# Rhizosphere Signaling: Insights into Plant-Rhizomicrobiome Interactions for Sustainable Agronomy

Fatima Jamil, Hamid Mukhtar, Mireille Fouillaud, Laurent Dufossé

► To cite this version:

Fatima Jamil, Hamid Mukhtar, Mireille Fouillaud, Laurent Dufossé. Rhizosphere Signaling: Insights into Plant-Rhizomicrobiome Interactions for Sustainable Agronomy. Microorganisms, 2022, 10 (5), 10.3390/microorganisms10050899. [https://doi.org/10.3390/microorganisms100508778](https://doi.org/10.3390/microorganisms100508778)

HAL Id: hal-04148778

https://hal.science/hal-04148778

Submitted on 3 Jul 2023

HAL is a multi-disciplinary open access
archive for the deposit and dissemination of sci-
entific research documents, whether they are pub-
lished or not. The documents may come from
teaching and research institutions in France or
abroad, or from public or private research centers.

L'archive ouverte pluridisciplinaire HAL, est
destinée au dépôt et à la diffusion de documents
scientifiques de niveau recherche, publiés ou non,
émanant des établissements d'enseignement et de
recherche français ou étrangers, des laboratoires
publics ou privés.

<figure><img src="image_1.png" /></figure>

Distributed under a Creative Commons Attribution 4.0 International License
# Rhizosphere Signaling: Insights into Plant-Rhizomicrobiome Interactions for Sustainable Agronomy

Article in Microorganisms · April 2022

DOI: 10.3390/microorganisms10050899

CITATIONS

20

READS

342

4 authors:

<figure><img src="image_2.png" /><figcaption>Fatima Jamil
University of Agriculture Faisalabad</figcaption></figure>

17 PUBLICATIONS 203 CITATIONS

SEE PROFILE

<figure><img src="image_3.png" /><figcaption>Hamid Mukhtar
Government College University, Lahore</figcaption></figure>

212 PUBLICATIONS 2,186 CITATIONS

SEE PROFILE

<figure><img src="image_4.png" /><figcaption>Mireille Fouillaud
University of La Réunion</figcaption></figure>

73 PUBLICATIONS 1,255 CITATIONS

SEE PROFILE

<figure><img src="image_5.png" /><figcaption>Laurent Dufossé
University of La Réunion</figcaption></figure>

307 PUBLICATIONS 6,186 CITATIONS

SEE PROFILE

Some of the authors of this publication are also working on these related projects:

<figure><img src="image_6.png" /></figure>

Protease production, purification and application in leather industry View project

<figure><img src="image_7.png" /></figure>

Lipase mediated transesterification of oils for the synthesis of biodiesel View project
<figure><img src="image_8.png" /></figure>

Review

# Rhizosphere Signaling: Insights into Plant-Rhizomicrobiome Interactions for Sustainable Agronomy

Fatima Jamil <fnref n="1" />, Hamid Mukhtar <fnref n="1" />*, Mireille Fouillaud <fnref n="2" />* and Laurent Dufossé <fnref n="3" />

**Abstract:** Rhizospheric plant-microbe interactions have dynamic importance in sustainable agriculture systems that have a reduced reliance on agrochemicals. Rhizosphere signaling focuses on the interactions between plants and the surrounding symbiotic microorganisms that facilitate the development of rhizobiome diversity, which is beneficial for plant productivity. Plant-microbe communication comprises intricate systems that modulate local and systemic defense mechanisms to mitigate environmental stresses. This review deciphers insights into how the exudation of plant secondary metabolites can shape the functions and diversity of the root microbiome. It also elaborates on how rhizosphere interactions influence plant growth, regulate plant immunity against phytopathogens, and prime the plant for protection against biotic and abiotic stresses, along with some recent well-reported examples. A holistic understanding of these interactions can help in the development of tailored microbial inoculants for enhanced plant growth and targeted disease suppression.

**Keywords:** rhizosphere; microbial metabolites; plant-microbe signaling; quorum sensing; phytohormones; defense priming; sustainable agriculture

## 1. Introduction

The rhizosphere is a most captivating environment, which harbors a variety of microorganisms that are deeply involved in plant-microbe communication. This high-density niche allows plants to interact with associated microorganisms through chemical signals that are produced in response to specific stimuli, which in turn activate many regulatory mechanisms [1]. Rhizospheric regions possess higher bacterial activity than non-rhizospheric regions. The composition of a microbiome is determined by different biotic and abiotic factors, i.e., the climate, type of soil, and chemical signals that are produced by the plant and its associated microbes [2,3].

Plants and microbes have diverse interactions that involve close interactions, either positive or negative, including mutualism (symbiosis), parasitism, and commensalism [4]. Positive interactions include those with microorganisms, e.g., rhizobia, plant growth-promoting rhizobacteria (PGPR), and mycorrhiza, which result in beneficial outcomes, such as growth promotion, nutrient accessibility, and protection against abiotic and biotic environmental stresses [5-7]. On the other hand, plant interactions with microbial pathogens result in negative outcomes, i.e., plant diseases [8,9]. The interaction between both partners depends on specialized signaling molecules or chemical signals that are also

**Citation:** Jamil, F.; Mukhtar, H.; Fouillaud, M.; Dufossé, L. Rhizosphere Signaling: Insights into Plant-Rhizomicrobiome Interactions for Sustainable Agronomy. *Microorganisms* **2022**, *10*, 899. https://doi.org/10.3390/microorganisms10050899

Academic Editor: Dilfuza Egamberdieva

Received: 21 March 2022

Accepted: 21 April 2022

Published: 25 April 2022

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

<figure><img src="image_9.png" /></figure>

**Copyright:** © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

<footnote n="1">¹ Institute of Industrial Biotechnology, Government College University, Lahore 54000, Pakistan; fatimajamil000@gmail.com</footnote>

<footnote n="2">² CHEMBIOPRO Chimie et Biotechnologie des Produits Naturels, Faculté des Sciences et Technologies, Université de la Réunion, F-97490 Sainte-Clotilde, Ile de La Réunion, France</footnote>

<footnote n="3">³ CHEMBIOPRO Chimie et Biotechnologie des Produits Naturels, ESIROI Département Agroalimentaire, Université de la Réunion, F-97490 Sainte-Clotilde, Ile de La Réunion, France; laurent.dufosse@univ-reunion.fr</footnote>

<footnote>* Correspondence: hamidwaseer@yahoo.com (H.M.); mireille.fouillaud@univ-reunion.fr (M.F.); Tel.: +092-3334245581 (H.M.); +262-262-483363 (M.F.)</footnote>
significant in cooperative, as well as competitive, microbial behavior [10,11]. The chemical cues or secondary metabolites act as mediators in plant–microbe and microbe–microbe communication and also trigger plant responses [12].

In the past decade, progress has been made in the understanding of the types of chemical signals that are responsible for controlling the activities of plants and associated microbes [13–15]. The most studied signaling compounds are N-Acyl homoserine lactones (N-AHLs), which are produced by a variety of bacterial taxa and regulate quorum sensing and pathogenicity within a bacterial population [16–18]. Likewise, plant roots secrete a variety of metabolites as exudates, including photosynthetically derived carbon compounds, e.g., organic acids, vitamins, flavonoids, polysaccharides, amino acids, and sugars. These root exudates create an enriched environment for the rhizomicrobiome to interact and increase diversity based on the composition of the exudates [15, 19, 20]. Moreover, plants release secondary metabolites against pathogens and insects that act as defensive signals [21,22]. Plants use adaptive strategies to enhance the defensive capacity of their innate resistance to biotic and abiotic factors by interacting with beneficial microbes [23,24]. To unravel the process of microbial interaction with plants, an understanding of the types of chemical communication between all members is necessary. Thus, the known microbial community and their interactions could help in the optimal use of beneficial microbes for better plant growth.

Some of the literature on different signaling molecules that participate in the devel-
opment of interactions within the rhizosphere for enhanced plant growth has been re-
viewed [15,25–28]. However, much still needs to be explored in terms of the significance
of these interactions as far as microbial or chemical diversity and the understanding of
signaling molecules are concerned. This review aims to enlighten our understanding of
rhizosphere signaling in plant–microbe communication, both cooperative and competi-
tive, and its significance in plant productivity and the development of sustainable agri-
culture systems. Nonetheless, the signaling compounds have a prodigious potential to
escalate plant functions when they are understood in depth.

2. Rhizosphere: A Pool of Plant–Microbe Signaling

The rhizosphere serves as a hotspot for diverse microbial activity. It is an intricate
ecosystem comprising nutrient-rich soil that surrounds the plant roots, which provides a
pool for plant–microbe communication. The term “Rhizomicrobiome” is defined as a mi-
crobial community that is present in the rhizosphere [29]. A variety of microorganisms
reside within the rhizosphere, including bacteria, fungi, nematodes, protists, and inverte-
brates [11]. Most of the microbiome studies within the context of rhizosphere signaling
have been focused on the bacteria and fungi that make up the major portion of the rhizo-
sphere microbiome. However, viruses that infect bacteria, which are known as phages,
have an influence on the dynamics of the rhizosphere microbiome. The most abundant
known phages in the soil virome include *Microviridae*, *Siphoviridae*, and *Podoviridae* [30].
The diversity and amount of identified viruses in the rhizosphere is much less, i.e., 2700
less than bacterial abundance, which amounts to around 10¹⁰ species per g of soil [31,32].
The complete biological entity comprising a plant and its associated microbial commu-
nity, i.e., the symbionts (facultative and obligate) and microbes that have parasitic rela-
tionships with the host plant, is referred to as a “holobiont” [33]. The cascade of intricate
chemical signals develops a communication within the rhizosphere that facilitates various
mechanisms in a holobiont, i.e., root–root interactions, biofilm formation, nutrient acqui-
sition, microbiota development, and resistance against pathogens [34–36]. Different types
of interactions between microbes and plants are depicted in Figure 1.
<figure><img src="image_10.png" /><figcaption>**Figure 1.** Schematic representation of interactions between rhizo-microorganisms and plants.</figcaption></figure>

According to the “rhizosphere effect”, this region is associated with a lesser microbial diversity but a higher bacterial abundance compared to bulk soil [37]. The recruitment of microbes within the rhizosphere directly depends on the soil properties, soil type, and plant metabolites [38]. Different plant genotypes and physicochemical soil properties develop specific environments for the selection of a promising microbiome [10,34]. Plant-derived metabolites or root exudates play a significant role in the shaping of the rhizomicrobiome by modifying the soil chemistry around the plant roots and serving as substrates for the growth of specific microbiota [39]. The root exudates differ both in quality and quantity depending on the type, nutritional status, and growth stage of the plant [40]. These root exudates, including both primary and secondary metabolites, contain 10–16% of the total plant nitrogen and 11% of the photosynthetically fixed carbon that actively tune the microbiota in the microbial reservoir that is within the vicinity of the plant roots [41]. Another factor that affects the rhizomicrobiome is the cellular response that is shown either by the microbes or the plants, which results in transformation, catabolism, and resistance to the chemical that is being sensed [11]. The release of root exudates into the rhizosphere by plants selects the desired microbial community by attracting it while deterring harmful communities, which in turn allows plants to be adaptable. This selection process for microbiota is known as “niche colonization” [42,43].

Signaling in the rhizosphere can be categorized into two major types based on the direction of the communication, i.e., the inter- and intraspecies microbial signaling and the interkingdom signaling between microbes and plants.

## 2.1. *Inter- or Intraspecies Signaling among Microorganisms*

Microbes in the rhizomicrobiome interact with each other by producing signaling molecules that adjust their gene expression [11]. Inter- or intraspecies communication among microbes occur via the quorum sensing mechanism, which involves cell density-dependent coordination. Quorum sensing (QS) is the cell-to-cell signaling process that takes place through the synthesis, release, and detection of chemical signals [44,45]. These chemical signals are also known as autoinducers (AIs) and they regulate the gene expression of some bacterial functions upon the recognition of the signal by the recipient, i.e., biofilm formation, adhesion, motility [46–48], propagation, virulence, metabolism [49], and symbiotic association [1].

Quorum sensing signals in bacteria are categorized into two groups: acyl-homoserine lactone (AHLs or AI-1), which is found in Gram-negative bacteria, and autoinducer peptides (AIPs), which are found in Gram-positive bacteria; and autoinducer type 2 (AI-2),
which has the traits of both AHLs and AIPs and is found in both Gram-negative and Gram-positive bacteria [50,51]. N-acyl homoserine lactone (N-AHL) has been majorly reported in various Gram-negative bacteria, including *Burkholderia* sp., *Pseudomonas syringae*, *Pseudomonas putida*, *Pseudomonas chlororaphis*, *Erwinia* sp., and *Serratia* sp. (Table 1) [52,53]. As well as AHLs, a diverse range of signals have been reported in Gram-negative bacteria, i.e., fatty acid methyl esters, 2-alkyl-quinolones, furanone, and γ-butyrolactones [16,50,54].

<table><caption>**Table 1.** Characterization of quorum sensing signaling molecules that are produced by different rhizomicrobes with respect to the type of communication within the rhizosphere.</caption><thead><tr><th>Type of Microbe</th><th>Rhizo-Microorganisms</th><th>Quorum Sensing Molecules</th><th>Type of Communication</th><th>Reference</th></tr></thead><tbody><tr><td rowspan="5">Gram-positive bacteria</td><td><i>Bacillus subtilis</i></td><td>ComX pheromone</td><td>Inter- and intraspecies</td><td>[6]</td></tr><tr><td><i>Streptomyces</i> spp.</td><td>Gamma-butyrolactones (A-factor) and methylenomycin furans (MMF1)</td><td>Interspecies</td><td>[55]</td></tr><tr><td><i>Staphylococcus aureus</i></td><td>Circular oligopeptide</td><td>Interspecies</td><td>[16]</td></tr><tr><td><i>Stenotrophomonas chelatiphaga</i></td><td>DSF (diffuse signal factor)</td><td>Interkingdom (poplar plant)</td><td>[56]</td></tr><tr><td><i>Bacillus velezensis</i></td><td>AI-2 synthetase (2-methyl-2,3,3,4-tetrahydroxytetrahydrofuran (THMF))</td><td>Interkingdom (maize plant)</td><td>[57]</td></tr><tr><td rowspan="7">Gram-negative bacteria</td><td><i>Burkholderia sp.</i></td><td>N-3-oxo-hexanoyl-homoserine lactone (3OC6-HSL)</td><td>Interkingdom (wheat and arabidopsis plant)</td><td>[58]</td></tr><tr><td><i>Serratia glossinae</i></td><td>N-hexanoyl-L-homoserine lactone (m/z 200) and N-octanoyl-L-homoserine lactone (m/z 228)</td><td>Interkingdom (rice plant)</td><td>[59]</td></tr><tr><td><i>Serratia plymuthica</i></td><td>N-butanoyl-HSL, N-hexanoyl-HSL, and N-3-oxo-hexanoyl-HSL (OHHL)</td><td>Interkingdom (oil seed rape)</td><td>[60]</td></tr><tr><td><i>Burkholderia graminis</i> M12 and <i>B. graminis</i> M14</td><td>N-(3-oxododecanoyl)-L-homoserine lactone (3-oxo-C12-HSL or OC12-HSL (where "O" indicates an oxo substitution at the third carbon atom)) and 3-oxo-C14-HSL (OC14-HSL)</td><td>Interkingdom (tomato plant)</td><td>[61]</td></tr><tr><td><i>Serratia marcescens</i></td><td>N-3-oxo-hexanoyl-homoserine lactone (3OC6-HSL)</td><td>Intraspecies and interkingdom (tobacco plant)</td><td>[62]</td></tr><tr><td><i>Burkholderia sp.</i> and <i>Pseudomonas</i> sp.</td><td>N-butyryl-homoserine lactone (C4-HSL)</td><td>Interkingdom (arabidopsis plant)</td><td>[63]</td></tr><tr><td><i>Ochrobactrum sp.</i></td><td>3O-C7-HSL and 3OH-C7-HSL</td><td>Interkingdom (bean plant)</td><td>[64]</td></tr><tr><td rowspan="3">Fungi</td><td><i>Stenotrophomonas maltophilia</i></td><td>DSF (diffuse signal factor)</td><td>Interkingdom (oil seed rape)</td><td>[65]</td></tr><tr><td><i>Serratia glossinae</i></td><td>N-octanoyl-L-homoserine lactone and N-hexanoyl-L-homoserine lactone</td><td>Interkingdom (sesame plant)</td><td>[59]</td></tr><tr><td><i>Candida albicans</i></td><td>Tyrosol, γ-butyrolactone, and farnesol</td><td>Intraspecies</td><td>[66]</td></tr></tbody></table>

Another type of QS bacterial signals is antibiotics, which have been reported for intra- or interspecies communication [67]. A recent study revealed some antibiotic signals in a bacterial strain that resided in the tobacco rhizosphere, *Lysobacter capsica*. The strain
possessed biocontrol potential due to its production of antifungal and antibiotic signals, i.e., cyclic lipodepsipeptides and cyclic and polycyclic tetramate macrolactams [68]. Fungi also produce quorum sensing signals that communicate with bacterial species, e.g., γ-heptalactone, tyrosol, γ-butyrolactone, dodecanol, and farnesol [69]. Fungal and bacterial interaction through QS signals creates a competition for existence among the associated microbes in the rhizosphere in terms of infecting the host [70].

