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Palma, M.D.;  Scotti, R.;  D’Agostino, N.;  Zaccardelli, M.;  Tucci, M. Direct Mechanism of Plant Stimulation by Plant-Growth-Promoting Microorganisms. Encyclopedia. Available online: (accessed on 11 December 2023).
Palma MD,  Scotti R,  D’Agostino N,  Zaccardelli M,  Tucci M. Direct Mechanism of Plant Stimulation by Plant-Growth-Promoting Microorganisms. Encyclopedia. Available at: Accessed December 11, 2023.
Palma, Monica De, Riccardo Scotti, Nunzio D’Agostino, Massimo Zaccardelli, Marina Tucci. "Direct Mechanism of Plant Stimulation by Plant-Growth-Promoting Microorganisms" Encyclopedia, (accessed December 11, 2023).
Palma, M.D.,  Scotti, R.,  D’Agostino, N.,  Zaccardelli, M., & Tucci, M.(2022, October 25). Direct Mechanism of Plant Stimulation by Plant-Growth-Promoting Microorganisms. In Encyclopedia.
Palma, Monica De, et al. "Direct Mechanism of Plant Stimulation by Plant-Growth-Promoting Microorganisms." Encyclopedia. Web. 25 October, 2022.
Direct Mechanism of Plant Stimulation by Plant-Growth-Promoting Microorganisms

Sustainable agricultural systems based on the application of phyto-friendly bacteria and fungi are increasingly needed to preserve soil fertility and microbial biodiversity, as well as to reduce the use of chemical fertilizers and pesticides. The different mechanisms of action triggered by plant-growth-promoting microorganisms (PGPMs) promote host-plant growth and improve its defense system.

