Abstract
Quorum sensing is a widespread mechanism in enormous number of bacteria for regulating various gene expression in a cell density-dependent manner through production and recognition of small molecules known as autoinducer. Diverse kinds of quorum-sensing networks are found in different bacterial species. Among various signal molecules, acyl homoserine lactone (AHL) signal molecules are the most and widely studied in bacteria. A number of simple to advanced techniques are being used to identify and characterize signal molecules. Production of signal molecules in a number of rhizospheric bacteria is documented. Rhizosphere is an active atmosphere where microbe-microbe and microbe-plant interaction is highest due to rich availability of nutrients provided in the form of root exudates. Several ecological and interdependent key characters of bacteria, like antibiotic, siderophore, or enzyme secretion, virulence factors of phytopathogens, as well as plant-microbe communications, are coordinated through quorum sensing (QS). In this chapter, we have provided brief fundamental aspects of quorum sensing and then addressed the recent trends on the significance of quorum sensing and signal molecules in microbe-microbe and microbe-plant interactions in the rhizosphere with special reference to plant growth-promoting rhizobacteria and plant health.
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16.1 Introduction
Since ages, scientist believed that the single cell prokaryotic bacterium lacking true nucleus is not capable of establishing a fundamental form of community attitude as a consequence of chemical conversation between the members of a community. Interdependent behavior by means of autoinducer compounds was first discovered in bacteria which are living in symbiotic association with a marine squid (Kaplan and Greenberg 1985; Verma and Miyashiro 2013). The fundamental part of this molecular conversation, termed as “quorum sensing” (QS), and the signaling molecules implicated were established through an extremely basic test: via adding together a formally habituated supernatant of a heavily developed bacterial culture to a fresh, low concentration culture, the characteristics of the high density culture were conferred (Eberhard 1972; Waters and Bassler 2005). The signaling compounds implicated in this conversation are called as “autoinducers,” as they were derived from within the bacterial cell and controlling their individual expression. The signaling compound can be perceived and reimported into these cells, consequently permitting the whole inhabitants to react to altering situation/necessities once a significant volume (equivalent to a particular cell density) or “quorum,” i.e., the minimum number of bacterial cell accumulated in a given volume to make the “decision” to switch on gene expression of QS-regulated genes, is achieved as described by Ahmad et al. (2011).
The marine bacterium Vibrio fischeri was the first bacterium to be examined for quorum sensing. As a communication compound, N-(3-oxo)-hexanoyl-L-homoserine lactone (3oxoC6-HSL) was recognized to regulate bioluminescence as a readily assessable result of supportive action. Currently, numerous chemical signaling compounds of bacterial origin have been recognized. AHL served as a universal signal molecule within Gram-negative bacteria (Galloway et al. 2011). Molecules of AHL are created by LuxI homologues, and comprise, clearly with LuxR homologues, a transcriptional regulator. AHL comprises a conserved homoserine lactone ring with an uneven N-acyl chain (Ahmad et al. 2008). Bacteria belonging to both Gram-positive and Gram-negative groups use QS messaging pathways to control a different group of physiological behavior of bacterial cells which includes symbiosis, competence, virulence, antibiotic production, conjugation, motility, sporulation, and biofilm formation (Rutherford and Bassler 2012).
Universally, Gram-negative bacteria utilize acylated homoserine lactones as autoinducers, and Gram-positive bacteria exploit processed oligopeptides for interaction (Miller and Bassler 2001). Commonly studied autoinducer signals are N-acyl homoserine lactones (von Bodman et al. 2003), although half a dozen of other molecules, including diketopiperazines, 4-hydroxy-2-alkylquinolines (HAQs), and autoinducer-3 (AI-3) in various Gram-negative bacteria (Jimenez et al. 2012), furanosyl borate diester in Vibrio harveyi (Chen et al. 2002), and c-butyrolactone in Streptomyces, have also been involved in quantity-based signaling (Yamada and Nihira 1998). While quorum-sensing peptides (QSPs) are especially reported from Gram-positive bacteria (Wynendaele et al. 2013), autoinducer-2 (AI-2) has been reported from both Gram-positive and Gram-negative bacteria (Pereira et al. 2013). Recently, Papenfort and Bassler (2016) have reviewed these aspects in much detail.
Various procedures and protocols used for finding and depiction of signal molecules are described by several authors as compiled by Rumbaugh (2011). Many simple techniques such as bioassays and chemical techniques such as thin-layer chromatography (TLC) and chromatographic and spectroscopic methods are regularly employed for recognition and classification of signal molecules (Gonzalez and Keshavan 2006; Kendall and Sperandio 2007). Fascinatingly, secretion of quorum-sensing interfering (QSI) molecules by eukaryotic microbes has created huge curiosity within the researchers because such molecules are capable of influencing the bacterial signaling system positively or negatively. In contrast, production of structural homologues to the many QS signal compounds has resulted in the improvement of additional QSI molecules that can be employed to manage pathogenic bacteria. Additionally, the construction of transgenic plants to facilitate the expression of bacterial QS genes until now is an effective approach to meddle with bacterial activities (Fray 2002; Hartmann and Schikora 2012).
The rhizosphere comprises an elevated amount of AHL-secreting bacteria in comparison to bulk soil, signifying their position in colonization (Elasri et al. 2001). This advocates that plants might be employing root-exuded molecules in the rhizosphere to obtain benefit of this bacterial information structure and control colonizing populations (Lugtenberg and Kamilova 2009; Lopez-Raez et al. 2012). Exudates from pea seedlings comprise compounds that impersonate components of QS molecules which advocate that plants are capable of selecting their microbial colleagues (Teplitski et al. 2000; Fatima et al. 2010). Perez-Montano et al. (2013) documented that Oryza sativa and Phaseolus vulgaris roots and seeds secrete molecules which exclusively meddle with the capability of plant-associated bacteria to develop biofilms, a crucial feature for bacteria-eukaryotic host communication. Plant host species have developed responses to AHLs. Medicago truncatula on contact to a broad concentration series of AHLs responded with a primary decline in different protein volume followed by increase of the same proteins afterward (Mathesius et al. 2003; Hartmann and Schikora 2012). A number of these proteins involved members of cytoskeleton structure/function, defense/stress response, isoflavone production, and metabolic enzyme families. This presents an interesting area of research as to how bacteria communicate among themselves and how plants have developed mechanisms to react to these signal compounds.
In the recent past, many articles and scientific literature have been published on the specific and general aspects of quorum sensing in plant pathogens and beneficial rhizobacteria (Singh et al. 2012; Hartmann and Schikora 2012; Hartmann et al. 2014; Kalia 2015; Schikora et al. 2016). In this chapter, we have reviewed extensive and updated literature to address the role of quorum sensing in plant growth-promoting rhizobacteria (PGPR), possible interaction mechanisms, and signaling in the rhizosphere relative to plant-microbe interaction.