Another important class of signaling molecules is volatile organic compounds (VOCs). Microbial VOCs are synthesized and released for long-distance communication among a microbial community and also in microbe-plant interaction [71]. VOCs are low molecular weight lipophilic compounds (100–500 Da) that are produced by various bacterial and fungal species through distinct metabolic pathways that are specific to the species genotype [72]. The VOCs of bacterial origin include alkanes, ketones, alkene, terpenoids, and sulfurs [73,74]. VOCs play an important role in microbe-microbe communication by serving as antimicrobial QS signaling molecules and influencing microbial activity, i.e., virulence, stress resistance, and biofilm formation [75,76]. These attributes are exemplified as a low concentration of nitric oxide (NO) influences the biofilm formation in bacterial species such as *P. aeruginosa*, *B. licheniformis*, and *S. marcescens* [77]. Apart from this, VOC signals have been reported to regulate plant growth (root architecture and hormonal signaling) and plant immunity against biotic and abiotic stresses [71]. Additional studies will further unravel other signaling mechanisms that are associated with microbial VOCs.

Hence, these intricate signaling mechanisms among rhizospheric microorganisms have a key role in the shaping of the rhizomicrobiome by recruiting specific microbes through inter- or intraspecies communication.

## 2.2. Interkingdom Signaling

Microbes and plants interact with each other via interkingdom signaling, which can influence plant growth by either inducing or suppressing gene expression. Interkingdom signaling can be subdivided into two categories based on the stimulus direction: microbe-plant signaling and plant-microbe signaling.

### 2.2.1. Microbe-Plant Signaling

In microbe-plant signaling, microbes produce and emit signals that induce symbiotic interactions with the plant. Microbial signals that are of rhizosphere origin can trigger definite changes in the plant transcriptome. As in plants, phytohormones are also produced by PGPR. These plant growth-stimulating signals can regulate the developmental processes of plants and can also provide plants with resistance to abiotic and biotic stresses. Many PGPRs, including *Azospirillum* spp., *Bacillus amyloliquefaciens*, *B. muralis*, *B. thuringiensis*, *Rhizobium* spp., and Pseudomonas spp., have been reported to produce a diverse group of phytohormones, e.g., auxin, abscisic acid, salicylic acid, cytokinin, gibberellin, and strigolactones [78–81]. A recent study in Nature reported three newly isolated strains of *Phoma* spp. in the rhizosphere of *Pinus tabulaeformis*. These strains secreted stress the resistance substance abscisic acid (ABA) when under drought stress, which triggered drought resistance mechanisms in the pine tree and also stimulated its antioxidant activities [82].

Most of the literature on microbe-plant communication has been focused on beneficial interactions, such as the induction of plant growth and plant defenses against biotic and abiotic stresses. Rhizospheric microbes that have plant-friendly associations include mycorrhiza, rhizobia, plant growth-promoting bacteria, and fungi (PGPR or PGPF) [11]. Microbial signals are recognized by plants as microbe-associated molecular patterns (MAMPs), i.e., flagellin, chitin, and lipopolysaccharides, via pattern recognition receptors (PRRs) that trigger a local defense through a hormonal signaling network, which in turn produces immune responses [83–85].
Quorum sensing signals have also been reported in interkingdom communication. Bacterial QS signals that are perceived by plants elicit various plant responses, e.g., AHLs (N-butanoyl homoserine lactone and N-hexanoyl homoserine lactone), which aid in the development of symbiotic association with plants and enhance root growth by modifying the hormonal levels in the plant [46,86]. Another bacterial QS molecule, DSF, stimulates innate immunity (the detection of harmful microbes via PRRs) in different plants [87]. Some other examples of QS sensing in interkingdom communication is presented in Table 1. As well as causing physiological changes in plants, bacterial QS molecules also provoke the plants into secreting molecules that mimic the QS molecules of pathogenic microbes [88,89]. For example, the p-coumaric acid that is produced by garlic [90], the isothiocyanate sulforaphane that is produced by broccoli [91], the curcumin that is produced by turmeric [92], and the patulin that is produced by fruits (apple, banana, pear, grape, etc.) [93]. Studies on AHL mimicry have shown that the mimicry molecule of bacterial AHL (AHL analog) specifically interferes with QS regulatory pathways and can either stimulate or inhibit the gene expression of the original QS receptor or host, as illustrated in Figure 2 [94,95]. This type of interference in microbial QS signaling for attenuating pathogenicity is known as quorum quenching (QQ) [44,96,97]. A recent study identified a quorum quenching mechanism in a novel bacterial strain, Acinetobacter sp. strain XN-10, which degraded the QS molecules of the AHL family that was acting against the QS-mediated pathogenicity. The strain suppressed the pathogenicity of *Pectobacterium carotovorum* subsp. *carotovorum* (Pcc), thereby protecting tissue maceration in potatoes, cabbage, and carrots [98]. Another study reported a quorum quenching defense mechanism against *Pseudomonas aeruginosa* infection in plants. Upon the interaction of the plant with *P. aeruginosa*, the plant-secreted QQ molecule (rosmarinic acid) mimicked and competed with the QS pathogenic signal (C4-HSL) and stimulated QS-mediated responses that provide disease protection to the plant, i.e., virulence factors and biofilm formation [88].

<figure><img src="image_11.png" /><figcaption>**Figure 2.** Schematic representation of quorum sensing (QS) and quorum quenching (QQ) inhibition of signal perception pathways. The binding of QQ agents to the LuxR receptors either inactivates quorum sensing receptors or reduces the quantity of receptors in the QS molecules for targeted gene expression.</figcaption></figure>

Rhizospheric bacteria have been reported to produce antimicrobial signaling compounds. These compounds stimulate systemic resistance in plants against phytopathogens by altering hormonal pathways, e.g., the di-acetyl phloroglucinol (DAPG) that is produced by *Pseudomonas* sp. [99]. It is common that microbially produced VOCs can induce plant growth and resistance to biotic stress [72,100]. Plants perceive and respond to
various VOC signals of PGPR or PGPF origins, such as undecanone and heptanol. For example, 2-heptanol and 2-undecanone, which are produced by *B. subtilis* and *B. amyloliquefaciens*, promote the growth of *Arabidopsis thaliana* when cultivated with these PGPR strains [101,102].

### 2.2.2. Plant-Microbe Signaling

Plants serve as residences for microbial communities, which include mutualists, commensals, and parasitic microorganisms. Plants respond to the microbial signals by secreting chemical compounds, which are known as root exudates. These include low molecular weight compounds (organic acids, sugar, aliphatic acids, fatty acids, amino acids, flavonoids, and secondary metabolites) and high molecular weight compounds (proteins and mucilage) [20,34,103]. The plant-microbe interaction through the secretion of phytochemicals affects the biology of the rhizosphere [104]. The secreted chemicals attract rhizospheric microbes toward the plant roots and develop either pathogenic or symbiotic interactions with them. The most studied plant-microbe interaction is the symbiotic relationship of legumes with nitrogen-fixing bacteria. The cascade of signals that is produced upon plant-microbe interaction forms root nodules. Rhizospheric microbes feed on these nodules and in turn provide the plant with an available form of nitrogen. Plant signals for nodule formation have been extensively studied over the last decade [15,105].

A recent work demonstrated pathogenic plant-microbe interaction through a brocoli plant induced defense system, which released root exudates upon interaction with fungal species. The root exudates (isothiocyanates (ITC) and glucosinolates (GLS)) showed antifungal potential against the rhizospheric microbes *Pseudomonas syringae*, *Sphingomonas suberifaciens*, and *Fusarium oxysporum* [106]. The chemical complexity and specificity of the root exudates depend on the genotype of the plant. The chemical signals of root exudates attract specific microorganisms for interaction [34,35]. For example, cumiber secretes citric acid, which attracts *Bacillus amyloliquefaciens*, whereas bananas secrete fumaric acid, which attracts *B. subtilis* N11, but both interactions result in biofilm formation [107]. Therefore, specific root exudates recruit specific microbial communities within the rhizosphere. Phytochemicals are also capable of stimulating the QS signaling mechanism in microbes, e.g., the flavonoids that are produced by legumes upregulate the gene expression of AHL genes in rhizobia [108].

Plants also release volatile organic compounds (VOCs) from different parts: leaves, flowers, fruits, and roots [109]. These include terpenoids, fatty acids, phenylpropanoids, and amino acids that constitute approx. 1% of the total plant secondary metabolites. VOCs can easily cross plant membranes and be released into the atmosphere or soil. In soil, they attract root colonizing pathogens and inhibit their growth [110].

Plant secretions, including root exudates, volatiles, and strigolactones, are widespread signaling compounds that bind with bacterial receptor proteins and elicit a response in microbes that regulates gene expression. The signaling molecules that have been identified so far are known to influence the developmental and defense processes of plants. These phytochemical compounds are responsible for shaping or adapting the rhizomicrobiome due to their specificity and complexity. However, many of these chemical compounds and their target functions are yet to be explored. The rhizosphere signaling mechanisms that are involved in the interactions between microorganisms and between the microorganisms and plants are represented in Figure 3.
<figure><img src="image_12.png" /><figcaption>**Figure 3.** Overview of rhizosphere communication in intra- or interspecies signaling among microorganisms and interkingdom signaling between microbes and plants. Myc, mycorrhizal; LCOs, lipo-chitooligosaccharides; Nod, nodulation; VOCs, volatile organic compounds; Ais, autoinducers; AHLs, N-acyl homoserine lactone; QSMs, quorum sensing molecules.</figcaption></figure>

**3. Significance of Signaling in Plant-Rhizomicrobiome Interaction**

The plant-microbe signaling in the rhizosphere contributes toward sustainable agronomy. Some features of rhizosphere signaling that have significant importance are elaborated here. A summary of the significant factors of rhizosphere signaling is shown in Figure 4.

<figure><img src="image_13.png" /><figcaption>**Figure 4.** Summary of significant factors of rhizosphere signaling. SAR, systemic acquired resistance; ISR, induced systemic resistance; LCOs, lipo-chitooligosaccharides; Nod, nodulation; Myc, mycorrhizal; PRR, pattern recognition receptor; PAMPs, pathogen-associated molecular patterns.</figcaption></figure>
### 3.1. *Nutrient Acquisition for Phytostimulation*

A plant can acquire nutrients from the rhizomicrobiome in two ways: either through symbiotic or non-symbiotic interactions with rhizospheric microorganisms.

#### 3.1.1. Signal-Mediated Symbiosis

Plants are known to develop synergistic interactions with the associated rhizomicrobiome. Nutrient acquisition is a crucial consequence of these interactions as once the symbionts have established the association, a cascade of signals results in the continuous exchange of nutrients between both symbionts. The most studied interkingdom signal-mediated interactions are the mutualistic associations between rhizobia and legumes and between AMF and non-vascular plants. These interactions have been extensively studied throughout the last decade; however, research is still ongoing with regards to signal-mediated symbiosis.

* Rhizobia-legume symbiotic interactions

Signal-mediated symbiosis plays a key role in nutrient acquisition for plants. Rhizobia provide a reduced form of nitrogen, i.e., ammonia, to plants and in exchange, the plants provide dicarboxylates to the rhizobia [111].

The symbiotic interactions between rhizobia and legumes are initiated after the secretion of phytochemicals by the roots of the host plant, i.e., flavonoid derivatives [112]. Flavonoids have been well studied regarding their role in legume-rhizobia symbiosis. They can accumulate auxin in the root tissues, which facilitates the nodulation process [113]. The flavonoids act as a chemical attractant for rhizobia and guide the rhizobial cells into activating the nodulation genes (nod, noe, and nol), which in turn synthesize nodulation (Nod) factors, i.e., lipo-chitooligosaccharides (LCOs) [114]. LCOs are major signaling molecules for the initiation of nodule formation, which is perceived by receptors that are present in the root epidermis of the host plant (known as kinases). This results in nodule formation in the roots of the legumes [15,115,116]. The legume secretions are rhizobia-specific and attract specific rhizobial species. Likewise, the rhizobia response is specific to the flavonoids, i.e., distinct LCOs diffuse through rhizobia and activate certain nodulation genes that are specific to legume species in order to develop an accurate symbiotic interaction [117,118]. LCOs can promote plant growth by modulating legume root architecture, which in turn enhances nutrient acquisition. This process has been implicated in the increase in the number of root hairs for increased nutrient uptake [119]. This behavior, including an increase in root surface area, length, and hair number, was observed in *Ara-bidopsis thaliana* that was inoculated with *Bradyrhizobium japonicum* [120]. As with flavonoids, some other signaling molecules have also been reported to activate nod genes, e.g., chalcones, betaines, vanillin [121], jasmonate, and aldonic acid [122]. Thus, these signaling compounds regulate the gene expression of particular partner symbionts for successful symbiosis.

The neighboring microbes of rhizobia in a phytomicrobiome assist in nodule formation by producing synergistic consortia that play an important role in the alleviation of abiotic stress, nutrient uptake, and disease resistance [118]. The co-inoculation of PGPR has shown drastic plant growth-promoting effects, e.g., *Mesorhizobium cicero* that was co-inoculated with *Bacillus* sp. and *Enterobacter aerogenes* demonstrated significantly enhanced root nodulation, uptake of nitrogen and phosphorous, and total protein content in the chickpea plant [123].

* Mycorrhizal symbiotic interactions

Mycorrhizal symbiosis involves the interactions between arbuscular mycorrhizal fungi (AMF) and land plants. The signaling pathways are quite similar to those in rhizobia-legume symbiosis. Plant secretions of strigolactones, which are known as branching factors (BFs), send signals to the AMF that, upon recognition, release mycorrhizal lipo-chitooligosaccharides (Myc factors) that are responsible for the development of the symbiotic interactions between plants and AMF [124,125]. As well as acting as AMF stimuli,
strigolactones are plant hormones that are capable of interfering with auxin transport [126]. Intriguingly, AMF penetrate through the epidermal cells of plant roots after perceiving plant signals. There, they start to differentiate into highly branched structures called arbuscles. AMF colonize, either intercellularly or intracellularly, within the cortical tissues that have a key role in the nutrient exchange between both symbionts [127,128]. A complex cascade of signals enhances the nutrient uptake of the roots, such as nitrates, amino acids, immobile ortho-phosphates, starch, and calcium, using specialized transporters. This improves the metabolic pathways of the plant while the host plant fulfills the carbohydrate requirements of the AMF in return [129–131].

Recently, studies have reported a tripartite interaction between three symbionts: AFM–rhizobia–plant (ARP). This tripartite interaction increases nitrogen fixation, helps the plant to survive in drought conditions [132,133], and enhances root soluble sugar content and dry weight, as well as increasing the total number of nodules [133,134]. Some of the literature also considered tripartite symbiosis to be an efficient interaction for plant growth [98,135–137]. Further research is required to understand the gene expression profiles and metabolic events that are associated with ARP tripartite interactions. Meta-genomics would provide better ways to monitor and understand the role of each partner that is involved in the symbioses within the rhizosphere.

### 3.1.2. Nutrient Acquisition without Symbiosis

Plants can acquire nutrients without symbiosis with rhizobia or AMF. Various microbes meet nutrient requirements via the production of certain metabolites [19,138,139]. During iron deficiency, certain microbes colonize the roots of a plant in iron deficient soil and produce chelating compounds to sequester iron from the soil. Bacterial colonization induces the gene expression that is responsible for iron uptake in plants in response to iron deficiency [139–141]. The phosphate requirements of the arabidopsis plant are provided by endophytic bacteria *Colletotrichum tofieldiae* via the translocation of phosphate through the roots [142]. The rhizospheric and endophytic consortium of *Bacillus* sp. and *Pseudomonas* sp. Has been shown to significantly enhance the phosphate solubilization efficiency of wheat cultivars that were growing in phosphate deficient soil [143]. Similarly, microbes other than rhizobia meet the nitrogen demands of non-leguminous plants [19,144]. The decomposition of organic matter by rhizospheric microbes enhances plant productivity and soil fertility by providing nutrients to plants. For example, lignocellulosic fungi, such as, *Pleurotus ostreatus*, *Phanerochaete*, and *Trichoderma harzianum*, and bacteria, including *Pseudomonas* sp., *Sporocytophaga* sp., *Cytophaga* sp., and *Streptomyces* sp., degrade plant biomass and release nutrients into the soil, which are taken up by the plants that are growing in nutrient-poor soil [145,146]. The soil phages or virus-like particles (VLPs) affect the availability of nutrients to plants by modulating mutations in microbial phylotypes or interfering with the structure and diversity of the bacterial population. These effects generate mutations in rhizodeposits and aid in nutrient uptake (N, S, and P) by the plants. Despite the lower abundance of the lysogenic virus community than the bacterial community, viruses play their role in the resilience of the rhizosphere microbiome [30].

