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Review

Soil Symphony: A Comprehensive Overview of Plant–Microbe Interactions in Agricultural Systems

by
Arpitha Chatchatnahalli Tharanath
1,
Raje Siddiraju Upendra
2 and
Karthik Rajendra
2,*
1
School of Applied Sciences, REVA University, Bangalore 560064, India
2
School of Electronics and Communication Engineering, REVA University, Bangalore 560064, India
*
Author to whom correspondence should be addressed.
Appl. Microbiol. 2024, 4(4), 1549-1567; https://doi.org/10.3390/applmicrobiol4040106
Submission received: 11 October 2024 / Revised: 25 November 2024 / Accepted: 25 November 2024 / Published: 27 November 2024
(This article belongs to the Special Issue Microbiome in Ecosystem, 3rd Edition)
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Abstract

:
The rhizosphere, a narrow region of soil surrounding plant roots, is an environment rich in microbial diversity that profoundly influences plants’ health, growth, and agricultural productivity. This microbial community, known as the rhizosphere microbiome, consists of a complex array of bacteria, fungi, archaea, and other microorganisms that engage in complex interactions with plant roots. These microorganisms contribute to nutrient cycling, mineral uptake facilitation, and protection against soil-borne pathogens, thereby promoting plant growth and resilience towards biotic and abiotic stresses. Additionally, microbial signaling molecules, including phytohormones such as auxins, cytokinin, gibberellins, ethylene, and abscisic acid, play a pivotal role in regulating these interactions by modulating plants’ responses to environmental stressors. Recent advancements in microbiomics have enabled a deeper understanding of the rhizosphere’s diversity, composition, and functions, paving the way for more sustainable agricultural practices. By harnessing the potential of the rhizosphere microbiome, innovative strategies can be developed to reduce dependency on synthetic agrochemicals, enhance soil fertility, and increase crop yields. This review discusses the diversity and mechanisms of plant–microbe interactions, focusing on the role of microbial signaling molecules, and explores their applications in promoting agricultural sustainability. The insights gained from microbiomics studies can revolutionize farming practices by reducing dependency on chemical inputs, enhancing crop productivity, and nurturing soil health and environmental sustainability.

1. Introduction

The rhizosphere, the soil region adjoining plant roots, hosts a complex and dynamic microbial community known as the rhizosphere microbiota. This microbiome plays a key role in shaping plant health, plant growth, and overall ecosystem functioning in agriculture [1]. The rhizosphere is a critical interface between the plant roots and the surrounding soil. This narrow region, packed with a distinct array of microorganisms, represents a vibrant ecosystem that strongly influences plants’ overall growth and development [2]. Within the rhizosphere, intricate interactions occur between plant roots and countless microbiomes, including fungi, bacteria, archaea, and other microorganisms. These interactions are symbiotic and often mutualistic, developing a complex web of relationships where microorganisms help in nutrient uptake, disease suppression, and stress tolerance mechanisms in the associated plants [3]. The significance of the rhizosphere microbiome lies in its multilayered contributions to plant health and productivity. These microbial communities involve themselves in various functions that are crucial for plant development, such as nutrient cycling, mineral uptake facilitation, and protection against soil-borne pathogens [4]. Furthermore, they assist in the synthesis of growth-promoting substances, such as auxins (e.g., indole-3-acetic acid), cytokinin, and gibberellins, which stimulate root growth and enhance overall plant development. Additionally, they produce enzymes, including cellulases, chitinases, and phosphatases, that facilitate the breakdown of complex organic compounds like cellulose, lignin, and chitin. This breakdown process releases simpler molecules that are more readily available for plant uptake, thereby enhancing the availability of essential nutrients such as nitrogen, phosphorus, and potassium, which are crucial for plant growth and productivity [5].
Understanding the intricate dynamics within the plant rhizosphere and characterizing the diversity, composition, and functions of its microbiome through microbiomics studies has become increasingly crucial for advancing sustainable agricultural practices [6]. By harnessing this knowledge, scientists and agronomists aim to develop innovative strategies that influence these microbial communities to reduce reliance on synthetic agrochemicals, enhance soil fertility, improve crop yields, and mitigate environmental impacts, thereby promoting a more sustainable agricultural approach [7]. Microbiomics studies focusing on the plant rhizosphere offer a promising path for unravelling the complexities of these interactions and provide insights into methods for harnessing the potential of rhizosphere microbiomes to ensure food security, promote sustainable farming practices, and maintain the ecological balance of agricultural systems [8].

2. Plant–Microbe Interactions: Nature’s Secret Superheroes

2.1. Diversity of Plant–Microbe Interaction

Exploring the various categories of plant–microbe interactions is necessary to comprehending their roles in agriculture, ecosystems, and environmental sustainability [9]. These interactions can be broadly classified into mutualistic, pathogenic, and commensalistic relationships, each with distinct impacts on plant health and ecosystem dynamics [10]. Figure 1 represents the diverse types of interactions involved in the rhizosphere, which includes plant–microbe interactions and microbe–microbe interactions.
Table 1 presents the distinct types of microbial interactions in soil, where ‘+’ represents a positive effect, ‘-’ depicts a negative effect, and ‘0’ represents a neutral or no effect.