16.2 Diversity of Quorum-Sensing Signal Molecules and Its Detection
Various types of quorum-sensing network, its regulatory mechanism involved in production of signal molecules, and gene expression have been reviewed by various workers (Atkinson and Williams 2009; Papenfort and Bassler 2016) and are not the subject for discussion of this chapter. However, we have briefly summarized here important aspect. Among different Gram-negative bacteria, biosynthesis of N-acyl homoserine lactones (HSL) takes place in several deviations of the molecular structure. The range of HSL molecules varies from short (C4-, C6-, and C8-) carbohydrate side chains to long (C12-, C14-, or even longer) side chains and consists of unsubstituted in addition to OH- and oxo-C3-substituted compounds. Despite the fact that HSLs are the universal autoinducers in Gram-negative bacteria, arrangements like AI-2 (alternative autoinducer; furanosyl borate diester), AI3, and quinolones (PQS) and a range of extra minute compounds are known as signaling molecules (Effmert et al. 2012). Additionally, lipid compounds, like cis-11-methyl-2-dodecenoic acid (also called as diffusible signal factor or DSF) (Wang et al. 2004a) and 3-hydroxy-palmitate methyl ester (3OH-PAME) (Flavier et al. 1997), have been recognized as QS-mediating molecules. Moreover, cyclic compounds, such as 2-heptyl-3-hydroxy-4-quinolone (PQS) and diketopiperazines (DKZ), also have been recommended as QS signals of Pseudomonads (Holden et al. 1999; McKnight et al. 2000). In Gram-positive bacteria, a range of incomplete cyclic peptides, AI-2 and butyrolactone, control cellular functions and activities via perceiving the cell quantity. AI-2 was anticipated as a “universal” QS indicator in bacteria, but this task is still uncertain since it might just be a secreted product of a common metabolic network (Folcher et al. 2001; Winzer et al. 2002; Lyon and Novick 2004). Diverse types of quorum-sensing molecules and their corresponding producing bacteria are presented in Table 16.1.
Cell-to-cell communication between rhizosphere microbes probably takes place universally since several strains obtained from the rhizosphere have been documented to produce QS signals. For instance, it has become evident that a diversity of proteobacterial rhizosphere isolates secrete and/or react to N-acyl homoserine lactone (AHL) QS signals, together with strains associated to species or genera of Pseudomonas chlororaphis, Pseudomonas putida, Pseudomonas syringae, Burkholderia, Serratia, Erwinia, and Ralstonia, in addition to rhizobial species (Ferluga et al. 2008). AHLs have also developed to work as interkingdom messenger molecules affecting plant gene interpretation, the initiation of systemic plant resistance, and influencing plant growth and development (Venturi and Fuqua 2013). In recent times, new categories of signals (e.g., pyrones and dialkylresorcinols) secreted by Gram-negative bacteria have been revealed which are predicted by LuxR proteins and found to be strongly connected to the AHL-responsive LuxR family (Brameyer et al. 2015); it is at present unidentified whether these signals are formed by rhizobacteria. One more group of QS signals in Gram-negative bacteria is the DSF family (diffusible signal factor, which are cis-2-unsaturated fatty acids); more bacterial species are presently being identified which generate DSF, together with rhizosphere-inhabiting species such as Burkholderia spp. and Stenotrophomonas maltophilia (Ryan et al. 2015). Fascinatingly, bacterial DSF signal molecules have also been currently resolved to bring about innate immunity in plants, therefore performing as interkingdom signal molecules (Kakkar et al. 2015). Several Gram-positive bacterial inhabitants in the rhizosphere utilize peptides (also known as pheromones) as QS signaling compounds; probably these molecules participate in numerous regulatory functions both at the intra- and interspecies level (Bassler 2002; Monnet et al. 2016).
An accurate, exact, and responsive chemical examination of quorum-sensing autoinducer compounds was a necessary requirement for novel studies of quorum-sensing-associated regulation in bacteria. By employing these methods, a detailed tracking of these QS compounds in the habitat and inside eukaryotic cell, populated by HSL-producing bacteria, was made possible (Gotz et al. 2007; Hartmann and Schikora 2012). In case of quorum-sensing compounds pertaining to N-acyl homoserine lactone group, it has been proved lucky for the progress of study in this area that the first accessible chromatographic tools were soon aided by extremely sensitive and specific biosensors. These biosensors get benefit of the careful establishment of promoters of HSL-regulated genes by autoinducer molecules. Different existing operon fusion constructs of HSL-activated genes with the lux-casette, gfp, rfp, or lacZ have been evaluated by Fekete et al. (2010b). Additionally, the quorum-sensing-controlled violacein secretion by Chromobacterium violaceum can be utilized effectively to initiate HSL production or deterioration, respectively (McClean et al. 1997). The indicated constructs are also present on plasmids and can be transmitted to other bacteria. On the other hand, HSL-biosensor bacteria should contain their personal HSL-secreting genes deleted or inactivated to circumvent self-activation. The constructs generally have different precision for both short and long side chain HSLs, but there are also reporter plasmids that permit recognition of most HSLs with comparable sharpness (Thomson et al. 2000; Andersen et al. 2001). However, one has to be cautious in the utilization of these biosensors, as their report may be somewhat partial and has to be incremented with other resources of chemical or immunological metabolite analysis. The existence of HSLs in definite environments and their ecological importance have been encouraged by the use of green fluorescent protein (GFP) or red fluorescent protein/DsRed (RFP) stuck to HSL-regulated promoters. The potency of HSL down to 20 nmol l−1 can be identified by means of these bioreporter constructs. However, this recognition is relatively discriminatory, because, for example, in the case of the reporter strain Pseudomonas putida F117, the confined reporter plasmid pAS-C8 is 100 times extra susceptible to 3-oxo-C12-HSL than C12-HSL (Steidle et al. 2001). Using these constructs, the in situ secretion of HSL compounds can be, for example, discovered on the surface of roots, consequently ensuing in the regulation of “landscapes” of HSLs on occupied surfaces (Gantner et al. 2006).
In microcolonies or polymer matrix-surrounded biofilms, where the dispersion is limited, the local concentration of HSLs can reach high peak values. By using mathematical models for the computation of the autoregulated HSL secretion in bacteria and restricted dispersion (Muller et al. 2006), local concentrations in the mmol l−1 range can be calculated, accepting just a volume of a 5-μm cube with enclosed Burkholderia cepacia. This fact can have ecological importance for communication with eukaryotic hosts inhabited by HSL-producing bacterial microcolonies or biofilms that could also add to compensate the potential deterioration of HSL by quorum-quenching reactions. With reference to chemical analysis, GC-based methods of HSL quantification were established first. To amplify the sensitivity of the technique, for example, selective ion monitoring of the mass spectrometry (MS) detection or derivatization of the ß-oxo group to an oxime was applied (Charlton et al. 2000). As analyzed by Fekete et al. (2007), reversed-phase HPLC coupled with MS for selective detection has been useful in nearly all cases (Morin et al. 2003). Frommberger et al. (2004) established a micro-electrospray interface to MS after nano-LC separation of the HSLs. Electrokinetic chromatography (MEKC) also has been employed effectively for the recognition of HSLs and detection by MS. The most effective separation of HSLs is with UPLC analysis, as described in detail by Li et al. (2006). The classification of enantiomers of HSLs in biological matrices also is achievable by means of an optimized GC-MS approach (Malik et al. 2009). The maximum precision of molecular mass detection of HSLs has been completed by using the positive ion Fourier transform ion cyclotron resonance mass spectrometry (FTICR-MS) with mass errors of the peaks less than 0.1 ppm, as described by Fekete et al. (2007).
Nevertheless, still after employing this highly resolving analytical instrument, it is suitable to use two independent analytical approaches (e.g., UPLC and FTICR-MS) to clearly recognize HSL molecules, particularly when the recognition is from very complex matrices, such as nutrient broth medium, frequently used in microbiology (Hartmann and Schikora 2012). One more autonomous technique for the examination of HSL molecules is based on immunochemistry. From several labs, monoclonal antibodies (MAB) have been produced against several HSL molecules (Kaufmann et al. 2006, 2008; Chen et al. 2010a, b). These MABs not only allow the research of the biological impact of scavenging HSL but also the investigation of reduced sample sizes and the localization of the allocation of HSL secreted by bacteria connected with eukaryotes (Park et al. 2007; Hartmann and Schikora 2012). For more details, readers are being suggested to read specific review article on the subject (Rumbaugh 2011).