### 3.2. *Regulation of Plant Immunity against Phytopathogens*

Biotic stresses cause a 30% loss in crop yield and a 15% loss in food worldwide due to various pathogen attacks, i.e., bacteria, fungi, viroids, viruses, protists, nematodes, and insects [147]. PGPR induce an innate immune response in plants against the phytopathogens in a sequential manner, i.e.: (i) perceive the stress stimulus; (ii) regulate defense responses by activating defense-related signaling pathways; and (iii) defense priming that prepares the plant to respond against the stress after recognition by the PGPR [148,149]. The perception of the stimulus by the plant triggers a local immune defense response that is translated into a systemic defense response, which is mediated by hormonal signaling pathways [150].
3.2.1. Pattern-Triggered Immunity (PTI)

Plant immunity is initiated by host–pathogen interactions, in which plant receptors and pattern recognition receptors (PRRs) recognize the pathogen- or microbe-associated molecular patterns (PAMPs or MAMPs) that induce the resistance mechanisms. After PAMP recognition, the plant triggers signaling modules, i.e., mitogen-activated protein kinases (MAPKs) and calcium-dependent protein kinases (CDPKs), which further triggers a signal cascade that is responsible for the activation of specific transcription factors that lead to the induction of multiple intracellular defense responses. The induction of the sig- nal cascade is either hormone-dependent (MAPKs and CDPKs) or -independent [12,151,152]. The plant signals that make up the signal cascade include methyl jasmonate (MeJA), azelaic acid (AzA), pipecolic acid (Pip), and salicylic acid (SA) signals that regu- late defense genes [153,154]. Some phytohormones, such as auxins, cytokinins, gibberel- lins, and abscisic acid, also take part in this signal cascade [28]. This type of defense re- sponse is known as MAMP- or PAMP-triggered immunity [155–157] or more generally as pattern-triggered immunity (PTI) [158], which is depicted in Figure 5.

<figure><img src="image_14.png" /><figcaption>**Figure 5.** Schematic representation of plant immunity against phytopathogens through pattern-triggered immunity (PTI) and effector-triggered immunity (ETI). PTI is activated through the recognition of pathogen-associated molecular patterns (PAMPs) by the pattern recognition receptors (PRRs) in plant cell walls. After PAMP recognition, the plant triggers a signal cascade that further induces multiple intracellular defense responses and activates defense genes. In response to PTI, pathogens secrete effectors that are recognized by nucleotide-binding (NB) and leucine-rich repeat (LRR) receptors (NLRs) and develop another defense layer called ETI. Activated NLRs with many intracellular signaling events trigger the hypersensitive response (HR).</figcaption></figure>

The induction of PTI stimulates intracellular defense responses, including stomatal closure, the deposition of callose, and the induction of reactive oxygen species (ROS) and antimicrobial metabolites (Figure 5) [158,159]. Several AHLs and diffusible signal factors (DSFs) have been identified as quorum sensing signals in phytopathogenic interactions. In the host–pathogen interaction between *Arabidopsis thaliana* and *Sclerotinia sclerotirum*, small sRNAs were abundantly identified in the signal pathways [160]. Plants produce secondary metabolites upon pathogen interaction, which are known as “phytoanticipins” or “phytoalexins” (Figure 5) [157,161]. The biosynthesis of these inducible compounds is regulated by phytohormone signaling pathways, phosphorylation, and defense-related
genes [162]. Capsidiol production in *Nicotiana benthamiana* has been shown to be mediated
by an ethylene signaling pathway that provides defense against *Phytophthora infestans*
[163].

3.2.2. Effector-Triggered Immunity (ETI)

In response to PTI signaling, pathogens resist the plant defense mechanisms by pro-
ducing effectors that prevent their detection by the host plant. This response mechanism
is known as effector-triggered susceptibility (ETS) [83,155,164]. Upon ETS activation, the
plant in turn develops another defense layer, which is known as effector-triggered im-
munity (ETI). ETI is activated upon the detection of pathogen effectors through a special-
ized intracellular protein, which is known as NB-LRR (nucleotide-binding and leucine-
rich repeat domains) [83,156,165]. NB-LRR is encoded by a plant resistance gene (R gene)
that mediates resistance to specific phytopathogens, i.e., viruses, oomycetes, fungi, nem-
atodes, and bacteria. It recognizes the specific pathogen effectors either by direct binding
or by changing its protein binding site during pathogen–effector binding [165], as de-
picted in Figure 5. The virulence specificity of pathogen effectors has been as yet undis-
covered because several PRRs can recognize specific pathogens and pathogens have
evolved effectors that dislocate the defense signaling of plants [166]. This protective mech-
anism is called the hypersensitive response (HR) [167]. For example, *Phytophthora infestans*
produces the effector protein (PexRD2), which increases its susceptibility to *Nicotiana ben-
thamiana* by suppressing the host’s defense signaling [168]. Effector proteins have also
been reported to attenuate hormonal signaling, i.e., salicylic acid and jasmonic acid signals
induce *P. infestans* colonization and infection in plants [169].

3.3. *Defense Priming*

Plants use adaptive strategies to enhance the defensive capacity of their innate re-
sistance. Warning signals or stimuli, such as pathogens, abiotic stresses, chemicals, PGPR,
and arthropods, trigger their innate resistance and prime the plants against secondary
stresses. This type of enhanced defense response state is known as priming. During this
phase, plants change at transcriptional, physiological, metabolic, and epigenetic levels
[23]. Primed plants show induced and more competent responses against stresses
[170,171]. Defense priming can be sustained throughout the life of a plant and can be
transferred on to the next generation. Defense priming is mediated by two induced sig-
naling resistance pathways: systemic acquired resistance and induced systemic resistance.

* Systemic acquired resistance (SAR)*

PTI and ETI trigger long-distance defense signals that induce resistance against the future localized infection via broad-spectrum phytopathogens, which involves the activation of proteins and pathogenesis-related (PR) genes. This type of long-distance immune priming that is induced by a pathogen is known as systemic acquired resistance (SAR). It is a salicylic acid (SA)-dependent pathway [83,153,172]. Salicylic acid is produced by various rhizobacteria that are responsible for activating PR genes, PTI, and ETI in SAR signaling [173].

SAR pathways are regulated by the key protein NPR1 (non-repressor of PR genes), which interacts with transcriptional co-factors that in turn induce the expression of pathogen-related proteins that are associated with systemic resistance [174]. SA binds with NPR1 and induces conformational changes in its structure to further expose it to transcriptional factors for PR gene activation (Figure 6) [175]. Jasmonic acid (JA) pathways in SAR protect the plant from necrotrophic pathogens by activating a regulatory protein: COI1 in the form of a ubiquitin complex. The activated protein complex participates in the defense of the plant [174].
<figure><img src="image_15.png" /><figcaption>**Figure 6.** Schematic representation of defense priming: (a) a picture depicting induced systemic resistance (ISR), which is induced by plant growth-promoting rhizobacteria that provide resistance to biotic stresses, and systemic acquired resistance (SAR), which is induced by phytopathogens that provide resistance to biotic and abiotic stresses; (b) a flowchart showing signal transduction pathway of ISR that are followed by jasmonate (JA) and ethylene (ET) plant hormones, which are encoded by the jar1 and etr1 genes, respectively, whereas SAR is followed by salicylic acid (SA), which is encoded by the sid1 and sid2 genes.</figcaption></figure>

SA pathways have been reported to induce the biosynthesis of flavonoids, i.e., pro-
anthocyanidins and catechin, which inhibit the proliferation of foliar rust fungus
*Melampsora larici-populina* in poplar trees [176]. SA and methyl jasmonate (MeJA) have
been shown to mediate the induction of defense-related genes and proteins against the
blight disease-causing pathogen *Xanthomonas axonopodis* *pv. manihotis* in cassava plants
[177]. *Trichoderma harzianum* has also been shown to induce systemic resistance via ET,
SA, and JA pathways against the cucumber mosaic virus in tomato plants [178]. *Tricho-
derma viride* has been reported to provide resistance against *Phytophthora infestans* infection
via SA signaling in potato plants [179].

* Induced systemic resistance (ISR)

The induction of defense signaling by a beneficial rhizomicrobiome, such as PGPR against phytopathogens and pests, is known as induced systemic resistance (ISR), which is an SA-independent pathway [83,180]. This defense signaling pathway also increases plants’ tolerance of abiotic and biotic stresses and is therefore also known as induced systemic tolerance [181,182]. The core difference between ISR and SAR is the dependency of SAR on the SA synthesis and accumulation by PGPR that activates SA signaling pathways, whereas ISR is SA-independent and includes ET and JA signaling pathways (Figure 6) [14].

Beneficial microbes do not possess virulence genes but they do have the potential to sensitize plants by exploiting them to perceive MAMPs that lead to the activation of ISR [183]. Defense priming by rhizobacteria overlaps under biotic and abiotic stresses.

ISR is regulated by the signaling pathways of phytohormones, including ethylene (ET) and jasmonic acid (JA) [184,185]. The reactive oxygen species (ROS) and reactive nitrogen oxygen species (RNOS) form a complex defense signaling network by stimulating the biosynthesis of JA, ET, and SA [186]. As an example, JA and ET were shown to regulate a defense response by stimulating the lipid transfer protein gene against *Fusarium*
*graminearum* [187]. Another defense response that is induced by JA and ET includes the RSL1 (recombinant *Solanum lycopersicum*) protein that triggers the gene expression of ET and JA against phytopathogens, e.g., *Alternaria alternata* and *Botrytis cinerea* [188]. ISR expression is usually determined by the type of bacterial strain and the plant in which resistance is induced [189]. PGPR consortiums have also been reported to induce ISR. For instance, a PGPR consortium was shown to trigger ISR in the cucumber plant by increasing its antioxidants and root vigor index while also regulating the photosynthetic machinery [190]. Moreover, the co-inoculation of AMF with *Pseudomonas* sp. reportedly enhanced the antioxidant machinery in the leaves and the phosphatase activity in the roots of lettuce plants under drought stress [191].

PGPR products that elicit defense priming include VOCs, LOCs, AHLs, ACC deaminase, antibiotics, siderophores, and lipopolypeptides [192,193]. The literature has reported that *Bacillus amyloliquefaciens* produced lipopolypeptides that primed the lettuce plant against *Rhizoctonia solani* [194]. AHLs from *Acidovorax radicus* N35 reportedly primed the defense response by stimulating the production of flavonoids, i.e., lutonarin and saponarin, in barley [195]. Furthermore, a siderophore-producing *Pseudomonas putida* mutant strain was shown to have an efficient biocontrol ability over the siderophore-deficient *Pseudomonas aeruginosa* mutant strain in controlling *Fusarium* wilt in tomato plants [196].

Many rhizobacteria have been reported to have parasitic traits due to the production of cell wall degrading enzymes, e.g., *Stenotrophomonas maltophilia* secretes proteases that have a parasitic action on *Bursaphelenchus xylophilus* (nematode) and *P. ultimum* (oomycetes) [197,198]. Some phages play a role in controlling the infection of a plant through bacterial phytopathogens. A recent study that was published in Nature reported that a combination of phages lessened the infection of tomato plants that was caused by *Ralstonia solanacearum* [199].

### 3.4. Regulation of Plant Defenses against Abiotic Stresses

Plants experience about 70% damage due to various abiotic stresses, including temperature, drought, nutrient deficiency, salinity, and heavy metal toxicity. A rhizomicrobium manages to ameliorate abiotic stresses through induced systemic tolerance via microbe-plant signaling, which involves biochemical and physiological changes in the plants [200]. Many PGPR have been reported to ameliorate abiotic stresses by adopting defense-related mechanisms, i.e., biofilm formation or the production of phytohormones, antibiotics, siderophores, hydrolytic enzymes, and quorum quenching compounds [201,202]. Rhizobacteria that possess the genetic capability to mitigate abiotic stresses include *Caulobacter*, *Rhizobia*, *Serratia*, *Flavobacterium*, *Erwinia*, *Chromobacterium*, *Burkholderia*, *Methylobacterium*, *Trichoderma*, *Micrococcus*, and *Pseudomonas* [203–205].

Plants manage to respond to abiotic stresses through a complex signal cascade that is activated following the perception of stress stimuli by the receptors or sensors that are in the plant cell walls. The sensed signals are then translated into intracellular signals through secondary messengers, i.e., calcium ions, nitric oxide, sugars, cyclic nucleotides, inositol phosphate, and ROS. These secondary messengers transduce the signaling pathways of the stress signals [206,207]. As a result, various physiological and metabolic responses become activated during different stages of plant development, such as the synthesis of jasmonic acid, ethylene, salicylic acid, abscisic acid [208,209], flavonoids, phenolic compounds [210], antioxidants, and osmolytes, as well as the activation of certain transcription factors for the expression of stress genes [211,212].

PGPR-produced phytohormones, mainly ethylene (ET), jasmonate (JT), salicylic acid (SA), abscisic acid (ABA), cytokinin, auxin, and gibberellins, regulate abiotic stress responses in plants. These hormones interact either synergistically or antagonistically to adjust their biosynthesis according to the stress response [213,214]. ABA biosynthesis genes are triggered upon osmotic stress to enhance its production, which is responsible for maintaining water balance through the closure of stomata [215]. ABA acts synergistically
with SA and antagonistically with ET to regulate osmotic stress, stomatal movement, and leaf senescence under drought conditions [216]. The exact mechanisms of bacterially produced phytohormones need to be explored further. However, some of the reported hormonal signaling pathways of rhizo-microorganisms in different host plants are presented in Table 2. PGPR can effectively stimulate antioxidant activity in plants under drought and salinity conditions. As a result, plants increase their antioxidant signaling, i.e., the production of redox enzymes and phenolic-like compounds (glycine, proline, and beta-ine) [217].

<table><caption>**Table 2.** Amelioration of abiotic stresses by rhizo-microorganisms using different signaling pathways in different plant species.</caption><thead><tr><th>Stress Type</th><th>Host Plant</th><th>Rhizo-Microorganisms</th><th>Signaling Pathways</th><th>Reference</th></tr></thead><tbody><tr><td rowspan="5">Salinity</td><td>Triticum aestivum</td><td>Arthrobacter protophormiae (SA3) and Dietzia natronolimnaea (STR1)</td><td>IAA, ET</td><td>[218]</td></tr><tr><td>Lycopersicum esculentum</td><td>Leclercia adecarboxylata</td><td>IAA</td><td>[219]</td></tr><tr><td>Triticum aestivum</td><td>Dietzia natronolimnaea</td><td>SOS, ABA</td><td>[220]</td></tr><tr><td>Cucumis sativus</td><td>Burkholderia cepacia, Promicromonospora sp., and Acinetobacter calcoaceticus</td><td>GA, ABA, SA</td><td>[221]</td></tr><tr><td>Cucumis sativus</td><td>Trichoderma asperellum</td><td>IAA, ABA, GA</td><td>[222]</td></tr><tr><td rowspan="4">Drought</td><td>Lolium multiflorum</td><td>Bacillus sp. and Pseudomonas sp.</td><td>ABA</td><td>[223]</td></tr><tr><td>Triticum aestivum, Zeamays</td><td>Bacillus sp. and Enterobacter sp.</td><td>IAA, SA</td><td>[224]</td></tr><tr><td>Oryza sativa</td><td>Pseudomonas fluorescens</td><td>ABA</td><td>[225]</td></tr><tr><td>Nicotiana tabacum</td><td>Glomus versiforme (AMF) and Bacillus methylotrophicus</td><td>ABA, IAA</td><td>[226]</td></tr><tr><td rowspan="4">Heat</td><td>Eucalyptus grandis</td><td>Brevibacterium linens</td><td>ET</td><td>[227]</td></tr><tr><td>Lycopersicum esculentum</td><td>Bacillus cereus</td><td>ET</td><td>[228]</td></tr><tr><td>Arabidopsis</td><td>Bacillus licheniformis</td><td>JA, ABA</td><td>[229]</td></tr><tr><td>Triticum aestivum</td><td>Bacillus safensis and Ochrobactrum pseudogrignonense</td><td>ROS</td><td>[230]</td></tr><tr><td rowspan="5">Low temperature</td><td>Triticum aestivum</td><td>Bacillus velezensis</td><td>ROS, ABA</td><td>[231]</td></tr><tr><td>Oryza sativa</td><td>Bacillus amyloliquefaciens</td><td>ABA, SA, JA, ET</td><td>[232]</td></tr><tr><td>Solanum lycopersicum</td><td>Funneliformis mosseae and Paraburkholderia graminis</td><td>ROS</td><td>[233]</td></tr><tr><td>Arabidopsis thaliana</td><td>Burkholderia phytofirmans</td><td>ROS</td><td>[234]</td></tr><tr><td>Oryza sativa</td><td>Enterobacter aerogenes</td><td>IAA, ET</td><td>[235]</td></tr><tr><td rowspan="4">Heavy metals</td><td>Cd</td><td>Stenotrophomonas maltophilia and Agrobacterium fa-brum</td><td>ET</td><td>[236]</td></tr><tr><td>Ni, Cd, and Al</td><td>Glycine max</td><td>Paecilomyces formosus and Penicillium funiculosum</td><td>IAA, GA</td><td>[237]</td></tr><tr><td>Cd, Cu, Pb, and Ni</td><td>Spartina maritima</td><td>Bacillus methylotrophicus, Bacillus licheniformis, and-Bacillus aryabhattai</td><td>COX, AOX</td><td>[238]</td></tr></tbody></table>
<table><tr><td></td><td><i>Solanum tuberosum</i></td><td><i>Bacillus sp.</i></td><td>ROS</td><td>[239]</td></tr><tr><td>As</td><td><i>Glycine max</i></td><td><i>Bradyrhizobium japonicum</i><br/>and <i>Azospirillum brasilense</i></td><td>IAA</td><td>[240]</td></tr></table>

IAA, indole acetic acid; ET, ethylene; GA, gibberellin; JA, jasmonic acid; ROS, reactive oxygen species; ABA, abscisic acid; SOS, salt overly sensitive; COX, cytochrome oxidase; AOX, alternative oxidase.