2.2. Positive Interactions

These interactions refer to mutually beneficial relationships between plants and microorganisms that impact the growth, development, and overall well-being of both partners. These interactions play vital roles in several ecological processes, including nutrient cycling, soil fertility, and plant resistance to environmental stresses. Several types of positive interactions exist in plant–microbe interactions, including mutualistic symbioses, commensalism, and facilitation [11].
Mutualistic interaction involves a beneficial relationship between plants and microorganisms, where both parties derive advantages [12]. Key microbial players are rhizobia (legume symbiosis: nitrogen-fixing bacteria such as Rhizobium and Bradyrhizobium form nodules on legume roots and, through this interaction, legumes gain access to nitrogen in the form of ammonium (NH4⁺), while rhizobia receive carbon compounds, such as sucrose, glucose, and other carbohydrates or organic acids, from the host plant, mycorrhizal association arbuscular mycorrhizal fungi (AMF) and ectomycorrhizal fungi (EMF) form associations with plant roots, improving nutrient uptake, specifically phosphorus in the form of phosphate (PO43−), and enhancing plant tolerance to stress) and mycorrhizal fungi, which form widespread networks of hyphae that outspread into the soil, facilitating water and nutrients uptake by plant roots. In return, the fungi receive organic carbon, such as glucose, fructose, and other sugars, from the host plant [13].
Protocooperation is a form of symbiotic relationship where organisms benefit from each other’s existence or activities without being completely dependent on each other for survival [14]. Protocooperation includes nitrogen-fixing bacteria in soil ecosystems that offer usable nitrogen to the nearby plants in the form of ammonium (NH4⁺) and other nitrogen compounds, while acquiring energy from nitrogen fixation, and mycorrhizal fungi, including AMF and EMF, which aid plants in nutrient uptake, particularly the uptake of phosphorus (as phosphate, PO43−), potassium, and micronutrients like zinc and copper, benefiting both parties [15]. Lichens, combined with fungi and algae, demonstrate mutual benefits through structural support and supplying carbohydrates [16].
Facilitation involves positive interactions where one organism boosts the survival or growth of another organism without obtaining direct benefits in return [17]. In plant–microbe interactions, facilitative interactions can occur between plants and soil microbiota that improve the soil structure, enhance nutrient availability (e.g., nitrogen, phosphorus, potassium, and micronutrients), and suppress pathogens, leading to improved plant growth and development. Some soil bacteria produce antibiotics that inhibit the growth of pathogenic microorganisms, hence indirectly benefiting neighboring plants [18].
Syntrophism (or syntrophy), also known as cross-feeding, is a biological phenomenon in which two or more distinct species interact in a mutually beneficial way to degrade complex organic compounds that neither organism could degrade alone) [19]. In the rhizosphere, syntrophic interactions play a critical role in the breakdown of organic compounds released by plant roots, particularly in anaerobic or low-oxygen microenvironments. Here, one organism breaks down a compound partially and releases metabolic byproducts, which are then utilized by another organism to finish the degradation process. This process is particularly important in the rhizosphere for the breakdown of complex organic compounds such as aromatic compounds (e.g., lignin, phenolic acids), long-chain fatty acids (e.g., palmitic acid, oleic acid), and certain amino acids (e.g., tryptophan, glutamine), which are difficult to degrade in oxygen-limited environments [20]. Understanding the dynamics and mechanisms of syntrophic interaction is essential to boosting biotechnological processes and managing microbial communities in anaerobic environments [21].
Commensalism involves one organism benefiting from an association but the other remaining unaffected. Some of the examples of commensalism include epiphytic bacteria (Pseudomonas fluorescens colonizing plant surfaces (leaves and stems) and delivering protection against pathogens through competition and antibiosis, without harming the host plant), epiphytic fungi (Cladosporium cladosporioides colonizing the internal tissues of plants without causing disease, and aiding in improving stress tolerance and plant growth), and non-pathogenic endophytes [22]. The manipulation of this interaction through biocontrol agents and beneficial microorganisms could be a promising approach to sustainable disease management in agriculture.
Overall, positive interactions are essential for maintaining the functioning of ecosystems, promoting plant health, and enhancing agricultural productivity. Understanding the mechanisms and ecological implications of these interactions is necessary for the sustainable management of agricultural and natural ecosystems [23].