16.3 Quorum Sensing in Plant Growth-Promoting Rhizobacteria
Quorum sensing provides a great competing benefit to bacteria enhancing their likelihood to stay alive, while they can explore more difficult habitats. QS in bacterial conversation is connected with the manufacturing and discharge of signal molecules, termed autoinducers, into the surrounding medium. On recognition of the signal compounds at a given concentration, transcription of definite genes controlled by this system is stimulate or withdrawn in the bacteria. There are different microbial mechanisms regulated by QS which include DNA transferase by conjugation, bioluminescence, siderophore production, biofilm formation, and moving ability of some bacteria, also termed as “swarming” (Fray 2002; Barriuso et al. 2008b). Streptomycetes, with high G+C-content, have been shown to control spore development as well as antibiotic manufacturing by a quorum-sensing indicator called A-factor. The separation of AHLs from bacteroids of R. leguminosarum advocates that quorum sensing might play a role in the mature nodule (Daniels et al. 2002). It is hypothesize that quorum sensing influences population flow in connection with host plants. Both siderophores and HSLs have been recommended to participate as chemical signal molecules for interspecies conversation among bacteria (Guan and Kamino 2001). However, insufficient information is available related to interspecies conversation in the natural microbial habitat. Mathesius et al. (2003) documented better discharge of AHL mimics in exudates of Medicago truncatula. The chemical composition of such active quorum sensing mimicking secondary metabolites is presently unidentified and also needs additional explanation (Teplitski et al. 2000; Chen et al. 2002; Podile et al. 2014).
QS-regulated gene expression is based not only on signal compounds but also on bacterial population thickness (Williams 2007). The requirement for a minimum level of the primary PGPR inocula to promote plant growth considerably sustains the thought that quorum sensing by microorganisms participates in plant-rhizobacteria communications (Persello-Cartieaux et al. 2003). Bacteria can respond to QS-like molecules secreted by other rhizospheric bacteria (Steidle et al. 2001) and by plants (Teplitski et al. 2000) and even eradicate the QS signal compounds secreted by other bacterial species (Dong et al. 2002). Other than producing regulatory peptides, Bacillus secretes enzymes to degrade the AHL moieties produced by Gram-negative bacteria. Genes encrypting for AHL-degrading enzymes, aiiA, have been established in B. thuringiensis and different subspecies (Lee et al. 2002). The occurrence of such proteins permits Bacillus strains to split the lactone bond of AHLs via hydrolysis, signifying a method for autoinducer-degrading activity, permitting these bacteria to struggle with other Gram-negative bacteria. Bacterial functions in the rhizosphere can, therefore, be changed directly by plants or other microorganisms via QS molecules (Podile et al. 2014).
In addition to motility and QS, bacterial major outer membrane protein (MOMP) also performs a crucial task in initial host identification. The MOMP of Azospirillum brasilense demonstrated better adhesion factor to exudates of cereals than exudates of legumes and tomatoes and could work as a bond implicated in root adsorption and cell accumulation of the bacterium (Burdman et al. 2001). Bacterial lipopolysaccharides (LPS), particularly the O-antigen chain, can also cooperate in root habitation (Dekkers et al. 1998a, b). On the other hand, it is strain related since the O-antigenic side chain of Pseudomonas fluorescens WCS374 does not help in potato root attachment (De Weger et al. 1989), while the O-antigen chain of P. fluorescens PCL1205 is implicated in tomato root colonization (Dekkers et al. 1998b). Several workers (Simons et al. 1996; Dekkers et al. 1998a; Compant et al. 2010) also reported that high bacterial growth rate and capability to produce vitamin B1 and secrete NADH dehydrogenases help in plant colonization.
Endophytes comprising a vital constituent of plant structure are frequently reported assisting in plant defense reactions by quorum-preventing methods. Fascinatingly however, endophytes are repeatedly observed to have quorum-sensing mechanisms that permit them to sustain their own inhabitation in host plants and counteract plant pathogens. For instance, strain PsJNT is described to set up endophytic relations with different plants and acknowledged to develop plant-rooting structure with improved vascular arrangements, enhance quantity of chlorophyll and phytohormones, and offer resistance to phytopathogens. Fascinatingly, Burkholderia phytofirmans strain PsJNT was reported to secrete quorum autoinducer 3-hydroxy-C8-homoserine lactone (Sessitsch et al. 2005). In addition, endophytic Serratia plymuthica with enormous biological control capability was found to hold high amount of homoserine lactone (HSL), namely, C4-HSL, C5-HSL, C6-HSL, C7-HSL, C8-HSL, 3-oxo derivatives (3-oxo-C6-HSL, 3-oxo-C7-HSL, 3-oxo-C8 HSL), and 3-hydroxy derivatives (3-hydroxy-C6-HSL, 3-hydroxy-C8-HSL). These AHL molecules were due to two quorum-sensing mechanisms in S. plymuthica (Liu et al. 2011). Additionally, the olive plant epiphyte (Pantoea agglomerans) and endophyte (Erwinia toletana) linked with olive knot infection were observed for the discharge of signals analogous to AHLs. This chemical communication changed the virulence of pathogen Pseudomonas savastanoi pv. savastanoi blamed for olive knot. This work is an illustration of tripartite connections among plant and connected microbes (Hosni et al. 2011).
The genome sequence of endophytic Gluconacetobacter diazotrophicus PAL5 based on Saccharum officinarum exposed the existence of quorum-sensing mechanisms and identification of eight AHLs, viz., C6, C8, C10, C12, and C14-HSL (Nieto-Penalver et al. 2012). A current description from Dourado et al. (2013) demonstrated the exploitation of quorum-sensing compounds for Methylobacterium (famous for displaying endophytic lifestyle) communications with plants. A series of genes were up- and downregulated in Methylobacterium and host plant at the same time facilitating colonization and symbiotic relations, presenting the reliance of plant-endophyte relations on quorum-sensing mechanisms. Rhizobacteria are extensively recognized to improve production of plants by nitrogen fixation and production of siderophores and phytohormone, decrease plant stress, induce systemic resistance, and have capability to attenuate phytopathogenic signals (Liu et al. 2012). Thus, maintaining quorum-sensing mechanisms and autoinducers may allow the endophytic isolates to talk with other connected endophytes in addition to the host plant, thus preserving symbiotic relationship and habitation inside the inner tissues of plants. Surely, there is a deficiency of information on such organization, which needs to be examined in deepness to search for the possible plant physiological modifications and resistance reactions such as release of ethylene, salicylic acid, and defense proteins during the initial stages of colonization.
16.4 Recent Reports on Quorum-Sensing-Associated Functions in Plant Growth-Promoting Bacteria
The rising demand for food and the apprehension related to food quality are the compelling activities advancing to new approaches in agriculture. An effective plant protection mechanism possesses a huge potential to make certain an adequate and high-quality food delivery. Biocontrol agents are well recognized and widely used; however their potential is not yet fully exploited. These days numerous products based on bacterial inoculum, primarily consisting of Bacillus, Pseudomonas, or Serratia spp., arrived at the market. The use of N2-fixing Rhizobia (e.g., Sinorhizobium meliloti), with improved secretion of specific AHLs, might augment the useful effects of bacteria and increase the effect to plant species generally not connected with the specific strain (Zarkani et al. 2013; Hernandez-Reyes et al. 2014). Further, a better comprehension of the communication among bacterial quorum-sensing compounds and eukaryotic host cells can unlock novel strategies in agriculture. Throughout the infection procedure, QS molecules administer the bacterial capability to form biofilms and other density-regulated traits. Those compounds participate in key role in the communication among bacterial and plant cells. Several workers documented the role of quorum sensing in plant disease control and phytopathogen transmission. Some of the reports are summarized briefly.
