Abstract
The complex interactions that exist between soil bacteria and plants have a significant impact on agricultural sustainability. These relationships, which can be pathogenic or symbiotic, are essential to comprehending and improving the health and productivity of plants. It has not been possible to fully understand the intricacies of these relationships using traditional methodologies. But the development of multi-omics technologies—genomics, transcriptomics, proteomics, and metabolomics—along with next-generation sequencing has completely changed our capacity to analyze and comprehend the dynamics between plants and microbes. With an emphasis on the use of various omics techniques, this brief overview investigates the complex mechanisms governing the interactions between microorganisms and plants. Researchers can create detailed interaction networks and identify regulatory pathways by combining multi-omics data. These revelations shed important light on the interactions, symbiosis, and disease that occur between microorganisms and plants. In the end, understanding these complex interactions has a great deal of potential to advance sustainable agricultural methods and guarantee global food security in the face of environmental difficulties.
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1 Introduction
Interactions between Plants and Microbes Occurs in different ways and at different levels. Although some are beneficial and also some have negative effects too. There are some interactions where plant gets benefit directly or indirectly [59]. Plant habitats within interflanodal spaces provide environments for microorganisms to colonize the surfaces of plant parts. Examples include the rhizosphere and the soil surrounding roots. These microbes, in turn, can produce compounds that promote plant growth, enhance resistance to abiotic or biotic stress, or protect against harmful pathogens [14]. Several studies have reported that one of the most benefial effect of plant–microbe interaction is disease suppressive property of soil microbiota [16]. Plant–Microbe interactions are not unidirectional. The host plant also provides novel metabolic capabilities to its microbial associates, leading to the adaptation of niche-specialized inhabitants that can either have positive (mutualistic), neutral (commensalistic), or deleterious (pathogenic) impact on plant fitness [22]. The plant microbiome, akin to an accessory genome, expands plant capabilities, offering a natural and sustainable mechanism to enhance plant adaptability amidst changing environmental dynamics caused by global climate shifts. Consequently, harnessing the potential of the plant microbiome may foster advancements in agricultural practices [57]. Plants can gets benefits from association of diverse group of root colonizing microbes and their mechanisms. For example Coumarin plant derived secondary metabolite alter the root microbiota and improve plant growth in iron-limiting soil Coumarin-microbiota interaction resolves iron starvation and regulates immune response [22].
In the dynamic interplay between plants and phytopathogens, the latter have evolved intricate invasion strategies to infiltrate hosts, aiming to benefit themselves while bypassing the host's defense mechanisms. Plants, in response, have developed robust defense mechanisms including physical barriers, preformed defenses, and innate immune systems to counteract these threats [30]. Moreover, plants face significant challenges from both abiotic and biotic stresses, which pose serious threats to crop yield. Abiotic stresses induce various changes at molecular, biochemical, physiological, and morphological levels, negatively impacting plant growth and productivity [28]. Notably, low temperatures significantly constrain the productivity and distribution of numerous plant species, especially vital agricultural crops. Epiphytic bacteria with ice-nucleating activity, such as Pseudomonas syringae, exacerbate frost injuries in cold-sensitive plants by impeding their ability to supercool, consequently facilitating the formation of ice crystals that damage membranes [15]. Conversely, certain epiphytic or endophytic Benefits and Mechanisms of Plant Growth-Promoting Rhizobacteria (PGPR) play a beneficial role in enhancing plant growth and resilience to stress. PGPR can trigger developmental changes in host plants, disrupt phytopathogen organization, induce systemic resistance against pathogens, modulate phytohormone production, and optimize nutrient and water utilization [36].