2.3. Negative Interactions

Negative interactions or pathogenic interactions involve detrimental effects on plant health due to microbial pathogens [24]. This includes plant interactions with fungal pathogens (fungi such as Phytophthora spp., Fusarium spp., and Botrytis spp. cause various plant diseases, including root rots leading to significant yield loss), bacterial pathogens (bacteria such as Pseudomonas syringae, Xanthomonas spp., and Ralstonia solanacearum infect plants and cause diseases such as bacterial spot, bacterial blight, and bacterial wilt), viral pathogens (viruses such as tobacco mosaic virus (TMV), potato virus Y (PVY), and tomato yellow leaf curl virus (TYLCV) infect plants, leading to symptoms such as leaf mottling, stunting, and reduced yield) [25].
Amensalism (Antagonism) is a type of interspecific interaction wherein one organism is harmed or inhibited while the other organism is unaffected or stays neutral. Amensalism can occur when certain microorganisms release allelochemicals or toxins that inhibit the growth or activity of other microorganisms or plant roots [26]. For example, Pseudomonas fluorescens produces a variety of toxins like pyocyanin, which can suppress plant root growth and inhibit the development of competing microorganisms. Some fungi, like Trichoderma spp. and Fusarium spp., produce secondary metabolites like antibiotics (e.g., trichothecenes, penicillin) that hinder the growth of competing microorganisms or plant pathogens in the soil [27,28]. This process is a competitive advantage for the producing organism while negatively affecting the growth of other organisms in the community. Understanding this interaction in the rhizosphere is crucial for revealing microbial community dynamics and their inferences for ecosystem functioning and plant health [29].
Competition occurs when plants and microorganisms contest for limited resources like nutrients, space, and water. Root exudates, comprising several organic compounds that are released by plants, play a significant role in shaping these competitive interactions by bringing together beneficial microorganisms, discouraging pathogens, and influencing the diversity and composition of the rhizosphere microbiome [30]. These exudates include compounds such as sugars (e.g., glucose, rhamnose, pentose, xylose, raffinose, ribose, mannitol, and sucrose), amino acids (all 20 proteinogenic amino acids, homoserine, l-hydroxyproline, mugineic acid, aminobutyric acid), organic acids (e.g., citric acid, sinapic acid, chorismic acid, hikimic acid, isocitric acid, caffeic acid, and malic acid), and phenolic compounds (e.g., flavonoids, benzoic acid) [31]. Microbial competition can directly impact plants’ growth and overall development by altering nutrient availability, overcoming pathogen propagation, and modifying plant hormone signaling pathways. Understanding the processes and effects of competition is essential for developing sustainable agricultural practices, enhancing plant yield, and managing soil microbial communities [32].
Parasitism in plant–microbe interactions is a key aspect of the rhizosphere with deep implications for plant health and ecosystem dynamics. In this type of interaction, certain microbial species use plants as hosts, obtaining nutrients and resources at the cost of the plant’s well-being. This detrimental relationship often results in stunted plant growth, decreased productivity, and increased susceptibility to pests and diseases [33]. Several types of parasitic microorganisms, like Xanthomonas spp. (bacteria), Fusarium spp. and Phytophthora spp. (fungi), and Meloidogyne spp. (nematodes), can infect plant roots, stems, and leaves, or other tissues, leading to symptoms extending from wilting and stunting to necrosis and death. Understanding the mechanisms and dynamics of parasitism is vital for formulating effective strategies to mitigate plant diseases and enhance agricultural yields, eventually contributing to sustainable agricultural practices [34].
Predation in the context of plant–microbe interactions refers to the feeding of one microbial organism on another. Predatory microorganisms play a fundamental role in regulating microbial populations and nutrient cycling. Predators including protozoa, such as amoebae and flagellates, vigorously feed on bacteria and other minor organisms in the soil [35]. This predation affects the composition and abundance of microbial communities, influencing nutrient mineralization and organic matter decomposition, and can impact plant health indirectly by altering nutrient availability and the dynamics of the microbiome in the rhizosphere [36]. Table 2 presents the diversity of plant-microbe interactions in agricultural systems.

3. Mechanisms of Plant–Microbe Interactions

These interactions involve complex molecular, physiological, and ecological mechanisms that facilitate communication and symbiotic relationships between plants and microbiomes [51]. Understanding these mechanisms is crucial for interpreting the changing aspects of these interactions and their influence on plant health, growth, and adaptation to environmental stresses [52]. This mechanism involves the molecular signaling pathways and physiological responses that mediate plant–microbe interactions, with a primary impact on microbial signaling molecules and the mechanisms by which beneficial microorganisms encourage plant growth, development, and stress tolerance [53].
Molecular signaling plays a leading role in facilitating communication connecting plants and microorganisms, allowing them to recognize and respond to each other’s presence [54]. Plants release signaling molecules, such as phytohormones and secondary metabolites, in response to microbial colonization or pathogen attack. These signaling molecules can modulate plant growth and development, activate defense responses, and promote symbiotic interactions with beneficial microorganisms [55].
Microorganisms also produce signaling molecules, such as quorum sensing molecules, which enable them to communicate and coordinate their activities within microbial communities [56]. Quorum sensing regulates various microbial behaviors, including virulence factor production, biofilm formation, and gene expression, in response to changes in population density [57].

3.1. Plant-Released Signals

Flavonoids exuded from plant roots serve as important signaling components in various plant–microbe interactions, such as the formation of mycorrhiza and the establishment of legume–rhizobia symbiosis [58]. Figure 2 depicts the various components of root exudates and their roles in the rhizosphere. In the context of AMF–plant interactions, flavonoids play a noteworthy role in hyphal growth, spore germination, root colonization, and differentiation. Beyond their involvement in AMF–host symbiosis, flavonoids also support the development of host-specific rhizobia by acting as chemo attractants and inducing nodulation (nod) genes responsible for synthesizing lipochitin–oligosaccharide signaling molecules known as Nod factors [59]. Table 3 presents the various signals released by plants in plant–microbe interactions.

