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Review article
01 2024
:18;
106050
doi:
10.1016/j.arabjc.2024.106050

Application of natural product-based quorum sensing inhibitors in plant pathogen control: A review

, , , , , , , , , ,
 State Key Laboratory of Green Pesticides, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang 550025, China

⁎Corresponding authors. xiangzhou@gzu.edu.cn (Xiang Zhou), syang@gzu.edu.cn (Song Yang)

Received: , Accepted: ,
© The Author(s) 2024
Disclaimer:
This article was originally published by Elsevier and was migrated to Scientific Scholar after the change of Publisher.
1Ai-Qun Chen and Zhou-Qing Long contributed equally.

Abstract

Abstract

Quorum sensing (QS), an intercellular communication process, depends on the generation, release, and detection of extracellular signaling molecules (autoinducers). Upon binding to their corresponding receptors, these autoinducers activate target genes, regulating various bacterial activities including bioluminescence, swimming and swarming motility, symbiosis, protein secretion, plasmid exchange, secondary metabolite production, and biofilm development. Many interactions between plants and microorganisms depend on bacterial QS systems, making them a powerful tool for regulating plant growth and controlling plant pathogens. As QS research deepens, more QS inhibitors (QSIs) emerge, exhibiting diversification. According to its structure, QSIs can be divided into furanone, lactone, substituted Homoserine Lactone (HSL), and Autoinducing Peptide (AIP), further divided into natural products and synthetic products. Natural QSIs primarily originate from animal, plant, and microbial sources. Thereby, QSIs play an important role in plant pathogen control. In order to systematically summarize and extend the application potential of natural product as vital antibacterial active constituent, the mechanisms and applications of natural product-based QSIs in plant pathogen control were discussed and highlighted. We hope this review will provide the comprehensive understanding of the function and underlying action mechanism of natural product-based antimicrobial molecule, and inspire the development of new bactericides targeting QS mechanisms.

Keywords

Natural products
Plant pathogenic bacteria
Autoinducers
Quorum sensing inhibitors

Abbreviations

EOs

Essential oils

GBLE

Ginkgo biloba leaf extract

PL

Pectin lyase

QS

Quorum sensing

QSI

Quorum sensing inhibitors

BDSF

cis-2-dodecenoic acid

CDSF

cis, cis11-methyldodeca-2,5-dienoic acid

AHL

Acyl homoserine lactones

PCWDE

Plant cell wall-degrading enzymes

OC8-HSL

N-oxo-octanoyl-L-homoserine lactone

C6-HSL

N-hexanoyl-L-homoserine lactone

3-oxo-C6-HSL

N-(3-oxo-hexanoyl)-L-homoserine lactone

3-oxo-C8-HSL

N-(3-Oxooctanoyl)-L-homoserine lactone

OHL

N-octanoyl-homoserine lactone

Acyl-HSL

Acylated-homoserine lactones

3-OH PAME

Methyl 3-hydroxypalmitate

3-OH-MAME

Methyl 3-hydroxymyristate

SA

Salicylic acid

HSL

Homoserine lactone

AIP

Autoinducing peptide

DSF

Diffusible signaling factor

GABA

γ-aminobutyric acid

CA

cinnamic acid

OOHL

N-3-oxo-octanoyl homoserine lactone

THY

thyme

MIC

Minimum inhibition concentration

AI-2

Autoinductor-2

C8-HSL

N-octanoyl-L-homoserine lactone

OHHL

N-(3-oxo)-hexanoyl-L-HL

OOHL

N-(3-oxo)-octanoyl-L-HL

HSL

Homoserine lactone ring

VOCs

Volatile organic compounds

EPS

Extracellular polysaccharide

1

1 Introduction

In recent years, concerns over food security and crop production have increased as the global population grows (Jamiołkowska, 2020). Crops in their growth and maturity processes are susceptible to various plant pathogens, which can infect host plants in various ways and spread illness to the leaves, stems, roots, vascular systems, and fruits of those plants (Moorman, 2014) (Yang et al., 2023b) (Peeters et al., 2013). Bacteria that parasitize plants and cause plant illnesses are referred to as plant pathogenic bacteria (Tampakaki, 2009). Most plant pathogenic bacteria attack the plant wounds on roots and leaves, colonize and spread to the wound site, and then further disrupt plant growth, making the plant more vulnerable to disease or apoptosis and lowering crop output. In other word, effective control of plant pathogenic bacteria can ensure high grain quality and even improve grain yield to a certain extent (Chakraborty and Newton, 2011). Therefore, research on plant pathogens is extremely important for crop protection.