The dynamic microbial plant environment is one of the many phenomena that showcase the amazing genomic adaptability and metabolic versatility of microbes, enabling them to survive in any type of ecological niche. It goes without saying that their interactions with plants have practical applications [57]. These benefits include enhancing nutrient uptake, producing hormones for use in growth regulation and defense against phytopathogens, as well as increasing resistance to stresses (Fig. 1). On the contrary, some harmful consequences such as diseases can destroy plant life by compromising the health of the plants and their immunity. In light of these gains in modern agricultural practices, scientists have contributed to seeking greater understanding of plant–microbe interactions and promoting the use of microbe-based bio-stimulants [51] that help improve sustainability in farming techniques. The rise of Omics technologies has changed the way to assess microbial diversity and describe plant–microbe relations in different ecological systems. At the level of molecular interactions among organisms, Omics sciences promote an integrated analysis based on combining large-scale datasets from various sources [27]. In turn, Multi-omics studies play a fundamental role in this field as they provide insights into the complexity of interrelations between plants and their associated microbes. These methods include simultaneous investigations of different omics datasets such as epigenome, metabolome, proteome, transcriptome, and genomes (Fig. 2) [38]. Microorganisms inhabit diverse plant habitats, including the rhizosphere, where they engage in intricate interactions with their plant hosts. These interactions involve the exchange of nutrients, signaling molecules, and defense mechanisms, shaping both plant and microbial communities [16]. Understanding the dynamics of plant–microbe interactions is critical for optimizing agricultural practices, enhancing crop productivity, and promoting sustainable ecosystem management [23].
In this context, the present manuscript aims to delve into the complexities of plant–microbe interactions, elucidating the molecular mechanisms underlying these relationships. By synthesizing recent advancements in transcriptomics, metabolomics, and proteomics, the manuscript seeks to provide comprehensive insights into the molecular dialogues between plants and microbes. The mechanisms involved in establishing plant–microbe interactions in the soil are highlighted in this review along with plant–microbe interactions for beneficial symbiotic relationships. The interactions between plants and microbes in the rhizosphere have been studied using a variety of omics techniques, including transciptomic, genomics, metabolomics, signalomics, and phenomics, which are also included in this review. Additionally, this review attempts to highlight a few essential proteins and metabolites of the pants that are necessary for establishing the advantageous plant–microbe relationship.
1.1 Plant microbe interaction
Plant–microbe interactions have many different forms, including symbiosis, parasitism, commensalism, mutualism, and competition. The more prevalent types of relationships are mutualism and commensalism, in which the association benefits one or both species [36]. Numerous studies have shown that root microbiota plays a favorable function in encouraging plant growth and resilience to both biotic and abiotic stressors, which is one of the many beneficial effects of plant–microbe interactions. Additionally, it has been demonstrated that bacteria associated with leaves affect host growth resilience to abiotic stresses and resistance to infections [45]. Almost all plant tissues are colonized by endophytic and mycorrhizal fungi, bacteria that create biofilms on the surfaces of roots and leaves, endophytes that live inside plant tissues, and nitrogen-fixing bacteria that are kept inside nodules on stems or roots and harmful organisms developing infection structures in the roots and on the leaves [8].
One of the main limiting factors and essential for plant development is nitrogen (N). In response to the availability of N in the soil, plants exhibit phenotypic plasticity that influences biomass allocation, elongation, and lateral root initiation. Certain plants and nitrogen-fixing bacteria combine to generate root nodules. For N-balancing, rhizobia and the actinomycete Frankia are very crucial [58]. Through improved photosynthetic efficiency, leaf gas exchange and water and nutrient uptake, the symbiotic association of Arbuscular Mycorrhizal Fungi (AMF) aids the host plants in tolerating a variety of environmental stress conditions, such as infections, heavy metal toxicity, desiccation, and acidity. AMF are widely used in agriculture as biofertilizers, and because of osmotic adjustment and increased antioxidant enzyme activity, over 70% of vascular plants can form a symbiotic relationship with AMF, particularly during dry circumstances [24]. Streptomyces species are useful as biofertilizers because of their capacity to stimulate plant development. In addition to being more competitive than other bacteria, they can produce spores and endure harsh soil conditions. Furthermore, they create a variety of lytic enzymes that can degrade insoluble organic polymers and provide nutrients that plants can consume [49]. It was demonstrated that the bacteria grew endophytically in the root, which greatly enhanced the plant's absorption of cadmium. The plant displayed enhanced growth and a reduction in metal-induced stress when the bacteria were present. Therefore, these bacteria that encourage plant growth can aid in phytoremediation as well as the creation of sustainable biomass [49]. Microorganisms and root exudates are crucial elements of the rhizosphere ecology and have a significant impact on how nutrients and metals are bioavailable. Bacteria get a plentiful supply of energy and nutrients from root exudates, and in exchange, bacteria encourage exudation from plant roots [33]. The plant-invading bacterium may either kill the plant before drawing nutrients from its dead cells, or it may attack the plant by taking nutrients from the healthy parts while keeping it alive. This interaction may cause a hypertensive response (HR) in either the host plant or non-host plant, depending on which is incompatible [7]. Bacteria have developed complex mechanisms for secreting siderophores, which allow them to sequester iron and change the growth of nearby enemy pathogens. For example, the inhibition of illnesses brought on by fungal pathogens has been connected to the release of iron-chelating compounds by advantageous Pseudomonas spp [23]. It has been demonstrated that a wide variety of microorganisms associated with plants emit substances that directly inhibit the growth of their competitors. Additionally, bacteria create a variety of compounds, such as broad-spectrum enzymes and antibiotics that are effective against fungal plant diseases that are phylogenetically unrelated. The degree of sensitivity of bacteria from various plant compartments to antagonistic action varied [23].
