An insight into conflict and collaboration between plants and microorganisms

Abstract

Plants and microorganisms have been co-evolving and interacting for billions of years. Prior researchers have explored the plant’s immune system responses and interaction with diverse microbes, but several ambiguities need further explanation. This review provides insight into mechanisms underlying plant–microbe interaction and knowledge dearth domains, along with possibilities to use beneficial microbes to improve plant growth, disease resistance, nutritional value, and productivity. Microorganisms in the phyllosphere and the rhizosphere could be beneficial or pathogenic. Host plants use their innate immune system and the antagonistic competence of plant-growth-promoting microbes against pathogens. The innate immune system of plants has two paramount protection forms involving different types of immune receptors, which assist in recognizing non-self-components. The first group of receptors is membrane-resident pattern recognition receptors (PRRs), which are responsible for sensing microbe-associated molecular patterns (MAMPs) and damage-associated molecular patterns (DAMPs). The second group consists of intracellular immune sensors, specifically resistance (R) proteins, astute in recognizing the structure or function of strain-specific pathogen effectors injected into host plant cells. Plants activate their pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) defense mechanisms to counter the infection. Plants benefit from certain microbes by promoting their growth, disease resistance, and resilience under various stress conditions in exchange for shelter and nutrients.

Graphical Abstract

Introduction

Plants are a crucial component of ecological system, playing a vital role in providing sustenance and meeting many essential living requirements. The pathogenic microbes are considered to widen the gap between the demand for and supply of agricultural products [1]. Plants and microbes also collaborate beneficially to accomplish shared objectives of nourishment and safeguarding inside a perpetually changing environment [2]. A wide array of microorganisms, encompassing bacteria, fungi, and viruses, inhabit a multitude of environments, such as lakes, ponds, rain, soil, sea, mountains, hot springs, plants, animals, and even humans [3]. Microbes are of paramount importance in sustaining life on Earth and have gone through evolutionary adaptations across many ecological niches over a significant period [4]. These tiny beings play a crucial role in initiating ecological processes, including biogeochemical cycles and food networks, while establishing essential linkages among themselves and with higher species [5]. Ensuring the long-term availability of food is a significant priority for countries at different levels of economic development, particularly in agricultural regions, where there is a pressing need for substantial growth in food production and supply [6].

Plant–microbe’s interaction background

The interactions between plants and surrounding microbial species are essential factors that jointly shape the composition and operation of the plant microbiome [7]. The interaction between plants and microbes is a complex, dynamic, and continuously developing process since the inception of life on Earth [8]. A wide range of microorganisms are found in land plants’ above ground and belowground portions. These bacteria are collectively referred to as the plant microbiome, and its members can live on or inside of plants [9]. Plants engage symbiotic partnerships with diverse microbes, including parasitic, commensal, or mutualistic associations [10]. In a parasitic symbiotic association, the symbiont resides predominantly or perpetually on either the inner or outer side of the host, benefiting itself while causing harm to the host, and the symbiont often exhibits a higher reproductive potential than the host [11]. Commensalism refers to a symbiotic relationship where one organism derives benefits while the other remains unaffected. The commensal bacteria obtained from healthy Arabidopsis plants elicit various forms of reactive oxygen species (ROS) production, which is contingent on the immunological receptors and exclusively dependent on the NADPH oxidase RBOHD. This selective inhibition specifically affects certain commensals, particularly Xanthomonas L148 [12, 13]. Mutualistic interaction refers to interaction between different species of organisms, wherein each species derives a net benefit according to its respective capabilities [14]. Since plants and microorganisms have lived together for a long time, they have formed a unique biological unit called a holobiont, comprising host and non-host species [15]. Both beneficial and harmful microbes, mainly bacteria and fungi, invade plants in agricultural and non-agricultural regions [16]. In beneficial relationships, microbes connect to roots, supply plants with mineral nutrients, and fix atmospheric nitrogen.

In response to pathogen invasion, plants have the ability to cry for aid and building beneficial rhizomicrobiomes. However, the ability of non-pathogenic strains to trigger the assembly of a rhizomicrobiome in plants to ward off pathogen invasion is still a mystery [17]. Parasites are living microorganisms that obtain their nourishment from hosts but do not inflict harm on those hosts. In contrast, pathogens are infectious microbes that cause sickness and damage to hosts [18]. Beneficial interactions play a role in the immediate promotion of plant growth and development through increasing phytohormone production, aversion of infectious microbes, and the lowering adverse effects of different stresses [19, 20]. Conversely, the negative interactions pose a significant risk to plants due to the saprotrophic nature of the invader’s microorganisms, which might induce necrotrophy in the colonized plants [21]. Biotrophy is the type of parasitism in which invader microbes feed on a living host plant without killing it, while necrotrophy is the mode through which parasitic microbes get their energy from dead or dying cells of the host plant [22]. Molecular analysis of fungal 18S rRNA/ITS region and bacterial 16S ribosomal RNA (rRNA) location has revealed a wide variety of microbes interacting with plants which include viruses, archaea, fungi, algae, and, to a lesser extent, protozoans and nematodes [23, 24] (Fig. 1). Viruses are diminutive intracellular parasites characterized by either DNA or an RNA genome enveloped by a defensive protein coat encoded by the virus, which can be conceptualized as mobile genetic entities, probably originating from cells, and distinguished by an extensive co-evolutionary relationship between the virus and its host [25].

Fig. 1

The typical interaction between plants and microorganisms

Archaea is a group of unicellular microorganisms that do not have cell nuclei and fall in the prokaryotic domain [26]. Notably, they constitute a substantial constituent of the plant microbiome, yet their precise role remains uncertain. In terms of genetic, metabolic, and structural characteristics, they are different from bacteria and eukarya. They can be found in the rhizosphere and endosphere but rarely in the phyllosphere [27]. According to recent research, archaea members of the plant microbiome promote plant growth, generate plant immunity, and evoke abiotic tolerance [28].

The paraphyletic group of eukaryotes, stereotypically single-celled, free-living, and heterotrophic organisms, is called protists [29]. One could not fully comprehend the plant microbiome without acknowledging the crucial role played by protists. Protists, including a wide range of unicellular eukaryotes, serve as consumers, mostly preying on tiny animals, bacteria, and fungi, and are crucial in carbon fixation through photosynthesis [30]. The impact of protists on plants’ nutritional intake, breakdown of organic debris, and overall health has been reported [31]. However, it is mainly unclear how plant protists and microbes interact in aboveground and belowground systems [32].

Algae comprise a diverse array of primitive photosynthetic organisms, from prokaryotic cyanobacteria to eukaryotic microalgae, typically categorized according to their color, form, and life cycle [33, 34]. Algae, akin to other microorganisms, establish mutualistic and symbiotic associations with plants by inhabiting both the surface of plants and the cellular components of their tissues. The literature has reported positive and negative interactions between algae and plants; however, additional research is necessary to comprehensively unravel the underlying mechanisms driving these interactions.

The aboveground part of a plant, specifically the leaf, is home to harmful and harmless microorganisms [35]. It is crucial to identify the specific components involved in plant defense systems against harmful microorganisms and thoroughly investigate these defense responses underlying processes [36]. Hence, it is imperative to comprehend the interplay between plants and various microorganisms in the phyllosphere and rhizosphere to acquire a comprehensive understanding of the beneficial and detrimental effects of microorganisms on plants. This understanding is essential for attaining the goal of maximizing agricultural productivity and ensuring long-term sustainability. The wide array of microorganisms interact with various plants, exerting both positive and negative effects. Though a myriad diverse microorganisms interact with various plant species, exerting positive and negative effects, the present review revolves around the comprehensive examination of the plan’s interaction with bacteria and fungi.

Plant’s response to pathogenic microorganisms

Pathogenic bacteria undergo multiplication within the intercellular spaces, referred to as the apoplast, after they infiltrate diverse pores, including stomata, hydathodes, and lesions [37]. Fungi spread their hyphae over, between, or through plant cells, or they directly enter the epidermal cells of plants [38]. Oomycetes, both pathogenic and symbiotic develop haustoria-feeding structures that can pierce host cells’ plasma membranes [39]. The proximity of the host plasma membranes, extracellular matrix, and haustorial plasma membranes determines the outcome of the interaction. To promote their own survival and development, pathogenic microbes release effector molecules (known as virulence factors) into the cells of the host plant [40].