To solve the problem caused by plant pathogenic bacteria, using traditional pesticides is a common control strategy. However, their misuse and abuse have caused a series of issues, such as pesticide residues polluting the living environment (Jamiołkowska, 2020) and bacterial resistance (Chen et al., 2016). On the one hand, it is urgently required to accelerate the development of new pesticides for the replacement and diminishing the use of highly toxic and high-risk pesticides. Natural products (Umetsu and Shirai, 2020), with a diversity of sources, structures, and functions, will provide new opportunities for pesticide research and development. At present, commercial pesticides based on natural products exist (Liu, 2004), but their research and development are still insufficient. On the other hand, to date, many studies have shown that microorganism drug resistance is related to quorum sensing (QS) regulation (Chen et al., 2016), because it is beneficial for bacteria to obtain host nutrients, escape host immune responses, and/or stimulate infection. Especially, bacterial QS system enable to product virulence factors including extracellular polymeric substances (EPS), phytotoxins, and biofilm, and result in formatting the barrier for escaping the harsh environment. For instance, biofilm enable bacteria to elevate resistance towards antibiotics approximately 1000-fold than planktonic bacteria, and resulting in reducing the bactericidal activity (Høiby et al., 2010). Therefore, modulation of QS system and inhibition of virulence, rather than attacking cell viability, is a promising tactic for controlling phytopathogenic bacterial infection and avoiding drug resistance issues (Zhou et al., 2020).

Quorum sensing inhibitors (QSIs) are recognized as effective and promising method for combating microbial infections. Given the merits of natural product, which includes being easy to obtain, low side effects, excellent chemically stable, low risk, and high activity, natural products were regarded as important source for discovering new QSI. The fact that various natural products including rotenone (botanical insecticide) and Taxol (anticancer agents) have also been shown to have the ability to inhibit bacterial QS activity. Normal bacterial growth and metabolism can be blocked by natural products through targeting and inhibiting the QS signaling pathways without triggering bacterial resistance. These types of natural products quorum sensing inhibitors, namely natural product-based QSIs, do not kill bacteria directly but rather reduce their growth pressure and promote their evolution (Jiang and Li, 2013). What’s more, some QSIs can target specific bacterial pathogens without affect the native microflora or beneficial microorganisms, and does not exert any direct selection pressure on the bacterial populations (Zhu et al., 2023). In order to excavate new natural quorum sensing inhibitors and guiding novel natural product-based bactericidal agent discovery, we summarized the source, mechanism of action and blocking mode of natural quorum-sensing inhibitors in Fig. 1. For many pathogenic bacteria, QS signaling not only molecules serve to inter or intra bacteria species communication but also is important for virulence toward plant (Diggle and Williams, 2017). Notably, phytochemicals are considered as the ideal QSI because plant could produce molecules that mimic the QS signal to affect the behavior of associated bacteria (Truchado et al., 2015). Interestingly, most natural product-based QSIs are no toxicity (Zhang et al., 2018a). According to the section 25(b) of FIFRA, an additional category of “minimum risk” pesticides (including most natural product such as oils, citric acid, eugenol, geraniol, and lauryl sulfate) are exempt from registration, implying that most natural product had the low environmental risk and excellent safety towards non-target organism (Cantrell et al., 2012, Helman and Chernin, 2014). Therefore, natural products have the unprecedented potential to discover and develop as QSIs for controlling plant bacterial infection.

Summary diagram of natural product-based quorum sensing inhibitors extraction, action pathway, and mode of action.
Fig. 1
Summary diagram of natural product-based quorum sensing inhibitors extraction, action pathway, and mode of action.

In recent years, as QS research continues, small molecule inhibitors of QS, providing a basis for exploring its mechanisms, have been discovered and developed. Therefore, QS-targeted small molecules had the promising prospect for controlling plant pathogenic bacteria infection. In this review, we will focus on the inhibitory effects of natural product QS inhibitors (QSIs) against phytopathogenic bacteria and summarize the partially reported QS mechanisms in phytopathogenic bacteria according to examples of the top ten bacterial plant pathogens (Table 1) suggested by John et al. (Mansfield et al., 2012).