In wild-type and Got-3 tomato plants, the bacterial endophyte Sphingomonas sp. LK11 isolated from Tephrosia apollinea leaves significantly improved shoot/root growth through the expression of glutaredoxin peroxiredoxin-, and glutathione S-transferase -related genes in the LK11 genome [24]. Specific root exudates from different plants show the unique selection of rhizospheric microbial communities. For example, the fumaric acid secreted by banana roots attracted B. Bacillus subtilis towards roots, resulting in the formation of biofilms, and the cucumber plant secreted citric acids from its roots, which in turn affected the attraction of Bacillus amyloliquefaciens [60]. The majority of protists that are known to interact with plants are members of the supergroup Rhizaria-Alveolata-Stramenopiles (SAR), specifically those that are part of the lineages Cercozoa (Rhizaria) and Oomycota (Stramenopiles). Few species of Oomycota are frequently seen living in close proximity to plant roots or leaves, including Pythium, Phytophthora, Peronospora, and Albugo [23].
1.2 Benefits and Mechanisms of Plant Growth-Promoting Rhizobacteria (PGPR)
By reducing the need of chemical-based fertilizers and increasing plant productivity, knowledge of the advantageous properties of natural PGPRs and their interactions could benefit agriculture. Indirect traits exhibited by PGPRs include pathogen suppression, for example, by releasing gaseous substances like hydrogen cyanide (HCN), inducing induced systemic resistance (ISR) and systemic acquired resistance (SAR), and ACC deaminase enzyme production to reduce the concentration of ethylene in plants. Direct traits include nutrient assimilation, phytohormone secretion and signaling, biological nitrogen (N2) fixation, and siderophore production for making iron available to the plants (Fig. 1) [60].
Numerous phytohormones that stimulate plant development have been shown to be produced by rhizosphere bacteria and phyllosphere-colonizing epiphytes. This is crucial to consider because different phytohormone combinations and individuals may have varying effects on plant growth. By generating the degradative enzyme 1‑aminocyclopropane‑1‐carboxylic acid (ACC)‐deaminase, bacteria such Pseudomonas spp., Burkholderia caryophylli, and Achromobacter piechaudii have been demonstrated to reduce the endogenous ethylene level in plants. The effects of ACC deaminase‐producing rhizobacteria on plants included increased root growth, and improved tolerance of salt and water stress [55].
The nitrogenase complex, an enzyme involved in the nitrogen-fixation mechanism in bacteria, is regulated by nitrogenase genes and is subject to genetic control. Structural genes stimulate Fe protein, iron-molybdenum cofactor production, and electron donation; regulatory genes synthesis and control enzymes. Rhizobacteria have the ability to solubilize inorganic phosphorus, which plants cannot absorb, and which can improve plant growth and output. Though ubiquitous in nature, iron is nonetheless inaccessible to plants. The most common type of iron is Fe3+. By secreting siderophores, which are low-molecular-weight iron-binding proteins that aid in the chelation of ferric iron (Fe3+), PGPRs aid in its solubilization. Fe3+ and siderophores are dissolved in a 1:1 combination by the bacterial cell membrane. Fe3+ is converted to Fe2+ and then liberated from siderophores to enter the cell. By releasing siderophores, PGPRs promote plant development and lessen a number of plant diseases [40].