The rivalry between plants and microbes has been continued for billions of years. To fight microbial infections, plants have developed a variety of immunological mechanisms that lead them to constantly shifting co-evolutionary successions termed Red Queen dynamics (Leigh Van Valen, 1973) [41]. According to Leigh Van Valen (1973), positive evolutionary adaptations in one species will harm others. So, the adversely affected species will exhibit evolutionary adaptations that, to a certain degree, will counteract the prior advantageous alterations. Plants are free of the adaptive immune system due to the absence of a circulatory system and particular immune cells [42], so when pathogenic bacteria attack, afflicted plants rely on their innate immune system within individual cells and systemic signaling processes that originate from the sites of infection [43]. This innate immune system consists of two interrelated surveillance components (receptors), one perceiving signals and the other reacting to pathogens. External signals are detected by pattern recognition receptors (PRRs) located on the outer membrane of cells. In contrast, internal danger signals are identified by nucleotide-binding domain and leucine-rich repeat (NB-LRR) receptors situated on cytoplasmic sensors (Fig. 2) [44, 45].

Fig. 2

The graphical view provides a schematic representation of plant mechanisms underlying innate pattern-triggered immunity (PTI) and effector-triggered immunity (ETI). The activation of PTI, as indicated by light orange arrows, occurs when pattern recognition receptors (PRRs) recognize pathogen-associated molecular patterns (PAMPs) or damage-related molecular patterns (DAMPs). Multiple PTI signaling processes take place, including the activation of mitogen-activated protein kinase (MAPK) cascades, extracellular calcium ions (Ca²⁺) influx into the cytosol, and the generation of reactive oxygen species (ROS). The production of antimicrobial substances and the activation of defense genes take place. But, pathogens use effectors to suppress PTI. The second immune layer, ETI, activated as pathogens are recognized by nucleotide-binding (NB) and leucine-rich-repeat (LRR) containing receptors (NLRs), denoted by the green arrows. NLRs detect pathogenic effectors indirectly or directly, causing a structural shift that activates the hypersensitive response (HR) or alternative defense mechanisms in conjunction with various intracellular signaling processes

The immune system limits the growth of microbial infections by recognizing molecules known as microbe-associated molecular patterns (MAMPs) that are not typically found in the plant’s body [46, 47]. Terrestrial plants have developed a sophisticated innate immune system consisting of receptors located in the cell membrane [known as pattern recognition receptors (PRRs)] and receptors found inside the cell [known as nucleotide-binding domain and leucine-rich repeat-containing receptors (NLRs)]. These receptors are capable of detecting substances released by pathogens in the extracellular space (apoplastic elicitors) and substances found within the cell (cytoplasmic elicitors). Once detected, the immune system is activated and triggers defensive responses against microbial pathogens [48]. PRRs are the first component of the immune system, responsible for identifying MAMPs present in a wide array of microbes [49,50,51], as well as damage-associated molecular patterns (DAMPs) originating from the host [52], while the second component involves disease resistance (R) proteins to counter the pathogens effectors [53]. The recognition of MAMPs or DAMPs by PRRs sets off a defense mechanism known as pattern-triggered immunity (PTI) [54, 55]. Receptor-like kinases (RLKs), often referred to as receptor kinases and receptor-like proteins (RLPs), have been recognized for their role as PRRs [56]. Signaling about PTI is transmitted via the interaction and activation of receptor-like cytoplasmic kinases (RLCKs) with PRR complexes [57, 58]. PRR complexes promote the activation of mitogen-activated protein kinase (MAPK) and calcium-dependent protein kinases (CDPK) cascades, which subsequently induce the required transcriptional reprogramming for the establishment of PTI [59, 60]. To effectively initiate an infection, pathogens hinder the plant cells’ quorum sensing PTI process by releasing specific proteins called effectors into the host plant cells’ inner and outer regions [61]. To counteract the infection strategy adopted by pathogens, plants respond to effectors through two mechanisms: direct attachment of R proteins to effectors or detection of host molecules referred to as guardees and decoys by pathogen effectors [62]. This identification of effectors results in effector-triggered immunity (ETI) [63]. The interaction between avirulence effector proteins and R gene-encoded proteins results in effector-triggered immunity (ETI), a powerful and quick resistance response associated with hypersensitive customized programmed cell death that stops the spread of pathogens within cells [64].

ETI is very effective in battling biotrophic pathogens in their first stages, and the usual comeback of ETI is the hypersensitive response (HR), in which the plant triggers controlled cell death in a particular area around the contaminated spot, thereby limiting the progression of the disease [65]. The ETI’s response to pathogens infection involves the generation of mobile immunological signals, such as salicylic acid (SA), which are subsequently conveyed from infected cells to unaffected tissues [66]. Alone, SA does not function as a mobile signaling molecule; nevertheless, it concentrates at the infection site and enhances the immune response inside the systemic tissue. After an initial infection, the plant’s distant tissues are protected by a systemic immune response named systemic acquired resistance (SAR) [67]. SA triggers SAR, activating the pathogenesis-related (PR) genes that defend against entering plant–microbe attacks. So, SA plays a crucial role in the immune response of plants by triggering defense mechanisms against infectious biotrophic pathogens [68].

In Arabidopsis thaliana, the synthesis of SA occurs via the isochorismate synthase (ICS) route and the phenylalanine ammonia-lyase (PAL) pathway (which is still not fully known) [69] as a response to pathogen infection. SA is sent as a volatile ester methyl salicylate (MeSA) signaling molecule to the systemic uninfected tissues [70]. The SA molecule signaling is perceived by members of the non-expressor of the pathogenesis-related genes (NPR) family in A. thaliana, including NPR1, NPR3, and NPR4 [71, 72]. The prevailing credence is that NPR1 is the primary regulator of SA signaling, and SA, utilizing thioredoxin, facilitates the monomerization of NPR1 and its subsequent entry into the nucleus [73]. Nuclear NPR1 and TGACG-binding transcription factors (TGA-TF) activate defensive genes, including pathogenesis-related 1 (PR-1), a genetic hallmark associated with the plant immune system response [74, 75].

In summary, several cell-surface receptors, RLKs, and RLPs have been discovered, but their precise biological roles and ligands associated with these receptors have yet to be determined. Further investigation is required to understand how plants differentiate between the MAMPs of pathogens and beneficial microbes, which will pave the way for novel approaches to resistant crop engineering. Enhancing understanding of NLR will improve plant defense against emerging pathogens that may evade cell-surface immunity. Identifying additional plant endogenous compounds that serve as DAMPs and DAMP receptors is very important to facilitate the transmission of DAMP signaling to systemic resistance and integrate DAMP signaling with other signaling pathways implicated in plant resistance to infections.

Plant–microbe interplay in the phyllosphere

The phyllosphere refers to the entirety of the aerial surface area of a plant that serves as a habitat for microorganisms, which could be further categorized into distinct regions, including the caulosphere (stems), phylloplane (leaves), anthosphere (flowers), and carposphere (fruits) [76]. The phyllosphere is an ecological niche for various microorganisms, including bacteria, filamentous fungi, yeasts, and algae [77, 78]. Phyllosphere microorganisms could be either endophytic, meaning they interact with the plant’s internal environment (intercellular spaces or within the plant cell) and obtain nutrition from the host tissues, or epiphytic, meaning they are in contact with the external environment and rely on nutrients that accumulate on leaves or are released from leaves [79, 80]. Certain bacteria can thrive in both endophyte and epiphyte environments. The phyllosphere generally has a higher microbial diversity level in the episphere than the endosphere. Bacterial colonization often occurs at several leaf surface areas, including the bases of trichomes, stomata, hydathodes, vein lines, epidermal cell crossings, and cuticle recesses [81]. Plant leaves’ cellular organization of the epidermal layer provides significant insights into their physiological characteristics and internal states, which are home to microorganisms, influencing their abundance and spatial arrangement on the leaf’s surface [82,83,84]. Aliphatic molecules in plant leaves cuticle layer regulate the leaf interface’s chemical and physical attributes, affecting the surface’s wettability and penetrability, making it easier for microbes to cling to it [85, 86]. The cuticle layer’s porous nature facilitates the infiltration of water and nutrients, which is crucial for the survival, growth, and establishment of epiphytic microbial colonies in the phyllosphere [87]. The hygroscopic bio-surfactant syringafactin secreted by Pseudomonas syringae rod-shaped Gram-negative bacteria onto the leaf cuticle layer enhances the accessibility and sustainability of sugar for unceasing growth and development of epiphytic microorganisms [88, 89]. A more significant number of Pantoea eucalypti 299R bacterial colonies was observed in close vicinity to the aqueous pores on the cuticles of the phyllosphere that release fructose [90, 91].

Interaction with phyllosphere bacteria

Microbiota, which are microbial communities associated with hosts, play a crucial role in the development, growth, and ability to respond to both non-living and living stress factors in healthy host organisms [92, 93]. The phyllosphere is a rich habitat for methylotrophic bacteria, including methylobacterium, methylocella, methylibium, methylophilus, hyphomicrobium, methylocapsa, and methylocystis [94]. The composition of the bacterial community is predominantly determined by factors such as the genetic makeup of the plant, the species’ characteristics, the plant’s immune response, its age, the climate, the composition of the soil, and its geographical location [95,96,97]. The phyllosphere harbors advantageous microorganisms that effectively assist plants in mitigating both abiotic and biotic stressors [98]. The impact of bacterial interactions on the biosynthesis of abscisic acid (ABA) in plants can be both advantageous and detrimental. Incorporating Bacillus pumilus and Azospirillum lipoferum into the plant resulted in a substantial elevation in the concentration of ABA [99, 100]. Phyllosphere bacteria tend to produce and exchange compatible solutes, amines, and sugars with plants, initiating induced systemic resistance in response to drought stress [101, 102]. The production of exopolysaccharides by phyllosphere bacteria has been demonstrated to indirectly augment the availability of water for plants [103].