Barriuso et al. (2008a) reported the role of N-acyl-homoserine lactone (AHL) quorum-sensing signaling compounds in plant growth promotion and the initiation of defense against salt stress. They utilized two Gram-negative, plant growth-promoting rhizobacteria, designated as M12 and M14, and were identified by 16S rDNA sequencing as Burkholderia graminis species. Both strains were found to produce a diversity of N-acyl-homoserine lactone (AHL) quorum-sensing signaling compounds. AHL generation was examined in vitro by thin-layer chromatography by applying AHL biosensors, and the characteristic of the AHLs produced was decided by liquid chromatography-tandem mass spectrometry. The in situ secretion of AHLs by M12 and M14 in the rhizosphere of Arabidopsis thaliana plants was distinguished by co-inoculation with green fluorescent protein-based biosensor strains and confocal laser scanning microscopy. To establish both plant growth promotion and defense against salt stress, these PGPRs were examined on wild-type tomato plants, in addition to their matching transgenics expressing YenI (short-chain AHL producers) and LasI (long-chain AHL producers). In wild-type tomato plants, it was found that only M12 improved the plant growth and this result vanished in both transgenic lines. On the opposing, M14 did not encourage development in wild-type tomatoes but did so in the LasI transgenic line. Resistance to salt stress was stimulated by M14 in wild-type tomato, but this outcome vanished in both transgenic lines. The strain M12, however, did not stimulate salt resistance in wild-type tomato but did so in LasI tomato plants. These outcomes disclose that AHL QS signaling compounds decide the capability of both PGPR strains M12 and M14 to enhance plant growth and to activate protection against salt stress.
Johnson and Walcott (2013) reported that Acidovorax citrulli convert from saprobic to pathogenic growth for seed-to-seedling distribution of bacterial fruit blotch (BFB) of cucurbits; they speculate that quorum sensing was implicated in the regulation of this procedure. Using aacI (luxI homologue) and aacR (luxR homologue) mutants of AAC00-1, they examined the task of QS in watermelon seed colonization and seed-to-seedling distribution of BFB. aacR and aacI mutants of AAC00-1 inhabited germinating watermelon seed at wild-type levels; on the other hand, BFB seed-to-seedling distribution was influenced in a cell thickness-attached approach. There were no important distinctions in BFB seedling transmission among watermelon seed penetrated with approximately 1 × 106 CFU of AAC00-1, the aacR or aacI deletion mutants (95.2, 94.9, and 98.3% BFB occurrence, correspondingly). On the contrary, when seed inoculum was decreased in the order of 1x103 CFU seed−1, BFB seed-to-seedling transmission dropped to 34.3% for the aacI mutant, which was considerably low than the wild type (78.6%). Fascinatingly, BFB seed-to-seedling distribution for the aacR mutant was not significantly unusual to the wild-type strain. This information advocates that QS takes part in the regulation of genes implicated in seed-to seedling spreading of BFB.
Alavi et al. (2013) accounted the role of DSF quorum-sensing system in controlling the progressive impact of Stenotrophomonas maltophilia on plants. They reported that the quorum-sensing molecule DSF (diffusible signal factor) is accountable for the directive of phenotypes in pathogenic Stenotrophomonas; to date, no helpful results were documented to be managed by it. They examined the role of DSF in the plant growth-promoting model strain S. maltophilia R551-3 using functional and transcriptomic analyses. For this intention, these workers correlated the wild-type strain with a mutant deficient in the rpfF (regulation of pathogenicity factors) gene that is necessary for the synthesis of DSF. Oilseed rape seeds coated with the wild-type strain demonstrated a statistically significant enhancement in germination rate compared with those coated with the rpfF mutant. Likewise, the wild-type strain displayed improved plant growth promotion and a better effectiveness in colonizing oilseed rape compared to the mutant strain. Furthermore, only the wild type was competent of establishing organized cell masses both in vitro and in the rhizosphere, a quality decided by DSF. Gene transcription analyses revealed that many genes documented to participate in plant inhabitation (e.g., cell motility, chemotaxis, multidrug efflux pumps, biofilm formation) are controlled by the rpf/DSF system in S. maltophilia. Additionally, these workers discovered novel prospective traits of spermidine, mainly for both growth enhancement and stress protection. In general, these results elucidated an association among the regulation of DSF and the constructive communication outcome with the plant host.
Zuniga et al. (2013) evaluated that by using appropriate mutant strains of Burkholderia phytofirmans PsJN, data can be acquired showing the significance of N-acyl homoserine lactone-mediated quorum sensing in well-organized inhabitation of Arabidopsis thaliana plants and the organization of an advantageous communication. These workers also noticed that bacterial deterioration of the auxin indole-3-acetic acid (IAA) takes part in plant growth-promoting characters and is crucial for successful root colonization.
Perez-Montano et al. (2014) found that bacterial surface components, particularly exopolysaccharides, in association with bacterial quorum-sensing molecules are vital for the formation of biofilms within the majority of species as examined until now. Biofilm formation permits soil bacteria to inhabit their neighboring territory and stay alive under frequent ecological stresses such as drought and nutrient limitation. This form of life is regularly important for continued existence in bacteria of the genera Mesorhizobium, Sinorhizobium, Bradyrhizobium, and Rhizobium. They also established that biofilm construction is essential for a most favorable root colonization and symbiosis among S. fredii SMH12 and Glycine max cv Osumi. In this bacterium, nod gene-activating flavonoids and the NodD1 protein are necessary for the evolution of the biofilm configuration from monolayer to microcolony. QS mechanisms are also essential for the complete growth of both types of biofilms. In fact, both the nodD1 mutant and the lactonase strain (the lactonase enzyme stop AHL buildup) are imperfect in soybean root inhabitation. The destruction of the lactonase strain in its colonization capability results in the decline of the symbiotic parameters. Fascinatingly, NodD1 jointly with flavonoids induces certain quorum-sensing mechanisms involved in the growth of the symbiotic biofilm. Therefore, S. fredii SMH12 through distinctive key compound, the flavonoid, competently forms biofilm, colonizes the legume roots, and induces the production of Nod factors, necessary for fruitful symbiosis. Oslizlo et al. (2015) demonstrated that Bacillus subtilis isolated from tomato rhizosphere displayed variety of the ComQXPA quorum-sensing mechanisms. This QS mechanism controls the secretion of anti-pathogenic and biofilm-activating compounds, for example, surfactins, which are responsible for the biocontrol activity of this bacterium.
Paungfoo-Lonhienne et al. (2016) established the role of quorum sensing in colonization and biofilm formation by Burkholderia Q208. They accounted that Burkholderia strain Q208, a PGPR of Australian sugarcane, exhibits an extremely conserved quorum-sensing mechanism, nominated as BraI/R, which is programmed by a cluster of three genes (braI, rsaL and braR), the results of which create and react to N-dodecanoyl-3-oxo-homoserine lactone. In the biofilm Burkholderia braI is upregulated (twofold), while, strangely, rsaL and braR are downregulated (to 0.35- and 0.45-fold of reference levels, respectively). The absolute counts of raw reads of rsaL (16,000) and braR (15,500) are higher than the mean (700) read number over all expressed genes, signifying that even though these genes are downregulated, BraI/R quorum sensing by Burkholderia Q208 continues to be effective in the sugarcane rhizosphere.
16.5 Role of Quorum Sensing in Rhizosphere Signaling and Plant-Microbe Interactions
The rhizosphere is a highly complex microecological niche rich in nutrient released by plant root and provides suitable environment for growth and multiplication of an array of soil microbial populations. Primary and secondary metabolites released in the form of plant root exudates are believed to shape, signal, and interfere with rhizosphere microflora by attracting beneficial microflora and combating pathogenic microflora. In a review by Venturi and Keel (2016) described various issues related to signaling in rhizosphere and divided the process in three groups: (i) signaling between microbes, (ii) from plants to microbes, and (iii) microorganisms to plants. Two major groups of small signaling molecules are recognized. First is the QS molecules released by bacteria and volatile organic compounds (VOCs) released by various bacteria and fungi. VOCs are assumed to play significant task in long-distance communication within microbial populations, microbe-microbe, along with plant-microbe cooperation within the rhizosphere (Bitas et al. 2013). VOCs are also known to also work as intra- and interspecies signals by influencing gene expression and microbial functions such as biofilm, virulence, and stress tolerance (Audrain et al. 2015). Various rhizobacteria isolated from rhizosphere are known to produce QS signal molecules, and respond to these molecules. For example species of Burkholderia, Pseudomonas, Rhizobia, and Sinorhizobium as depicted in Table 16.1, and impact of QS on plant-microbe interaction is presented in Fig. 16.1.