Enzymatic pathways, including phosphatases and protein kinases, i.e., calcium-dependent protein kinases (CDPKs), mitogen-activated protein kinases (MAPKs), and receptor-like kinases, have been reported to regulate dephosphorylation and phosphorylation in the management of abiotic stresses in plants [241]. Plants can deregulate the salt-sensitive gene expression under salinity stress via calcium ion signaling pathways [242]. PGPR-mediated stress resistance is involved in these signaling pathways that modulate the transcription factors in order to enhance the expression of stress-responsive genes [232]. For instance, *Bacillus amyloliquefaciens* has been shown to ameliorate the salt stress response in *Oryza sativa* by upregulating MAPK and CDPK pathways [243]. Another study showed an improved salinity stress resistance in wheat plants following inoculation with bacterial strains, i.e., *Enterobacter cloacae*, *Pseudomonas fluorescens*, *Pseudomonas putida*, and *Serratia ficaria*, which elevated the Na+/K+ ratio [244].

## 4. Conclusions and Future Perspectives

The interaction intricate chemical signaling between plants and their associated microbiome deciphers the communication dynamics that are underway within the rhizosphere and their outcomes in terms of plant productivity and development. Over the last decade, quorum sensing has been studied in the gene expression of both beneficial and harmful interactions between inter- and intramicrobial species and in the interkingdom signaling between plants and PGPR, i.e., nitrogen-fixing bacteria and rhizobia. Most of the plant metabolites that have been reported to date have been characterized by the *Ara-bidopsis thaliana* plant model. The recent literature suggests that other plants need to be investigated for the analysis of more plant metabolites and chemical cues. Expanding the research on rhizosphere communities will aid in the discovery of new chemical cues and their potential to enhance plant productivity in terms of symbiosis, resistance against environmental stresses, and immunity or defense mechanisms toward phytopathogens. Based on experimental evidence, there is no doubt that plants create an environment that recruits a specific rhizomicrobiome and shape microbial associations that are beneficial for their growth. Therefore, the escalating pressure of the demand for high crop production has opened up new avenues for research on rhizosphere signaling to reduce dependency on synthetic processes and agrochemicals. The alterations in the metabolic pathways of plants, microbes, rhizodeposits, and signaling molecules could be effective in the development of a rhizomicrobiome that is beneficial for effective plant productivity and resistance toward biotic and abiotic stresses, which could ultimately lead to more sustainable agriculture. Moreover, future research can be expanded by using novel "multi-omics techniques", which encompass genomics, proteomics, transcriptomics, phenomics, metagenomics, metabolomics, metatranscriptomics, metaproteomics, and metagenomics and could reveal multi-layered information about new chemical cues, cellular mechanisms, signaling mechanisms, and plant genes. Furthermore, future research on rhizosphere engineering is essential to dissect the targeted outcomes of the beneficial plant-microbe communications that could broaden the application of sustainable agriculture.

**Author Contributions:** Conceptualization, F.J., H.M., and M.F.; validation, H.M. and L.D.; writing—original draft preparation, F.J.; writing—review and editing, H.M., F.J., L.D., and M.F. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research received no external funding.
**Institutional Review Board Statement:** Not applicable.

**Informed Consent Statement:** Not applicable.

**Data Availability Statement:** Not applicable.

**Acknowledgments:** Laurent Dufossé deeply acknowledges the strong financial support from the Conseil Régional de Bretagne and the Conseil Régional de La Réunion for research activities that are dedicated to microbial biotechnology.

**Conflicts of Interest:** The authors declare no conflict of interest.

**Abbreviations**

<table><tr><td>PGPR</td><td>Plant growth-promoting rhizobacteria</td></tr><tr><td>N-AHL</td><td>N-Acyl homoserine lactone</td></tr><tr><td>AIs</td><td>Autoinducers</td></tr><tr><td>QS</td><td>Quorum sensing</td></tr><tr><td>QQ</td><td>Quorum quenching</td></tr><tr><td>VOC</td><td>Volatile organic compound</td></tr><tr><td>MAMP</td><td>Microbe-associated molecular pattern</td></tr><tr><td>PRR</td><td>Pattern recognition receptor</td></tr><tr><td>DSF</td><td>Diffusible factor</td></tr><tr><td>ITC</td><td>Isothiocyanate</td></tr><tr><td>GLS</td><td>Glucosinolates</td></tr><tr><td>AMF</td><td>Arbuscular mycorrhizal fungus</td></tr><tr><td>Nod</td><td>Nodulation</td></tr><tr><td>LCOs</td><td>Lipo-chitooligosaccharides</td></tr><tr><td>BF</td><td>Branching factor</td></tr><tr><td>PAMP</td><td>Pathogen-associated molecular pattern</td></tr><tr><td>MAPKs</td><td>Mitogen-activated protein kinases</td></tr><tr><td>CDPKs</td><td>Calcium-dependent protein kinases</td></tr><tr><td>PTI</td><td>Pattern-triggered immunity</td></tr><tr><td>ROS</td><td>Reactive oxygen species</td></tr><tr><td>ETS</td><td>Effector-triggered susceptibility</td></tr><tr><td>ETI</td><td>Effector-triggered immunity</td></tr><tr><td>NB-LRRs</td><td>Nucleotide binding and leucine-rich repeat domains</td></tr><tr><td>HR</td><td>Hypersensitive response</td></tr><tr><td>SA</td><td>Salicylic acid</td></tr><tr><td>NPR1</td><td>Non-expressor of pathogenesis-related genes</td></tr><tr><td>SAR</td><td>Systemic acquired resistance</td></tr><tr><td>JA</td><td>Jasmonic acid</td></tr><tr><td>ET</td><td>Ethylene</td></tr><tr><td>MeJA</td><td>Methyl jasmonate</td></tr><tr><td>AzA</td><td>Azelaic acid</td></tr><tr><td>Pip</td><td>Pipecolic acid</td></tr><tr><td>ISR</td><td>Induced systemic resistance</td></tr><tr><td>ACC</td><td>1-Aminocyclopropane-1-carboxylic acid</td></tr><tr><td>ABA</td><td>Abscisic acid</td></tr><tr><td>AOX</td><td>Alternative oxidases</td></tr><tr><td>COX</td><td>Cytochrome oxidase</td></tr><tr><td>GA</td><td>Gibberellin</td></tr><tr><td>SOS</td><td>Salt overly sensitive</td></tr></table>
## References

1. Checcucci, A.; Marchetti, M. The Rhizosphere Talk Show: The Rhizobia on Stage. *Front. Agron.* **2020**, *2*, https://doi.org/10.3389/fagro.2020.591494.

2. Hartmann, A.; Schmid, M.; Van Tuinen, D.; Berg, G. Plant-Driven selection of microbes. *Plant Soil* **2009**, *321*, 235–257. https://doi.org/10.1007/s11104-008-9814-y.

3. Bais, H.P.; Weir, T.L.; Perry, L.G.; Gilroy, S.; Vivanco, J.M. The role of root exudates in rhizosphere interactions with plants and other organisms. *Annu. Rev. Plant Biol.* **2006**, *57*, 233–266. https://doi.org/10.1146/annurev.arplant.57.032905.105159.

4. Martin, B.D.; Schwab, E. Current Usage of Symbiosis and Associated Terminology. *Int. J. Biol.* **2013**, *5*, 32. https://doi.org/10.5539/ijb.v5n1p32.

5. Zolla, G.; Badri, D.V.; Bakker, M.; Manter, D.K.; Vivanco, J.M. Soil microbiomes vary in their ability to confer drought tolerance to Arabidopsis. *Appl. Soil Ecol.* **2013**, *68*, 1–9. https://doi.org/10.1016/j.apsoil.2013.03.007.

6. Selvakumar, G.; Panneerselvam, P.; Ganeshamurthy, A.N. Bacterial mediated alleviation of abiotic stress in crops. In *Bacteria in Agrobiology: Stress Management*; Springer: Berlin/Heidelberg, Germany, 2012; pp. 205–224. https://doi.org/10.1007/978-3-662-45795-5_10.

7. Mendes, R.; Kruijt, M.; de Bruijn, I.; Dekkers, E.; Van Der Voort, M.; Schneider, J.H.; Piceno, Y.M.; DeSantis, T.Z.; Andersen, G.L.; Bakker, P.A.; et al. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. *Science* **2011**, *332*, 1097–1100. https://doi.org/10.1126/science.1203980.

8. Sarma, B.K.; Yadav, S.K.; Singh, S.; Singh, H.B. Microbial consortium-mediated plant defense against phytopathogens: Read-dressing for enhancing efficacy. *Soil Biol. Biochem.* **2015**, *87*, 25–33. https://doi.org/10.1016/j.soilbio.2015.04.001.

9. Venturi, V.; Fuqua, C. Chemical signalling between plants and plant-pathogenic bacteria. *Annu. Rev. Phytopathol.* **2013**, *51*, 17–37. https://doi.org/10.1146/annurev-phyto-082712-102239.

10. Lareen, A.; Burton, F.; Schäfer, P. Plant root-microbe communication in shaping root microbiomes. *Plant Mol. Biol.* **2016**, *90*, 575–587. https://doi.org/10.1007/s11103-015-0417-8.

11. Venturi, V.; Keel, C. Signaling in the rhizosphere. *Trends Plant Sci.* **2016**, *21*, 187–198. https://doi.org/10.1016/j.tplants.2016.01.005.

12. Zipfel, C.; Oldroyd, G.E.D. Plant signalling in symbiosis and immunity. *Nature* **2017**, *543*, 328–336. https://doi.org/10.1038/nature22009.

13. Chagas, F.O.; Pessotti, R.D.C.; Caraballo-Rodríguez, A.M.; Pupo, M.T. Chemical signaling involved in plant–microbe interactions. *Chem. Soc. Rev.* **2018**, *47*, 1652–1704. https://doi.org/10.1039/c7cs00343a.

14. Bukhat, S.; Imran, A.; Javaid, S.; Shahid, M.; Majeed, A.; Naqqash, T. Communication of plants with microbial world: Exploring the regulatory networks for PGPR mediated defense signaling. *Microbiol. Res.* **2020**, *238*, 126486. https://doi.org/10.1016/j.micres.2020.126486.

15. Oldroyd, G.E.D. Speak, friend and enter: Signalling systems that promote beneficial symbiotic associations in plants. *Nat. Publ. Gr.* **2013**, *11*, 252–263.

16. Borges, A.; Simões, M. Quorum Sensing Inhibition by marine bacteria. *Mar. Drugs* **2019**, *17*, 427. https://doi.org/10.3390/md17070427.

17. Cheng, F.; Ma, A.; Zhuang, G.; Fray, R. Exogenous N-acyl-homoserine lactones enhance the expression of flagella of *Pseudomonas syringae* and activate defence responses in plants. *Mol. Plant Pathol.* **2018**, *19*, 104–115. https://doi.org/10.1111/mpp.12502.

18. Schenk, S.T.; Hernández-Reyes, C.; Samans, B.; Stein, E.; Neumann, C.; Schikora, M.; Reichelt, M.; Mithöfer, A.; Becker, A.; Kogel, K.H.; et al. N-acyl-homoserine lactone primes plants for cell wall reinforcement and induces resistance to bacterial pathogens via the salicylic acid/oxylipin pathway. *Plant Cell* **2014**, *26*, 2708–2723. https://doi.org/10.1105/tpc.114.126763.

19. Jacoby, R.; Peukert, M.; Succurro, A.; Koprivova, A.; Kopriva, S. The Role of Soil Microorganisms in plant mineral nutrition – Current Knowledge and Future Directions. *Front. Plant Sci.* **2017**, *8*, 1617–1617. https://doi.org/10.3389/fpls.2017.01617.

20. Bais, H.P.; Park, S.-W.; Weir, T.L.; Callaway, R.M.; Vivanco, J.M. How plants communicate using the underground information superhighway. *Trends Plant Sci.* **2004**, *9*, 26–32. https://doi.org/10.1016/j.tplants.2003.11.008.

21. Li, Y.; Kong, D.; Fu, Y.; Sussman, M.R.; Wu, H. The effect of developmental and environmental factors on secondary metabolites in medicinal plants. *Plant Physiol. Biochem.* **2020**, *148*, 80–89. https://doi.org/10.1016/j.plaphy.2020.01.006.

22. Rudrappa, T.; Czymmek, K.J.; Paré, P.W.; Bais, H.P. Root-Secreted malic acid recruits beneficial soil bacteria. *Plant Physiol.* **2008**, *148*, 1547–1556. https://doi.org/10.1104/pp.108.127613.

23. Mauch-Mani, B.; Baccelli, I.; Luna, E.; Flors, V. Defense priming: an adaptive part of induced resistance. *Annu. Rev. Plant Biol.* **2017**, *68*, 485–512. https://doi.org/10.1146/annurev-arplant-042916-041132.

24. Hilker, M.; Schmülling, T. Stress priming, memory, and signalling in plants. *Plant Cell Environ.* **2019**, *42*, 753–761. https://doi.org/10.1111/pce.13526.

25. Bakker, P.A.H.M.; Berendsen, R.L.; Doornbos, R.F.; Wintermans, P.C.A.; Pieterse, C.M.J. The rhizosphere revisited: Root microbiomics. *Front. Plant Sci.* **2013**, *4*, 165. https://doi.org/10.3389/fpls.2013.00165.

26. Miller, J.B.; Oldroyd, G.E.D. The role of diffusible signals in the establishment of rhizobial and mycorrhizal symbioses. In *Signalling and Communication in Plant Symbiosis*; Springer: Berlin/Heidelberg, Germany, 2011; pp. 1–30. https://doi.org/10.1007/978-3-642-20966-6_1.

27. Berendsen, R.L.; Pieterse, C.M.J.; Bakker, P.A.H.M. The rhizosphere microbiome and plant health. *Trends Plant Sci.* **2012**, *17*, 478–486. https://doi.org/10.1016/j.tplants.2012.04.001.
28. Pieterse, C.M.J.; Leon-Reyes, A.; Van der Ent, S.; Van Wees, S.C.M. Networking by small-molecule hormones in plant immunity. *Nat. Chem. Biol.* **2009**, *5*, 308–316. https://doi.org/10.1038/nchembio.164.

29. Olanrewaju, O.S.; Ayangbenro, A.S.; Glick, B.R.; Babalola, O.O.; Ayangbenro, A. Plant health: Feedback effect of root exudates-rhizobiome interactions. *Appl. Microbiol. Biotechnol.* **2019**, *103*, 1155–1166. https://doi.org/10.1007/s00253-018-9556-6.

30. Pratama, A.A.; Terpstra, J.; de Oliveria, A.L.M.; Salles, J.F. The Role of Rhizosphere Bacteriophages in Plant Health. *Trends Microbiol.* **2020**, *28*, 709–718. https://doi.org/10.1016/j.tim.2020.04.005.

31. Sharma, R.S.; Nayak, S.; Malhotra, S.; Karmakar, S.; Sharma, M.; Raiping, S.; Mishra, V. Rhizosphere provides a new paradigm on the prevalence of lysogeny in the environment. *Soil Tillage Res.* **2019**, *195*, 104368. https://doi.org/10.1016/j.still.2019.104368.

32. Li, Y.; Sun, H.; Yang, W.; Chen, G.; Xu, H. Dynamics of Bacterial and Viral Communities in Paddy Soil with Irrigation and Urea Application. *Viruses* **2019**, *11*, 347. https://doi.org/10.3390/v11040347.

33. Simon, J.-C.; Marchesi, J.; Mougel, C.; Selosse, M.-A. Host-Microbiota interactions: From holobiont theory to analysis. *Microbiome* **2019**, *7*, 1–5. https://doi.org/10.1186/s40168-019-0619-4.

34. Sasse, J.; Martinoia, E.; Northen, T. Feed Your Friends: Do plant exudates shape the root microbiome? *Trends Plant Sci.* **2018**, *23*, 25–41. https://doi.org/10.1016/j.tplants.2017.09.003.

35. Mommer, L.; Kirkegaard, J.; van Ruijven, J. Root-Root Interactions: Towards a rhizosphere framework. *Trends Plant Sci.* **2016**, *21*, 209–217. https://doi.org/10.1016/j.tplants.2016.01.009.

36. Rosier, A.; Bishnoi, U.; Lakshmanan, V.; Sherrier, D.J.; Bais, H.P. A perspective on inter-kingdom signaling in plant-beneficial microbe interactions. *Plant Mol. Biol.* **2016**, *90*, 537–548. https://doi.org/10.1007/s11103-016-0433-3.

37. Hein, J.W.; Wolfe, G.V.; Blee, K.A. Comparison of Rhizosphere Bacterial Communities in *Arabidopsis thaliana* mutants for systemic Acquired Resistance. *Microb. Ecol.* **2008**, *55*, 333–343. https://doi.org/10.1007/s00248-007-9279-1.

38. Schlaeppi, K.; Bulgarelli, D. The Plant Microbiome at Work. *Mol. Plant-Microbe Interact.* **2015**, *28*, 212–217. https://doi.org/10.1094/mpmi-10-14-0334-fi.

39. Yang, C.-H.; Crowley, D.E. Rhizosphere microbial community structure in relation to root location and plant iron nutritional status. *Appl. Environ. Microbiol.* **2000**, *66*, 345–351. https://doi.org/10.1128/aem.66.1.345-351.2000.

40. Malusà, E.; Pinzari, F.; Canfora, L. Efficacy of biofertilizers: Challenges to improve crop production. In *Microbial Inoculants in Sustainable Agricultural Productivity*; Springer: New Delhi, India, 2016; pp. 17–40. https://doi.org/10.1007/978-81-322-2644-4_2.