Analysis of the effects of inoculating Azospirillum brasilense Sp245 on the growth of Triticum aestivum ‘Pro INTA-Oasis’ under drought conditions revealed that the treated group had significantly higher levels of Mg, K, Ca, water status, and elastic adjustment than the control group which suggests that Azospirillum, in particular, may be required to improve grain quality and anthesis during drought [104]. Applying the phyllosphere bacteria Bacillus megaterium PB50 (MK979284) to a drought vulnerable rice cultivar, CO51, increased its ability to tolerate drought by increasing the relative water content and levels of total sugars, proteins, proline, calcium, abscisic acid, phenolic compounds, potassium, and indole acetic acid along with the upregulation of stress-related genes, including heat shock protein (HSP70), late embryogenesis abundant (LEA), responsive to ABA gene 16B (RAB16B), basic-region leucine zipper (bZIP23), and stress-responsive NAC1 (SNAC1), highlighting the significant role of phyllosphere bacteria in enhancing drought tolerance in plants [105,106,107]. The foliar spraying of M. arborescens, B. subtilis + S. maltophilia, S. maltophilia, B. megaterium, and E. hormaechei significantly increased the maize shoot dry weight by 10.40%, 9.53%, 8.86%, 8.73%, and 6% respectively, compared to the control. M. arborescens and S. maltophilia produced indole-3-acetic acid (I.A.A.), which increased the shoot’s dry weight. E. hormaechei showed a discernible increase in nitrogenase activity, phosphate solubilization, and IAA production, which was the most efficient way to improve nutrient uptake in maize plants [108, 109].

The bacterial strains Pantoea agglomerans F.F., Bacillus subtilis BA-142, Acinetobacter baumannii CD-1, and Bacillus megaterium-GC subgroup A. MFD-2 application on cucumbers (Cucumis sativus L.) and tomatoes (Lycopersicon esculentum L.) showed substantial positive impact on the plant’s growth traits and elevated the concentrations of magnesium (Mg), copper (Cu), nitrogen (N), phosphorus (P), calcium (Ca), sodium (Na), zinc (Zn), potassium (K), manganese (Mn), and iron (Fe) in the fruit. Maximum plant height, fruit output per plant, and mean fruit weight were attained with Pantoea agglomerans F.F. in tomato farming, and B. megaterium-GC subgroup A. MFD-2 treatment resulted in the most notable fruits in breadth, length, and dry matter. Utilizing A. baumannii CD-1 led to the maximum harvest of tomato fruits per plant. Applying P. agglomerans F.F. resulted in the most outstanding plant height, fruit output, fruit weight, fruit breadth, fruit length, and dry matter content in cucumber plants. The study showcased the importance of employing A. baumannii CD-1, P. agglomerans F.F., and B. megaterium-GC subgroup A. MFD-2 to augment the growth, productivity, and mineral composition of tomatoes and cucumbers [110,111,112,113].

Interaction with phyllosphere fungi

Fungi exert both good and harmful effects on plant life through various mechanisms (Table 1). Phyllosphere fungi have demonstrated advantageous, detrimental, or antagonistic roles on their host, particularly in the context of crop plants [114]. The relationship between plants and fungi dates back to the evolutionary age of higher plants [115]. Epiphytic fungi are exposed to the outside environment and rely on nutrients either accumulated on leaves from the atmosphere or secreted from leaves [116]. On the other hand, endophytic fungi establish direct contact with the internal environment of the plant and ingest nutrients from the host’s tissues [79]. This phenomenon shows that plants have more control over endophytic fungal colonization compared to epiphytic. Fungi might be symbiotic, saprophytic, or pathogenic, although the differences between these lifestyles may not always be readily evident [117]. Beneficial fungi play a crucial role in supporting their hosts by promoting growth, synthesizing secondary metabolites, and enhancing their ability to withstand both biotic and abiotic challenges [118]. Conversely, pathogenic fungi are responsible for inducing infections that result in crops’ decreased agronomic production and pose significant risks to food security [119]. The involvement of epiphytic and endophytic fungi in leaf litter decomposition is substantial since they contribute to recycling carbon and nutrients within ecological systems [120, 121]. Therefore, comprehensively understanding the association between plants and phyllosphere epiphytic and endophytic fungi is of utmost significance.

Table 1 Fungi with different roles in plant life

Some phyllosphere fungi cause serious infections that reduce crop production, such as corn pink ear rot, caused by many Fusarium species, although F. proliferatum (Matsushima) Nirenberg and F. verticillioides (Sacc.) Nirenberg (syn. F. moniliforme Sheldon) are the main culprit, and F. graminearum Schwabe causes maize red ear rot [122]. Tomatoes encounter significant challenges in the form of fungal infections, including late blight caused by Phytophthora infestans (fungus-like eukaryotic) and black spots, which are attributed to Alternaria sp., posing substantial risks to tomato production [123]. The sugarcane crop in tropical and subtropical regions faces challenges with significant economic losses as a result of fungal diseases, including rust disease (Puccinia melanocephela), red rot (Glomerella tucumanensis, Colletotrichum falcatum), pokkah boeng (Fusarium moniliforme), pineapple disease (Ceratocystis paradoxa), eye spot disease (Bipolaris sacchari), and smut disease (Ustilago scitaminea) [124]. Pathogenic fungi produce various toxins, including low-molecular-weight secondary metabolites that can cause necrotic spots, wilting, chlorosis, and stunted growth, which causes plant diseases and the disturbance of physiological functions, ultimately leading to plant death [125]. Hypoxylon rubiginosum was found to effectively reduce dieback disease in Fraxinus excelsior seedlings by the production of antifungal metabolites phomopsidin and 10-hydroxyphomopsidin which are the secondary metabolites of H. rubiginosum, constrained the growth of Hymenoscyphus fraxineus [126]. Endophytic fungi have a crucial role in improving plant health and protecting them against different bacterial infections by producing a diverse range of antibacterial secondary metabolites, including acetol, acetic acid, hexanoic acid, peptides, polyketides, aliphatic compounds, phenylpropanoids, alkaloids, and terpenoids which effectively reduce diseases occurrence [127].

Indeed, some reasonable efforts have been made to explore the positive and negative aspects of the interaction between plants and phyllosphere microorganisms, but several essential areas still need further investigation. Further in-depth investigations are necessary to understand the spatiotemporal distribution of macro and trace nutrients and their impact on the variety and quantity of phyllosphere microbiomes. Gaining insight into the correlation between pathogen invasion and the phyllosphere microbiota response at the community level might improve our comprehension of the interactions between plants, beneficial and pathogens microbes. It is unclear how the phyllosphere microbiomes react to pathogen threats in a way that benefits the host plants. We still need to learn more about the molecular processes behind the endophytic and epiphytic fungicide fungal response in the crop phyllosphere.

Plant–microbes interplay in the rhizosphere

Ecosystem biology research has mostly been concentrated on the aboveground parts of plants, neglecting the equally significant but less explored realm of plant roots below the ground. The interaction between plant roots and microbes in soil is a dynamic process that involves different types of signaling, physical, genetic, molecular, and chemical connections [134]. The release of diverse compounds by plant roots serves as a source of nourishment for soil microbes, hence creating a conducive environment for the development of microorganisms [135]. An extensive variety of particular exudates and metabolites regulate these interactions. Molecules of such nature are present in the vicinity or within the roots of plants, and their concentration varies depending on the distance from the place of production [136].

Plants need a minimum of 16 essential macro and micronutrients to support their growth and development, as well as improve production [137]. The absence of any nutrient in the soil might have a negative impact on the intended traits of agricultural plants [138]. The availability of nutrients in the soil is influenced by the soil’s characteristics, ambient conditions, and plant attributes [139]. The rhizosphere microenvironment serves as the primary interface for the exchange of energy and materials between the plant roots and the surrounding soil environment [140].

Plants regulate microbe’s diversity and population in rhizosphere

It has been shown that the roots of many plant species can release carbon between 10 and 250 µg per gram (mg C/g), which corresponds to about 10–40% of the photosynthetic assimilate [141]. During the process of elongation, plant roots produce a pressure of around 7 kg/cm² or more than 100 psi at their growing root tips, which enables the roots to travel downwards into the earth. Furthermore, the secretion of mucilage by the root cap and epidermal cells serves the purpose of providing lubrication, hence mitigating the risk of root damage [142]. In addition, the shed cells secrete mucilage, a polysaccharide-rich material that can attract both beneficial and pathogenic microbes [143]. The composition of exudates may differ based on their origin, although they can encompass a broad spectrum of constituents (Table 2).