rhizobiome gene expression beneficial soil microbes plant growth

1. Introduction

Sustainable intensification that limits the ecological footprint is one of the main challenges humans will face in agriculture. The growing demand to reduce the use of chemicals is currently leading to a greater focus on more environmentally friendly crop management [1].
Beyond the well-known mycorrhizal fungi and Rhizobium bacteria, other non-symbiotic rhizobacteria (PGPR) and fungi (PGPF) are recognized as plant-growth-promoting microorganisms (PGPMs). A large amount of commercial PGPM-based products are currently available and used in organic and integrated agriculture for their ability to increase plant development and growth and improve plant health by strengthening crop resistance to (a)biotic stresses [2][3][4]. Commercial microbial consortia, generally consisting of a mix of rhizosphere bacteria (mainly Pseudomonas spp. and Bacillus spp.), useful fungi (Trichoderma spp.), nitrogen-fixing bacteria (principally Azotobacter spp. and Azospirillum spp.), or arbuscular mycorrhizal fungi, are receiving considerable attention for their additive/synergistic biostimulant effects on inoculated plants [5]. Microbial consortia can be designed as agricultural probiotics, as they stimulate the recovery of functional, beneficial microbial groups and supply the natural microbiome reduced by crop domestication [6]. Furthermore, they are used in plant microbiome engineering to modify the structure of pre-existing microbial communities [7].
Despite the above-mentioned beneficial effects, some limitations need to be overcome for large-scale exploitation of PGPMs in agriculture [3][8]. Indeed, PGPM use is still quite limited because of (i) the low availability of high-throughput methods for their screening, isolation, and characterization; (ii) constraints in the large-scale production technologies at industrial level; (iii) the lability of the formulations on the market and the few efforts in producing innovations related to the improvement of the shelf-life of PGPM formulations; (iv) the dearth of innovative and effective strategies and methods for their delivery (i.e., the development of adequate and reliable carriers based on the most advanced nanobiotechnologies) [9][10]; (v) the lack or ineffectiveness of regulations and guidelines that restrict their commercialization [11]; and (vi) the small number of well-trained operators responsible for quality control and biosecurity of the formulations. Nevertheless, the number of agrochemical companies and start-ups developing and marketing microbial products has significantly increased in recent years [12].
Although the use of PGPMs is having great success in innovative agricultural practices and considerable progress has been made in characterizing the complexity of plant–PGPM interactions, there are still several open questions regarding how microbial assembly is established, developed, and maintained throughout the plant’s life cycle. High-throughput technologies and ‘omics’ sciences have accelerated the understanding of plant relationships with microbial communities and especially of (i) how plants and microbes intimately interact, and (ii) how microbes affect plant development, fitness, health, and adaptation to environmental perturbation, (a)biotic stress susceptibility/tolerance, nutrient transfer, cycling, etc. [13][14]. In recent years, huge strides have been made in the field of metagenomics, hence allowing researchers to identify and characterize mutualistic and antagonistic plant microbial communities starting from the DNA directly extracted from an environmental sample [15].
RNA-based studies are the basic requirement to study the temporal evolution of the complex interaction process between the host plant and the microbes. At present, most reports only focus on host transcriptomics, whose goal is to investigate the transcriptome dynamics and derive gene expression patterns to identify the key processes activated in the plant following the beneficial interaction with soil microbes and to describe the plant adaptation response [16][17][18][19][20].
Dual RNA-sequencing or multi-species transcriptomics, that is the parallel analysis of transcriptome dynamics and gene expression profiles of microbes and their hosts, is much less usual despite being essential to reveal the molecular mechanisms that mediate host/microbe interplay [21][22].
A further level of analysis concerns the identification and quantification of the chemical compounds and the characterization of the metabolic alterations that occur during host–microbe communication [23]. Indeed, metabolomics is increasingly used to unravel the chemical complexity underlying the interactions between plant hosts and their associated microbial communities [24]. Knowing what metabolic changes are taking place is essential to identify which plant metabolites are key players in favoring the interaction with the rhizosphere microbiome, which microbe chemical classes are necessary to establish an effective cooperation relationship and ultimately to reconstruct metabolic models for specific communities of interactors. The next step is to integrate data and knowledge across the omics cascade to investigate plant–microbe relationships at multiple biological scales, moving from the gene to ecosystem levels. The complementation of omics data (i.e., holomics) allows researchers (i) to get a more precise overview and a systems-level understanding of the plant holobiont (namely, the plant and its associated microbes), (ii) to unlock the molecular reprogramming at play in both host and microbe community during the interaction, and (iii) to resolve the structure and functioning of agricultural ecosystems [25].
The ultimate goal is to move from basic to applied research, i.e., to manipulate these interactions to make them even more efficient. This means, on the one hand, improving plant health and increasing productivity and, on the other, developing sustainable disease management strategies, remodeling the microbiome in soil systems, promoting soil health and ecosystem homeostasis, and fostering the sustainability of ecosystems.

2. Overview of the Mechanisms Modulated by PGPMs to Improve Plant Growth

Most of the PGPMs that populate the rhizosphere [26] are associated with the root system and exert a phytostimulating effect, attributable to both direct and indirect mechanisms. Direct mechanisms include nutrient availability in soil (e.g., solubilization and mobilization of nutrients) and the production of phytohormones [27][28]. The exploitation of lytic enzymes, antibiotics, siderophores, and volatile and non-volatile metabolites, as well as the induction of systemic resistance (ISR) for the suppression of harmful phytopathogens, have been reported as the main indirect mechanisms through which PGPMs promote plant growth and development [29][30].
Hydrogen cyanide (HCN) is a volatile secondary metabolite synthetized by several PGPMs [31][32] that can control the level of deleterious microbes in the rhizosphere. For example, the suppression of tomato root knot disease caused by Meloidogyne javanica is mediated by HCN-producing P. fluorescens [33]. Recently, a large body of evidence has demonstrated that PGPM stimulation of plant growth results also from complex chemical signaling mediated by volatile organic compounds (VOCs) [34][35]. VOC production is widespread and can be very different between PGPR and PGPF [36]. VOCs produced by both P. fluorescens SS101 and B. subtilis SYST2 increased plant biomass [34][37]. Plant exposure to VOCs emitted by different Trichoderma spp. was found to significantly improve the chlorophyll content, size, and biomass of plants [38].
Table 1 lists some examples of growth benefits conferred to plants by different PGPMs, as well as the various mechanisms involved.
Table 1. Different mechanisms of plant growth promotion used by PGPMs.