41. Jones, P.; Garcia, B.; Furches, A.; Tuskan, G.A.; Jacobson, D. Plant host-associated mechanisms for microbial selection. *Front. Plant Sci.* **2019**, *10*, 862. https://doi.org/10.3389/fpls.2019.00862.

42. Mendes, R.; Garbeva, P.; Raaijmakers, J.M. The rhizosphere microbiome: Significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. *FEMS Microbiol. Rev.* **2013**, *37*, 634–663. https://doi.org/10.1111/1574-6976.12028.

43. Bai, Y.; Müller, D.B.; Srinivas, G.; Garrido-Oter, R.; Potthoff, E.; Rott, M.; Dombrowski, N.; Münch, P.C.; Spaepen, S.; Remus-Emsermann, M.; et al. Functional overlap of the Arabidopsis leaf and root microbiota. *Nature* **2015**, *528*, 364–369. https://doi.org/10.1038/nature16192.

44. Hong, K.W.; Koh, C.L.; Sam, C.-K.; Yin, W.-F.; Chan, K.-G. Quorum Quenching Revisited—From Signal Decays to Signalling Confusion. *Sensors* **2012**, *12*, 4661–4696. https://doi.org/10.3390/s120404661.

45. Helman, Y.; Chernin, L. Silencing the mob: Disrupting quorum sensing as a means to fight plant disease. *Mol. Plant Pathol.* **2015**, *16*, 316–329. https://doi.org/10.1111/mpp.12180.

46. Schikora, A.; Schenk, S.T.; Hartmann, A. Beneficial effects of bacteria-plant communication based on quorum sensing molecules of the N-acyl-homoserine lactone group. *Plant Mol. Biol.* **2016**, *90*, 605–612. https://doi.org/10.1007/s11103-016-0457-8.

47. Hassan, R.; Shaaban, M.I.; Bar, F.A.; El-Mahdy, A.; Shokralla, S. Quorum sensing inhibiting activity of *Streptomyces coelicoflavus* Isolated from Soil. *Front. Microbiol.* **2016**, *7*, 659. https://doi.org/10.3389/fmicb.2016.00659.

48. Chu, W. Role of the quorum-sensing system in biofilm formation and virulence of *Aeromonas hydrophila*. *Afr. J. Microbiol. Res.* **2011**, *5*, 5819–5825. https://doi.org/10.5897/ajmr10.684.

49. Atkinson, S.; Williams, P. Quorum sensing and social networking in the microbial world. *J. R. Soc. Interface* **2009**, *6*, 959–978. https://doi.org/10.1098/rsif.2009.0203.

50. Vendeville, A.; Winzer, K.; Heurlier, K.; Tang, C.M.; Hardie, K. Making ‘sense’ of metabolism: Autoinducer-2, LUXS and pathogenic bacteria. *Nat. Rev. Genet.* **2005**, *3*, 383–396. https://doi.org/10.1038/nrmicro1146.

51. Winzer, K. Bacterial cell-to-cell communication: Sorry, can't talk now—gone to lunch! *Curr. Opin. Microbiol.* **2002**, *5*, 216–222. https://doi.org/10.1016/s1369-5274(02)00304-1.

52. Zhang, W.; Li, C. Exploiting Quorum Sensing Interfering Strategies in Gram-negative bacteria for the enhancement of environmental applications. *Front. Microbiol.* **2016**, *6*, 1535. https://doi.org/10.3389/fmicb.2015.01535.

53. Ferluga, S.; Steindler, L.; Venturi, V. N-acyl homoserine lactone quorum sensing in Gram-negative rhizobacteria. In *Secondary Metabolites in Soil Ecology*; Springer: Berlin/Heidelberg, Germany, 2008; pp. 69–90. https://doi.org/10.1007/978-3-540-74543-3_4.

54. Sindhu, S.S.; Sehrawat, A.; Sharma, R.; Dahiya, A.; Khandelwal, A. Belowground microbial crosstalk and rhizosphere biology. In *Plant-Microbe Interactions in Agro-Ecological Perspectives*; Springer: Singapore, 2017; pp. 695–752. https://doi.org/10.1007/978-981-10-6593-4_29.

55. Aigle, B.; Corre, C. Waking up Streptomyces Secondary Metabolism by Constitutive Expression of Activators or Genetic Disruption of Repressors. *Methods Enzymol.* **2012**, *517*, 343–366. https://doi.org/10.1016/b978-0-12-404634-4.00017-6.
56. Ulrich, K.; Kube, M.; Becker, R.; Schneck, V.; Ulrich, A. Genomic analysis of the endophytic *Stenotrophomonas* strain 169 reveals features related to plant-growth promotion and stress tolerance. *Front. Microbiol.* **2021**, *12*, 1542. https://doi.org/10.3389/fmicb.2021.687463.

57. Xiong, Q.; Liu, D.; Zhang, H.; Dong, X.; Zhang, G.; Liu, Y.; Zhang, R. Quorum sensing signal autoinducer-2 promotes root colonization of Bacillus velezensis SQR9 by affecting biofilm formation and motility. *Appl. Microbiol. Biotechnol.* **2020**, *104*, 7177–7185. https://doi.org/10.1007/s00253-020-10713-w.

58. Zhao, Q.; Yang, X.-Y.; Li, Y.; Liu, F.; Cao, X.-Y.; Jia, Z.-H.; Song, S.-S. N-3-oxo-hexanoyl-homoserine lactone, a bacterial quorum sensing signal, enhances salt tolerance in Arabidopsis and wheat. *Bot. Stud.* **2020**, *61*, 8–12. https://doi.org/10.1186/s40529-020-00283-5.

59. Jung, B.K.; Khan, A.R.; Hong, S.-J.; Park, G.-S.; Park, Y.-J.; Kim, H.-J.; Jeon, H.-J.; Khan, M.A.; Waqas, M.; Lee, I.-J.; et al. Quorum sensing activity of the plant growth-promoting rhizobacterium *Serratia glossinae* GS2 isolated from the sesame (*Sesamum indicum* L.) rhizosphere. *Ann. Microbiol.* **2017**, *67*, 623–632. https://doi.org/10.1007/s13213-017-1291-1.

60. Liu, X.; Bimerew, M.; Ma, Y.; Müller, H.; Ovadis, M.; Eberl, L.; Berg, G.; Chernin, L. Quorum-Sensing signaling is required for production of the antibiotic pyrrolnitrin in a rhizospheric biocontrol strain of *Serratia plymuthica*. *FEMS Microbiol. Lett.* **2007**, *270*, 299–305. https://doi.org/10.1111/j.1574-6968.2007.00681.x.

61. Barriuso, J.; Solano, B.R.; Fray, R.G.; Cámara, M.; Hartmann, A.; Mañero, F.J.G. Transgenic tomato plants alter quorum sensing in plant growth-promoting rhizobacteria. *Plant Biotechnol. J.* **2008**, *6*, 442–452. https://doi.org/10.1111/j.1467-7652.2008.00331.x.

62. Ryu, C.-M.; Choi, H.K.; Lee, C.-H.; Murphy, J.F.; Lee, J.-K.; Kloepper, J.W. Modulation of Quorum Sensing in Acyl-homoserine Lactone-Producing or -Degrading Tobacco Plants Leads to Alteration of Induced Systemic Resistance Elicited by the Rhizobacterium Serratia marcescens 90-166. *Plant Pathol. J.* **2013**, *29*, 182–192. https://doi.org/10.5423/ppj.si.11.2012.0173.

63. Song, S.; Jia, Z.; Xu, J.; Zhang, Z.; Bian, Z. N-butyryl-homoserine lactone, a bacterial quorum-sensing signaling molecule, induces intracellular calcium elevation in Arabidopsis root cells. *Biochem. Biophys. Res. Commun.* **2011**, *414*, 355–360. https://doi.org/10.1016/j.bbrc.2011.09.076.

64. Imran, A.; Saadalla, M.J.A.; Khan, S.-U.; Mirza, M.S.; Malik, K.A.; Hafeez, F.Y. Ochrobactrum sp. Pv2Z2 exhibits multiple traits of plant growth promotion, biodegradation and N-acyl-homoserine-lactone quorum sensing. *Ann. Microbiol.* **2014**, *64*, 1797–1806. https://doi.org/10.1007/s13213-014-0824-0.

65. Alavi, P.; Müller, H.; Cardinale, M.; Zachow, C.; Sanchez, M.B.; Martinez, J.L.; Berg, G. The DSF Quorum Sensing System Controls the Positive Influence of *Stenotrophomonas maltophilia* on Plants. *PLoS ONE* **2013**, *8*, e67103. https://doi.org/10.1371/journal.pone.0067103.

66. De Sordi, L.; Mühlschlegel, F.A. Quorum sensing and fungal-bacterial interactions in Candida albicans: A communicative network regulating microbial coexistence and virulence. *FEMS Yeast Res.* **2009**, *9*, 990–999. https://doi.org/10.1111/j.1567-1364.2009.00573.x.

67. Andersson, D.I.; Hughes, D. Microbiological effects of sublethal levels of antibiotics. *Nat. Rev. Microbiol.* **2014**, *12*, 465–478. https://doi.org/10.1038/nrmicro3270.

68. Brescia, F.; Marchetti-Deschmann, M.; Musetti, R.; Perazzolli, M.; Pertot, I.; Puopolo, G. The rhizosphere signature on the cell motility, biofilm formation and secondary metabolite production of a plant-associated Lysobacter strain. *Microbiol. Res.* **2020**, *234*, 126424. https://doi.org/10.1016/j.micres.2020.126424.

69. Hartmann, A.; Schikora, A. Quorum Sensing of Bacteria and Trans-Kingdom Interactions of N-Acyl Homoserine Lactones with Eukaryotes. *J. Chem. Ecol.* **2012**, *38*, 704–713. https://doi.org/10.1007/s10886-012-0141-7.

70. Clinton, A.; Rumbaugh, K.P. Interspecies and Interkingdom Signaling via Quorum Signals. *Isr. J. Chem.* **2016**, *56*, 265–272. https://doi.org/10.1002/ijch.201400132.

71. Bitas, V.; Kim, H.-S.; Bennett, J.W.; Kang, S. Sniffing on Microbes: Diverse Roles of Microbial Volatile Organic Compounds in Plant Health. *Mol. Plant-Microbe Interact.* **2013**, *26*, 835–843. https://doi.org/10.1094/mpmi-10-12-0249-cr.

72. Kanchiswamy, C.N.; Malnoy, M.; Maffei, M. Bioprospecting bacterial and fungal volatiles for sustainable agriculture. *Trends Plant Sci.* **2015**, *20*, 206–211. https://doi.org/10.1016/j.tplants.2015.01.004.

73. Kai, M.; Effmert, U.; Piechulla, B. Bacterial-Plant-Interactions: Approaches to Unravel the Biological Function of Bacterial Volatiles in the Rhizosphere. *Front. Microbiol.* **2016**, *7*, 108. https://doi.org/10.3389/fmicb.2016.00108.

74. Tyc, O.; Zweers, H.; de Boer, W.; Garbeva, P. Volatiles in Inter-Specific Bacterial Interactions. *Front. Microbiol.* **2015**, *6*, 1412. https://doi.org/10.3389/fmicb.2015.01412.

75. Audrain, B.; Farag, M.A.; Ryu, C.-M.; Ghigo, J.-M. Role of bacterial volatile compounds in bacterial biology. *FEMS Microbiol. Rev.* **2015**, *39*, 222–233. https://doi.org/10.1093/femsre/fuu013.

76. Schmidt, R.; Cordovez, V.; de Boer, W.; Raaijmakers, J.; Garbeva, P. Volatile affairs in microbial interactions. *ISME J.* **2015**, *9*, 2329–2335. https://doi.org/10.1038/ismej.2015.42.

77. Barraud, N.; Schlecheck, D.; Klebensberger, J.; Webb, J.S.; Hassett, D.J.; Rice, S.A.; Kjelleberg, S. Nitric Oxide Signaling in *Pseudomonas aeruginosa* Biofilms Mediates Phosphodiesterase Activity, Decreased Cyclic Di-GMP Levels, and Enhanced Dispersal. *J. Bacteriol.* **2009**, *191*, 7333–7342. https://doi.org/10.1128/jb.00975-09.

78. Taghavi, S.; Garafola, C.; Monchy, S.; Newman, L.; Hoffman, A.; Weyens, N.; Barac, T.; Vangronsveld, J.; van der Lelie, D. Genome Survey and Characterization of Endophytic Bacteria Exhibiting a Beneficial Effect on Growth and Development of Poplar Trees. *Appl. Environ. Microbiol.* **2009**, *75*, 748–757. https://doi.org/10.1128/aem.02239-08.
79. Duca, D.; Lorv, J.; Patten, C.L.; Rose, D.; Glick, B.R. Indole-3-acetic acid in plant-microbe interactions. *Antonie Van Leeuwenhoek* **2014**, *106*, 85-125. https://doi.org/10.1007/s10482-013-0095-y.

80. Fahad, S.; Hussain, S.; Bano, A.; Saud, S.; Hassan, S.; Shan, D.; Khan, F.A.; Khan, F.; Chen, Y.; Wu, C.; et al. Potential role of phytohormones and plant growth-promoting rhizobacteria in abiotic stresses: Consequences for changing environment. *Environ. Sci. Pollut. Res.* **2015**, *22*, 4907-4921. https://doi.org/10.1007/s11356-014-3754-2.

81. Raheem, A.; Shaposhnikov, A.; Belimov, A.A.; Dodd, I.C.; Ali, B. Auxin production by rhizobacteria was associated with improved yield of wheat (*Triticum aestivum* L.) under drought stress. *Arch. Agron. Soil Sci.* **2018**, *64*, 574-587. https://doi.org/10.1080/03650340.2017.1362105.

82. Zhou, X.R.; Dai, L.; Xu, G.F.; Wang, H.S. A strain of Phoma species improves drought tolerance of Pinus tabulaeformis. *Sci. Rep.* **2021**, *11*, 1-11. https://doi.org/10.1038/s41598-021-87105-1.

83. Pieterse, C.M.J.; Zamioudis, C.; Berendsen, R.L.; Weller, D.M.; Van Wees, S.C.M.; Bakker, P.A.H.M. Induced Systemic Resistance by Beneficial Microbes. *Annu. Rev. Phytopathol.* **2014**, *52*, 347-375. https://doi.org/10.1146/annurev-phyto-082712-102340.

84. Vos, I.A.; Pieterse, C.; Van Wees, S. Costs and benefits of hormone-regulated plant defences. *Plant Pathol.* **2013**, *62*, 43-55. https://doi.org/10.1111/ppa.12105.

85. Zamioudis, C.; Pieterse, C.M.J. Modulation of Host Immunity by Beneficial Microbes. *Mol. Plant-Microbe Interact.* **2012**, *25*, 139-150. https://doi.org/10.1094/mpmi-06-11-0179.

86. von Rad, U.; Klein, I.; Dobrev, P.I.; Kottova, J.; Zazimalova, E.; Fekete, A.; Hartmann, A.; Schmitt-Kopplin, P.; Durner, J. Response of Arabidopsis thaliana to N-hexanoyl-dl-homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere. *Planta* **2008**, *229*, 73-85. https://doi.org/10.1007/s00425-008-0811-4.

87. Kakkar, A.; Nizampatnam, N.R.; Kondreddy, A.; Pradhan, B.B.; Chatterjee, S. *Xanthomonas campestriscell*-cell signalling molecule DSF (diffusible signal factor) elicits innate immunity in plants and is suppressed by the exopolysaccharide xanthan. *J. Exp. Bot.* **2015**, *66*, 6697-6714. https://doi.org/10.1093/jxb/erv377.

88. Corral-Lugo, A.; Daddaoua, A.; Ortega, A.; Espinosa-Urgel, M.; Krell, T. Rosmarinic acid is a homoserine lactone mimic produced by plants that activates a bacterial quorum-sensing regulator. *Sci. Signal.* **2016**, *9*, ra1. https://doi.org/10.1126/scisignal.aaa8271.

89. Hartmann, A.; Rothballer, M.; Hense, B.A.; Schröder, P. Bacterial quorum sensing compounds are important modulators of microbe-plant interactions. *Front. Plant Sci.* **2014**, *5*, 131. https://doi.org/10.3389/fpls.2014.00131.

90. Jakobsen, T.H.; van Gennip, M.; Phipps, R.K.; Shanmugham, M.S.; Christensen, L.D.; Alhede, M.; Skindersoe, M.E.; Rasmussen, T.B.; Friedrich, K.; Uthe, F.; et al. Ajoene, a Sulfur-Rich Molecule from Garlic, Inhibits Genes Controlled by Quorum Sensing. *Antimicrob. Agents Chemother.* **2012**, *56*, 2314-2325. https://doi.org/10.1128/aac.05919-11.

91. Ganin, H.; Rayo, J.; Amara, N.; Levy, N.; Krief, P.; Meijler, M.M. Sulforaphane and erucin, natural isothiocyanates from broccoli, inhibit bacterial quorum sensing. *MedChemComm* **2013**, *4*, 175-179. https://doi.org/10.1039/c2md20196h.

92. Rudrappa, T.; Bais, H.P. Curcumin, a Known Phenolic from Curcuma longa, Attenuates the Virulence of *Pseudomonas aeruginosa* PAO1 in Whole Plant and Animal Pathogenicity Models. *J. Agric. Food Chem.* **2008**, *56*, 1955-1962. https://doi.org/10.1021/jf072591j.