Table 2 Various root exudates involved in microbes regulation in rhizosphere

Several investigations have discovered that the type and frequency of rhizosphere microbial communities are distinctive to plant species, indicating that either the plants themselves or the soil in a particular site exert dominance [144, 145]. Various root exudates (Table 2) serve as both nutrients and communication molecules for microorganisms, play a crucial role in shaping the composition of the rhizosphere microbiota [146].

The nature of exudates depends on the plant species and soil type, which has a significant influence on the microorganisms found in the area between the roots, affecting both their plenty and variety in the soil. In a sense, exudates impose control on the rhizosphere microorganism via two primary mechanisms, first by attracting certain bacteria serving as their source of nutrients like A. thaliana secretes malic acid in the region where the roots are growing to lure B. subtilis [147], and second by repelling certain species as maize root produce benzoxazinoids, which are secondary metabolites with antibacterial properties, with the ability to suppress the growth of actinobacteria, proteobacteria, and pathogenic microbial inhabitants [148].

Phenolic acid secreted by the roots of A. thaliana barley acts as an antibacterial agent to inhibit microorganisms in the rhizosphere [149, 150]. Camalexin, released by the roots of A. thaliana in the soil, has a beneficial influence on the microorganisms residing in the roots, leading to improved plant development [151]. Another research has reported that A. thaliana roots release coumarin under iron deficiency, which benefits symbiotic organisms that enhance the host’s iron intake [152]. The roots of sweet basil (Ocimum basilicum L.) emit rosmarinic acid, which has potent antibacterial properties, particularly against P. aeruginosa [153]. The exudates generated by plant roots consist of several phosphate-solubilizing compounds, such as nicotinic acid and 3-hydroxypropionic acid, which play a crucial role in regulating phosphorus absorption in both tobacco plants and rhizosphere microorganisms [154, 155]. The roots of white lupins (Lupinus albus L.) release protons and citrate to stop rhizosphere bacteria and fungi from breaking down carboxylates, which are essential for solubilizing phosphate [156]. A. thaliana root derived three exudate compounds, including galactinol, threonine, and 4-hydroxybutyric acid, were incubated with phosphorus-solubilizing bacterial strains Enterobacter cloacae, P. pseudoalcaligenes, and B. thuringiensis under either inorganic (calcium phosphate) or organic (phytin) forms of plant-unavailable phosphorus increased phosphorus availability and bacterial strains growth [157, 158]. Root-secreted strigolactones have a significant impact on soil microbes and trigger various reactions in AM fungi, such as spore germination, hyphal branching, mitochondrial activity, genetic reprogramming, and the creation of chitin oligosaccharides, which, in return, promote initial symbiotic reactions in the host plant [159]. An important rice root-produced enzyme, zaxinone synthase (OsZAS2), has a role in the synthesis of zaxinone and regulating the degree of fungal colonization [160]. Rhizathalene A from healthy A. thaliana roots [161] and momilactone A from rice roots are crucial for controlling pathogens [162].

Unrevealing and validating secretion mechanisms of exudates from the roots of diverse plant species responding to external factors may be hard and tedious, but it is a worthwhile work in the near future. Future research should investigate the effects of several external and internal variables on the composition of root exudates to understand the physiological process and molecular mechanisms that regulate rhizosphere microbiota.

Plant fungi symbiosis in the rhizosphere

Arbuscular mycorrhizal fungi (AMF) are microorganisms that typically have a tuft of hairs or cilia, rely on other living things to survive, and can form a mutually beneficial relationship with bumpily 70–90% of land-dwelling plant species [167,168,169]. The symbiotic partner plants obtain essential nutrients from the soil, mostly nitrogen (N) and phosphorus (P), through the assistance of partner fungi, and in exchange, they share approximately 20% of their photosynthetic assimilate in the form of fatty acids and carbohydrates [170]. AMF enhances plants’ ability to cope with biotic stress and adverse environmental conditions by bolstering their resilience through symbiotic relationships [171, 172]. Verticillium dahliae has antibacterial properties and promotes the colonization of tomato and cotton plants by manipulating their microbiomes through the suppression of hostile microorganisms [173].

AMF releases Myc factors detected by plant receptors, initiating conserved symbiosis signaling pathways common to both AM and root nodulation symbiosis [174, 175]. Host roots emit strigolactones, which may stimulate the germination of AMF spores and promote the formation of fungal hyphae. The fungal branching hyphae protrude toward the host plants’ root [176]. Upon reaching the surface of the plant root, the expanding hyphae generate hyphopodia. Subsequently, the plant’s epidermal cells undergo a series of events, which involve the relocation of nuclei and alterations to microtubules and the endoplasmic reticulum [177]. The outcome of this process is the development of prepenetration apparatus (PPA), which guides hyphae as they traverse the root epidermal cells [178]. The fungal organism proliferates within the intercellular spaces, where hyphae penetrate the cortical tissues of plant roots and undergo multiplication as intricately branching arboreal formations referred to as arbuscules within the plant’s cortical cells [179].

The peri-arbuscular membrane is the continuous layer of the plant plasma membrane that borders and separates arbuscules from the plant cytoplasm [180]. The highly branched arbuscules increase the surface available for exchanging vital nutrients, such as phosphorus and nitrogen, between arbuscular mycorrhizal fungi and plant hosts through a symbiotic relationship [181]. In a symbiotic relationship, AMF receives carbohydrates and lipids their host plants produce [182, 183].

Sugar delivery

Sucrose is the end-product of photosynthesis, which takes place in plant leaves and is transported to down parts of the plant, including the roots, by the phloem [184]. In the AMF-colonized roots of host plants, the produced sucrose carried by sugar transporters and SWEETS is broken down into sugars (glucose and fructose) by the enzymes invertase and sucrose synthases [185, 186]. The coexistence of mycorrhizal fungus in the roots of host plants enhances the sink capacity, which promotes the transportation of sucrose from the phloem by increasing the activities of multiple sucrose transporters in both the leaves and the colonized roots [187, 188]. Sucrose transporters such as sugar transporter (SUT), monosaccharide transporter (MST), and SWEETs tightly regulate the process of unloading sucrose from the phloem, its breakdown and subsequent exportation toward Arbuscular cells [189,190,191]. The carbon supplied to AMF is mainly glucose and fructose, which are transferred across the peri-arbuscular and fungal plasma membranes in the arbuscular cells [192]. For instance, the glomeromycotan monosaccharide transporter (GpMST1), found in Glomeromycota fungi, plays a crucial role in the uptake of sugar (glucose) from host plants during a symbiotic relationship [128]. The sugar transporter RiMST2, present in Glomus sp., is expressed inside intraradical structures and plays a crucial role in importing sugar from the host plant [129].

Fatty acid delivery

Plastids are responsible for synthesizing plant fatty acids (FA) from acetyl-CoA, which serves as the fundamental unit of the fatty acid chain [193]. In this process, a malonyl-acyl carrier protein (ACP) acts as the carbon source for all following expansion cycles [194]. Acetyl-CoA carboxylase (ACCase) facilitates acetyl-CoA conversion to malonyl-CoA, whereas fatty acid synthase (FAS) facilitates the following elongation cycles. Each iteration involves the addition of two carbon atoms to the acyl chain, leading to the formation of C16:0-ACP [195]. During elongation, the acyl chains are chemically linked to the soluble ACP by a thioester bond. Acyl-ACP thioesterase enzyme catalase the degradation of the acyl chains, hence impeding the elongation of fatty acid chains derived from the ACP [196]. AMFs cannot synthesize fatty acids (lipids) de novo and instead get them from their host plants [197]. In both symbiotic and non-symbiotic scenarios, investigations utilizing isotope-labeled carbon sources have provided evidence that AMFs are incapable of synthesizing fatty acids (FA) inside the extraradical mycelium (ERM) [198, 199]. The study conducted by reference [200] examined the genome of Rhizophagus irregularis and found no genes specifically responsible for the production of cytosolic type I FA synthase (FAS). This enzyme is crucial for the synthesis of palmitic acid (C16:0 FA) from acetyl-coenzyme A (CoA) and malonyl-CoA [201]. Subsequent genomic investigations of other fungal species have confirmed that AMF lacks genes that encode cytosolic fatty acid synthase (FAS). AMF possesses mitochondrial type II fatty acid synthase (FAS) enzymes, namely ACP malonyl-transferase (FAS1) and 3-oxoacyl-ACP synthase (FAS2), which are involved in the synthesis of octanoyl-ACP (8:0) [202,203,204]. The expression of several genes involved in the production of different fatty acids, including ketoacyl-ACP synthase I (MtKAS II), pyruvate kinase (MtPK), enoyl-ACP reductase I (MtENR I), ketoacyl-ACP reductase (MtKAR), and acyl-ACP thioesterase B (MtFATM), was increased in plants during symbiosis and are considered crucial for AMF symbiosis [205, 206].