3. Direct Mechanism of Plant Stimulation by PGPMs

3.1. Role of PGPMs in the Availability of Soil Nutrients and in the Uptake of Nutrients

Plant nutrition is essential for optimal agricultural production, thus an adequate supply of nitrogen (N), phosphorus (P), and sulfur (S) forms and ionic species is necessary and usually added to the soil as synthetic fertilizers [58]. However, the increase in the use of chemical fertilizers does not proportionally guarantee crop yields and has a long-term impact on the environment in terms of water and soil pollution, depletion of soil fertility, and carbon footprint [59]. Phyto-friendly soil microbes are a very promising alternative to conventional fertilizers [60][61].
More than a half of the N released into the soil by the conventional N-based fertilizers is lost through the processes of denitrification, runoff, leaching, and erosion. Despite the abundance of nitrogen in the Earth’s atmosphere, the gaseous form of nitrogen is not readily accessible to plants until its conversion into ammonia [62]. In this context, PGPMs can support nitrogen assimilation mainly through mineralization and nitrogen fixation [63], hence enhancing N use efficiency [49]. For example, free-living, associative, and endophytic nitrogen-fixing bacteria have been found to increase plant growth, vigor, and yield in various non-leguminous crops such as rice (Table 1), wheat and sugarcane [39][64]. Recently, fertilizer formulations that included free-living N2-fixing bacteria along with organic and inorganic N forms proved to be a promising strategy for reducing N leaching and improving growth in sugarcane and macadamia plants [65][66]. The presence of fungal inoculants, mostly belonging to the genus Trichoderma (Table 1), optimizes nitrogen-use efficiency (NUE) in lettuce (Lactuca sativa L.) and rocket (Eruca sativa Mill.), favoring the uptake of the native N of the soil and improving N uptake by roots in conditions of scarce availability [48][49]. Inorganic N in the form of nitrate (NO3) and ammonium (NH4+) can be uptaken by plants directly from the soil because of the activation of nitrate (NRT)/ammonium (AMT) transporters, which have been thought to be the key components for improving NUE [67][68][69]. Recently, Calvo et al. [70] found that root stimulation with mixtures of PGPR belonging to the genus Bacillus increased nutrient uptake in Arabidopsis thaliana, affecting the transcriptional levels of both NRT and AMT transporters. Otherwise, following the stimulation of tobacco roots with T. asperellum, the increased expression of several high-affinity NRT genes and the down-regulation of the AMT1 gene suggested a preferential induction of the NRT transporter system for nitrate acquisition [71].
Despite being present in large amounts in the soil, P is a major plant-growth-limiting nutrient because inorganic phosphate (orthophosphate; Pi), the chemical form that can be assimilated by the plant, is available at low concentrations [72]. The mechanisms involved in the solubilization/mineralization of P from inorganic and organic forms in soil are well-documented in PGPMs [73]. In this regard, several PGPMs have been shown to enhance P assimilation and, as a consequence, growth and the yield when applied to crops (Table 1). Paenibacillus and Trichoderma are promising candidates for crop inoculation because of their ability to solubilize Pi mainly through the acidification of the soil environment by the production of organic acids [74][75]. Plant acquisition of Pi and its homeostasis is mediated by phosphate transporters (PTs) [72] and PGPMs could favor these processes through the transcriptional modulation of members in the PT gene family [76]. Recently, attention to the regulatory effects of PGPR on PT genes has been reported for the phosphate-solubilizing rhizobacterium Pseudomonas sp. P34-L. This strain significantly increased P accumulation in wheat and this ability correlates with reduced transcript levels of the TaPT4 gene as an indicator of phosphorus deficiency [77].
Finally, a greater availability of many nutrients such as calcium, magnesium, sulfur, iron and zinc is necessary for the development of physiological and metabolic processes in plants [78]. In a low-nutrient-intake scenario, the zinc solubilization activity of PGPR (Table 1) has been reported as a new sustainable approach to overcome zinc deficiency and increase plant growth [43]. Interestingly, T. harzianum T-203 (Table 1) increased the concentrations of several macro- and micro-nutrients (e.g., P, Fe, and Zn) in the roots of cucumber, through the mineralization of organic matter in the soil [51].