Table 1 Phytopathogen and their hosts.
Phytopathogen Hosts Reference
Pseudomonas syringae Olive, snap bean, and strawberries, et al. (Hirano and Upper, 2000)
Ralstonia solanacearum Banana, potato, and tobacco, et al. (Li et al., 2016)
Agrobacterium tumefaciens Microalgae (Cha et al., 2011)
Xanthomonas oryzae pv. oryzae Rice (Yu et al., 2018)
Xanthomonas campestris pathovars Grapefruit, lime, and lemon (Ference et al., 2018)
Xanthomonas axonopodis pv. manihotis Cassava plants (Castiblanco et al., 2013)
Erwinia amylovora Apple and pear (Pique et al., 2015)
Xylella fastidiosa Grape and citrus (Rapicavoli et al., 2018)
Dickeya Rice corn and potato, et al. (Zhou et al., 2015)
Pectobacterium carotovorum Carrot, cabbage, cucumber, et al. (Opara and Asuquo, 2016)
Pseudomonas fuscovaginae Maize, sorghum, wheat, et al. (Uzelac et al., 2017)

2

2 Overview of quorum sensing system

QS is a significant mediator of inter-species communication, referring to the fact that the signaling molecules released by bacteria also increase in density when the bacterial population density reaches a specific concentration. As shown in Fig. 2, the receptor monitors signaling molecules upon reaching a certain threshold. Subsequently, after transmission, this affects target gene transcription. Bacteria adapt by regulating gene expression in response to external environmental changes and regulating bacterial social behavior, including bioluminescence, bacterial motility, symbiosis, protein secretion, plasmid exchange, secondary metabolite production, and biofilm development. The term QS was first proposed by Fuqua et al. (Fuqua et al., 1994) in summarizing the newly discovered LuxR and LuxI homologous families in different bacterial species. In the 1970s, Nealson provided a preliminary explanation of the bioluminescence phenomenon of Vibrio fischeri (Nealson, 1977). The bacteria generate an autoinducer, which accumulates in the culture medium until reaching a critical concentration and then triggers the synthesis of the luminescence system at the transcriptional level. Subsequently, Engebrecht et al. (Engebrecht et al., 1983) found in the bioluminescence of Gram-negative bacteria Vibrio fischeri that the regulatory gene required for the enzyme activity and the expression of the luminous phenotype (Lux) in the light reaction was the lux operon. In 1981, Eberhard et al. (Eberhard et al., 1981) verified the autoinducer’s structure of luciferase, which was N-(3-oxohexanoyl)-3-aminodihydro-2(3H)-furanon. With an extensive study of QS, many researchers found that most Gram-negative bacteria generally use acyl homoserine cyclolactones (AHL) to sense quorum sensing (Whitehead et al., 2001). Among them, AHL is a transcription regulator targeting the LuxR family. The combination of the two produces an AHL-LuxR complex that binds multiple promoters and activates transcription of the lux operator (Eberl, 1999). QS regulation is often determined by the two-component system LuxI/LuxR, which is responsible for synthesizing N-acyl homoserine lactone. LuxR is the AHL receptor protein and activating transcription factor, a transcription regulation gene responsible for AHL (Schaefer et al., 2013). Furthermore, ahlD encodes an AHL hydrolase, mainly responsible for AHL degradation (Park et al., 2003), and AHL is a long chain containing different numbers of carbon. In plant pathogenic bacteria (Fig. 3), there are diffusible signal factor (DSF) in the Xanthomonas pathway in addition to AHL. The signaling molecule DSF is synthesized and released by the biological synthetase RpfF, and sensed and transmitted by RpfC, thus triggering the regulation pathway of the whole quorum sensing. The DSF analog is also present in the genus Ralstonia solanacearum, generated by PhcB, sensed and transmitted by PhcS to further regulate the behavior of QS. These signal factors regulate different genes though various ways to further regulate the social activities of molecules and the communication between molecules.

Bacterial behavior regulated by quorum sensing.
Fig. 2
Bacterial behavior regulated by quorum sensing.
Quorum sensing pathway map in plant pathogens.
Fig. 3
Quorum sensing pathway map in plant pathogens.