These data indicate that plants transport lipids to AMF to maintain colonization. However, there is still uncertainty regarding the potential reactivity of extraradical mycelium (ERMs) of AMF toward fatty acids (FAs) in natural situations. However, it is conceivable that Rhizophagus species can produce spores without a symbiotic association when they come into contact with plant or bacterial exudates. Moreover, it is plausible to consider that the existence of fatty acids (FAs) in these exudates augments the spore formation mechanism in fungi that establish themselves on plant roots. Further inquiry is required to ascertain whether non-symbiotic spores are also generated in natural soils due to specific fatty acids and whether this holds any ecological significance.

Phosphorus (P) uptake

Roots colonized by AMF have the ability to directly absorb nutrients through the root epidermis and root hairs or indirectly transfer from exterior mycorrhizal hyphae to root cortical cells, where arbuscules play a crucial role in facilitating the symbiotic association [207]. AMF mycelium absorbs P, which is then moved to intraradicular fungi tissues and discharged into the peri-arbuscular space where arbuscule cells are located. Transport proteins may play a role in facilitating the symbiotic transport of P by the fungi. P is a vital element for plants, and AMF improves P uptake by increasing the surface area available for absorption and movement of limited P resources [208]. Rice relies on a symbiotic association to acquire 70% of its P from AMF [209]. AMF has been found to enhance the function of various P transporters in different host plants, including OsPT11 (Rice) [210], StPT3 (Potato) [211], and MtPT4 (M. truncatula) [212], where these transporters are known to play a role in importing P from the symbiotic interface, where the AMF releases it into the root cells. The roots inhabited by AMF frequently demonstrate diminished expression of phosphorus (P) transporters that are linked to the direct absorption pathway for P [213]. The symbiotic association with AMF decreased the expression of rice genes, including OsPT2 and OsPT6, which are involved in the direct absorption of P. This suggests that the symbiotic relationship with AMF may impede the direct absorption of P.

Recently found genes, namely MtPT4 (M. truncatula) and LjPT4 (Lotus japonicas), play a significant role in both direct and indirect (nonmycorrhizal) techniques for P acquisition in the roots of the host plant [214]. Reports indicate that P transporters, specifically GiPT (Glomus intraradices) and GvPT (G. versiforme), located on the outer hyphae of AMF are responsible for the uptake of P from the soil [130, 131]. The findings of a study indicated that there was a notable increase in the expression of P transporters, specifically GigmPT (Gigaspora margarita) and GmosPT (G. Mosseae), in both extraradical mycelium and arbuscular cells [132]. The suppression of GigmPT resulted in a reduction in the colonization of AMF, suggesting its involvement in aiding the transfer of P from the peri-arbuscular region to mycorrhizal fungi is essential for the symbiotic relationship with AMF. Moreover, previous studies have demonstrated that GigmPT plays a significant role in facilitating the translocation of reuptake and detecting P inside the AMF symbiotic association.

Further investigation is required to fully understand the molecular mechanisms that control the uptake and movement of P in the symbiotic relationship between arbuscular AMF and their host plants.

Nitrogen (N) uptake

The plant nitrogen (N) demand fulfillment is dependent on the conversion of organic nitrogen into inorganic nitrogen, such as ammonium cation (NH₄⁺) or nitrate (NO₃⁻), with the help of microorganisms [215]. The investigation conducted by reference revealed that the presence of AMF leads to a higher absorption rate of the ammonium cation ¹⁵NH₄⁺ and nitrate ¹⁵NO₃⁻, which implies that the symbiotic relationship between AMF and plants promotes N uptake in comparison to plants lacking symbiotic association. The interconnection between the intraradical mycelium (IRM) and the extraradical mycelium (ERM) within the root results in the formation of a cohesive and uninterrupted structure [216]. Numerous experimental studies have demonstrated that ERM has the capacity to assimilate approximately 42% of N via the mycorrhizal absorption pathway in plants [217, 218]. In addition, 75% of the nitrogen present in Zea maize leaves was absorbed by the ERM of G. aggregatum [219]. AMF predominantly assimilates N in ERM via the glutamate synthase, also referred to as glutamine oxoglutarate aminotransferase (GS/GOGAT) cycle, in the form of ammonium, which is subsequently metabolized into arginine, which serves as the major transport form from the ERM to IRM, where it is further broken down into urea and ornithine. Plants absorb ammonium NH₄⁺ from the symbiotic interface, produced from urea hydrolysis [220, 221]. The translocation of nutrients from the peri-arbuscular apoplast to the cytoplasm of cortical cells in plant roots is facilitated by transporters present in the peri-arbuscular membrane (PAM) [222].

The roots of Lotus japonicus that were colonized by Gigaspora margarita demonstrated a notable increase in the expression of the LjAMT2.2 gene, which is recognized for its pivotal involvement in nitrogen uptake during symbiotic relationship with AMF [133]. A study on the mutualistic association between soybean roots and AMF found that GmAMT1.4, GmAMT3.1, GmAMT4.1, GmAMT4.3, and GmAMT4.4 genes were significantly expressed. In addition, analysis of promoter reporters revealed a high expression of GmAMT4.1 genes, particularly in arbuscular cortical cells [223]. A study observed a considerable increase in the expression of genes associated with the ammonium transporter (AMT), specifically CaAMT2;1/2;2/2, 3, in roots that AMF infested. The expression of the β-glucuronidase gene in the cortical cells of chilli roots colonized by AMF was regulated by two promoter fragments, namely a 1112 bp CaAMT2;1 and a 1400 bp CaAMT2;2. Evaluating the colonization of AMF at different levels of NH₄⁺ concentrations revealed that a sufficient, yet not excessive, availability of NH₄⁺ promoted the growth of chilli peppers and the establishment of AMF colonization [224]. The expression levels of SbAMT4 and SbAMT3;1 gene were discovered to be 20- and 70-fold greater in cortical cells of Sorghum bicolor (L.) roots colonized by AMF than non-colonized [225]. A notable level of MtAMT2; 3, 4, 6 transcripts have been documented in M. truncatula during AM symbiosis. In addition, the MtNIP1 protein has demonstrated a substantial elevation in gene expression, which is important in N absorption [226]. Nitrate (NO₃⁻) transporters stimulated by AMF have been documented in many plant species, such as cucumber (Cucumus sativus L.) [227], grapevine [228], Lycium barbarum [229], M. truncatula [230], and L. japonicus [231]. The presence of AMF led to the proliferation of SlNRT2.3 gene expression within the inner cortical cells of the host plant’s roots. This phenomenon can potentially facilitate the advantageous impacts of AMF on the uptake of NO₃⁻ from the soil and its subsequent distribution to host plants [232].

The low-affinity nitrate transporter OsNPF4.5 activation was significantly enhanced, exclusively in arbuscules cells, by mycorrhizal fungi on rice roots [233]. The gene ZmAMT3, which encodes an AMF-induced transporter for ammonium [NH₄]⁺, has been identified in the cortical cells of maize roots that possess arbuscules, and its encoded protein was present in the peri-arbuscular membrane [234]. The expression of the nitrate transporter gene OsNPF4.5 in rice roots, as well as its counterparts ZmNPF4.5 in Zea maize and SbNPF4.5 in Sorghum bicolor, was significantly enhanced by the presence of mycorrhizal colonization. In addition, the elimination of OsNPF4.5 resulted in a 45% decrease in the uptake of N through symbiosis and a significant reduction in the presence of arbuscules when NO₃⁻ was used as the nitrogen input [235, 236].

However, more research is required to identify the precise roles and subcellular distribution of these mycorrhiza-induced nitrate transporters (NRTs) in promoting nitrate (NO₃⁻) transfer in symbiotic relationships, which should be prioritized in future research endeavors. Yet, an absence of research exists about the transportation of other nutrients inside the AMF symbiosis. It remains unclear how other nutrient flows or non-nutritional advantages affect the carbon expenses of the symbiotic relationship for the host plant.