3.2. Role of PGPMs in Hormonal Balance

Colonization of the rhizosphere is known to be associated with profound changes in hormone homeostasis. Phytohormones act as messengers to coordinate cellular activities and to regulate plant growth, modification of root and shoot architecture, and synthesis of secondary metabolites [79][80][81]. Auxins are an important class of phytohormones that influence the size of shoot and root meristems [82]. Phyto-friendly soil microbes can directly affect plant auxin metabolism (Table 1) by synthesizing auxins [83] or indirectly by influencing the level of endogenous plant auxin [46].
Several studies involving different strains of Aeromonas punctata, Azospirillum brasilense, and Burkholderia cepacian suggest that auxin synthesis may be the main cause of the stimulating effect of some PGPR strains on host plants [80][84], while some PGPF (Table 1) can promote root growth also by influencing the level of endogenous plant auxin [56].
Since PGPMs can have both beneficial and harmful effects on the plant depending on their quantity and environmental conditions, the plant can perceive them as weak biotrophic pathogens. The synthesis of auxins by PGPR may be part of a strategy to suppress the resistance of the host allowing for a more effective colonization. Therefore, the ability to synthesize auxins and their quantity are important characteristics of a PGPR strain, as they can determine the strain’s impact on the plant to a large extent. PGPR can also influence auxin transport by altering the activity of auxin influx and efflux carriers. For example, Bacillus sp. LZR216 negatively regulates the synthesis of auxin transporters AUX1 and PIN1, -2, and -3 [45], while treatment with Burkholderia phytofirmans PsJN results in greater expression of PIN2 and PIN3 [46].
Meents et al. [53] reported that the exposure of A. thaliana to Piriformospora indica (Table 1) significantly increases auxin levels and induces the expression of auxin-responsive genes in lateral root primordia and root elongation zone within 1 day. Elevated auxin levels were also recorded in the Mortierella hyalina/Arabidopsis root interaction, but no downstream effects were observed on the auxin-responsive genes [53]. Some strains of T. virens and T. atroviride are known to produce indole-3-acetic acid (IAA) and auxin compounds that affect plant growth and root development [56][85], resulting in greater nutrient absorption efficiency. On the other hand, some secondary metabolites can act as auxin-like molecules. Vinale et al. [54] reported that 6-n-pentyl-6H-pyran-2-one (6PP) from Trichoderma can be considered an auxin-like compound or can act as an auxin inducer.
Another important phytohormone affected by PGPMs is ethylene. It plays a key role in plant growth and developmental processes such as ripening, senescence, and abscission, and in regulating the defense response of plants to various (a)biotic stresses [86]. Phyto-friendly soil microorganisms can influence plant ethylene homeostasis (Table 1) by affecting the expression of the genes that encode for enzymes responsible for the synthesis of ethylene such as ACC-synthase (ACS) and ACC-oxidase (ACO) [46][87], or by expressing ACC-deaminase, thereby reducing the amount of ethylene in the plant by degrading its precursor, 1-aminocyclopropane-1-carboxylic acid (ACC) [88][89]. The resulting changes in ethylene levels can affect root system development. Mayak et al. [90] reported an increase in the number of roots in mung bean plants treated with two strains of Pseudomonas putida that produce IAA.
The ability to produce ACC-deaminase is also present in PGPF, as in the case of T. asperellum, which exhibits a reduced ability to promote root elongation of canola seedlings when a specific ACC gene is knocked out [55]. PGPMs with ACC-deaminase activity are known to mitigate the damaging effects of abiotic stresses on plant growth and development, such as high salinity, soil pollution by heavy metals and organic pollutants, floods, drought, and mineral deficiency [16][91]. Treatment with bacterial consortia (Aneurinibacillus aneurinilyticus and Paenibacillus spp.) significantly reduced (∼60%) stress-stimulated ethylene levels (Table 1) and its associated growth inhibition in Allium sativum L. [47]. In Brotman et al. [16], ACC-deaminase-silenced Trichoderma mutants were less effective in providing salt-stress tolerance, suggesting that Trichoderma, similarly to bacteria that produce ACC deaminase, can promote plant growth under abiotic stress, lowering ameliorative increases in ethylene levels and promoting high antioxidant capacity.


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