Plant cell wall binding, active ion transport into cell vacuoles, intracellular complexation with peptide ligands like phytochelatins (PCs) and metallothioneins (MTs), and sequestration of metal-siderophore complexes in root apoplasm or soils are some of the mechanisms underlying plant metal tolerance. Because Low Molecular Weight Organic Acids (LMWOAs) can exclude metals and metalloids (such as As, Cr, Cd, and Pb) through chelation in the rhizosphere or apoplast, preventing the metal ions from entering the cell symplast, root exudation has been considered one of the most significant strategies developed by plants to tolerate high metal concentrations [33].
Because they produce phytotoxic chemicals, microbes are important agents of both disease incidence and biocontrol. Plant disease severity is influenced by variables such as host susceptibility, environment, and pathogen population size. Through competing for nutrients, defense mechanisms, and antagonism, microorganisms manage harmful bacteria. As bacteria prevent the growth of other microorganisms in their immediate area, antagonistic bacteria can inhibit the spread of infections. Furthermore, the pathogenic microorganisms may grow slowly or not at all as a result of the fast-growing microbes using the nutrients for their own growth and depleting them for other purposes. A few bacteria control plant hormone levels and create resistance in the plant system to protect the plant from diseases. Actinobacteria, Acidobacteria, and Firmicutes are the three fundamental bacterial taxa that have been shown to regulate the Fusarium wilt disease on a massive scale [60].
Microbial colonies are embedded in micro-architectural structures called biofilms. Microbial collaboration is necessary for the secretion of extracellular polymeric materials needed to construct biofilms. These secretions give bacteria a selective advantage by shielding them from rivals and antimicrobial substances, triggering enzymatic reactions that need for a high cell density, and allowing them to acquire new genes through horizontal gene transfer. Research has demonstrated that the bacterial endophyte Enterobacter sp., which forms biofilm-mediated microcolonies on the root hairs of finger millet, creates a chemical and physical barrier that keeps the pathogen Fusarium graminearum from colonizing the roots [23].
1.3 Multi-omics approach for studying plant-microbial interactions:
Multi-omics studies, which use an integrated method to investigate several molecular levels within organisms, represent a paradigm change in biological research. Through the integration of various "-omics" fields such as proteomics, metabolomics, transcriptomics, and genomes, researchers can get a thorough comprehension of intricate biological systems. With this method, complex relationships between genes, proteins, metabolites, and other biomolecules can be explored, providing hitherto unheard-of insights into biological processes and phenomena. In the coming section different omics approaches such as transcriptomics, genomics, metabolomics, proteomics, Signalomic and pheromonic approaches in relation to plant and microbe interactions will be discussed.
1.4 Transcriptomic approach
Beneficial bacteria associated with plants play a pivotal role in fostering growth and warding off diseases. Utilizing Benefits and Mechanisms of Plant Growth-Promoting Rhizobacteria (PGPR) as biofertilizers or biocontrol agents offers a cost-effective alternative to conventional fertilizers, thereby enhancing crop productivity. Evaluating bacterial transcriptomic responses to root exudates provides valuable insights into gene expression and regulation under rhizospheric conditions, essential for unraveling the mechanisms governing plant–microbe interactions [63].
The advent of next-generation sequencing has spurred a surge in transcriptomic studies examining changes in host gene expression during interactions with plant growth-promoting bacteria (PGPB). While many of these studies have focused on the Nipponbare rice cultivar, investigations have extended to other plants like wheat, sugarcane, and tobacco. Notably, the PGPB employed in these studies exhibit significant variability, including species such as A. brasilense, H. seropedicae, B. subtilis, B. anthina, and P. kururiensis. Despite variations in experimental conditions and host-PGPB combinations, certain consistent gene expression trends have emerged, particularly regarding defense responses, hormone signaling, and nutrient transport in host plants during PGPB interactions. These studies lay a foundation for further exploration into host genetic pathways regulating plant-PGPB interactions [39].