A new type of signaling molecule, the small polypeptide AIP (Fig. 4a), has been identified in Gram-positive bacteria and is associated with a receptor protein on the bacterial cell membrane (Kociolek, 2009). The signaling molecules released by bacteria interact with the sensor elements of the histidine kinase two-component signaling system. Upon binding of AIP to its transcription factor, it can induce activation of the kinase activity within the binary system, leading to receptor phosphorylation and subsequent transfer of the phosphorylated receptor to the cytoplasmic regulator, activating the transcription and expression of the genes involved. The phosphorylated regulator stimulates further AIP molecule production, thereby facilitating QS (Kleerebezem et al., 1997).

Common quorum sensing systems model mediated by signals. (a) AIP; (b) AI-1 and AI-2.
Fig. 4
Common quorum sensing systems model mediated by signals. (a) AIP; (b) AI-1 and AI-2.

Additionally, a fascinating discovery is that the signaling molecule Autoinductor-2 (AI-2) is frequently observed in bacterial interspecific communication (Bassler, 1999; Schauder and Bassler, 2001). In 1999, Surette et al. (Surette et al., 1999) revealed that along with AI-1, the AI-2 signal response system (Fig. 4b) is also a common QS system in Gram-positive and Gram-negative bacteria and is related to a variety of Lux receptors and the Lsr transporter (Kociolek, 2009). In 2001, Ren et al. (Ren et al., 2001) suggested that halogenated furanones can be AI-1 to regulate QS and also by AI-2, meaning that halogenated furanones are both intraspecific and interspecific QS signals. After, they also concluded that brominated furanones have inhibitory effects on Bacillus subtilis biofilm formation and clustering, which may inhibit Bacillus subtilis not only by inhibiting bacterial growth but also by interfering with QS, colonization, and biofilm formation (Ren et al., 2002). However, to our knowledge, there are barely reports of AI-2 mediated quorum sensing in plant pathogens.

QS is a new target of microbial resistance and anti-infection. Many plant pathogen behaviors are regulated by QS. In many studies, introducing a drug exhibits the capacity to trigger the generation of low-level AHL signaling molecules that are intricately linked to QS. These molecules facilitate the mediation of corresponding group sensing mechanisms. Furthermore, the drug effectively hinders the specific intra- and interspecific transmission of bacteria, thereby suppressing bacterial virulence factor expression and ultimately mitigating bacterial pathogenicity. At the same time, QSIs have no selective pressure on bacteria, reducing the generation of bacterial resistance (Zhao et al., 2020).

3

3 Research overview of natural products

3.1

3.1 Overview of natural products

Natural products refer to extracts from animals, plants, and microorganisms or endogenous substances and their metabolites (Stan et al., 2021). Since times immemorial, natural products have played a crucial role in the development of new drugs, with the characteristics of rich resources. Plants, for example, are known to produce a diverse range of secondary metabolites such as terpenoids, alkaloids, polyacetylenes, flavonoids, and unusual amino acids and sugar (Benner, 1993). These rich resources are mainly derived from microorganisms, plants, animals, minerals, and yeast that humans have long used as insect repellents and fungicides. For example (Fig. 5), rotenone, an organic compound extracted from leguminous plant roots in the genus Caulis, can be used to kill aphids and caterpillars (Davidson, 1930). Taxol isolated from Taxus chinensis is used as an anti-tumor agent (Wani et al., 1971). Artemisinin is extracted from the traditional Chinese medicinal plant Artemisia annua and has demonstrated remarkable efficacy in treating malaria and cancer (Nosten and White, 2007; Peter et al., 2021). Ginkgo biloba leaf extract, containing bioactive ginkgo flavones and ginkgolides, is widely used to treat cardio–cerebrovascular disease and coronary heart disease. Active substances isolated from Catharanthus roseus, including vinblastine and vincristine, have been identified as effective anti-tumor agents and are utilized in treating malignancies (Zhang and Hu, 2020). Additionally, baicalein, a flavonoid monomer compound extracted from the Lamiaceae plant Scutellaria baicalensis, demonstrates potential to treat Parkinson's disease (Zhang et al., 2017). In summary, an increasing number of researchers are focusing on natural products to control plant pathogens, yielding exciting research outcomes. Natural products with anti-plant pathogenic bacteria activities mainly include alkaloids, sugars, hormones, polysaccharides, proteins, and lactones.

Structure of some natural active compounds.
Fig. 5
Structure of some natural active compounds.