93. Rasmussen, T.B.; Bjarnsholt, T.; Skindersoe, M.E.; Hentzer, M.; Kristoffersen, P.; Ko¨te, M.; Nielsen, J.; Eberl, L.; Givskov, M. Screening for Quorum-Sensing Inhibitors (QSI) by Use of a Novel Genetic System, the QSI Selector. *J. Bacteriol.* **2005**, *187*, 1799-1814. https://doi.org/10.1128/jb.187.5.1799-1814.2005.

94. Bauer, W.D.; Mathesius, U. Plant responses to bacterial quorum sensing signals. *Curr. Opin. Plant Biol.* **2004**, *7*, 429-433. https://doi.org/10.1016/j.pbi.2004.05.008.

95. Gao, M.; Teplitski, M.; Robinson, J.B.; Bauer, W.D. Production of Substances by *Medicago truncatula* that Affect Bacterial Quorum Sensing. *Mol. Plant-Microbe Interact.* **2003**, *16*, 827-834. https://doi.org/10.1094/mpmi.2003.16.9.827.

96. Kusari, P.; Kusari, S.; Spiteller, M.; Kayser, O. Implications of endophyte-plant crosstalk in light of quorum responses for plant biotechnology. *Appl. Microbiol. Biotechnol.* **2015**, *99*, 5383-5390. https://doi.org/10.1007/s00253-015-6660-8.

97. Teplitski, M.; Mathesius, U.; Rumbaugh, K.P. Perception and Degradation of N-Acyl Homoserine Lactone Quorum Sensing Signals by Mammalian and Plant Cells. *Chem. Rev.* **2011**, *111*, 100-116. https://doi.org/10.1021/cr100045m.

98. Zhang, W.; Luo, Q.; Zhang, Y.; Fan, X.; Ye, T.; Mishra, S.; Bhatt, P.; Zhang, L.; Chen, S. Quorum Quenching in a Novel *Acinetobacter* sp. XN-10 Bacterial Strain against *Pectobacterium carotovorum* subsp. *carotovorum*. *Microorganisms* **2020**, *8*, 1100. https://doi.org/10.3390/microorganisms8081100.

99. Weller, D.M.; Mavrodi, D.V.; Van Pelt, J.A.; Pieterse, C.M.J.; Van Loon, L.C.; Bakker, P.A.H.M. Induced Systemic Resistance in Arabidopsis thaliana Against *Pseudomonas syringae* pv. tomato by 2,4-Diacetylphloroglucinol-Producing Pseudomonas fluorescens. *Phytopathology* **2012**, *102*, 403-412. https://doi.org/10.1094/phyto-08-11-0222.

100. Groenhagen, U.; Baumgartner, R.; Bailly, A.; Gardiner, A.; Eberl, L.; Schulz, S.; Weisskopf, L. Production of Bioactive Volatiles by Different Burkholderia ambifaria Strains. *J. Chem. Ecol.* **2013**, *39*, 892-906. https://doi.org/10.1007/s10886-013-0315-y.

101. Kai, M.; Haustein, M.; Molina, F.; Petri, A.; Scholz, B.; Piechulla, B. Bacterial volatiles and their action potential. *Appl. Microbiol. Biotechnol.* **2009**, *81*, 1001-1012. https://doi.org/10.1007/s00253-008-1760-3.

102. Ryu, C.-M.; Farag, M.A.; Hu, C.-H.; Reddy, M.S.; Wei, H.-X.; Paré, P.W.; Kloepper, J.W. Bacterial volatiles promote growth in *Arabidopsis*. *Proc. Natl. Acad. Sci. USA* **2003**, *100*, 4927-4932. https://doi.org/10.1073/pnas.0730845100.

103. Bertin, C.; Yang, X.; Weston, L.A. The role of root exudates and allelochemicals in the rhizosphere. *Plant Soil* **2003**, *256*, 67-83. https://doi.org/10.1023/a:1026290508166.
104. Zhang, Y.; Ruyter-Spira, C.; Bouwmeester, H.J. Engineering the plant rhizosphere. *Curr. Opin. Biotechnol.* **2015**, *32*, 136-142.
https://doi.org/10.1016/j.copbio.2014.12.006.

105. Downie, J.A. The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. *FEMS Microbiol. Rev.* **2010**, *34*, 150-170. https://doi.org/10.1111/j.1574-6976.2009.00205.x

106. Rios, J.; Pascual, J.; Guillen, M.; Lopez-Martinez, A.; Carvajal, M. Influence of foliar Methyl-jasmonate biostimulation on exudation of glucosinolates and their effect on root pathogens of broccoli plants under salinity condition. *Sci. Hortic.* **2021**, *282*, 110027. https://doi.org/10.1016/j.scienta.2021.110027.

107. Zhang, N.; Wang, D.; Liu, Y.; Li, S.; Shen, Q.; Zhang, R. Effects of different plant root exudates and their organic acid components on chemotaxis, biofilm formation and colonization by beneficial rhizosphere-associated bacterial strains. *Plant Soil* **2014**, *374*, 689-700. https://doi.org/10.1007/s11104-013-1915-6.

108. Pérez-Montaño, F.; Alias-Villegas, C.; Bellogín, R.A.; del Cerro, P.; Espuny, M.R.; Jiménez-Guerrero, I.; López-Baena, F.J.; Ollero, F.; Cubo, T. Plant growth promotion in cereal and leguminous agricultural important plants: From microorganism capacities to crop production. *Microbiol. Res.* **2014**, *169*, 325-336. https://doi.org/10.1016/j.micres.2013.09.011.

109. Dudareva, N.; Negre, F.; Nagegowda, D.A.; Orlova, I. Plant Volatiles: Recent Advances and Future Perspectives. *Crit. Rev. Plant Sci.* **2006**, *25*, 417-440. https://doi.org/10.1080/07352680600899973.

110. Rasmann, S.; Köllner, T.G.; Degenhardt, J.; Hiltpold, I.; Toepfer, S.; Kuhlmann, U.; Gershenzon, J.; Turlings, T.C.J. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. *Nature* **2005**, *434*, 732-737. https://doi.org/10.1038/nature03451.

111. Poole, P.; Ramachandran, V.; Terpolilli, J. Rhizobia: From saprophytes to endosymbionts. *Nat. Rev. Genet.* **2018**, *16*, 291-303.
https://doi.org/10.1038/nrmicro.2017.171.

112. Janczarek, M.; Rachwał, K.; Marzec, A.; Grządziel, J.; Palusińska-Szysz, M. Signal molecules and cell-surface components involved in early stages of the legume-rhizobium interactions. *Appl. Soil Ecol.* **2015**, *85*, 94-113. https://doi.org/10.1016/j.apsoil.2014.08.010.

113. Hassan, S.; Mathesius, U. The role of flavonoids in root-rhizosphere signalling: Opportunities and challenges for improving plant-microbe interactions. *J. Exp. Bot.* **2012**, *63*, 3429-3444. https://doi.org/10.1093/jxb/err430.

114. Lerouge, P.; Roche, P.; Faucher, C.; Maillet, F.; Truchet, G.; Promé, J.C.; Dénarié, J. Symbiotic host-specificity of *Rhizobium meliloti* is determined by a sulphated and acylated glucosamine oligosaccharide signal. *Nature* **1990**, *344*, 781-784.
https://doi.org/10.1038/344781a0.

115. Oldroyd, G.E.; Murray, J.D.; Poole, P.S.; Downie, J.A. The Rules of Engagement in the Legume-Rhizobial Symbiosis. *Annu. Rev. Genet.* **2011**, *45*, 119-144. https://doi.org/10.1146/annurev-genet-110410-132549.

116. Limpens, E.; van Zeijl, A.; Geurts, R. Lipochitooligosaccharides Modulate Plant Host Immunity to Enable Endosymbioses. *Annu. Rev. Phytopathol.* **2015**, *53*, 311-334. https://doi.org/10.1146/annurev-phyto-080614-120149.

117. Smith, D.L.; Gravel, V.; Yergeau, E. Editorial: Signaling in the Phytomicrobiome. *Front. Plant Sci.* **2017**, *8*, 611.
https://doi.org/10.3389/fpls.2017.00611.

118. Smith, D.L.; Praslickova, D.; Ilangumaran, G. Inter-organismal signaling and management of the phytomicrobiome. *Front. Plant Sci.* **2015**, *6*, 722. https://doi.org/10.3389/fpls.2015.00722.

119. Oláh, B.; Brière, C.; Bécard, G.; Dénarié, J.; Gough, C. Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. *Plant J.* **2005**, *44*, 195-207.
https://doi.org/10.1111/j.1365-313x.2005.02522.x.

120. Khan, A.L.; Hamayun, M.; Kim, Y.-H.; Kang, S.-M.; Lee, J.-H.; Lee, I.-J. Gibberellins producing endophytic Aspergillus fumigatus sp. LH02 influenced endogenous phytohormonal levels, isoflavonoids production and plant growth in salinity stress. *Process Biochem.* **2011**, *46*, 440-447. https://doi.org/10.1016/j.procbio.2010.09.013.

121. Cooper, J. Early interactions between legumes and rhizobia: Disclosing complexity in a molecular dialogue. *J. Appl. Microbiol.* **2007**, *103*, 1355-1365. https://doi.org/10.1111/j.1365-2672.2007.03366.x.

122. Mabood, F.; Souleimanov, A.; Khan, W.; Smith, D. Jasmonates induce Nod factor production by Bradyrhizobium japonicum. *Plant Physiol. Biochem.* **2006**, *44*, 759-765. https://doi.org/10.1016/j.plaphy.2006.10.025.

123. Benjelloun, I.; Alami, I.T.; El Khadir, M.; Douira, A.; Udupa, S. Co-Inoculation of *Mesorhizobium ciceri* with Either *Bacillus* sp. or *Enterobacter aerogenes* on Chickpea Improves Growth and Productivity in Phosphate-Deficient Soils in Dry Areas of a Mediterranean Region. *Plants* **2021**, *10*, 571. https://doi.org/10.3390/plants10030571.

124. Schmitz, A.M.; Harrison, M.J. Signaling events during initiation of arbuscular mycorrhizal symbiosis. *J. Integr. Plant Biol.* **2014**, *56*, 250-261. https://doi.org/10.1111/jipb.12155.

125. Ruyter-Spira, C.; Al-Babili, S.; van der Krol, S.; Bouwmeester, H. The biology of strigolactones. *Trends Plant Sci.* **2013**, *18*, 72-83.
https://doi.org/10.1016/j.tplants.2012.10.003.

126. Waldie, T.; McCulloch, H.; Leyser, O. Strigolactones and the control of plant development: Lessons from shoot branching. *Plant J.* **2014**, *79*, 607-622. https://doi.org/10.1111/tpj.12488.

127. Kaschuk, G.; Leffelaar, P.A.; Giller, K.E.; Alberton, O.; Hungria, M.; Kuyper, T.W. Responses of legumes to rhizobia and arbuscular mycorrhizal fungi: A meta-analysis of potential photosynthate limitation of symbioses. *Soil Biol. Biochem.* **2010**, *42*, 125-127. https://doi.org/10.1016/j.soilbio.2009.10.017.

128. Phour, M.; Sehrawat, A.; Sindhu, S.S.; Glick, B.R. Interkingdom signaling in plant-rhizomicrobiome interactions for sustainable agriculture. *Microbiol. Res.* **2020**, *241*, 126589. https://doi.org/10.1016/j.micres.2020.126589.
129. Vangelisti, A.; Natali, L.; Bernardi, R.; Sbrana, C.; Turrini, A.; Hassani-Pak, K.; Hughes, D.; Cavallini, A.; Giovannetti, M.; Giordani, T. Transcriptome changes induced by arbuscular mycorrhizal fungi in sunflower (*Helianthus annuus* L.) roots. *Sci. Rep.* **2018**, *8*, 1–14. https://doi.org/10.1038/s41598-017-18445-0.

130. Maillet, F.; Poinsot, V.; André, O.; Puech-Pagès, V.; Haouy, A.; Gueunier, M.; Cromer, L.; Giraudet, D.; Formey, D.; Niebel, A.; et al. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. *Nature* **2011**, *469*, 58–63. https://doi.org/10.1038/nature09622.

131. MacLean, A.M.; Bravo, A.; Harrison, M.J. Plant Signaling and Metabolic Pathways Enabling Arbuscular Mycorrhizal Symbiosis. *Plant Cell* **2017**, *29*, 2319–2335. https://doi.org/10.1105/tpc.17.00555.

132. Ben Laouane, R.; Meddich, A.; Bechtaoui, N.; Oufdou, K.; Wahbi, S. Effects of Arbuscular Mycorrhizal Fungi and Rhizobia Symbiosis on the Tolerance of Medicago Sativa to Salt Stress. *Gesunde Pflanz.* **2019**, *71*, 135–146. https://doi.org/10.1007/s10343-019-00461-x.

133. Hao, Z.; Xie, W.; Jiang, X.; Wu, Z.; Zhang, X.; Chen, B. Arbuscular Mycorrhizal Fungus Improves Rhizobium–Glycyrrhiza Seedling Symbiosis under Drought Stress. *Agronomy* **2019**, *9*, 572. https://doi.org/10.3390/agronomy9100572.

134. Tang, T.-T.; Xie, M.-M.; Chen, S.-M.; Zhang, S.-M.; Wu, Q.-S. Effects of Arbuscular Mycorrhizal Fungi and Rhizobia on Physiological Activities in White Clover (*Trifolium repens*). *Biotechnology* **2019**, *18*, 49–54. https://doi.org/10.3923/biotech.2019.49.54.

135. Sui, X.-L.; Zhang, T.; Tian, Y.-Q.; Xue, R.-J.; Li, A.-R. A neglected alliance in battles against parasitic plants: Arbuscular mycorrhizal and rhizobial symbioses alleviate damage to a legume host by root hemiparasitic *Pedicularis* species. *New Phytol.* **2019**, *221*, 470–481. https://doi.org/10.1111/nph.15379.

136. Sakamoto, K.; Ogiwara, N.; Kaji, T.; Sugimoto, Y.; Ueno, M.; Sonoda, M.; Matsui, A.; Ishida, J.; Tanaka, M.; Totoki, Y.; et al. Transcriptome analysis of soybean (*Glycine max*) root genes differentially expressed in rhizobial, arbuscular mycorrhizal, and dual symbiosis. *J. Plant Res.* **2019**, *132*, 541–568. https://doi.org/10.1007/s10265-019-01117-7.

137. Selvaraj, A.; Thangavel, K.; Uthandi, S. Arbuscular mycorrhizal fungi (*Glomus intraradices*) and diazotrophic bacterium (*Rhizobium BMBS*) primed defense in blackgram against herbivorous insect (*Spodoptera litura*) infestation. *Microbiol. Res.* **2020**, *231*, 126355. https://doi.org/10.1016/j.micres.2019.126355.

138. Fabiańska, I.; Gerlach, N.; Almario, J.; Bucher, M. Plant-mediated effects of soil phosphorus on the root-associated fungal microbiota in *Arabidopsis thaliana*. *New Phytol.* **2019**, *221*, 2123–2137. https://doi.org/10.1111/nph.15538.

139. Verbon, E.H.; Trapet, P.L.; Stringlis, I.; Kruijs, S.; Bakker, P.A.; Pieterse, C.M. Iron and Immunity. *Annu. Rev. Phytopathol.* **2017**, *55*, 355–375. https://doi.org/10.1146/annurev-phyto-080516-035537.

140. Martínez-Medina, A.; Van Wees, S.C.; Pieterse, C.M. Airborne signals from *Trichoderma* fungi stimulate iron uptake responses in roots resulting in priming of jasmonic acid-dependent defences in shoots of *Arabidopsis thaliana* and *Solanum lycopersicum*. *Plant Cell Environ.* **2017**, *40*, 2691–2705. https://doi.org/10.1111/pce.13016.

141. Zamioudis, C.; Korteland, J.; Van Pelt, J.A.; Hamersveld, M.; Dombrowski, N.; Bai, Y.; Hanson, J.; Van Verk, M.C.; Ling, H.; Schulze-Lefert, P.; et al. Rhizobacterial volatiles and photosynthesis-related signals coordinate MYB 72 expression in *Arabidopsis* roots during onset of induced systemic resistance and iron-deficiency responses. *Plant J.* **2015**, *84*, 309–322. https://doi.org/10.1111/tpj.12995.

142. Hiruma, K.; Gerlach, N.; Sacristan, S.; Nakano, R.T.; Hacquard, S.; Kracher, B.; Neumann, U.; Ramirez, D.; Bucher, M.; O’Connell, R.J.; et al. Root Endophyte *Colletotrichum tofieldiae* Confers Plant Fitness Benefits that Are Phosphate Status Dependent. *Cell* **2016**, *165*, 464–474. https://doi.org/10.1016/j.cell.2016.02.028.

143. Emami, S.; Alikhani, H.A.; Pourbabaee, A.A.; Etesami, H.; Motasharezadeh, B.; Sarmadian, F. Consortium of endophyte and rhizosphere phosphate solubilizing bacteria improves phosphorous use efficiency in wheat cultivars in phosphorus deficient soils. *Rhizosphere* **2020**, *14*, 100196. https://doi.org/10.1016/j.rhispb.2020.100196.