3.2. Microbial Signalling Molecules in Plant–Microbe Interactions

Microbial signaling molecules play a significant role in mediating communication between plants and microbiota, facilitating the setting-up of symbiotic relationships and controlling plant responses to environmental stimuli [81]. Phytohormones, like auxins, cytokinin, gibberellins, ethylene, and abscisic acid, are key regulators of plant growth, development, and stress responses [82]. These phytohormones can be produced by both plants and microorganisms and serve as signaling molecules that modulate plant–microbe interactions [83].
Quorum sensing (QS) is a communication system utilized by bacterial cells, involving chemical signals known as autoinducers, to regulate the behaviour of whole populations of both Gram-positive and Gram-negative bacteria. Three classes of signaling molecules, Al-1, Al-2, and Al-3, have been identified, each with slightly divergent functions. However, it is important to note that quorum sensing encompasses not only interactions between bacteria but also a broader range of interspecies interactions [84]. Quorum sensing allows microorganisms to sense the population densities of other organisms and adjust their gene expression patterns accordingly, enabling them to coordinate collective behaviours like biofilm formation, virulence factor production, and antibiotic synthesis [85].

3.3. Physiological Mechanisms of Plant Growth Promotion by Beneficial Microbiome

Beneficial microorganisms increase plant growth, confer tolerance to environmental stresses, and enhance nutrient acquisition through various physiological processes. One such mechanism is the release of plant growth-promoting substances, including cytokinin, indole-3-acetic acid (IAA), gibberellins, and enzymes engaged in nutrient solubilization [86]. These substances stimulate plant growth by encouraging cell division, elongation, and differentiation, as well as enhancing plants’ nutrient uptake and utilization efficiency [65].
They also improve nutrient acquisition by solubilizing insoluble forms of nutrients, like iron, phosphorus, and zinc, in the soil by means of producing organic acids, siderophores, and phosphate-solubilizing enzymes. This increases the availability of essential nutrients to plants, thereby promoting their growth and development [87].
Besides promoting plant growth and nutrient acquisition, beneficial microorganisms confer tolerance to environmental stresses by stimulating systemic resistance mechanisms in plants [88]. Systemic acquired resistance (SAR) and induced systemic resistance (ISR) are two key defense mechanisms that enhance plant immunity and protect plants against pathogens and environmental stresses [89]. Beneficial microorganisms trigger these resistance mechanisms by priming the immune systems of plants through the production of elicitors, antimicrobial compounds, and VOCs, which activate defense responses in the plant [90]. Figure 3 shows the mechanisms of plant stress tolerance (both biotic and abiotic stresses) induced by beneficial microorganisms.
Plant–microbe interactions involve complex molecular signaling pathways and physiological responses that mediate communication and symbiotic relationships between plants and microorganisms [91]. Microbial signaling molecules, like phytohormones and quorum sensing molecules, play key roles in coordinating these interactions, while beneficial microorganisms promote plant growth and stress tolerance through physiological mechanisms, including the production of growth-promoting substances, nutrient solubilization, and the induction of systemic resistance [92]. Table 4 presents the various physiological responses seen in plant–microbe interactions. Apprehending these mechanisms is necessary for utilizing the potential of plant–microbe interactions to enhance agricultural productivity and promote sustainable crop production in diverse environmental conditions [93].

4. Applications of Plant–Microbe Interactions in Agriculture and Environmental Sustainability

Plant–microbe interactions have noteworthy implications for sustainable agriculture and environmental management (Nadeem et al. 2013) [100]. This section highlights the potential of harnessing beneficial plant–microbe interactions to improve crop productivity, reduce the use of synthetic fertilizers and pesticides, and enhance soil health and fertility [9]. It is an extensively accepted fact that certain novel and prominent microbial strains, referred as plant growth-promoting microorganisms (PGPMs), improve plant growth, protect plants from pathogens, improve plant fitness, and help to uphold soil health under extreme environmental conditions [101,102].
The microbiomes accompanying plant ecosystems have been categorized into three categories, e.g., rhizospheric, phyllospheric, and endophytic [103]. The phyllosphere (leaves—phylloplane, stems—caulosphere, fruits—carposphere, and flowers—anthosphere) is a regular niche for interaction among microorganisms and plants [104].
The unselective use of chemical fertilizers and pesticides has triggered huge environmental losses over the years. However, the predicted increasing demand for food in the upcoming years and decades demands the use of increasingly productive and effective agriculture [105]. Numerous studies performed in recent years have demonstrated how the PGPMs can be an effective alternative to and a valid environmentally friendly substitute for chemical industry products [106].

4.1. Plant Health and Productivity in Agriculture

Plant–microbe interactions significantly enhance plant health and productivity in agricultural systems. Beneficial microorganisms like PGPRs and mycorrhizal fungi aid in promoting plants’ nutrient uptake, growth, stress tolerance, and development [107]. PGPRs fix atmospheric nitrogen, solubilize phosphorus, produce phytohormones, and suppress pathogens, thus encouraging plant growth and health [108]. For example, inoculation with Azospirillum brasilense in maize was reported to increase the plants’ yield by 15–30% through enhanced nitrogen fixation and root growth [109]. Similarly, the application of Pseudomonas fluorescens in wheat led to a significant yield increase of up to 20% by improving phosphorus solubilization and disease resistance [108]. Likewise, mycorrhizal fungi construct symbiotic associations with roots, facilitating nutrient uptake (especially phosphorus) and improving water absorption, thus enhancing plant growth and stress resilience [110]. For instance, Glomus intraradices, an arbuscular mycorrhizal fungus, has been documented to increase tomato yields by over 25% due to improving the nutrient and water uptake [111]. Moreover, beneficial microorganisms act as biological control agents, antagonizing plant pathogens and reducing the need for synthetic pesticides, further contributing to plant health and productivity [112].