Phytocompounds secreted by plant roots promote microbial interaction and also influence plant-microbe interactions (Zhang et al. 2015). Plant-produced signals have been studied only in well-established association such as legume-rhizobia symbiosis and mycorrhizal associations as reviewed by other workers and are not topic of discussion here (Downie 2010; Oldroyd 2013). The role of QS in plant-microbe association is now becoming more evident, since many rhizobacteria employ QS molecules to colonize plant surface or plant-associated environment through QS-mediated gene expression (Von Bodman et al. 2003; Newton and Fray 2004). On the other hand, plant-derived compounds are reported to interfere in bacterial quorum sensing. Recently a bacterial subfamily of LuxRs proteins produced by bacteria interacts with plant small molecules and not with QS. LuxRs is expected to respond plant signals indicating a more complex interkingdom signaling mechanism (Venturi and Fuqua 2013; Gonzalez and Venturi 2013). Various signals produced by PGPR are now characterized, and the best studied AHLs are found to influence plant physiology and plant-microbe interaction such as induction of plant defense against pathogens, pest, and abiotic stressor, which results in promotion of plant growth and development (Shoresh et al. 2010; Zamioudis and Pieterse 2012; Cameron et al. 2013; Pieterse et al. 2014).
Terrestrial plants related to different genera are recognized to generate AHL-mimic molecules for defense system in opposition to pathogen and communication with connected bacterial communities, both inside and outside the plant tissues (Perez-Montano et al. 2013). Quorum-mimicking AHLs are synthesized and secreted in close proximity by different plant species varying from seedlings to a mature plant (Teplitski et al. 2011).
Mathesius et al. (2003) have reported the modulatory role of signaling molecules, AHLs, on plant physiology based on differential proteome analysis and found that protein-related defense, stress, flavonoid metabolism, hormones, and many regulatory proteins were differentially expressed in plants treated with AHLs. von Rad and his colleagues have reported the upregulation of auxin and downregulation of cytokinin genes and influence the ratio of auxin and cytokinin in the treated model plant with C6-HSL (von Rad et al. 2008). Hartmann and Schikora (2012) and Schenk et al. (2012) proposed a double role of the AHL molecules in Arabidopsis thaliana. Short acyl chain AHLs, like C4 or C6, were revealed to increase the growth rate, primarily elongating the roots (von Rad et al. 2008; Bai et al. 2012; Liu et al. 2012; Schenk et al. 2012), in contrast to molecules with longer acyl chains (e.g., C12 or C14).
Recently, Hartmann et al. (2014) described the impact of AHLs on plant growth in plant species and found that it is more complex. However, in some studied cases, it may be very specific such as in mung bean and Medicago truncatula plants. Long-chain 3-oxo-C14-HSL produced by Sinorhizobium meliloti showed increase in root nodulation in Medicago truncatula (Veliz-Vallejos et al. 2014). It was interesting to note that the increased number of nodules was observed only after a treatment with 3-oxo-C14-HSL, the predominant AHL of S. meliloti, and treatment with other AHLs showed no effect. In mung bean plants, only the 3-oxo-C10-HSL, but not the unsubstituted C10-HSL or C12-HSL, was able to induce adventitious roots (Bai et al. 2012).
In a study conducted on barley treated with C6-, C8-, and C10-HSLs indicated modulatory role in the activity of glutathione S-transferase and dehydroascorbate reductase. On the other hand, in yam bean, no influence was measured (Gotz-Rosch et al. 2015). Yet another interesting example is the modification of plant cell walls in AHL-primed plants. In this primed stage, plants upregulated the transcription of numerous genes pertaining to secondary metabolism (e.g., phenols). In consequence, upon a challenge with pathogens, those plants accumulate callose and phenolic compounds (Schenk and Schikora 2015). In a recent review article, Schikora et al. (2016) described the effect of quorum-sensing molecules of the N-acyl homoserine lactone group on plant physiology and significance in the development of stress tolerance mechanism in plants against stressors (Fig.16.1).
16.6 Conclusion and Future Direction
Research carried out in the last decades has shown that quorum sensing is a widespread global regulatory mechanism of gene expression in a density-dependent manner among several bacteria including both pathogenic and beneficial species. Plant-associated bacteria such as PGPR, both free living and symbiotic, have been investigated, which use QS to regulate specific traits. Some of these are important in the interaction with other bacteria or the host plant. These bacteria produce small molecules called autoinducer. Various types of complex QS network are present in bacteria, but the most commonly studied system in Gram-negative bacteria is found to possess AHL-based LuxR/LuxI homologous systems. The signal molecules contribute not only in signaling within bacterial population in the rhizosphere but also contribute in plant-microbe interactions.
Interestingly plants are able to react or hamper bacterial QS which clearly indicated its significance in plant-bacteria interactions. Many bacteria in rhizosphere produce AHL-degrading enzymes, thus exhibiting phenomenon of quorum quenching. On the other hand, plant metabolites can also inhibit QS thus showing QS-mimic activity. Recent reports indicated that bacteria produce compounds which act as receptor for plant signals. Researchers have provided evidences that the treatment of plant with AHLs results in plant response which induces resistance to pathogens and stressor. Studying the dynamics of AHL production and degradation and response of plant-associated microbial biome will certainly help to fully explore the role of QS in plant-microbe interaction.
Now it has been established that plant is able to control the recruitment of root microbiome and to select specific microbes of desired function. Therefore, there is a greater need to understand how plant root-associated bacteria such as free-living PGPR are recruited by plants. Further, the role of QS-mediated signaling and other signaling mechanisms in the rhizosphere contributing in the establishment and maintenance of dynamic root microbiome needs to be studied. It is expected that an enhanced understanding on all these aspects will open new avenues to modulate root microbiome through the use of appropriate consortium of beneficial microbes for improved crop productivity and soil health.