With a focus on Oryza sativa's reaction to the plant growth-promoting bacteria Azospirillum brasilense and Herbaspirillum seropedicae, Wiggins et al. [61] carried out a thorough proteome analysis that revealed complex molecular dynamics underlying plant–microbe interactions. Their research revealed a notable downregulation of defense-related genes, including thionin, chitinases, PR, and cinnamoyl-CoA-reductase genes. This suggests that these advantageous bacteria may be suppressing plant defensive systems. On the other hand, Magnaporthe oryzae increased a number of genes related to defense and stress response, such as chitinases, peroxidases, glycosyl hydrolases, and WRKY transcription factors, indicating an improved defense response to pathogenic invaders. Additionally, the study revealed the differential expression of transcription factors, nitrate reductases, and hormone signaling genes, as well as the overexpression of transporters involved in the uptake of sugar and nitrogen, highlighting the complex regulating mechanisms modulated by these plant growth-promoting bacteria. Furthermore, Thomas et al. [54] built upon these discoveries by clarifying the differential expression of different transporters, genes linked to the synthesis of flavonoids, elements of hormone signaling, and genes related to pathogenesis (Table 1), thereby deepening our comprehension of the complex interactions between plants and advantageous microorganisms. When taken as a whole, these studies offer insightful information about the molecular processes regulating interactions between microbes and plants, as well as the consequences for plant health and yield.
1.5 Genomic approach
One of the biggest challenges in agriculture nowadays is to increase yield and sustainability of crop production as the global population is approaching nine billion people by 2050. Soil quality is believed to be an integrative indicator of environmental quality, food security, and economic viability. Study indicators are required to track alterations in soil quality. Because soil microorganisms react quickly to disturbances, studying them has several benefits, including the potential to yield immediate information about the health of the soil. In the past ten years, new methods based on organisms, enzymatic processes, and molecules have been created to diagnose soil health and supplement current physicochemical properties [6].
Because it is in charge of the mineralization of organic matter, soil microbial activity plays a crucial role in the maintenance of life on Earth. This has an impact on nutrient availability and recycling, as well as plant bioremediation and nutrition processes. Soil microorganism populations are highly diverse, and new developments in molecular biology have revealed even more intricate layers of diversity. Currently, through techniques that omit the use of artificial media for microbiological studies, it is possible to analyze the microbial composition of certain environments, especially when it comes to microorganisms that cannot be cultured ex situ. A recent review published by Altowayti et al. [4] describes three groups of culture-independent techniques for analyzing the biomass, diversity and catabolic activity of microbial communities.
For example, by using metagenomic applications, we may reproduce the molecular processes that give rise to biodiversity in an experimental setting and use this knowledge to explore nutrient intake and transport systems in detail. The processing of nutrients that the root may acquire and transfer depends heavily on the microbial communities found in the rhizosphere of plants. Ammonia is produced by certain microorganisms from atmospheric nitrogen. While some soil organisms recycle nutrients from dead plants and animals, others change elements like iron and magnesium into forms that plants can utilize [19].
Applications that are in development and those that are currently merely visible have enormous potential. Thus, the developments that would result from these advancements will usher in a new phase of growth for crop nutrition research and soil science. These technologies allow us to understand the structure and function of organisms that have never been found before or that were not able to be cultivated. For instance, sequenced the metagenomes of samples taken from forests, tundra, grasslands, and cold and hot deserts [42].
Genes linked to osmoregulation and dormancy were more abundant in the desert ecosystems, while genes involved in food cycling and the breakdown of organic substances obtained from plants were less abundant. It will be feasible to understand how microbial communities might survive in conditions with limited water and nutrients by researching the physiological pathways in which the products of these genes are involved [41]. Below we summarize that the Next-generation sequencing has been instrumental in sequencing the genomes of model and agriculturally important plants, showcasing methodological diversity and sequencing chronology.
The metabolic capacities of microbes can be applied in new ways to plant nutrition strategies thanks to genomic technologies, which can also be used to identify in greater detail the mechanisms plants use to better utilize nutrients. These tools can encourage the development of novel technologies for plant feeding, even though the majority are still expensive. Even though some of these technologies are still in the early stages of development and require optimization, their successful application in certain contexts has sparked increased interest from the scientific community and business community in the identification of critical molecules, metabolic pathways, and crop nutrition applications [19].
Since metagenomics offers direct access to microbial communities that live in habitats (optimal or limiting), in all of their complexity, and regardless of whether they can be successfully farmed, it has the potential to completely transform plant nutrition. The process of isolating and characterizing functional genes, along with the sequencing of entire metagenomes, holds promise for uncovering novel metabolic processes and producing useful data regarding the optimal utilization of fertilizers and manures from a sustainable development standpoint.
The good news is that there is growing interest in carrying out more in-depth analyses. For example, [20] demonstrated that new generations of life scientists are able to develop strategies to generate and take advantage of information in the new era of sequencing and genomic sciences.