4.2. Enhanced Nutrient Acquisition

Plant–microbe interactions play a vital role in enhancing nutrient acquisition by plants, specifically in nutrient-limited environments. Microorganisms, like mycorrhizal fungi and nitrogen-fixing bacteria, form symbiotic associations with plants and facilitate nutrient uptake from the soil [113]. Mycorrhizal fungi extend their hyphal networks into the soil, increasing the surface area for nutrient absorption by up to 700% compared to non-mycorrhizal plants, thereby enhancing the uptake of essential nutrients like phosphorus, nitrogen, and micronutrients such as zinc and copper [114,115]. In nutrient-poor soils, plants without mycorrhizal associations often exhibit a stunted growth and reduced yield, highlighting their reliance on these symbiotic fungi for nutrient acquisition [116].
Nitrogen-fixing bacteria, such as Rhizobium in legume root nodules, tranform atmospheric nitrogen into ammonia through nitrogen fixation, providing plants with a readily available source of nitrogen for growthe and development [117]. Studies have shown that leguminous plants with rhizobia symbiosis can acquire up to 60% more nitrogen compared to non-symbiotic plants, which often exhibit limited growth in nitrogen-deficient soils. Additionally, correlations between reduced microbial populations (e.g., due to soil degradation or low microbial diversity) and inhibited plant growth further emphasize the significance of these interactions, as plants lacking adequate microbial associations struggle to meet their nutrient needs and exhibit lower biomass and productivity [118].

4.3. Enhanced Nutrient Cycling and Soil Health

Plant–microbe interactions are essential for enhancing nutrient cycling and soil health in agricultural systems. Mycorrhizal fungi and nitrogen-fixing bacteria facilitate nutrient mobilization and uptake by plants, thus improving the soil fertility and promoting sustainable crop production [119]. These microorganisms contribute to efficient nutrient cycling by converting atmospheric nitrogen into plant-available forms like ammonium (NH4⁺) and nitrate (NO3−), which are directly usable by plants. Studies indicate that nitrogen-fixing bacteria can increase the nitrogen availability by up to 50% in nitrogen-deficient soils, significantly enhancing crop growth [120]. Mycorrhizal fungi enhance the cycling of phosphorus by breaking down soil-bound phosphates, increasing the phosphorus availability by 30–50% in some agricultural settings. These interactions also improve the uptake of specific micronutrients, such as zinc and copper, by facilitating their movement to plant roots. An improved soil structure arises from microbial secretions, such as polysaccharides and organic acids, which bind soil particles into stable aggregates. This aggregation improves the soil aeration, water retention, and root penetration, creating a healthier and more resilient soil environment [121]. Additionally, soil microbiomes, including beneficial bacteria, fungi, and protozoa, promote disease suppression and soil health by encouraging competitive exclusion, antibiotic production, and the induction of plant defenses, leading to healthier soils and resilient plants [122].

4.4. Soil Erosion Control and Phytoremediation

Plant–microbe interactions play key roles in controlling soil erosion and phytoremediation practices [123]. Mycorrhizal fungi, particularly AMF, promote soil stability by enhancing soil aggregation and stabilization, while plant root systems anchor soil, preventing erosion and promoting soil resilience. This occurs via the secretion of a compound called glomalin, a glycoprotein that binds soil particles together, forming stable soil aggregates. These aggregates improve soil structure by creating a network that resists breakdown, enhancing water infiltration and reducing surface runoff that contributes to erosion. Additionally, mycorrhizal hyphae extend into the soil and physically interweave with soil particles, further anchoring the soil and reinforcing structural integrity. Moreover, plant root systems, in combination with mycorrhizal fungi, anchor soil layers and prevent erosion by reducing soil detachment and displacement during heavy rainfall or wind events. These interactions are integral to sustainable land management and environmental conservation efforts, as they help preserve soil integrity, support nutrient retention, and promote ecosystem health over time. These interactions contribute to sustainable land management practices and environmental conservation efforts by preserving soil integrity and ecosystem health [124].

4.5. Improvement of Stress Tolerance

These interactions contribute to the improvement of plant stress tolerance, allowing plants to withstand various environmental stresses. Beneficial microorganisms can provoke systemic resistance mechanisms in plants, such as SAR and ISR, which enhance plant immunity and protect against pathogens [125]. Additionally, microbial inoculants containing PGPR have been shown to boost plants’ tolerance to abiotic stresses, including salinity, drought, and heavy metal toxicity, through mechanisms such as osmotic adjustment, antioxidant enzyme activity, and hormone regulation [126].

