The complexity of these systems, which are influenced by a myriad of factors and can vary by cell type, organ, and developmental stage, presents a major intellectual and technical challenge for researchers²⁴.

Next-generation research directions: The future of plant-microbe research will be defined by a shift from a descriptive science to a more predictive and engineering-driven discipline²⁵. The advent of multi-omics has provided a holistic view of microbial functions, which is now enabling the next wave of research focused on intentional manipulation and control²⁵.

One major direction is microbiome engineering, the intentional modification of plant-associated microbial communities to enhance specific traits, such as improved stress tolerance or disease suppression²⁵. Researchers are now working to develop new bio-fertilizers and biopesticides by identifying and harnessing beneficial microbes and their functional traits²⁵. This field will be significantly accelerated by the use of computational advancements, including AI and machine learning, which are enabling the predictive modeling of microbial functions and the identification of key microbial consortia with agricultural benefits²⁵.

Furthermore, the discovery of novel evolutionary pathways in plants has opened up the potential for synthetic biology and the creation of “designer enzymes”²⁵. By tracing the genetic and molecular paths plants have taken to perform unique chemical reactions, researchers can now recreate and optimize these processes in a laboratory setting²⁵. The process could lead to the production of new catalysts and bioactive compounds that can modulate plant-microbe interactions with high precision²⁶.

Finally, the increasing use of “pan-omics” the combination of pan-genomics, pan-transcriptomics, pan-proteomics, and pan-metabolomics (Table 3) will be crucial for accounting for the genetic and functional variation that exists across different plant accessions and their associated microbiomes²⁶. This comprehensive, systems-level approach is necessary to develop more resilient crop varieties that can withstand the complex abiotic and biotic stresses of a rapidly changing global climate²⁷.

CONCLUSION

Research conducted from 2015 to 2025 has fundamentally reshaped the understanding of plant-microbe interactions by establishing the plant holobiont as a central biological and ecological unit. Advances in molecular signaling and multi-omics approaches have revealed that plant fitness and productivity are governed by highly coordinated, bidirectional communication with associated microbial communities. Although PGPR-based biofertilizers and microbial biocontrol agents show strong potential, inconsistent field performance remains a major limitation. Integrating systems biology, synthetic microbiology, and predictive modeling is essential to translate laboratory insights into stable, field-ready agricultural solutions. Collectively, these developments position plant–microbe research as a cornerstone of sustainable and climate-resilient agriculture.

SIGNIFICANCE STATEMENT

This review provides a decade-scale synthesis of key conceptual, molecular, and technological advances in plant microbe interaction research, emphasizing the transition from reductionist studies to a holistic holobiont framework. By consolidating evidence from multi-omics, molecular signaling, and applied microbiome studies, it highlights how microbial communities can be strategically leveraged to enhance crop productivity and stress tolerance. The analysis underscores current limitations in field translation and identifies microbiome engineering and computational prediction as critical future directions. These insights are highly relevant for researchers, agronomists, and policymakers aiming to develop sustainable, biologically driven agricultural systems under changing environmental conditions.

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