144. Martin, F.M.; Uroz, S.; Barker, D.G. Ancestral alliances: Plant mutualistic symbioses with fungi and bacteria. *Science* **2017**, *356*, eAAD4501. https://doi.org/10.1126/science.aad4501.

145. Singh, S.; Nain, L. Microorganisms in the Conversion of Agricultural Wastes to Compost. *Proc. Indian Natl. Sci. Acad.* **2014**, *80*, 473. https://doi.org/10.16943/ptinsa/2014/v80i2/4.

146. Ahmed, S.; Rahman, S.; Hasan, M.; Paul, N.; Sajib, A.A. Microbial degradation of lignocellulosic biomass: Discovery of novel natural lignocellulolytic bacteria. *BioTechnologia* **2018**, *99*, 137–146. https://doi.org/10.5114/bta.2018.75657.

147. Haggag, W.M.; Abouziena, H.F.; Abd-El-Kreem, F.; El Habbasha, S. Agriculture biotechnology for management of multiple biotic and abiotic environmental stress in crops. *J. Chem. Pharm. Res.* **2015**, *7*, 882–889.

148. Balmer, A.; Pastor, V.; Gamir, J.; Flors, V.; Mauch-Mani, B. The ‘prime-ome’: Towards a holistic approach to priming. *Trends Plant Sci.* **2015**, *20*, 443–452. https://doi.org/10.1016/j.tplants.2015.04.002.

149. Selosse, M.-A.; Bessis, A.; Pozo, M.J. Microbial priming of plant and animal immunity: Symbionts as developmental signals. *Trends Microbiol.* **2014**, *22*, 607–613. https://doi.org/10.1016/j.tim.2014.07.003.

150. Edenancé, N.; Esánchez-Vallet, A.; Egoffner, D.; Emolina, A. Disease resistance or growth: The role of plant hormones in balancing immune responses and fitness costs. *Front. Plant Sci.* **2013**, *4*, 155. https://doi.org/10.3389/fpls.2013.00155.

151. Pandey, S.S.; Singh, S.; Babu, C.S.V.; Shanker, K.; Srivastava, N.K.; Shukla, A.K.; Kalra, A. Fungal endophytes of *Catharanthus roseus* enhance vindoline content by modulating structural and regulatory genes related to terpenoid indole alkaloid biosynthesis. *Sci. Rep.* **2016**, *6*, 26583. https://doi.org/10.1038/srep26583.

152. Tena, G.; Boudsocq, M.; Sheen, J. Protein kinase signaling networks in plant innate immunity. *Curr. Opin. Plant Biol.* **2011**, *14*, 519–529. https://doi.org/10.1016/j.pbi.2011.05.006.
153. Shah, J.; Zeier, J. Long-distance communication and signal amplification in systemic acquired resistance. *Front. Plant Sci.* **2013**, *4*, 30. https://doi.org/10.3389/fpls.2013.00030.

154. Pieterse, C.M.J.; Van der Does, D.; Zamioudis, C.; Leon-Reyes, A.; Van Wees, S.C.M. Hormonal Modulation of Plant Immunity. *Annu. Rev. Cell Dev. Biol.* **2012**, *28*, 489–521. https://doi.org/10.1146/annurev-cellbio-092910-154055.

155. Gimenez-Ibanez, S.; Chini, A.; Solano, R. How Microbes Twist Jasmonate Signaling around Their Little Fingers. *Plants* **2016**, *5*, 9. https://doi.org/10.3390/plants5010009.

156. Dodds, P.N.; Rathjen, J.P. Plant immunity: Towards an integrated view of plant-pathogen interactions. *Nat. Rev. Genet.* **2010**, *11*, 539–548. https://doi.org/10.1038/nrg2812.

157. Couto, D.; Zipfel, C. Regulation of pattern recognition receptor signalling in plants. *Nat. Rev. Immunol.* **2016**, *16*, 537–552. https://doi.org/10.1038/nri.2016.77.

158. Li, B.; Meng, X.; Shan, L.; He, P. Transcriptional Regulation of Pattern-Triggered Immunity in Plants. *Cell Host Microbe* **2016**, *19*, 641–650. https://doi.org/10.1016/j.chom.2016.04.011.

159. Clay, N.K.; Adio, A.M.; Denoux, C.; Jander, G.; Ausubel, F.M. Glucosinolate Metabolites Required for an *Arabidopsis* Innate Immune Response. *Science* **2009**, *323*, 95–101. https://doi.org/10.1126/science.1164627.

160. Derbyshire, M.; Mbengue, M.; Barascud, M.; Navaud, O.; Raffaele, S. Small RNAs from the plant pathogenic fungus *Sclerotinia sclerotiorum* highlight host candidate genes associated with quantitative disease resistance. *Mol. Plant Pathol.* **2019**, *20*, 1279-1297, doi:10.1111/mpp.12841.

161. Baetz, U.; Martinoia, E. Root exudates: The hidden part of plant defense. *Trends Plant Sci.* **2014**, *19*, 90–98. https://doi.org/10.1016/j.tplants.2013.11.006.

162. Jeandet, P.; Hébrard, C.; Deville, M.-A.; Cordelier, S.; Dorey, S.; Aziz, A.; Crouzet, J. Deciphering the Role of Phytoalexins in Plant-Microorganism Interactions and Human Health. *Molecules* **2014**, *19*, 18033–18056. https://doi.org/10.3390/molecules191118033.

163. Rin, S.; Mizuno, Y.; Shibata, Y.; Fushimi, M.; Katou, S.; Sato, I.; Chiba, S.; Kawakita, K.; Takemoto, D. EIN2-Mediated signaling is involved in pre-invasion defense in *Nicotiana benthamiana* against potato late blight pathogen, *Phytophthora* infestans. *Plant Signal. Behav.* **2017**, *12*, e1300733. https://doi.org/10.1080/15592324.2017.1300733.

164. Pel, M.J.C.; Pieterse, C.M.J. Microbial recognition and evasion of host immunity. *J. Exp. Bot.* **2013**, *64*, 1237–1248. https://doi.org/10.1093/jxb/ers262.

165. Jones, J.D.G.; Dangl, J.L. The plant immune system. *Nature* **2006**, *444*, 323–329. https://doi.org/10.1038/nature05286.

166. Boller, T.; He, S.Y. Innate Immunity in Plants: An Arms Race Between Pattern Recognition Receptors in Plants and Effectors in Microbial Pathogens. *Science* **2009**, *324*, 742–744. https://doi.org/10.1126/science.1171647.

167. Hasegawa, M.; Mitsuhara, I.; Seo, S.; Imai, T.; Koga, J.; Okada, K.; Yamane, H.; Ohashi, Y. Phytoalexin Accumulation in the Interaction Between Rice and the Blast Fungus. *Mol. Plant-Microbe Interact.* **2010**, *23*, 1000–1011. https://doi.org/10.1094/mpmi-23-8-1000.

168. King, S.R.; McLellan, H.; Boevink, P.C.; Armstrong, M.R.; Bukharova, T.; Sukarta, O.; Win, J.; Kamoun, S.; Birch, P.R.; Banfield, M.J. *Phytophthora* infestans RXLR Effector PexRD2 Interacts with Host MAPKKKε to Suppress Plant Immune Signaling. *Plant Cell* **2014**, *26*, 1345–1359. https://doi.org/10.1105/tpc.113.120055.

169. Boevink, P.C.; Wang, X.; McLellan, H.; He, Q.; Naqvi, S.; Armstrong, M.R.; Zhang, W.; Hein, I.; Gilroy, E.M.; Tian, Z.; et al. A Phytophthora infestans RXLR effector targets plant PP1c isoforms that promote late blight disease. *Nat. Commun.* **2016**, *7*, 10311. https://doi.org/10.1038/ncomms10311.

170. Martinez-Medina, A.; Flors, V.; Heil, M.; Mauch-Mani, B.; Pieterse, C.; Pozo, M.J.; Ton, J.; van Dam, N.M.; Conrath, U. Recognizing Plant Defense Priming. *Trends Plant Sci.* **2016**, *21*, 818–822. https://doi.org/10.1016/j.tplants.2016.07.009.

171. Bruce, T.J., Matthes, M.C., Napier, J.A. and Pickett, J.A., 2007. Stressful "memories" of plants: evidence and possible mechanisms. *Plant science*, *173*, 6, 603-608. https://doi.org/10.1016/j.plantsci.2007.09.002

172. Dempsey, D.A.; Klessig, D.F. SOS-Too many signals for systemic acquired resistance? *Trends Plant Sci.* **2012**, *17*, 538–545. https://doi.org/10.1016/j.tplants.2012.05.011.

173. Ádám, A.L.; Nagy, Z.; Kátay, G.; Mergenthaler, E.; Viczián, O. Signals of Systemic Immunity in Plants: Progress and Open Questions. *Int. J. Mol. Sci.* **2018**, *19*, 1146. https://doi.org/10.3390/ijms19041146.

174. Beckers, G.J.M.; Spoel, S.H. Fine-Tuning Plant Defence Signalling: Salicylate versus Jasmonate. *Plant Biol.* **2006**, *8*, 1–10. https://doi.org/10.1055/s-2005-872705.

175. Wu, Y.; Zhang, D.; Chu, J.Y.; Boyle, P.; Wang, Y.; Brindle, I.D.; De Luca, V.; Després, C. The *Arabidopsis* NPR1 protein is a receptor for the plant defense hormone salicylic acid. *Cell Rep.* **2012**, *1*, 639–647. https://doi.org/10.1016/j.celrep.2012.05.008.

176. Ullah, C.; Tsai, C.; Unsicker, S.B.; Xue, L.; Reichelt, M.; Gershenzon, J.; Hammerbacher, A. Salicylic acid activates poplar defense against the biotrophic rust fungus *Melampsora larici-populina* via increased biosynthesis of catechin and proanthocyanidins. *New Phytol.* **2019**, *221*, 960–975. https://doi.org/10.1111/nph.15396.

177. Yoodee, S.; Kobayashi, Y.; Songnuan, W.; Boonchird, C.; Thitamadee, S.; Kobayashi, I.; Narangajavana, J. Phytohormone priming elevates the accumulation of defense-related gene transcripts and enhances bacterial blight disease resistance in cassava. *Plant Physiol. Biochem.* **2018**, *122*, 65–77. https://doi.org/10.1016/j.plaphy.2017.11.016.

178. Vitti, A.; Pellegrini, E.; Nali, C.; Lovelli, S.; Sofo, A.; Valerio, M.; Scopa, A.; Nuzzaci, M. Trichoderma harzianum T-22 Induces Systemic Resistance in Tomato Infected by Cucumber mosaic virus. *Front. Plant Sci.* **2016**, *7*, 1520. https://doi.org/10.3389/fpls.2016.01520.
179. Purwantisari, S.; Priyatmojo, A.; Sancayaningsih, R.P.; Kasiamdari, R.S.; Budihardjo, K. Systemic inducing resistance against late blight by applying antagonist Trichoderma Viride. *J. Physics Conf. Ser.* **2018**, *1025*, 012053. https://doi.org/10.1088/1742-6596/1025/1/012053.

180. Doornbos, R.F.; Geraats, B.P.J.; Kuramae, E.E.; Van Loon, L.C.; Bakker, P.A.H.M. Effects of Jasmonic Acid, Ethylene, and Sali-cyclic Acid Signaling on the Rhizosphere Bacterial Community of *Arabidopsis thaliana*. *Mol. Plant-Microbe Interact.* **2011**, *24*, 395–407. https://doi.org/10.1094/mpmi-05-10-0115.

181. Farag, M.A.; Zhang, H.; Ryu, C.-M. Dynamic Chemical Communication between Plants and Bacteria through Airborne Signals: Induced Resistance by Bacterial Volatiles. *J. Chem. Ecol.* **2013**, *39*, 1007–1018. https://doi.org/10.1007/s10886-013-0317-9.

182. Yang, J.; Kloepper, J.W.; Ryu, C.-M. Rhizosphere bacteria help plants tolerate abiotic stress. *Trends Plant Sci.* **2009**, *14*, 1–4. https://doi.org/10.1016/j.tplants.2008.10.004.

183. Bittel, P.; Robatzek, S. Microbe-associated molecular patterns (MAMPs) probe plant immunity. *Curr. Opin. Plant Biol.* **2007**, *10*, 335–341. https://doi.org/10.1016/j.pbi.2007.04.021.

184. Lorenzo, O.; Solano, R. Molecular players regulating the jasmonate signalling network. *Curr. Opin. Plant Biol.* **2005**, *8*, 532–540. https://doi.org/10.1016/j.pbi.2005.07.003.

185. Von Dahl, C.C.; Baldwin, I.T. Deciphering the Role of Ethylene in Plant–Herbivore Interactions. *J. Plant Growth Regul.* **2007**, *26*, 201–209. https://doi.org/10.1007/s00344-007-0014-4.

186. Choudhary, D.K.; Johri, B.N. Interactions of Bacillus spp. and plants—with special reference to induced systemic resistance (ISR). *Microbiol. Res.* **2009**, *164*, 493–513. https://doi.org/10.1016/j.micres.2008.08.007.

187. Sun, Y.; Xiao, J.; Jia, X.; Ke, P.; He, L.; Cao, A.; Wang, H.; Wu, Y.; Gao, X.; Wang, X. The role of wheat jasmonic acid and ethylene pathways in response to *Fusarium graminearum* infection. *Plant Growth Regul.* **2016**, *80*, 69–77. https://doi.org/10.1007/s10725-016-0147-1.

188. Singh, V.; Singh, D.; Gautam, J.K.; Nandi, A.K. RSI1/FLD is a positive regulator for defense against necrotrophic pathogens. *Physiol. Mol. Plant Pathol.* **2019**, *107*, 40–45. https://doi.org/10.1016/j.pmpp.2019.04.005.

189. Kilic-Ekici, O.; Yuen, G.Y. Comparison of strains of Lysobacter enzymogenes and PGPR for induction of resistance against Bipolaris sorokiniana in tall fescue. *Biol. Control* **2004**, *30*, 446–455. https://doi.org/10.1016/j.biocontrol.2004.01.014.

190. Wang, C.-J.; Yang, W.; Wang, C.; Gu, C.; Niu, D.-D.; Liu, H.-X.; Wang, Y.-P.; Guo, J.-H. Induction of Drought Tolerance in Cucumber Plants by a Consortium of Three Plant Growth-Promoting Rhizobacterium Strains. *PLoS ONE* **2012**, *7*, e52565. https://doi.org/10.1371/journal.pone.0052565.

191. Kohler, J.; Hernández, J.A.; Caravaca, F.; Roldán, A. Plant-growth-promoting rhizobacteria and arbuscular mycorrhizal fungi modify alleviation biochemical mechanisms in water-stressed plants. *Funct. Plant Biol.* **2008**, *35*, 141–151. https://doi.org/10.1071/fp07218.

192. Gupta, G.; Parihar, S.S.; Ahirwar, N.K.; Snehi, S.K.; Singh, V. Plant growth promoting rhizobacteria (PGPR): Current and future prospects for development of sustainable agriculture. *J. Microb. Biochem. Technol.* **2015**, *7*, 096–102.

193. Beneduzi, A.; Ambrosini, A.; Passaglia, L.M. Plant growth-promoting rhizobacteria (PGPR): Their potential as antagonists and biocontrol agents. *Genet. Mol. Biol.* **2012**, *35*, 1044–1051. https://doi.org/10.1590/s1415-47572012000600020.

194. Chowdhury, S.P.; Uhl, J.; Grosch, R.; Alquéres, S.; Pittroff, S.; Dietel, K.; Schmitt-Kopplin, P.; Borriss, R.; Hartmann, A. Cyclic Lipopeptides of *Bacillus amyloliquefaciens* subsp. *plantarum* Colonizing the Lettuce Rhizosphere Enhance Plant Defense Responses Toward the Bottom Rot Pathogen *Rhizoctonia solani*. *Mol. Plant-Microbe Interact.* **2015**, *28*, 984–995. https://doi.org/10.1094/mpmi-03-15-0066-r.

195. Han, S.; Li, D.; Trost, E.; Mayer, K.F.; Vlot, A.C.; Heller, W.; Schmid, M.; Hartmann, A.; Rothballer, M. Systemic Responses of Barley to the 3-hydroxy-decanoyl-homoserine Lactone Producing Plant Beneficial Endophyte *Acidovorax radicis* N35. *Front. Plant Sci.* **2016**, *7*, 1868. https://doi.org/10.3389/fpls.2016.01868.

196. Patil, S.; Bheemaraddi, M.C.; Shivannavar, C.T.; Gaddad, S.M. Biocontrol activity of siderophore producing *Bacillus subtilis* CTS-G24 against wilt and dry root rot causing fungi in chickpea. *IOSR J. Agric. Vet. Sci.* **2014**, *7*, 63–68. https://doi.org/10.9790/2380-07916368.

197. Dunne, C.; Crowley, J.J.; Moënne-Loccoz, Y.; Dowling, D.N.; Bruijn, S.; O'Gara, F. Biological control of *Pythium ultimum* by *Stenotrophomonas maltophilia* W81 is mediated by an extracellular proteolytic activity. *Microbiology* **1997**, *143*, 3921–3931. https://doi.org/10.1099/00221287-143-12-3921.

198. Huang, X.; Liu, J.; Ding, J.; He, Q.; Xiong, R.; Zhang, K. The investigation of nematocidal activity in *Stenotrophomonas maltophilia* G2 and characterization of a novel virulence serine protease. *Can. J. Microbiol.* **2009**, *55*, 934–942. https://doi.org/10.1139/w09-045.