4.6. Protection Against Pathogens

Plant–microbe interactions play a fundamental role in safeguarding plants against pathogens and diseases, thus improving plant health and reducing yield losses. Beneficial microorganisms can suppress the growth and activity of plant pathogens through several mechanisms, including competition for resources, the production of antimicrobial compounds, the induction of systemic resistance, and the modulation of plant defense responses [127]. The significance of the symbiotic relationships among plants and microorganisms lies in strengthening the native plant’s immune system against pathogenic attacks. The fundamental defensive strategies composed by core microorganisms include elevating the antioxidant ability of plants through the reconfiguration of defense-related enzymes, regulating quorum sensing mechanisms, and stimulating the phenylpropanoid pathway to promote the synthesis of phenolics, deposition of lignin, and initiation of transgenerational defense responses [128]. The microbiome acts as a frontline defense against plant pathogens by outcompeting harmful microorganisms for space and nutrients. Beneficial microorganisms can produce antimicrobial compounds or ISR, boosting their ability to defend against pathogens [8]. For example, Pseudomonas fluorescens, PGPR, protects against the pathogenic fungus Fusarium oxysporum in tomato plants by producing antibiotics like 2,4-diacetylphloroglucinol (DAPG), which directly inhibits pathogen growth. Similarly, Bacillus subtilis, another beneficial bacterium, is effective against Rhizoctonia solani, a soil-borne pathogen that affects various crops by producing lipopeptides that target and suppress it [129].

4.7. Environmental Sustainability and Bioremediation

Plant–microbe interactions are helpful in promoting environmental sustainability, particularly through bioremediation practices. Phytoremediation, for example, involves utilizing plants and associated microorganisms to remediate contaminated soils or water [130]. Hyperaccumulator plants such as Brassica juncea (Indian mustard), Helianthus annuus (sunflower), and Pteris vittata (Chinese brake fern) can absorb and accumulate pollutants, while associated microorganisms aid in the detoxification or degradation of contaminants, effectively cleansing the environment ([131]. Moreover, microorganisms contribute to biodegradation by breaking down pollutants in soil or water through enzymatic processes, thus playing a crucial role in environmental cleanup efforts and promoting sustainability [132]. Associated microorganisms further support this detoxification process. For example, Pseudomonas putida can degrade hydrocarbons such as benzene, toluene, and xylene, which are commonly found in petroleum-contaminated sites, while Rhizobium species can help break down organic contaminants like pesticides. Together, these plants and microorganisms effectively cleanse the environment; for instance, in certain applications, pollutant concentrations can be reduced by up to 90% over several months depending on the contaminant and conditions [133].
Moreover, microorganisms play a pivotal role in biodegradation through enzymatic processes. Deinococcus radiodurans, known for its radiation resistance, can metabolize organic solvents and heavy metals, while Phanerochaete chrysosporium, a white-rot fungus, produces enzymes like lignin peroxidase and manganese peroxidase that degrade persistent organic pollutants (POPs) such as polychlorinated biphenyls (PCBs) and dioxins. These microbial actions are essential to environmental cleanup efforts, offering eco-friendly alternatives to chemical and physical remediation methods, and significantly promoting sustainability [134].

5. Future Directions and Challenges

Despite advances in understanding plant–microbe interactions, several challenges and opportunities remain for further research and application. Future research directions can be aimed at illuminating the complex dynamics of plant–microbe interactions in natural and agricultural ecosystems [135]. There are various challenges associated with scaling up microbial-based technologies for widespread adoption in agriculture and there is an indefinite need for interdisciplinary approaches to address key research gaps and promote the sustainable use of these interactions in agricultural and environmental frameworks. These interactions are fundamental processes that shape plant growth, health, and adaptation to environmental stress [136]. Understanding and harnessing these interactions hold great promise for advancing sustainable agriculture, improving crop resilience, and mitigating environmental challenges in the face of global environmental change [137].
The mechanisms of plant–pathogen interactions are complex and involve a series of molecular and physiological processes. Microbial pathogens produce virulence factors, such as toxins, cell wall-degrading enzymes, and effector proteins, to colonize plant tissues and suppress host defenses [138]. For example, Pseudomonas syringae produces the toxin coronatine, which suppresses plant immune responses, while cell wall-degrading enzymes like cellulases, xylanases, and pectinases, produced by pathogens such as Botrytis cinerea, break down plant cell walls to facilitate infection. Pathogen-derived effector proteins, like Avr proteins in bacterial pathogens, target specific plant proteins to subvert immune responses and promote colonization [139].
In response, plants activate a range of defense mechanisms, including physical, chemical, and immune responses. Physical barriers include the formation of lignified cell walls and the accumulation of callose to reinforce the plant’s cell structure. Chemical defenses encompass the production of antimicrobial compounds such as phytoalexins and ROS to inhibit pathogen growth. Additionally, plants initiate immune responses through signaling pathways that recognize pathogens and trigger defense responses. This includes the use of pattern recognition receptors (PRRs), such as FLS2 (which detects flagellin) and EFR (which recognizes bacterial elongation factors), as part of pattern-triggered immunity (PTI). When pathogens deliver effectors into plant cells, plants employ effector-triggered immunity (ETI) as a second layer of defense, often involving resistance (R) proteins that detect these effectors, activating a robust response which sometimes leads to localized cell death (hypersensitive response) to contain the pathogen ([140,141].
The effective management of plant diseases relies on integrated pest management (IPM) approaches that merge cultural, chemical, and biological control methods [142]. Cultural practices, like crop rotation, sanitation, and the use of resistant crop varieties, can help reduce disease incidence by minimizing the prevalence of pathogen inocula and creating unfavorable conditions for pathogen proliferation [143]. Chemical control involves the use of fungicides, bactericides, and other pesticides to suppress pathogen growth and spread. Biological control methods, including the use of beneficial microorganisms, biocontrol agents, and microbial antagonists, offer environmentally friendly alternatives to chemical pesticides and can help manage plant diseases sustainably [144]. Biological control methods provide sustainable alternatives by harnessing beneficial microorganisms and antagonistic microorganisms to suppress pathogens. For example, Bacillus subtilis and Trichoderma harzianum produce antibiotics and compete with pathogens for resources, thereby preventing infections. These biocontrol agents not only reduce the need for chemical pesticides but also support soil health and biodiversity, making them valuable tools in sustainable agriculture [145].