Plant-growth-promoting rhizobacteria (PGPRs) direct and indirect effects

The interaction between plant roots and microbes has pivotal effects on plant growth, development, physiology, yield, and health through nutritional, biochemical, molecular, and edaphic factors [237]. The constituents of the plant root exudates attract a diverse population of microorganisms, particularly plant-growth-promoting rhizobacteria (PGPR) [238]. The rhizosphere zone facilitates the flow of chemical elements that form inter-species interactions between roots and microbes [239]. Various physical and chemical limitations of rhizosphere control the functional mode of microorganisms, which in turn affects the breakdown of soil organic matter, nutrient uptake, root organic acid secretion, respiration process, symbiotic nitrogen fixation, genetic exchange, gradient diffusion, and the enhancement of nutrient use efficiency [240]. Plants get nutritional and defensive assistance from soil-borne or root-colonizing PGPRs [241]. Proteobacteria and Actinobacteria are the two most prevalent phyla of endophytic PGPR, followed by Bacteroidetes and Firmicutes [242, 243]. These endophytic PGPR enter plant tissues using lateral roots, wounds, cracks, lenticel, germinating sprouts, and other plant structures [244, 245]. Endophytic PGPR bacteria have a diverse role in the metabolism of carbohydrates, internal defense, node germination, and nitrogen capture via nitrogenase [246, 247]. PGPR bio-inoculation, through hydrolysis, transforms organic and inorganic insoluble phosphate compounds into soluble forms of phosphorus, which can be readily taken up and enhance germination rates, increase biomass content, and supply vital nutrients such as nitrogen (N), phosphorus (P), and potassium (K) to plant roots [248]. The PGPRs produce different types of substances (Table 3) which fuels plant growth and defense either directly through the phytostimulation and bio-fertilization activity [249] or indirectly by bio-pesticides (Fig. 3) [250].

Table 3 Plant growth and disease resistance promoting PGPRs

Fig. 3

Direct and indirect roles of plant-growth-promoting rhizobacteria (PGPRs) in plant growth, protection, and promotion

Direct effects mechanism

The direct involvement of rhizosphere microorganisms in plant growth and development is defined by fulfilling plants diverse requirements in different conditions.

Nitrogen (N) fixation

Nitrogen (N) is the most vulnerable nutrient to depletion among fertilizers, and its presence in the soil is influenced by factors such as the nature of the soil, tillage, fertilizer supply, crop rotation, and precipitation. The crop could only retrieve less than 50% of the applied nitrogen quantity. Despite nitrogen from the atmosphere being present in significant levels, over 78%, but it does not exist in a shape readily available for plant roots to ingest from the soil [286]. Biological nitrogen fixation (BNF) is the process by which atmospheric N₂ is converted into ammonia (NH₃) with the help of the enzyme nitrogenase [287]. Bacteria could carry out BNF in a symbiotic connection with legumes or higher plants, like alder, providing carbon to the allied bacteria that fix nitrogen (N). It can also happen non-symbiotically with the rhizosphere’s free-living auto or heterotrophic bacteria [288, 289]. Within the symbiotic bacteria group, there are genera such as Frankia, which are allied with dicotyledonous species; certain Azospirillum, which are associated with grasses species; and Rhizobium, are connected to leguminous species [290]. Meanwhile, non-symbiotic bacteria include Nostoc, Anabaena, and Cyanobacteria, and species include Clostridium, Beijerinckia, and Azotobacter [291]. A metatranscriptomic analysis of maize plant roots revealed increased expression of nitrogen-fixing (nif) genes and enhanced N fixation when treated with Azospirillum brasilense nitrogen-fixing strain, another multispecies inoculum of PGPRs [253]. The genes that encode the enzymes needed to fix atmospheric nitrogen into a form that is obtainable by living things are known as nif genes. Another research showed that K. pneumoniae Fr and B. pumilus S1r1 strains inoculation fixed atmospheric N and offered maize plants an alternative means of obtaining N for a greater yield with less fertilizer-N application [292]. An investigation of the wheat treated with Azorhizobium caulinodans strain demonstrated increased nitrogenase activity, leading to considerable improvements in dry weight and nitrogen content compared to untreated controls [252].

Enhanced comprehension of plant function and microorganism interactions within a specific environment could be achieved using a comprehensive strategy utilizing genomics, transcriptomics, and proteomics technologies. Integrating these methods in the context of long-lasting pollution from established or newly emergent contaminants might provide new possibilities for achieving advantages in phytoremediation.

Phosphate (P) solubilization

After nitrogen (N), phosphorus (P) is a crucial ingredient in plant nutrition, which takes part in almost all significant metabolic activities, including energy transmission, photosynthesis, respiration, signal transduction, and macromolecule manufacturing [293]. P is almost evenly distributed between inorganic (P_i) and organic (P_o) forms [294]. However, plants cannot access P due to its 95–99% being in precipitated, insoluble, and immobilized states [295]. Rhizosphere bacteria play a crucial role in the dissolution and mineralization of P, facilitating its absorbability as monobasic (H₂PO₄⁻) and dibasic (HPO₄²⁻) ions. Inorganic phosphorus (P_i) becomes soluble primarily when the pH of the soil drops because of the synthesis of organic acids with low molecular weight. For organic phosphorus (P_o), contrariwise, phosphatase hydrolyzes phosphoric esters to cause mineralization [296, 297]. Some of the significant PSBs (Table 3) have been reported. In an investigation, two PSB strains, Burkholderia sp. (MTCC 8369) and Gluconacetobacter sp. (MTCC 8368), were applied to rice variety Jyothi PTB 39 in pot culture tests, which increased soluble P content and enhanced plant development metrics [254]. An investigation used PSB strains on maize, including Paenibacillus sp. B1, Pseudomonas sp. (B10, B14, SX1, SX2), and Sphingobium sp. SX14 were able to solubilize inorganic P (Ca₃ (PO4)₂, AlPO_4, and FePO₄), but only B1 and B10 solubilize organic P (lecithin). SX14 and B1 had the most incredible IAA production ability among all strains, except for SX1. B1 caused the most remarkable growth in total dry weight, root length, shoot length and total P and N. Further, it was observed through confocal laser scanning microscopy (CLSM) that Paenibacillus sp. B1 strain labeled with a green fluorescent protein (GFP) mostly inhabited root surfaces, as well as the epidermal and cortical tissue, which can survive by generating spores in harsh environments, extending the shelf life of the bio-fertilizer [255]. A study demonstrated that endophytic Pseudomonas strains L321, L228, and L111 exhibited excellent phosphate solubilization ability. Strain L321 specifically demonstrated this quality under phosphate-deficient conditions, leading to the solubilization of insoluble phosphate and promoting the growth of Pisum sativum L. plants, which may be an excellent living bacterial fertilizer option for practical use [256].

However, unresolved issues associated with PSB still prevent their blind application from achieving the goals. PSB’s dephosphorylation has the risk of creating circumstances favorable for harmful bacteria. Therefore, precautions should be taken to ensure safety and avoid unwanted consequences. To evaluate the effective use of PSB, further research into the functions of various soil mineral components and associated microbes is required to elucidate the precise process of mineral transformation at various application phases.

Potassium (K) solubilization

Potassium (K) is essential for several plant processes, including growth, development, stress tolerance, digestion, and reproduction. Rhizosphere bacteria, known as potassium-solubilizing bacteria (KSB), convert insoluble potassium (K) into soluble forms that plants pick up quickly for growth and enhance production. These KSB include a wide range of bacteria (Table 3) that are among the many saprotrophic bacteria which carry out K-solubilization. Soil contains large quantities of K-containing minerals, including orthoclase, muscovite, illite, biotite, mica, and feldspar, in a stable form that plants cannot directly absorb [298]. Generally, KSB adopts three strategies to release K such as (i) acidification, which is a process that releases organic or inorganic acids into potassium silicate or aluminium silicate in a state that is soluble in plants, dissolving the potassium aluminosilicate complex [260], (ii) creation of extracellular polymer substances (EPS) that form biofilm surrounding mineral rocks and, release K⁺ into a form that is accessible to plants, (iii) producing siderophore, where organic acids combine with Ca⁺², Fe⁺², Al⁺³, and Si⁺⁴ to generate chelating complexes that release K⁺ into the interchangeable K pool [299]. Application of KSB is an eco-friendly approach to enhance K uptake by plants suffering from K deficit, reducing reliance on chemical fertilizers [261]. The use of cyanobacteria and B. amyloliquefaciens, B. subtilis in tomato plants positively affected tomato yield by improving leaf structural traits, increasing fruit harvest, enhancing the quality of the fruit, and improving various parameters such as quantity of fruit per plant (76%), fruit size (50%), fruit width (50%), fruit weight (33%), ascorbic acid content (75%), total soluble solids (26%), and fruit N, P, and K contents compared to the control [300]. It has been reported that the use of KSB with K and P carrying minerals on sorghum increased K uptake by 41%, 93%, and 79%, P absorption by 71%, 110%, and 116%, and dry matter yield by 48%, 65%, and 58% clay, sandy, and calcareous soils, respectively [301]. The KSB, consisting of Rahnella aquatilis, P. orientalis, and P. agglomerans, were used on rice in field and pot experiments with fifty percent of the suggested K fertilizer dosage (K₂SO₄, 44% K₂O), led to a significant increase in grain yield by approximately 20–52% in the field and 20–38% in the pot, with an improvement in dry matter translocation efficiency (DME), dry matter translocation (DMT), dry matter remobilization (DMR), and the contribution of pre-anthesis assimilates (CA) from the leaves and stem to the grain in contrast to control [302]. Co-inoculating R. aquatilis and P. agglomerans KSB strains on Canola (Brassica napus L.) in both non-saline and saline soil conditions boosted grain output by 39.7% and 51.1% and decreased the need for K₂SO₄ treatment by 13.3% and 12.4%, respectively [303]. The KSB strains E. cloacae R33 and E. cloacae R13 increased the K uptake in the sugarcane ratoon and new sugarcane plantation, respectively [304].