References
Ahmad I, Aqil F, Ahmad F et al (2008) Quorum sensing in bacteria: potential in plant health protection. In: Ahmad I, Hayat S, Pichtel J (eds) Plant-bacteria interactions: strategies and techniques to promote plant growth. Wiley, Germany, pp 129–153
Ahmad I, Khan MSA, Husain FM et al (2011) Bacterial quorum sensing and its interference: methods and significance. In: Ahmad I, Ahmad F, Pichtel J (eds) Microbes and microbial technology: agricultural and environmental applications. Springer, New York, pp 127–161
Alavi P, Muller H, Cardinale M et al (2013) The DSF quorum sensing system controls the positive influence of Stenotrophomonas maltophilia on plants. PLoS One 8(7):e67103
Andersen JB, Heydorn A, Hentzer M (2001) gfp-based N-acyl homoserine lactone sensor systems for detection of bacterial communication. Appl Environ Microbiol 67:575–585
Atkinson S, Williams P (2009) Quorum sensing and social networking in the microbial world. J R Soc Interface 6:959–978
Audrain B, Farag MA, Ryu CM et al (2015) Role of bacterial volatile compounds in bacterial biology. FEMS Microbiol Rev 39:222–233
Bai X, Todd CD, Desikan R et al (2012) N-3-oxo-decanoyl-L homoserine lactone activates auxin-induced adventitious root formation via hydrogen peroxide- and nitric oxide-dependent cyclic GMP signaling in mung bean. Plant Physiol 158:725–736
Barriuso J, Solano BR, Fray RG et al (2008a) Transgenic tomato plants alter quorum sensing in plant growth-promoting rhizobacteria. Plant Biotechnol J 6:442–452
Barriuso J, Solano BR, Lucas JA et al (2008b) Ecology, genetic diversity and screening strategies of plant growth promoting rhizobacteria. (PGPR). In: Ahmad I, Pichtel J, Hayat S (eds) Plant-bacteria interaction, strategies and techniques to promote plant growth. Wiley, Germany, pp 1–13
Bassler BL (2002) Small talk. Cell-to-cell communication in bacteria. Cell 109:421–424
Bitas V, Kim HS, Bennet JW et al (2013) Sniffing on microbes: diverse roles of microbial volatile organic compounds in plant health. Mol Plant-Microbe Interact 26:835–843
Braeken K, Daniels R, Ndayizeye M et al (2008) Quorum sensing in bacteria-plant interactions. In: Nautiyal C, Dion P (eds) Molecular mechanisms of plant and microbe coexistence. Springer, Berlin, pp 265–289
Brameyer S, Bode HB, Heermann R (2015) Languages and dialects: bacterial communication beyond homoserine lactones. Trends Microbiol 23:521–523
Burdman S, Dulguerova G, Okon Y et al (2001) Purification of the major outer membrane protein of Azospirillum brasilense, its affinity to plant roots, and its involvement in cell aggregation. Mol Plant-Microbe Interact 14:555–558
Cameron DD, Neal AL, van Wees SC et al (2013) Mycorrhiza-induced resistance: more than the sum of its parts? Trends Plant Sci 18:539–545
Chapalain A, Vial L, Laprade N (2013) Identification of quorum sensing-controlled genes in Burkholderia ambifaria. Microbiol Open 2:226–242
Charlton TS, De Nys R, Netting A et al (2000) A novel and sensitive method for the quantification of N-acyl 3-oxohomoserine lactones using gas chromatography-mass spectrometry: application to a model bacterial biofilm. Environ Microbiol 2:530–541
Chen X, Schauder S, Potier N et al (2002) Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415:545–549
Chen X, Buddrus-Schiemann K, Rothballer M et al (2010a) Detection of quorum sensing molecules in Burkholderia cepacia culture supernatants with enzyme-linked immunosorbent assays. Anal Bioanal Chem 398:2669–2676
Chen X, Kremmer E, Gouzy MF et al (2010b) Development and characterization of rat monoclonal antibodies for N-acylated homoserine lactones. Anal Bioanal Chem 398:2655–2667
Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants. Their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678
Daniels R, De Vos DE, Desair J et al (2002) Quorum sensing in Rhizobium etli CNPAF512 affects growth and symbiotic nitrogen fixation. J Biol Chem 277:462–468
De Weger LA, Bakker PAHM, Schippers B et al (1989) Pseudomonas spp with mutational changes in the O-antigenic side chain of their lipopolysaccharides are affected in their ability to colonize potato roots. In: Lugtenberg BJJ (ed) Signal molecules in plant-microbe interactions. Springer, Berlin, pp 197–202
Dekkers LC, Phoelich CC, van der Fits L et al (1998a) A site specific recombinase is required for competitive root colonization by Pseudomonas fluorescens WCS365. PNAS 95:7051–7056
Dekkers LC, van der Bij AJ, Mulders IHM et al (1998b) Role of the O-antigen of lipopolysaccharide, and possible roles of growth rate and of NADH, ubiquinone oxidoreductase (nuo) in competitive tomato root-tip colonization by Pseudomonas fluorescens WCS365. Mol Plant-Microbe Interact 11:763–771
Dong H, Gusti AR, Zhang Q et al (2002) Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl Environ Microbiol 68:1754–1759
Dourado MN, Bogas AC, Pomini AM et al (2013) Methylobacterium-plant interaction genes regulated by plant exudate and quorum sensing molecules. Braz J Microbiol 44:1331–1339
Downie JA (2010) The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiol Rev 34:150–170
Duanis-Assaf D, Steinberg D, Chai Y et al (2016) The luxs based quorum sensing governs lactose induced biofilm formation by Bacillus subtilis. Front Microbiol 6:1517
Eberhard A (1972) Inhibition and activation of bacterial luciferase synthesis. J Bacteriol 109:1101–1108
Effmert U, Kalderas J, Warnke R et al (2012) Volatile mediated interactions between bacteria and fungi in the soil. J Chem Ecol 38:665–703
Elasri M, Delorme S, Lemanceau P et al (2001) Acylhomoserine lactone production is more common among plant associated Pseudomonas spp than among soil borne Pseudomonas spp. Appl Environ Microbiol 67:1198–1209
Fatima Q, Zahin M, Khan MSA et al (2010) Modulation of quorum sensing controlled behaviour of bacteria by growing seedling, seed and seedling extracts of leguminous plants. Indian J Microbiol 50:238–242
Fekete A, Rothballer M, Frommberger M et al (2007) Identification of bacterial N-acyl homoserine lactones (AHLs) with a combination of ultra-performance liquid chromatography (UPLC), ultra-high-resolution mass spectrometry, and in-situ biosensors. Anal Bioanal Chem 387:455–467
Fekete A, Rothballer M, Hartmann A et al (2010) Identification of bacterial autoinducers. In: Kraemer R, Jung K (eds) Bacterial signaling. Wiley, Germany, pp 95–111
Ferluga S, Steindler L, Venturi V (2008) N-acyl homoserine lactone quorum sensing in Gram-negative rhizobacteria. In: Karlovsky P (ed) Secondary metabolites in soil ecology. Springer, Berlin, pp 69–90
Flavier AB, Clough SJ, Schell MA et al (1997) Identification of 3-hydroxypalmitic acid methyl ester as a novel autoregulator controlling virulence in Ralstonia solanacearum. Mol Microbiol 26:251–259
Folcher M, Gaillard H, Nguyen LT et al (2001) Pleiotropic functions of a Streptomyces pristinaespiralis autoregulator receptor in development, antibiotic biosynthesis, and expression of a superoxide dismutase. J Biol Chem 276:44297–44306
Fray RG (2002) Altering plant–microbe interaction through artificially manipulating bacterial quorum sensing. Ann Bot 89:245–253
Frommberger M, Schmitt-Kopplin P, Ping G et al (2004) A simple and robust set-up for on-column sample preconcentration-nano-liquid chromatography-electrospray ionization mass spectrometry for the analysis of N-homoserine lactones. Anal Bioanal Chem 378:1014–1020
Galloway WR, Hodgkinson JT, Bowden SD et al (2011) Quorum sensing in Gram-negative bacteria: small-molecule modulation of AHL and Al-2 quorum sensing pathways. Chem Rev 111:28–67