6. Conclusions

Plant–microbe interactions have deep impacts on plant health and productivity by influencing various aspects of plants’ physiology and metabolism, and through improving nutrient acquisition, enhancing stress tolerance, and protecting plants against pathogens. Mycorrhizal fungi and nitrogen-fixing bacteria facilitate nutrient uptake, while other beneficial microorganisms induce systemic resistance mechanisms and inhibit pathogen growth, contributing to increased plant growth, yield, and agricultural sustainability. These interactions involve a wide range of microorganisms, including bacteria, fungi, archaea, and viruses, which interact with plants through diverse mechanisms. Understanding the dynamics of these interactions is essential to elucidating ecosystem functioning, optimizing agricultural practices, and promoting environmental sustainability. This paper delves into the mechanisms, significance, and applications of these interactions in agriculture and environmental sustainability and highlights their promising applications in sustainable agriculture and environmental management. Furthermore, exploration of the soil microbiome needs to step beyond assessments of composition to incorporate functional attributes of soil microbiomes.

Author Contributions

Conceptualization & methodology: A.C.T.; Data curation: K.R.; Writing—original draft preparation: A.C.T.; Writing—review and editing: K.R. and R.S.U. All authors have read and agreed to the published version of the manuscript.

Funding

This research does not have any funding by any Institution.

Data Availability Statement

Data are contained within this article.

Acknowledgments

The authors would like to thank REVA University for their continuous support and encouragement in carrying out the research work.

Conflicts of Interest

The authors declare no conflicts of interest.