1.6 Metabolic approach
Being sessile, plants have evolved a variety of strategies to communicate with nearby microbes. These include the production of attractants for symbiotic organisms and defensive systems against diseases. Plant–microbe communications are genetically encoded, but they also depend on metabolites for synthesis, transport, and metabolism. Plants release metabolites into the soil in the form of root exudates in order to successfully interact with soil microbes.
However, studying the function of metabolites in multi-organism systems is far from straightforward, and as a result, our understanding of metabolic interactions—particularly in relation to plant immunity—lags behind that of the genetics underlying these interactions. However, the past ten years have seen a notable advancement in our understanding of the part metabolites play in plant–microbe interactions and the development of metabolomics techniques to better analyze these interactions [13].
The plant immune response, which defends plants against a range of pests, includes many metabolites. Experiments with leaf pathogens have provided the majority of our information about these metabolites. Indolic glucosesinolates and camalase, two defensive chemicals generated from tryptophan in Arabidopsis, are among the greatest examples. The foundation of the "mustard oil bomb" is made up of glucosenolates, which are sulfur-rich secondary compounds of the Caparales [34].
Characterizing the entire range of bioactive chemicals generated by plant pathogens is a crucial task for metabolomic studies in plant–microbe interactions. These compounds have the potential to be non-protein effectors that target the plant, [46] and some of their byproducts are harmful to human beings as well [2].
Exudation of roots is the main way that plants can influence the microbiota. In fact, root exudates are crucial to the metabolomics of plant–microbe interactions in the roots. They mediate interactions between plants and pathogens and rhizosphere symbionts, regulating their impact on defense, nutrient uptake, performance, and response to abiotic stress. Metabolic techniques shed light on the complex biochemical interactions that occur between microorganisms and plants, clarifying important pathways and metabolites that are essential to these interactions. Aliferis et al. [3] showed that when Bradyrhizobium japonicum is injected into Glycine max, isoflavonoids are upregulated, highlighting their function in symbiotic nitrogen fixation. Comparably, Bulgarelli et al. [10] found that Arabidopsis thaliana produced more flavonoids in response to different rhizosphere bacteria, suggesting that these substances influence plant–microbe communication. The induction of benzoxazinoids in Zea mays colonized by Pseudomonas fluorescens was discovered by Chaparro et al. [12], underscoring their role in plant defense. Additionally, Toju et al. [56] discovered that Oryza sativa was connected to arbuscular mycorrhizal fungus by enhanced levels of strigolactones, which may indicate a function in symbiotic signaling. Gibberellins have been shown by Hacquard et al. [21] to be upregulated in Medicago truncatula following colonization by Rhizophagus irregularis, suggesting a potential role in the encouragement of plant development. According to Stringlis et al. [53], Solanum lycopersicum treated with Trichoderma harzianum produced more glucosinolates, suggesting that these metabolites are involved in plant defense mechanisms. Collectively, these investigations shed light on the complex metabolic processes that underlie interactions between microbes and plants, and how these processes affect the health and yield of plants. (Table 1)
1.7 Proteomic approach
Plant–pathogen interactions are studied by proteomics methodologies, which are mostly associated with liquid chromatography and tandem mass spectrometry techniques. Identification of proteins and how they alter during infection are crucial processes in proteomics. Using semi-quantitative methodology, it exposes a range of bacterial proteins in the environment. These techniques include sample analysis, protein extraction, fractionation, and isolation using mass spectrometry, as well as additional testing using a proteome database. Rather to determining whether or not a protein can be made, proteomics identifies the components of a functional protein that the cell produces. It also gives details on the precise count of active pathways within the sample [50].
Proteomics tracks phosphorylation changes in proteins that are critical to protein function, enabling the identification of signal transduction pathways. It is now known that phosphorylation events and important receptor kinases regulate a number of early plant–microbe signaling events. These include the autoregulation of nodule numbers and the early detection and signal transduction of Nod factor perception [31].
Proteome-based approaches have become more widely used in plant pathology in recent years, partly because of advances that have made them easier to use and repeat. 2-DE and MS are arguably still the most popular analytical methods for protein identification and profiling. Although 2-DE and fluorescence 2-D difference gel electrophoresis (DIGE) have advanced this technique, many gel-free proteomic techniques have also been developed recently due to a number of inherent drawbacks associated with gel-based proteomics, such as cost, insensitivity to low copy proteins, reproducibility, and inability to characterize entire proteomes [17].