There is a lack of understanding of the molecular processes of KSB that need more investigation, especially concerning the persistence of the inoculant in soil, evaluation of soil mineralogical characteristics before inoculation, and contrast to alternative PGPRs. Additional research focusing on the molecular processes that KSB strains utilize to solubilize fixed K and their application in different locations might create a potent potash bio-fertilizer to enhance K deficient soils, whether regular or affected by stresses. It is crucial to comprehend all the aspects that enhance the functions of KSB and the involvement of non-potassium-solubilizing (NKSB) in K mineralization to use them effectively on a large scale.

Siderophore production

Siderophores are tiny iron-chelating molecules with a high affinity for iron released by microorganisms like bacteria and fungi to solubilize Fe³⁺ for uptake [305, 306]. Like several other elements, iron is crucial for several biological processes, such as oxygen consumption, nitrogen fixation, electron transport, DNA, RNA, and protein synthesis. The soil lacks adequate soluble iron for the optimal growth of microbes and plants [307]. PGPRs use TonB-dependent transporters (TBDTs), which are bacterial outer membrane proteins that bind and transport ferric chelates (siderophores) to supply iron nourishment to either themselves or their host plant [308]. Siderophore-producing microorganisms (SPM) create several iron-chelating chemicals that can alleviate plant stress in iron-deficient soil and synthesize siderophore, which functions as a bio-fertilizer and biocontrol agent for plants and serves as a hallmark of sustainable agriculture and is environmentally benign for crop cultivation in depleted soil [309]. There is a significant number of siderophore-producing bacterial (SPB) genera (Table 3) which produce siderophores with more than 500 diverse chemical structures. Bacterial siderophore named pyoverdine produced by Pseudomonas fluorescent spp. strain (C7R12) was applied on A. thaliana cultivated in low-iron circumstances, potentially improved plant growth and defense [310]. Priming seeds of wheat cultivars Ekada70 and Salavat Yulaev with B. subtilis 10-4 enhanced drought tolerance by elevating endophytic siderophore levels and decreasing lipid peroxidation, proline concentration, and electrolyte leakage in primed seedlings [311]. Streptomyces ciscaucasicus strain GS2 isolated from Malus domestica roots generated ferrioxamines siderophore, which helps to prevent apple replant disease and boosts apple plant development and productivity [312]. The B. subtilis strain LSBS2 obtained from the rhizosphere of the sesame (Sesamum indicum) plant produced bacillibactin siderophore under iron-deficient conditions, which increased the production of indole acetic acid (IAA), ammonia, hydrogen cyanide (HCN), and nutrient availability, including iron, in the sesame plant [313]. Siderophores producing PGPRs have also been effectively preventing various plant diseases, such as wheat root rot, cotton damping-off, vascular wilts, peanut stem rot, and potato seed piece decay [314]. The hydroxamate derived by siderophore-producing A. chrococcum RRLJ 203 strain effectively inhibits the growth of F. solani, F. udum, F. oxysporum, F. moniliforme, Fomes lamnensis, and Ustulina zonata [315]. Siderophore-producing PGPRs serve as biological control agents (BCAs) by inhibiting the pathogen’s access to iron nutrients, leading to enhanced crop production [316]. Siderophore-producing PGPR suppressed Colletotrichum gossip, which promoted plant development in cotton seedlings, and the RBT 13 strain of P. fluorescent has antagonistic activity toward various bacterial and fungal plant diseases [317, 318].

Siderophores have essential roles in several fields of life, including the medical sector, agriculture, ecology, and bioremediation, making them an important subject of scientific interest. Comprehensive details on the PGPR’s interaction with plants and their role in metal uptake by siderophores, the exact location of siderophores in plant tissues, and various types of siderophores to fulfill mineral nutritional requirements are currently mostly ambiguous. The precise impact of these iron-chelating chemicals on disease suppression as biocontrol agents remains uncertain. The exact role of protein in siderophore-mediated immunity has yet to be thoroughly elucidated. Siderophores visibly induce significant physiological changes in plants, but the precise details of pathways need further investigation. Enhanced comprehension of how siderophores improve plant immunity might lead to the development of innovative crop protection tactics. It is essential to establish a link between the molecular properties of siderophores and their function and apply the obtained knowledge in diverse biotechnological fields linked with medicine, agriculture, the food industry, bioremediation, and pollution biodegradation.

Phytohormones production

Various PGPRs can synthesize hormones that regulate plant growth, development, and structural changes in reaction to gravity or light, as well as biotic and abiotic stresses. Indole-3-acetic acid (IAA) is the predominant plant hormone in the auxin class, which regulates multiple facets of plant propagation [319, 320]. Approximately 80% of rhizobacteria that inhabit seed or root surfaces are involved in synthesizing IAA and collaborate with endogenous IAA of plants to enhance cell division, nutrient absorption, seed germination, vegetative growth, photosynthesis, root and xylem growth, pigment production, metabolite synthesis, stress tolerance, and formation of lateral and adventitious roots [321, 322]. Bacterial strains (Table 3) such as P. polymyxa RC05, B. RC23, B. RC03, B. subtilis OSU142, B. simplex RC19, B. megaterium RC01, Comamonas acidovorans RC41, A. brasilense Sp245 Acromobacter insolitus S3, P. plecoglossicida B3, and E. hormaechei W1 have been reported to be involved in plant growth and development and resistance under biotic and abiotic stresses [262, 263, 323].

Ethylene is a gaseous hormone present in very low concentrations and is well known as a stress hormone because its levels increase significantly during different environmental and biological stresses. Specific PGPRs possess an essential enzyme, 1-aminocyclopropane-1-carboxylate (ACC) deaminase, which controls ethylene production by metabolizing ACC, a precursor of ethylene production in plants, into alpha-ketobutyrate and ammonia, assists in maintaining plant growth and development during stressful situations by decreasing the ethylene synthesis generated by stress [324]. Glutamicibacter sp. YD01 mitigated the negative impacts of salt stress on rice plants by regulating ethylene and ROS levels, balancing ion levels, promoting photosynthesis, and boosting the expression of stress-responsive genes [264]. Gibberellins are gibberellic acids (GAs) including GA1, GA3, GA4, and GA7, among them GA1 and GA4 being common in different plants, which regulate transitions among various stages of plant growth and development, including activities like cell division and elongation [325, 326]. Bacterial strains (Table 3) enhanced gibberellic acid 4 (GA4), SA, chlorophyll levels, biomass, water potential, P and K while reduced electrolytic leakage, sodium ion concentration, peroxidase, catalase, and polyphenol oxidase activities in cucumber plants under salinity and drought stress ultimately increased growth and defense [266]. An examination of cabbage seedlings treated with bacterial strains (Table 3) boosted levels of GA, SA, and IAA, as well as leaf area. [267]. Cytokinins stimulates roots and shoots cytokinesis, and influence cell differentiation and development, impacting leaf senescence, axillary bud growth, apical dominance, and biotic and abiotic factors [327]. The bacterial strain P. fluorescens G20-18, A. brasilense RA 17, and B. subtilis enhanced tomato resilience, wheat growth, lettuce ABA levels respectively. [328, 329]. Pre-sowing wheat seeds treated with the cytokinin-producing B. subtilis IB 22 induced prompt canopy closing and increased yield by 40% under the circumstances of mild drought [270].

PGPRs can indeed enhance plant growth and productivity by creating or metabolizing hormones. However, in specific plant–microbe interactions, the stimulation of plant growth by microbes necessitates both the generation of microbial hormones and the plant’s sensitivity to these hormones, which requires further investigation. The mechanism of hormone synthesis by PGPRs is still not fully understood. Hormones production in the soil is not an independent process but works in synergy with other plant growth-promoting rhizobacteria (PGPRs) processes. IAA bacterial synthesis is a process that involves inhibiting plant growth by harmful rhizobacteria. Further research is required to pinpoint the bacterial-induced processes that regulate ethylene signaling and responsiveness in the presence of salt and other stress.

Indirect effects mechanism

PGPRs also support plant growth, production, and disease resistance through indirect mechanisms with multiple modes.