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Applmicrobiol 04 00106 g001
Figure 1. Different types of interactions in the rhizosphere.
Figure 1. Different types of interactions in the rhizosphere.
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Figure 2. Constituents of root exudates and their functions in the rhizosphere.
Figure 2. Constituents of root exudates and their functions in the rhizosphere.
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Figure 3. Mechanisms of plant stress tolerance induced by beneficial microorganisms.
Figure 3. Mechanisms of plant stress tolerance induced by beneficial microorganisms.
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Table 1. Categories of microbial interactions in soil.
Table 1. Categories of microbial interactions in soil.
InteractionSp. ASp. B
Positive
Interactions		Protocooperation++
Syntrophism
Mutualism
Facilitation
Commensalism+0
Neutralism00
Negative
Interactions		Amensalism (Antagonism)0-
Competition--
Parasitism+-
Predation+-
Table 2. Diversity of plant–microbe interactions in agricultural system.
Table 2. Diversity of plant–microbe interactions in agricultural system.
Interaction TypeMicrobial GroupPlant ResponseExampleReference
SymbiosisRhizobiumNitrogen fixationLegume-rhizobia symbiosisSchiessl et al. 2019 [37]
AMFNutrient uptake, Stress toleranceMycorrhizal symbiosisMitra et al. 2021 [38]
FrankiaNitrogen fixationActinorrhizal symbiosisSellstedt and Richau, 2013 [39]
MutualismPlant growth-promoting rhizobacteria (PGPR)Growth promotion, stress resistanceRhizobacteria-plant symbiosisKabiraj etal. 2020 [40]
Mycorrhizal fungiNutrient acquisition, disease resistanceMycorrhizal symbiosisJacott et al. 2017 [41]
Endophytic bacteriaDisease resistance, growth promotionEndophytic bacteria-plant symbiosisVandana et al. 2020 [42]
CommensalismPlant growth-promoting fungiAltered root exudationBacterial colonization of the rhizospherede la Fuente Cantó et al. 2020 [43]
Nitrogen-fixing cyanobacteriaNitrogen fixation, growth promotionCyanobacterial-plant symbiosisRai et al. 2019 [44]
AmensalismAllelopathic microorganismsInhibition of competing plantsAllelopathy in soil microbial communities[45]
CompetitionSoil bacteria and fungiNutrient competition, antibiotic productionFungal colonization of the rhizosphereEssarioui et al. 2017 [46]
Root pathogensDisease development, reduced growthPathogen-plant interactions in the rhizosphereAkram et al. 2017 [47]
AntibiosisAntibiotic-producing bacteriaSuppression of pathogens, pestsAntibiosis in soil microbiomeChandra, and Kumar, 2017 [48]
Antifungal-producing fungiSuppression of fungal pathogensFungal-plant interactionsNguyen et al. 2020 [49]
Allelopathic plantsInhibition of microbial growthPlant–microbe interactions in allelopathic systemsCipollini et al. 2012 [50]
Table 3. Plant-released signals in plant–microbe interactions:.
Table 3. Plant-released signals in plant–microbe interactions:.
Signal TypeDescriptionReference
Root ExudatesOrganic compounds released by roots into the rhizosphere, including sugars, root colonization amino acids and organic acids.[60,61]
Volatile Organic Compounds (VOCs)Gaseous compounds emitted by plants that can attract or repel microorganisms, affect microbial growth and behaviour. Ex. Terpenes (limonene, pinene), Alcohols (ethanol), Aldehydes (hexanal).[62,63]
PhytohormonesPlant hormones like auxins, gibberellins, and cytokinin that regulate plant growth and development, and can also influence microbial activities[64,65]
Secondary MetabolitesChemical compounds (Alkaloids (nicotine, caffeine), Flavonoids (quercetin, kaempferol), Saponins) produced by plants that can have antimicrobial properties, influence microbial community composition, or modulate microbial activities[66,67]
Quorum Sensing MoleculesSignaling molecules (Acyl-homoserine lactones (AHLs), Pheromones (cis-2-dodecenoic acid) produced by plants and microorganisms to communicate and regulate gene expression in response to population density.[68,69]
Reactive Oxygen Species (ROS)ROS (such as, Hydrogen peroxide (H2O2), Superoxide anion (O2−), Hydroxyl radical (•HO) produced by plants as signaling molecules in response to microbial colonization or stress.[70,71]
Lipids and Fatty AcidsLipids and fatty acids released by plants that can influence microbial colonization and activity in the rhizosphere.[72,73]
Phenolic CompoundsPhenolic compounds such as phenolic acids (ferulic acid, caffeic acid), tannins, flavonoids produced by plants with antimicrobial properties, involved in defense against pathogens and modulation of microbial communities[74,75]
Volatile TerpenesTerpenes (monoterpenes (limonene, pinene), sesquiterpenes (farnesene, caryophyllene) (released by plants with diverse biological activities, including antimicrobial properties and modulation of microbial communities.[76,77]
Peptides and ProteinsPeptides and proteins released by plants that can act as signaling molecules or antimicrobial agents against pathogens.[78,79]
Microbial MetabolitesMetabolites like antibiotics (penicillin, streptomycin), exopolysaccharides, volatile fatty acids produced by microorganisms in response to plant signals, influencing plant–microbe interactions and rhizosphere ecology.[80]
Table 4. Physiological responses in plant–microbe interactions.
Table 4. Physiological responses in plant–microbe interactions.
Physiological ResponsePlant–Microbe InteractionExampleReference
Nutrient UptakeMycorrhizal SymbiosisAMF facilitate nutrient uptake in plants by extending their hyphae into the soil to access nutrients like phosphorus and nitrogen.[94]
Growth PromotionPGPRRhizobacteria in the rhizosphere produce plant growth-promoting constituents such as auxins and cytokinin, stimulating root and shoot growth in plants.[95]
Stress ToleranceISRBeneficial microorganisms like Bacillus spp. and Trichoderma spp. stimulate systemic resistance in plants, enhancing their tolerance to environmental stresses such as drought, salinity, and pathogens.[96]
Disease ResistanceAntagonistic InteractionsCertain microorganisms such as Streptomyces spp. and Bacillus cereus in the rhizosphere produce antimicrobial composites that hinder the growth of pathogens, providing disease resistance to the host plant.[97]
Hormonal RegulationPhytohormone ProductionMicroorganisms like Azospirillum brasilense and Rhizobium leguminosarum produce phytohormones like auxins, cytokinin, and gibberellins, which regulate various physiological processes in plants such as growth and development[98]
Root Architecture ModificationIndirect Effects on Soil MicrobiomePlant–microbe interactions influence root architecture, with some microorganisms promoting lateral root formation and others inhibiting primary root growth, thereby affecting nutrient uptake and soil structure.[99]
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Tharanath, A.C.; Upendra, R.S.; Rajendra, K. Soil Symphony: A Comprehensive Overview of Plant–Microbe Interactions in Agricultural Systems. Appl. Microbiol. 2024, 4, 1549-1567. https://doi.org/10.3390/applmicrobiol4040106

AMA Style

Tharanath AC, Upendra RS, Rajendra K. Soil Symphony: A Comprehensive Overview of Plant–Microbe Interactions in Agricultural Systems. Applied Microbiology. 2024; 4(4):1549-1567. https://doi.org/10.3390/applmicrobiol4040106

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Tharanath, Arpitha Chatchatnahalli, Raje Siddiraju Upendra, and Karthik Rajendra. 2024. "Soil Symphony: A Comprehensive Overview of Plant–Microbe Interactions in Agricultural Systems" Applied Microbiology 4, no. 4: 1549-1567. https://doi.org/10.3390/applmicrobiol4040106

APA Style

Tharanath, A. C., Upendra, R. S., & Rajendra, K. (2024). Soil Symphony: A Comprehensive Overview of Plant–Microbe Interactions in Agricultural Systems. Applied Microbiology, 4(4), 1549-1567. https://doi.org/10.3390/applmicrobiol4040106

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