3.2

3.2 Antibacterial activity of natural products against plant pathogens

Numerous natural product extracts exhibit inhibitory effects against plant pathogens. In 1995, Kulik (Kulik, 1995) conducted a comprehensive review on the antibacterial properties of algal compounds derived from natural products against plant pathogenic bacteria and fungi, establishing a solid foundation for subsequent researchers to assess algal compound efficacy for combating plant pathogenic bacteria. Subsequently, Paulert et al. (Paulert et al., 2007) studied a crude polysaccharide extract from the cell wall of Ulva fasciata, which had a good antibacterial effect on Xanthomonas campestris and Erwinia carotovora. In addition, the relationship between natural products and pathogenic bacteria can be summarized in the following two ways. On the one hand, the same active substance inhibited the growth of one or more plant pathogenic test bacteria, but to varying degrees (Pretorius et al., 2003). For example, Cheng et al. (Cheng et al., 2008) proposed that cinnamaldehyde affects the inhibitory activity of Laetiporus sulphureus better than that of Lenzites betulina, while eugenol shows the opposite inhibitory effects. On the other hand, the same pathogen has different sensitivities to different extracts. For example, Badawy et al. (Badawy and Rabea, 2016) concluded through experiments that among the ten monoterpene compounds tested, only geraniol and thymol possessed high inhibitory activity against the four plant pathogens Erwinia carotovora, Ralstonia solanacearum, Rhodococcus fascians, and Rhzobium radioactor.

In the plant pathology field, the controlling effect of natural products on plant pathogens has attracted the attention of many researchers. In the next study, a large number of natural product fungicides will be found and commercialized.

4

4 Natural product-based quorum sensing inhibitors

In the late 1920s, the discovery of antibiotics played an important role in mitigating bacterial infection. The majority of antibiotics directly eliminate harmful bacteria by rupturing cell membranes, preventing essential protein production, and obstructing DNA replication and transcription (Nikaido, 2009). If bacteria want to survive in a group, they must be able to adapt to the living environment of nearby groups and adjust their genes to adapt to the new group environment constantly. Thereby, bacterial QS system was a result of microorganisms made themself live and constantly adapt to the sharp environment.

In recent years, many researchers have found that the drug resistance mechanism in some microorganisms is associated with QS. In this section, AHL-mediated QSIs are mainly illustrated due to in-depth research about AHL. There are three ways with AHL as the model to interfere with QS in pathogenic bacteria. The major contributing factor is blocking AHL synthesis. The second is promoting AHL hydrolysis to inactivate it and prevent the accumulation of signaling molecule concentrations. The third is interfering with signaling molecule binding to the receptor protein LuxR (Fig. 6) (Lianhui, 2019).

Three modes of action about quorum sensing inhibitors.
Fig. 6
Three modes of action about quorum sensing inhibitors.

With an increase in the depth of QS research, the number of QSIs is also increasing. A QSI should be chemically stable and resistant to metabolism and disposal by the higher host organism (Rasmussen and Givskov, 2006). There is currently a high need for them, so finding and developing safe and non-toxic QSIs is urgent. Natural product-derived QSIs possess the advantages of high selectivity, low toxicity, easy degradation, and resistance to plant pathogens (He et al., 2006). Natural products and their derivatives also play an important role in QSIs (Feng et al., 2022; Xiao et al., 2023; Yang et al., 2023a) (Due to the variety of natural product derivatives, they will not be covered in this article). The main sources of plant pathogen QSIs studied so far include microorganisms, plants, and animals, among others. As far as the literature we surveyed was concerned, there were no reports on animal derived QSIs.

4.1

4.1 Quorum-sensing inhibitors from plant-derived extracts

Since early times, many plant-produced secondary metabolites have been used as antimicrobial agents and can inhibit bacterial toxin and biofilm formation (Barbieri et al., 2017). Secondary metabolites synthesized in plants have been studied more frequently as potential anti-harmful microorganisms, including alkaloids, flavonoids, tannins, saponins, coumarins, terpenoids, and phenolic compounds.

As people become more environmentally conscious, research into plant-derived fungicides is increasing. Likewise, research into QS inhibition via plant-originated compounds is becoming more advanced. Many plant-based natural products can block QS signal production or propagation to combat QS pathogens and may be potential anti-QS compounds. One of the first plant-derived QSIs identified were halogenated furanones produced by marine red algae that could affect the QS system in Gram-negative bacteria by interfering with AHL binding to the receptor protein LuxR (Kjelleberg et al., 1997). Below, we summarize QSIs derived from plant-based natural products and their antagonistic effects against phytopathogenic bacteria (Table 2, Fig. 7).