Plant–microbe proteome investigations reveal complex molecular conversations that are essential for defense, symbiosis, and adaptation. Research like that by Zhang et al. [65] show that catalase is upregulated in Arabidopsis in response to Pseudomonas syringae, underscoring the significance of detoxification from reactive oxygen species in defensive signaling. Similar to this, Pandey et al. [43] show that Fusarium oxysporum-challenged Solanum lycopersicum induces pathogenesis-related proteins, providing insight into plant defense mechanisms against fungal infections. Furthermore, a study conducted by Rao et al. [47] highlights the significance of cell wall reinforcement in plant defense by demonstrating the overexpression of peroxidase in Oryza sativa following Magnaporthe oryzae infection. Furthermore, Jaiswal et al. [25] clarify the overexpression of proteins specific to nodules in Glycine max during symbiotic relationships with Bradyrhizobium japonicum, highlighting the importance of nitrogen fixation in the mutualism between plants and microbes. Wu et al. [62] make a further contribution by demonstrating that glutathione S-transferase is upregulated in Zea mays that have been inoculated with Rhizobium leguminosarum, suggesting that this enzyme is involved in detoxification and the oxidative stress response. Together, our results highlight how dynamic plant–microbe interactions are and how important proteomic methods are to understanding their complexity (Table 1).
1.8 Signalomic and pheromonic approach
Microbes use chemical signals that is developed in the rhizosphere to communicate with the plant and with each other in a complex manner. Plants emit a range of metabolites in response to changes in gene expression. They show Mutual relationships that are essential for root-to-root interactions, nutrient availability, microorganism accumulation, biofilm formation of soil microbial communities, and the suppression of soil-borne diseases are established through such communication [37]. For rhizobacteria and other soil microbes to have a healthy symbiotic relationship with their phytobionts, signalling is a crucial process. The amount and type of rhizobacteria as well as the structural and physical heterogeneity of the soil are influenced by the many signalling molecules emitted in the rhizospheric zone. Rhizospheric signalling systems can generally be divided into three main groups: (i) through plant to microorganisms signaling low molecular weight chemicals secreted by plants,(ii) by microbial signalling among and across species, primarily through quorum-sensing molecules; and (iii) microorganisms to plant signaling by microbial produced compounds [52].
Microbial communities, comprising mutualisms, commensals, and parasitic microbes, dwell within plants. Plants release chemical compound which are known as root exudates to response the microbial signals. These consist of large molecular weight substances like proteins and mucilage and low molecular weight substances including organic acids, sugar, fatty acids, amino acids, flavonoids, and secondary metabolites. About one percent of secondary metabolites are volatile organic compounds (VOCs), which are released by plants from their leaves, flowers, fruits, and roots. VOCs are known to be highly permeable, attracting pathogens, and to restrict growth. Rhizobia and legumes interact symbiotically by secreting phytochemicals from the roots of the host plant. Flavonoids, which accumulate auxin in root tissues, attract rhizobia and activate nodulation genes, resulting in the formation of lipo-chitooligosaccharides (LCOs). LCOs are important signaling molecules that trigger the formation of nodules which sense by receptors in the host plant's root epidermis. Similarly the formation of the symbiotic relationships between plants and Arbuscular Mycorrhizal Fungi (AMF) is facilitated by the release of mycorrhizal lipo-chitooligosaccharides (Myc factors) by the AMF in response to signals from strigolactones found in plant secretions, sometimes referred to as branching factors (BFs) [26].
Microorganisms use a vital communication mechanism called quorum sensing (QS) to build interactions with their hosts. In order for bacteria to coordinate their behavior in a population-dependent manner, they must produce and detect signal molecules. N-acyl homoserine lactones (AHLs) are an example of an autoinducer that is linked to QS and is involved in the production of biofilms and pathogenicity in the bacterial population. Oligopeptide autoinducers, which may undergo post-translational modifications, serve as lead molecules for gram-positive bacteria. Transporters are necessary for peptides to enter the extracellular environment. Diffusible signal factors regulate QS in various organisms, involving inter-kingdom signaling pathways [1].