Gantner S, Schmid M, Durr C et al (2006) In situ quantitation of the spatial scale of calling distances and population density-independent N-acylhomoserine lactone-mediated communication by rhizobacteria colonized on plant roots. FEMS Microbiol Ecol 56:188–194
Gonzalez JE, Keshavan ND (2006) Messing with bacterial quorum sensing. Microbiol Mol Biol Rev 70:859–875
Gonzalez JF, Venturi V (2013) A novel widespread interkingdom signaling circuit. Trends Plant Sci 18:167–174
Götz C, Fekete A, Gebefuegi I et al (2007) Uptake, degradation and chiral discrimination of N-acyl-D/L-homoserine lactones by barley (Hordeum vulgare) and yam bean (Pachyrhizus erosus) plants. Anal Bioanal Chem 389:1447–1457
Götz-Rösch C, Sieper T, Fekete A et al (2015) Influence of bacterial N-acyl-homoserine lactones on growth parameters, pigments, antioxidative capacities and the xenobiotic phase II detoxification enzymes in barley and yam bean. Front Plant Sci 6:205
Guan LL, Kamino K (2001) Bacterial response to siderophore and quorum sensing chemical signals in the seawater microbial community. BMC Microbiol 1:27
Hartmann A, Schikora A (2012) Quorum sensing of bacteria and trans-kingdom interactions of N-acyl homoserine lactones with eukaryotes. J Chem Ecol 38:704–713
Hartmann A, Rothballer M, Hense BA et al (2014) Bacterial quorum sensing compounds are important modulators of microbe-plant interactions. Front Plant Sci 5:131
Hernández-Reyes C, Schenk ST, Neumann C et al (2014) N-acyl homoserine lactones-producing bacteria protect plants against plant and human pathogens. Microb Biotechnol 7:580–588
Holden MT, Ram Chhabra S, de Nys R et al (1999) Quorum-sensing cross-talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other Gram-negative bacteria. Mol Microbiol 33:1254–1266
Hosni T, Moretti C, Devescovi G et al (2011) Sharing of quorum-sensing signals and role of interspecies communities in a bacterial plant disease. ISME J 5:1857–1870
Imran A, Saadalla MJA, Khan SU et al (2014) Ochrobactrum sp. Pv2Z2 exhibits multiple traits of plant growth promotion, biodegradation and N-acyl-homoserine-lactone quorum sensing. Ann Microbiol 64:1797–1806
Jiang J, Wu S, Wang J et al (2015) AHL-type quorum sensing and its regulation on symplasmata formation in Pantoea agglomerans YS19. J Basic Microbiol 55:607–616
Jimenez PN, Koch G, Thompson JA et al (2012) The multiple signaling systems regulating virulence in Pseudomonas aeruginosa. Microbiol Mol Biol Rev 76:46–65
Johnson KL, Walcott RR (2013) Quorum sensing contributes to seed-to-seedling transmission of Acidovorax citrulli on watermelon. J Phytopathol 161:562–573
Kakkar A, Nizampatnam NR, Kondreddy A (2015) Xanthomonas campestris cell–cell signaling molecule DSF (diffusible signal factor) elicits innate immunity in plants and is suppressed by the exopolysaccharide xanthan. J Exp Bot 66:6697–6714
Kalia VC (ed) (2015) Quorum sensing vs. quorum quenching: a battle with no end in sight. Springer, India
Kaplan HB, Greenberg EP (1985) Diffusion of autoinducer is involved in regulation of the Vibrio fischeri luminescence system. J Bacteriol 163:1210–1214
Kaufmann GF, Sartorio R, Lee SH et al (2006) Antibody interference with N-acyl homoserine lactone-mediated bacterial quorum sensing. J Am Chem Soc 128:2802–2803
Kaufmann GF, Park J, Mee JM et al (2008) The quorum quenching antibody RS2-1G9 protects macrophages from the cytotoxic effects of Pseudomonas aeruginosa quorum sensing signaling molecule N-3-oxo dodecanoylhomoserine lactone. Mol Immunol 45:2710–2714
Kay E, Dubuis C, Haas D (2005) Three small RNAs jointly ensure secondary metabolism and biocontrol in Pseudomonas fluorescens CHA0. Proc Natl Acad Sci U S A 102:17136–17141
Kendall MM, Sperandio V (2007) Quorum sensing by enteric pathogens. Curr Opin Gastroenterol 23:10–15
Khan SR, Mavrodi DV, Jog GJ et al (2005) Activation of the phz operon of Pseudomonas fluorescens 2-79 requires the LuxR homolog PhzR, N-(3-OHHexanoyl)-l-homoserine lactone produced by the LuxI homolog PhzI, and a cis-acting phz box. J Bacteriol 187:6517–6527
Lee J, Zhang L (2015) The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell 6:26–41
Lee SJ, Park SY, Lee JJ et al (2002) Genes encoding the N-acyl homoserine lactone-degrading enzyme are widespread in many subspecies of Bacillus thuringiensis. Appl Environ Microbiol 68:3919–3924
Li X, Fekete A, Englmann M et al (2006) Development of a solid phase extraction-ultra pressure liquid chromatography method for the determination of N-acyl homoserine lactones from bacterial supernatants. J Chromatogr A 1134:186–193
Liu X, Jia J, Popat R et al (2011) Characterisation of two quorum sensing systems in the endophytic Serratia plymuthica strain G3: differential control of motility and biofilm formation according to life-style. BMC Microbiol 11:26
Liu F, Bian Z, Jia Z et al (2012) The GCR1 and GPA1 participate in promotion of Arabidopsis primary root elongation induced by N-acyl-homoserine lactones, the bacterial quorum sensing system. Mol Plant-Microbe Interact 25:677–683
López-Ráez JA, Bouwmeester H, Pozo MJ (2012) Communication in the rhizosphere, a target for pest management. In: Lichtfouse E (ed) Agroecology and strategies for climate change, sustainable agriculture reviews. Springer, Netherlands, pp 109–133
Lugtenberg BJ, Kamilova F (2009) Plant growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556
Lyon GJ, Novick C (2004) Peptide signaling in Staphylococcus aureus and other Gram-positive bacteria. Peptides 25:1389–1403
Malik AK, Fekete A, Gebefuegi I et al (2009) Single drop microextraction of homoserine lactones based quorum sensing signal molecules, and the separation of their enantiomers using gas chromatography mass spectrometry in the presence of biological matrices. Microchim Acta 166:101–107
Mathesius U, Mulders S, Gao M et al (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. PNAS 100:1444–1449
McClean KH, Winson MK, Fish L (1997) Quorum sensing and Chromobacterium violaceum: exploitation of the violacein production and inhibition for the detection of N-acyl homoserine lactonase. Microbiology 143:3703–3711
Mcknight SL, Iglewski BH, Pesci EC (2000) The Pseudomonas quinolone signal regulates rhl virulence factor production and biofilm formation in Pseudomonas aeruginosa. J Bacteriol 182:2702–2708
Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199
Monnet V, Juillard V, Gardan R (2016) Peptide conversations in Gram-positive bacteria. Crit Rev Microbiol 42:339–351
Morin D, Grasland B, Vallee-Rehel K et al (2003) On-line high performance liquid chromatography-mass spectrometry detection and quantification of N-acyl homoserine lactone quorum sensing signal molecules, in the presence of biological matrices. J Chromatogr A 1002:79–92
Müller J, Kuttler C, Hense BA (2006) Cell-cell communication by quorum sensing and dimension-reduction. J Math Biol 53:672–702
Newton JA, Fray RG (2004) Integration of environmental and host-derived signals with quorum sensing during plant-microbe interactions. Cell Microbiol 6:213–224
Nieto-Penalver CG, Bertini EV, de Figueroa LIC (2012) Identification of N-acyl homoserine lactones produced by Gluconacetobacter diazotrophicus PAL5 cultured in complex and synthetic media. Arch Microbiol 194:615–622
Oldroyd GE (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263
Oslizlo A, Stefanic P, Vatovec S et al (2015) Exploring ComQXPA quorum sensing diversity and biocontrol potential of Bacillus spp. isolates from tomato rhizoplane. Microb Biotechnol 8:527–540
Pang Y, Liu X, Ma Y et al (2009) Induction of systemic resistance, root colonisation and biocontrol activities of the rhizospheric strain of Serratia plymuthica are dependent on N-acyl homoserine lactones. Eur J Plant Pathol 124:261–268