199. Wang, X.; Wei, Z.; Yang, K.; Wang, J.; Jousset, A.; Xu, Y.; Shen, Q.; Friman, V.-P. Phage combination therapies for bacterial wilt disease in tomato. *Nat. Biotechnol.* **2019**, *37*, 1513–1520. https://doi.org/10.1038/s41587-019-0328-3.

200. Shrivastava, P.; Kumar, R. Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. *Saudi J. Biol. Sci.* **2015**, *22*, 123–131. https://doi.org/10.1016/j.sjbs.2014.12.001.

201. Enebe, M.C.; Babalola, O.O. The impact of microbes in the orchestration of plants' resistance to biotic stress: A disease management approach. *Appl. Microbiol. Biotechnol.* **2018**, *103*, 9–25. https://doi.org/10.1007/s00253-018-9433-3.

202. Kumar, A.; Verma, J.P. Does plant-Microbe interaction confer stress tolerance in plants: A review? *Microbiol. Res.* **2018**, *207*, 41–52. https://doi.org/10.1016/j.micres.2017.11.004.
203. Meena, K.K.; Sorty, A.M.; Bitla, U.M.; Choudhary, K.; Gupta, P.; Pareek, A.; Singh, D.P.; Prabha, R.; Sahu, P.K.; Gupta, V.K.; et al. Abiotic Stress Responses and Microbe-Mediated Mitigation in Plants: The Omics Strategies. *Front. Plant Sci.* **2017**, *8*, 172. https://doi.org/10.3389/fpls.2017.00172.

204. Sorty, A.M.; Meena, K.K.; Choudhary, K.; Bitla, U.M.; Minhas, P.S.; Krishnani, K.K. Effect of Plant Growth Promoting Bacteria Associated with Halophytic Weed (*Psoralea corylifolia* L) on Germination and Seedling Growth of Wheat Under Saline Conditions. *Appl. Biochem. Biotechnol.* **2016**, *180*, 872–882. https://doi.org/10.1007/s12010-016-2139-z.

205. Gopalakrishnan, S.; Sathya, A.; Vijayabharathi, R.; Varshney, R.K.; Gowda, C.L.; Krishnamurthy, L. Plant growth promoting rhizobia: Challenges and opportunities. *3 Biotech* **2015**, *5*, 355–377. https://doi.org/10.1007/s13205-014-0241-x.

206. Bhargava, S.; Sawant, K. Drought stress adaptation: Metabolic adjustment and regulation of gene expression. *Plant Breed.* **2013**, *132*, 21–32. https://doi.org/10.1111/pbr.12004.

207. Chaves, M.M.; Flexas, J.; Pinheiro, C. Photosynthesis under drought and salt stress: Regulation mechanisms from whole plant to cell. *Ann. Bot.* **2009**, *103*, 551–560. https://doi.org/10.1093/aob/mcn125.

208. Todaka, D.; Nakashima, K.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Toward understanding transcriptional regulatory networks in abiotic stress responses and tolerance in rice. *Rice* **2012**, *5*, 6. https://doi.org/10.1186/1939-8433-5-6.

209. Qin, F.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Achievements and Challenges in Understanding Plant Abiotic Stress Responses and Tolerance. *Plant Cell Physiol.* **2011**, *52*, 1569–1582. https://doi.org/10.1093/pcp/pcr106.

210. Tiwari, S.; Singh, P.; Tiwari, R.; Meena, K.K.; Yandigeri, M.; Singh, D.P.; Arora, D.K. Salt-tolerant rhizobacteria-mediated induced tolerance in wheat (*Triticum aestivum*) and chemical diversity in rhizosphere enhance plant growth. *Biol. Fertil. Soils* **2011**, *47*, 907–916. https://doi.org/10.1007/s00374-011-0598-5.

211. Atkinson, N.J.; Lilley, C.J.; Urwin, P.E. Identification of Genes Involved in the Response of *Arabidopsis* to Simultaneous Biotic and Abiotic Stresses. *Plant Physiol.* **2013**, *162*, 2028–2041. https://doi.org/10.1104/pp.113.222372.

212. Prasch, C.M.; Sonnewald, U. Simultaneous Application of Heat, Drought, and Virus to *Arabidopsis* Plants Reveals Significant Shifts in Signaling Networks. *Plant Physiol.* **2013**, *162*, 1849–1866. https://doi.org/10.1104/pp.113.221044.

213. Nishiyama, R.; Watanabe, Y.; Leyva-Gonzalez, M.A.; Van Ha, C.; Fujita, Y.; Tanaka, M.; Seki, M.; Yamaguchi-Shinozaki, K.; Shinozaki, K.; Herrera-Estrella, L.; et al. *Arabidopsis* AHP2, AHP3, and AHP5 histidine phosphotransfer proteins function as redundant negative regulators of drought stress response. *Proc. Natl. Acad. Sci. USA* **2013**, *110*, 4840–4845. https://doi.org/10.1073/pnas.1302265110.

214. Peleg, Z.; Blumwald, E. Hormone balance and abiotic stress tolerance in crop plants. *Curr. Opin. Plant Biol.* **2011**, *14*, 290–295. https://doi.org/10.1016/j.pbi.2011.02.001.

215. Xiong, L.; Lee, H.; Ishitani, M.; Zhu, J.-K. Regulation of Osmotic Stress-responsive Gene Expression by theLOS6/ABA1 Locus in *Arabidopsis*. *J. Biol. Chem.* **2002**, *277*, 8588–8596. https://doi.org/10.1074/jbc.m109275200.

216. Gazzarrini, S. Cross-talk in Plant Hormone Signalling: What *Arabidopsis* Mutants Are Telling Us. *Ann. Bot.* **2003**, *91*, 605–612. https://doi.org/10.1093/aob/mcg064.

217. Halo, B.A.; Khan, A.L.; Waqas, M.; Al-Harrasi, A.; Hussain, J.; Ali, L.; Adnan, M.; Lee, I.-J. Endophytic bacteria (*Sphingomonas* sp. LK11) and gibberellin can improve *Solanum lycopersicum* growth and oxidative stress under salinity. *J. Plant Interact.* **2015**, *10*, 117–125. https://doi.org/10.1080/17429145.2015.1033659.

218. Barnawal, D.; Bharti, N.; Pandey, S.S.; Pandey, A.; Chanotiya, C.S.; Kalra, A. Plant growth-promoting rhizobacteria enhance wheat salt and drought stress tolerance by altering endogenous phytohormone levels and *TaCTR1/TaDREB2* expression. *Physiol. Plant.* **2017**, *161*, 502–514. https://doi.org/10.1111/ppl.12614.

219. Kang, S.-M.; Shahzad, R.; Bilal, S.; Khan, A.L.; Park, Y.-G.; Lee, K.-E.; Asaf, S.; Khan, M.A.; Lee, I.-J. Indole-3-acetic-acid and ACC deaminase producing *Leclercia adecarboxylata* MO1 improves *Solanum lycopersicum* L. growth and salinity stress tolerance by endogenous secondary metabolites regulation. *BMC Microbiol.* **2019**, *19*, 80. https://doi.org/10.1186/s12866-019-1450-6.

220. Bharti, N.; Pandey, S.S.; Barnawal, D.; Patel, V.K.; Kalra, A. Plant growth promoting rhizobacteria *Dietzia natronolimnaea* modulates the expression of stress responsive genes providing protection of wheat from salinity stress. *Sci. Rep.* **2016**, *6*, 34768. https://doi.org/10.1038/srep34768.

221. Kang, S.-M.; Khan, A.L.; Waqas, M.; You, Y.-H.; Kim, J.-H.; Kim, J.-G.; Hamayun, M.; Lee, I.-J. Plant growth-promoting rhizobacteria reduce adverse effects of salinity and osmotic stress by regulating phytohormones and antioxidants in *Cucumis sativus*. *J. Plant Interact.* **2014**, *9*, 673–682. https://doi.org/10.1080/17429145.2014.894587.

222. Zhao, L.; Zhang, Y.-Q. Effects of phosphate solubilization and phytohormone production of *Trichoderma asperellum* Q1 on promoting cucumber growth under salt stress. *J. Integr. Agric.* **2015**, *14*, 1588–1597. https://doi.org/10.1016/s2095-3119(14)60966-7.

223. He, A.; Niu, S.; Yang, D.; Ren, W.; Zhao, L.; Sun, Y.; Meng, L.; Zhao, Q.; Paré, P.W.; Zhang, J. Two PGPR strains from the rhizosphere of Haloxylon ammodendron promoted growth and enhanced drought tolerance of ryegrass. *Plant Physiol. Biochem.* **2021**, *161*, 74–85. https://doi.org/10.1016/j.plaphy.2021.02.003.

224. Jochum, M.; McWilliams, K.; Borrego, E.J.; Kolomiets, M.V.; Niu, G.; Pierson, E.A.; Jo, Y.-K. Bioprospecting Plant Growth-Promoting Rhizobacteria That Mitigate Drought Stress in Grasses. *Front. Microbiol.* **2019**, *10*, 2106. https://doi.org/10.3389/fmicb.2019.02106.

225. Saakre, M.; Baburao, T.M.; Salim, A.P.; Ffancies, R.M.; Achuthan, V.P.; Thomas, G.; Sivarajan, S.R. Identification and Characterization of Genes Responsible for Drought Tolerance in Rice Mediated by *Pseudomonas fluorescens*. *Rice Sci.* **2017**, *24*, 291–298. https://doi.org/10.1016/j.rsci.2017.04.005.
226. Begum, N.; Wang, L.; Ahmad, H.; Akhtar, K.; Roy, R.; Khan, M.I.; Zhao, T. Co-inoculation of Arbuscular Mycorrhizal Fungi and the Plant Growth-Promoting Rhizobacteria Improve Growth and Photosynthesis in Tobacco Under Drought Stress by Up-Regulating Antioxidant and Mineral Nutrition Metabolism. *Microb. Ecol.* **2021**, *83*, 971–988. https://doi.org/10.1007/s00248-021-01815-7.

227. Chatterjee, P.; Kanagendran, A.; Samaddar, S.; Pazouki, L.; Sa, T.-M.; Niinemets, Ü. Influence of Brevibacterium linens RS16 on foliage photosynthetic and volatile emission characteristics upon heat stress in *Eucalyptus grandis*. *Sci. Total Environ.* **2020**, *700*, 134453. https://doi.org/10.1016/j.scitotenv.2019.134453.

228. Mukhtar, T.; Rehman, S.U.; Smith, D.; Sultan, T.; Seleiman, M.F.; Alsadon, A.A.; Amna, Ali, S.; Chaudhary, H.J.; Solieman, T.H.I.; et al. Mitigation of Heat Stress in Solanum lycopersicum L. by ACC-deaminase and Exopolysaccharide Producing *Bacillus cereus*: Effects on Biochemical Profiling. *Sustainability* **2020**, *12*, 2159. https://doi.org/10.3390/su12062159.

229. Sukkasem, P.; Kurniawan, A.; Kao, T.-C.; Chuang, H.-W. A multifaceted rhizobacterium *Bacillus licheniformis* functions as a fungal antagonist and a promoter of plant growth and abiotic stress tolerance. *Environ. Exp. Bot.* **2018**, *155*, 541–551. https://doi.org/10.1016/j.envexpbot.2018.08.005.

230. Sarkar, J.; Chakraborty, B.; Chakraborty, U. Plant Growth Promoting Rhizobacteria Protect Wheat Plants Against Temperature Stress Through Antioxidant Signalling and Reducing Chloroplast and Membrane Injury. *J. Plant Growth Regul.* **2018**, *37*, 1396–1412. https://doi.org/10.1007/s00344-018-9789-8.

231. El-Daim, I.A.A.; Bejai, S.; Meijer, J. *Bacillus velezensis* 5113 Induced Metabolic and Molecular Reprogramming during Abiotic Stress Tolerance in Wheat. *Sci. Rep.* **2019**, *9*, 1–18. https://doi.org/10.1038/s41598-019-52567-x.

232. Tiwari, S.; Prasad, V.; Chauhan, P.S.; Lata, C. *Bacillus amyloliquefaciens* Confers Tolerance to Various Abiotic Stresses and Modulates Plant Response to Phytohormones through Osmoprotection and Gene Expression Regulation in Rice. *Front. Plant Sci.* **2017**, *8*, 1510. https://doi.org/10.3389/fpls.2017.01510.

233. Caradonia, F.; Francia, E.; Morcia, C.; Ghizzoni, R.; Moulin, L.; Terzi, V.; Ronga, D. Arbuscular Mycorrhizal Fungi and Plant Growth Promoting Rhizobacteria Avoid Processing Tomato Leaf Damage during Chilling Stress. *Agronomy* **2019**, *9*, 299. https://doi.org/10.3390/agronomy9060299.

234. Su, F.; Jacquard, C.; Villaume, S.; Michel, J.; Rabenoelina, F.; Clément, C.; Barka, E.A.; Dhondt-Cordelier, S.; Vaillant-Gaveau, N. Burkholderia phytofirmans PsJN reduces impact of freezing temperatures on photosynthesis in *Arabidopsis thaliana*. *Front. Plant Sci.* **2015**, *6*, 810. https://doi.org/10.3389/fpls.2015.00810.

235. Pramanik, K.; Mitra, S.; Sarkar, A.; Maiti, T.K. Alleviation of phytotoxic effects of cadmium on rice seedlings by cadmium resistant PGPR strain *Enterobacter aerogenes* MCC 3092. *J. Hazard. Mater.* **2018**, *351*, 317–329. https://doi.org/10.1016/j.jhaz-mat.2018.03.009.

236. Zafar-Ul-Hye, M.; Naeem, M.; Danish, S.; Khan, M.J.; Fahad, S.; Datta, R.; Brtnicky, M.; Kintl, A.; Hussain, G.S.; El-Esawi, M.A. Effect of Cadmium-Tolerant Rhizobacteria on Growth Attributes and Chlorophyll Contents of Bitter Gourd under Cadmium Toxicity. *Plants* **2020**, *9*, 1386. https://doi.org/10.3390/plants9101386.

237. Bilal, S.; Shahzad, R.; Imran, M.; Jan, R.; Kim, K.M.; Lee, I.-J. Synergistic association of endophytic fungi enhances Glycine max L. resilience to combined abiotic stresses: Heavy metals, high temperature and drought stress. *Ind. Crop. Prod.* **2020**, *143*, 111931. https://doi.org/10.1016/j.indcrop.2019.111931.

238. Mesa-Marín, J.; Del-Saz, N.F.; Rodríguez-Llorente, I.D.; Redondo-Gómez, S.; Pajuelo, E.; Ribas-Carbó, M.; Mateos-Naranjo, E. PGPR Reduce Root Respiration and Oxidative Stress Enhancing *Spartina maritima* Root Growth and Heavy Metal Rhizoaccumulation. *Front. Plant Sci.* **2018**, *9*, 1500. https://doi.org/10.3389/fpls.2018.01500.

239. Gururani, M.A.; Upadhyaya, C.P.; Baskar, V.; Venkatesh, J.; Nookaraju, A.; Park, S.W. Plant Growth-Promoting Rhizobacteria Enhance Abiotic Stress Tolerance in Solanum tuberosum Through Inducing Changes in the Expression of ROS-Scavenging Enzymes and Improved Photosynthetic Performance. *J. Plant Growth Regul.* **2013**, *32*, 245–258. https://doi.org/10.1007/s00344-012-9292-6.

240. Armendariz, A.L.; Talano, M.A.; Nicotra, M.F.O.; Escudero, L.; Breser, M.L.; Porporatto, C.; Agostini, E. Impact of double inoculation with Bradyrhizobium japonicum E109 and *Azospirillum brasilense* Az39 on soybean plants grown under arsenic stress. *Plant Physiol. Biochem.* **2019**, *138*, 26–35. https://doi.org/10.1016/j.plaphy.2019.02.018.

241. Singh, R.P.; Usha; Rizvi, S.M.H.; Sonia; Jaiwal, P.K. *Genetic Engineering for Enhancing Abiotic Stress Tolerance*; Springer: Dordrecht, The Netherlands, 2003; pp. 223–243. https://doi.org/10.1007/978-94-017-0109-9_10.

242. Hrynkiewicz, K.; Zloch, M.; Kowalkowski, T.; Baum, C.; Niedojadło, K.; Buszewski, B. Strain-Specific bioaccumulation and intracellular distribution of Cd²⁺ in bacteria isolated from the rhizosphere, ectomycorrhizae, and fruitbodies of ectomycorrhizal fungi. *Environ. Sci. Pollut. Res.* **2015**, *22*, 3055–3067. https://doi.org/10.1007/s11356-014-3489-0.

243. Chauhan, P.S.; Lata, C.; Tiwari, S.; Chauhan, A.S.; Mishra, S.K.; Agrawal, L.; Chakrabarty, D.; Nautiyal, C.S. Transcriptional alterations reveal *Bacillus amyloliquefaciens* -rice cooperation under salt stress. *Sci. Rep.* **2019**, *9*, 1–13. https://doi.org/10.1038/s41598-019-48309-8.

244. Nadeem, S.M.; Zahir, Z.A.; Naveed, M.; Nawaz, S. Mitigation of salinity-induced negative impact on the growth and yield of wheat by plant growth-promoting rhizobacteria in naturally saline conditions. *Ann. Microbiol.* **2013**, *63*, 225–232. https://doi.org/10.1007/s13213-012-0465-0.