Antibiotic synthesis

Antibiotics are compounds that are effective against harmful microorganisms and save the lives of living organisms. Some of the common PGPRs that generate antibiotics include several strains of Bacillus, Azospirillum, Serratia, Rhizobium, and Pseudomonas, and their biocontrol strategies mostly rely on the generation of antibiotics like 2,4-diacetyl phloroglucinol, phenazine-1-carboxylic acid, oomycin, pyrrolnitrin, kanosamine, pyoluteorin, pantocin, and zwittermicin-A, which involves endogenous signals cascade such as sensor kinases, N-acyl homoserine lactones, and sigma factors [330, 331]. Several studies have demonstrated that plants can be saved by antibiotics produced by PGPRs, particularly when a single treatment of specific strains (Table 3) is used to reduced severity of leaf blight in taro (Colocasia esculenta) caused by P. colocasiae up to 30–50% in vitro and 88.75–99.37% under greenhouse condition and improved plant growth. An investigation showed that A8a, a strain of B. acidiceler, inhibited P. cinnamomi by 76% in a potato dextrose agar vitro test by emitting volatiles like 6,10-dimethyl-5,9-undecadien-2-one, 3-amino-1,3-oxazolidin-2-one, and 2,3,5-trimethyl pyrazine, which indicates that these bacteria have the potential to be employed in the biocontrol methods of soil-borne oomycetes using their volatile emissions ability [272].

Hydrolytic enzyme manufacturing

Hydrolytic enzymes, also known as hydrolases, are responsible for the hydrolysis of several biomolecules, including carbohydrates, glycosides, esters, peptides, lipids, proteins, fats, and nucleic acids, into their fundamental constituents [332]. Biocontrol of phytopathogens such as Agroathelia rolfsii, Fusarium oxysporum, Rhizoctonia solani, and Pythium ultimum is achieved by a variety of bacterial strains, including S. marcescens, B. subtilis, B. cereus, and B. huringiensis, which produce hydrolytic enzymes like cellulases, protease, glucanase, and chitinase, which causes swelling in the hyphae, hyphal tip, hyphal curling, and bursting of the hyphal tip, which affect the physical integrity of the pointed pathogens’ cell wall and inhibits pathogens infection [273, 274]. The hydrolase synthesis, IAA generation, potassium and phosphate solubilization, and 1-aminocyclopropane-1-carboxylic acid deaminase activity were shown by B subtilis S42, P. azotoformans C2-114, and E. cloacae S81, which suggest that the use of hydrolase-producing rhizobacteria as a bio-fertilizer can enhance soil quality and increase crop production through improving plant height, biomass, root length, surface area, diameter, volume, and tuber fresh weight in Jerusalem artichoke [275]. S. bicolor mycorrhizosphere-isolated Paenibacillus sp. strain B2 has plant-growth-promoting capability along with an antagonistic activity toward cell integrity of two soil-borne pathogenic including fungi P. parasitica and F. oxysporum through the use of proteolytic, cellulolytic, pectinolytic, and chitinolytic enzymes activities established it as growth-promoting and biocontrol agent [276]. Despite advancements in comprehending the functions of hydrolytic enzymes derived from plant-associated PGPRs in facilitating host colonization and stimulating the plant immune system, progress in this area remains hindered by the presence of toxic by-products resulting from pretreatment procedures and the exorbitant expenses associated with different hydrolases, which need further research.

Induced systematic resistance

Plants have exhibited natural resistance via systemic acquired resistance (SAR) and induced systemic resistance (ISR), which are activated by pathogenic and non-pathogenic bacteria, respectively [333, 334]. Bacterial strains of Bacillus spp. and Pseudomonas spp. have shown broad-spectrum disease resistance. B. cereus AR156 triggers plant defense mechanism by stimulating the production of callose and hydrogen peroxide, as well as activating superoxide dismutase (SOD) and peroxidase (POD) via mitogen-activated protein kinases (MAPKs) and SA signaling pathways [277]. Multiple studies have shown beneficial bacteria in the plant rhizosphere enhance plant health. However, there is a pressing need for in-depth research on the mechanism governing the equilibrium between effective identification and the intensity of the host immune response. The genes and transcription factors involved in defense response form a complex network via signaling crosstalk, requiring thorough understanding to optimize the plant protection system.

Exopolysaccharides synthesis

Exopolysaccharides (EPSs) are a class of long-chain polysaccharides composed of repeating sugar units, primarily including rhamnose, galactose, and glucose in different proportions, secreted by bacteria in response to physiological stressors, enabling the formation of biofilms and promoting adherence to plant root surfaces [335, 336]. Bacterial EPS can significantly mitigate drought stress in plants by enhancing soil composition and water retention, facilitating bacterial colonization and biofilm creation, and regulating plant reactions to water scarcity, which, in turn, allows plants to allocate more time for metabolic adaptations to drought [337]. EPS-producing bacterial strains (Table 3) mitigated the negative impacts of moisture stress, increased leaf protein and sugar content, maintained higher chlorophyll content and fluorescence, and performance indices in Shahkar-2013 and Inqilab-91 wheat genotypes effectively under rain-fed circumstances [278]. Another study found that under salt stress, the bacterial strain P. anguilliseptica SAW 24 produced exopolysaccharides, formed biofilms, and enhanced plant height, fresh weight, and dry weight of Vicia faba L. [279]. Nevertheless, further investigation into EPS is necessary to enhance the resilience of crops against non-living factors and gain a deeper comprehension of the fundamental physiological and molecular processes involved, enabling the effective utilization of EPS-producing bacteria in crop cultivation to sustain productivity and guarantee food availability.

Conclusion and future aspects

The global population is experiencing overgrowth, resulting in a widening disparity between the demand for and supply of food. The agriculture sector is under pressure to increase crop production to meet the demand for necessary food. Contemporary agricultural practices heavily depend on the extensive utilization of agrochemicals to reach the objective of maximizing productivity. This reliance continuously raises environmental risks, global climate change, agricultural land depletion, rapid urbanization, and pervasive agrochemical application. Consequently, these factors collectively negatively influence crop production and ecological systems on a global scale. Thus, reducing the application of chemical fertilizers and pesticides for plant growth and protection should be a top priority to achieve eco-friendly and sustainable agricultural development. Plant–microbe interaction potential should be considered a better alternative for high production, disease resistance, and sustainability in agriculture.

Researchers have made reasonable efforts to replace or minimize the application of synthetic fertilizers and pesticides to get healthy and high-production crops by regulating plant–microbe interaction. Countless beneficial and pathogenic microorganisms coexist with plants above the ground in the phyllosphere and below in the rhizosphere in the form of endophytes, epiphytes, or both. The latest scientific investigations have provided evidence indicating that bacteria and fungi establish robust connections with their host plants, thereby facilitating plant growth and impeding plant disease occurrence. In response, plants have evolved mechanisms to interact with beneficial microorganisms and cope with detrimental pathogens. The reported research has shown that microorganisms have increased plant growth, flowering, seed germination, proper development of roots and shoots, soil fertility, solubilization of nutrients like phosphate and potassium, plant protection against different pathogens, disease resistance, resilience under various biotic and abiotic stresses like salinity and drought. However, further enhanced comprehension of the underlying mechanisms of phytohormone activities in plant–microbes interactions would facilitate the identification of novel strains with more potential to mitigate the adverse impacts of different stress in diverse regions and serve as an alternative approach to alleviate stress in agricultural practices. Identifying novel microorganisms that synthesize valuable hydrolytic enzymes is a feasible alternative to managing phytopathogens. Additional research is necessary to comprehend the genetic variability of beneficial microbes and host plants and incorporate them into breeding initiatives that enhance plant productivity and disease resistance through heritable patterns.

It has been reported that plants have evolved two types of immunity that consist of different modules of immune receptors, which allow the recognition of non-self-components that are either unique to a particular strain of microbe or conserved among members of a microbial class and are the foundation of existing conceptions of the plant inborn immune system. The first category of receptors is membrane-resident pattern recognition receptors (PRRs), which are responsible for detecting microbe-associated molecular patterns (MAMPs) that are widely conserved on the cell surface, while the second class of intracellular immune sensors, specifically resistance (R) proteins, capable of recognizing either the structure or function of strain-specific pathogen effectors that are transported into host plant cells. A further extensive elucidation of inherent defense mechanisms in host plants during or after pathogen infection, including cell wall components, metabolic enzymes, molecular mechanism, cellular signaling, and their modulation, would benefit developing disease-resistant varieties with high production and sustainability. Identifying newly evolved phytopathogens with an emphasis on mining and annotating genes associated with the plant–microbe interaction from the genomes of both partners is crucial.

Advanced technologies, such as next-generation sequencing and omic methodologies, including transcriptomics, metabolomics, proteomics, genomics, and bioinformatics, can help to explore the complexities of plant–microbe interactions and ascertain the molecular and physiological mechanisms involved. A comprehensive understanding of the genetic and molecular mechanisms that govern the interaction between plant microbes will significantly enhance the efficacy of resistance breeding strategies and accelerate the development of crop resilience. This will contribute to the overarching goal of cultivating plants resistant to both biotic and abiotic stressors, with a particular focus on crops.