Papenfort K, Bassler BL (2016) Quorum sensing signal-response systems in Gram-negative bacteria. Nat Rev Microbiol 14:576–588
Park J, Jagasia R, Kaufmann GF et al (2007) Infection control by antibody disruption of bacterial quorum sensing signaling. Chem Biol 14:1119–1127
Paungfoo-Lonhienne C, Lonhienne TGA, Yeoh YK et al (2016) Crosstalk between sugarcane and a plant-growth promoting Burkholderia species. Sci Rep 6:37389
Pereira CS, Thompson JA, Xavier KB (2013) AI-2-mediated signalling in bacteria. FEMS Microbiol Rev 37:156–181
Perez-Montano F, Jimenez-Guerrero I, Sanchez-Matamoros C et al (2013) Rice and bean AHL-mimic quorum-sensing signals specifically interfere with the capacity to form biofilms by plant-associated bacteria. Res Microbiol 164:749–760
Pérez-Montaño F, Jiménez-Guerrero I, Del Cerro P et al (2014) The symbiotic biofilm of Sinorhizobium fredii SMH12, necessary for successful colonization and symbiosis of Glycine max cv Osumi, is regulated by quorum sensing systems and inducing flavonoids via NodD1. PLoS One 9(8):e105901
Persello-Cartieaux F, Nussaume L, Robaglia C (2003) Tales from the underground: molecular plant-rhizobacteria interactions. Plant Cell Environ 26:189–199
Pieterse CM, Zamioudis C, Berendsen RL et al (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375
Podile AR, Vukanti RVNR, Sravani A et al (2014) Root colonization and quorum sensing are the driving forces of plant growth promoting rhizobacteria (PGPR) for growth promotion. Proc Natl Acad Sci India Sect B Biol 80:407–413
Rumbaugh KP (ed) (2011) Quorum sensing: methods and protocols. Methods in molecular biology. Springer, New York
Rutherford ST, Bassler BL (2012) Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb Perspect Med 2:a012427
Ryan RP, An SQ, Allan JH et al (2015) The DSF family of cell–cell signals: an expanding class of bacterial virulence regulators. PLoS Pathog 11:e1004986
Sanchez-Contreras M, Bauer WD, Gao MS et al (2007) Quorum-sensing regulation in rhizobia and its role in symbiotic interactions with legumes. Philos Trans R Soc B 362:1149–1163
Schenk ST, Schikora A (2015) AHL-priming functions via oxylipin and salicylic acid. Front Plant Sci 5:784
Schenk ST, Stein E, Kogel KH et al (2012) Arabidopsis growth and defense are modulated by bacterial quorum sensing molecules. Plant Signal Behav 7:178–181
Schikora A, Schenk ST, Hartmann A (2016) Beneficial effects of bacteria-plant communication based on quorum sensing molecules of the N-acyl homoserine lactone group. Plant Mol Biol 90:605–612
Schmid N, Pessi G, Deng Y et al (2012) The ahl- and bdsf-dependent quorum sensing systems control specific and overlapping sets of genes in Burkholderia cenocepacia H111. PLoS One 7(11):e49966
Sessitsch A, Coenye T, Sturz AV et al (2005) Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with plant-beneficial properties. Int J Syst Evol Microbiol 55:1187–1192
Shoresh M, Harman GE, Mastouri F et al (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43
Simons M, van der Bij AJ, de Weger LA (1996) Gnotobiotic system for studying rhizosphere colonization by plant growth-promoting Pseudomonas bacteria. Mol Plant-Microbe Interact 9:600–607
Singh BN, Singh HB, Singh A et al (2012) Lagerstroemia speciosa fruit extract modulates quorum sensing-controlled virulence factor production and biofilm formation in Pseudomonas aeruginosa. Microbiology 158:529–538
Steidle A, Sigl K, Schuhegger R et al (2001) Visualization of Nacylhomoserine lactone-mediated cell-cell communication between bacteria colonizing the tomato rhizosphere. Appl Environ Microbiol 67:5761–5770
Suppiger A, Schmid N, Aguilar C (2013) Two quorum sensing systems control biofilm formation and virulence in members of the Burkholderia cepacia complex. Virulence 4:400–409
Teplitski M, Robinson JB, Bauer WD (2000) Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol Plant-Microbe Interact 13:637–648
Teplitski M, Mathesius U, Rumbaugh KP (2011) Perception and degradation of N-acyl homoserine lactone quorum sensing signals by mammalian and plant cells. Chem Rev 111:100–116
Thomson NR, Crow MA, Mcgowan SJ et al (2000) Biosynthesis of carbapenem antibiotic and prodigiosin pigment in Serratia is under quorum sensing control. Mol Microbiol 36:539–556
Veliz-Vallejos DF, van Noorden GE, Yuan M et al (2014) A Sinorhizobium meliloti-specific N-acyl homoserine lactone quorum-sensing signal increases nodule numbers in Medicago truncatula independent of autoregulation. Front Plant Sci 5:551
Venturi V, Fuqua C (2013) Chemical signaling between plants and plant-pathogenic bacteria. Annu Rev Phytopathol 51:17–37
Venturi V, Keel C (2016) Signaling in the Rhizosphere. Trends Plant Sci 21:187–198
Verma SC, Miyashiro T (2013) Quorum sensing in the squid-vibrio symbiosis. Int J Mol Sci 14:16386–16401
von Bodman SB, Bauer WD, Coplin DL (2003) Quorum sensing in plant-pathogenic bacteria. Annu Rev Phytopathol 41:455–482
von Rad U, Klein I, Dobrev PI et al (2008) The response of Arabidopsis thaliana to N -hexanoyl DL-homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere. Planta 229:73–85
Wang LH, He Y, Gao Y et al (2004a) A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol Microbiol 51:903–912
Wang H, Zhong Z, Cai T et al (2004b) Heterologous overexpression of quorum-sensing regulators to study cell-density-dependent phenotypes in a symbiotic plant bacterium Mesorhizobium huakuii. Arch Microbiol 182:520–525
Waters CM, Bassler BL (2005) Quorum sensing, cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346
Williams P (2007) Quorum sensing, communication and cross-kingdom signaling in the bacterial world. Microbiology 153:3923–3938
Williams P, Câmara M (2009) Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Curr Opin Microbiol 12:182–191
Winzer K, Hardie KR, Williams P (2002) Bacterial cell-to-cell communication: sorry, can’t talk now-gone for lunch! Curr Opin Microbiol 5:216–222
Wynendaele E, Bronselaer A, Nielandt J et al (2013) Quorumpeps database: chemical space, microbial origin and functionality of quorum sensing peptides. Nucleic Acids Res 41:D655–D659
Yamada Y, Nihira T (1998) Microbial hormones and microbial chemical ecology. In: Barton DHR, Nakanishi K (eds) Comprehensive natural products chemistry. Elsevier Sciences, Amsterdam, pp 377–413
Zamioudis C, Pieterse CM (2012) Modulation of host immunity by beneficial microbes. Mol Plant-Microbe Interact 25:139–150
Zarkani AA, Stein E, Rohrich CR et al (2013) Homoserine lactones influence the reaction of plants to rhizobia. Int J Mol Sci 14:17122–17146
Zhang Y, Ruyter-Spira C, Bouwmeester HJ (2015) Engineering the plant rhizosphere. Curr Opin Biotechnol 32:136–142
Zúñiga A, Poupin MJ, Donoso R (2013) Quorum sensing and indole-3-acetic acid degradation play a role in colonization and plant growth promotion of Arabidopsis thaliana by Burkholderia phytofirmans PsJN. Mol Plant-Microbe Interact 26:546–553
Acknowledgment
We are grateful to the Chairman, Department of Agricultural Microbiology, AMU, Aligarh, India for providing support to complete this task. We are also thankful to Mr. Faizan Abul Qais, research scholar, Department of Agricultural Microbiology, AMU, Aligarh, for his cooperation in preparing Fig. 16.1 of this chapter.
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Altaf, M.M., Khan, M.S.A., Abulreesh, H.H., Ahmad, I. (2017). Quorum Sensing in Plant Growth-Promoting Rhizobacteria and Its Impact on Plant-Microbe Interaction. In: Singh, D., Singh, H., Prabha, R. (eds) Plant-Microbe Interactions in Agro-Ecological Perspectives. Springer, Singapore. https://doi.org/10.1007/978-981-10-5813-4_16
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