Plants are able to detect signalling chemicals produced by microorganisms, which can impact their development, gene expression, immune system, and stress response [44]. Every single cell in plants carries a variety of innate immune receptors that are capable of detecting invasion signals. Pattern recognition receptors (PRRs) on cell surfaces identify endogenous signals produced during cellular breakdown known as damage-associated molecular patterns (DAMPs), or molecular structures characteristic of microbes, known as microbe-associated molecular patterns (MAMPs), and thereby accumulate pattern-triggered immunity (PTI) [48]. Certain pathogens have the ability to introduce particular effector proteins into plant cells and cause effector-triggered immunity (ETI), which is triggered when disease-resistant proteins encoded by the R genes recognize the effectors [64]. MAMPs induce priming and systemic defense responses by beneficial bacteria in the rhizosphere. MAMPs can cause systemic acquired resistance (SAR, which is primarily brought on by pathogens. Plant hormones regulate both PTI and ETI,the main signals are salicylic acid (SA, jasmonic acid (JA, and ethylene (ET, the three stress hormones. Yet, recent research has shown that gibberellic acid (GA and the growth hormones Brassinosteroids (BRs also have significant effects. BRs were discovered to be essential for numerous other stages of plant development, including as seed germination, vegetative and reproductive development, senescence, and responses to various stimuli. Initially, they were thought to be a group of hormones that promoted growth [64]. Different plant phytohormons also produced by the microbes such as auxin, cytokinin, indole acetic acid, Volatile Organic Compounds etc. In situations where there is a nutrients deficiency, plants may consume VOCs produced by bacterial metabolism [44]. The ipdC gene of Azospirillum brasilense is the first example of how IAA controls bacterial gene expression. It has been documented that the phytopathogen Agrobacterium tumefaciens uses IAA as an inhibitory signal molecule to suppress the production of its viral genes [29].
Pheromones, which control spore germination, the synthesis of secondary metabolites, structural transformation, and enzyme secretion, are released by individual species of fungi to interact with one another. Pheromones arise from alleles at the MAT locus, where diffusible peptides known as a-factor and α-factor are produced by Saccharomyces cerevisiae [1].
2 Conclusion
In conclusion, this multiomics-based study clarified complex plant–microbe interactions in soil. The microbial manipulation of plant defense systems is suggested by the downregulation of defense-related genes such as chitinases, cinnamoyl-CoA-reductase, and the PR gene.On the other hand, increased expression of genes related to stress response (like chitinase and peroxidase) and nutrient transporters (like nitrate transporters) highlights the need for plants to adapt and optimize their nutrient uptake when they are surrounded by helpful microorganisms. The complex hormonal signaling pathways involved are revealed by the differential expression of transcription factors such as auxin response factor and ethylene-responsive genes, such as ACC oxidase genes. Proteomic and metabolomic investigations show that complex molecular responses to microbial presence are indicated by the overexpression of pathogenesis-related proteins and enzymes involved in nitrogen assimilation. These findings establish the foundation for focused treatments to improve plant–microbe interactions by providing scientific insights into the molecular mechanisms underlying those interactions. These findings offer scientific insights into the molecular mechanisms underpinning plant–microbe interactions, laying the groundwork for targeted interventions to enhance agricultural productivity and ecosystem sustainability.
Data availability
No datasets were generated or analysed during the current study.
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Acknowledgements
This work was supported Gujarat Technological University, Govt. of Gujarat. One of the authors (MS) acknowledges the, Gujarat Technological University, Govt. of Gujarat for providing financial assistance in the form of ‘‘Post Doc Fellowship’’ Sanction order Letter no. GTU/PDF_O/U/2023/7045 and Seed money Scheme of IQAC Gujarat Technological University Reference No. GTU/IQAC/SMS_C5/Sanction Letter/2023/4983.
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Manju Shri and Neelam Nathani; Writing—review and editing the manuscript.Vaibav Bhatt and Neelam Nathani conceptualized and finalized the manuscript. Priyanka Bhimani Parul Mahavar, Bhumi Rajguru and Manju Shri, writing – original draft manuscript.
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Bhimani, P., Mahavar, P., Rajguru, B. et al. Unveiling the green dialogue: advancements in omics technologies for deciphering plant–microbe interactions in soil. Discov. Plants 1, 4 (2024). https://doi.org/10.1007/s44372-024-00004-3
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DOI: https://doi.org/10.1007/s44372-024-00004-3