Table 2 Quorum sensing inhibitors of natural products from plants against plant pathogens.
Plant-Derived QSIs Phytopathogen QS signal system/related gene Targeted function Reference
Plant oil Thyme oil Xanthomonas oryzae pv. oryzae DSF, BDSF Virulence (Singh et al., 2017)
Citronella oil Citronellal Xanthomonas oryzae pv. oryzae DSF, BDSF Biofilm, swimming and clustering (Singh et al., 2018)
Cabbage, leek, and onion The extracts of cabbage, leek, and onion Pseudomonas syringae pv. tabaci 3-oxo-C8-HSL / (Kim et al., 2008)
Radix Salviae Miltiorrhizae Protocatechualdehyde Ralstonia solanacearum / / (Li et al., 2016)
Plant essential oil Geraniol Erwinia carotovora and Pseudomonas fluorescens / Motilities, EPS production, and biofilm (Zhang et al., 2021)
Black fragrant beans Hydroxycoumarins Ralstonia solanacearum fliA and flhC Biofilm formation, the swimming (Yang et al., 2016)
Cinnamon, thyme, lavender, eucalyptus EOs Ralstonia solanacearum / Biofilm formation, the swimming, swarming and twitching motilities (Hosseinzadeh et al., 2013)
Bacteria, yeast, plants and animals GABA Agrobacterium tumefaciens OC8-HSL Virulence (Chevrot et al., 2006)
Plant extracts and exudates Garlic extract and p-coumaric acid Agrobacterium tumefaciens NTL4 TraI\R / (Bodini et al., 2009)
Plant phenolic acid SA Pectobacterium carotovorum and Pseudomonas syringae LuxR-like regulator, fliC Biofilm formation, motility and N-acylhomoserine lactone production (Lagonenko et al., 2013)
Plant phenolic acid SA and CA Pectobacterium aroidearum and P. carotovorum sp. brasiliense AHL PCWDEs and Virulence factor (Barnard and Salmond, 2007) (Joshi et al., 2016)
Plant extracts Cinnamic, coumaric, syringic and salicylic acids and catechol Pectobacterium / Motility, biofilm formation and extracellular enzyme activities (Joshi et al., 2015)
Essential oil Hexanal Erwinia carotovora subsp. carotovora / Biofilm movement and EPS production (Zhang et al., 2018b)
The plant source of quorum sensing inhibitor.
Fig. 7
The plant source of quorum sensing inhibitor.

4.1.1

4.1.1 Plant-derived extracts anti-Pseudomonas syringae

Pseudomonas syringae, a Gram-negative plant pathogen, is widely recognized as the most important bacterial threat to global agriculture attributable to its pervasive distribution and capacity to infest diverse cash crops, encompassing corn, tobacco, tomato, legume, cucumber, kiwi fruit, and members of the leguminaceae family. After successfully infecting plants and causing disease, Pseudomonas syringae can exert its virulence effect by mediating biofilm formation (Laue et al., 2006) and siderophore production (Taguchi et al., 2010). In 2008, Kim et al. (Kim et al., 2008) discovered that natural aqueous extracts derived from cabbage, leek, and onion (designated as QSI-83) effectively suppressed the QS activity in Pseudomonas syringae pv. tabaci without interfering with its growth, and suggested that the three aqueous extracts might be antagonists of acyl homoserine lactones or might inhibit autoinducers synthesis.

In 2021, Zhang et al. (Zhang et al., 2021) evaluated the antibacterial activity of plant essential oils, indicated that all of 10 EO components showed the QSI effect on the biofilm formation of mixed culture (Erwinia carotovora and Pseudomonas fluorescens) at the ratio of 1:1. Among these, geraniol exhibited the best QSI effect. It significantly inhibited the swimming, clustering, convulsive movement, extracellular polysaccharide production, and biofilm biomass of two bacterial biofilms.

4.1.2

4.1.2 Plant-derived extracts anti-Ralstonia solanacearum

Ralstonia solanacearum (R. solanacearum) are Gram-negative bacteria, during their investigation into anti-QSIs, researchers unexpectedly discovered that naturally purified molecular compounds isolated from plants exhibited remarkable anti-QS effects, and a unique category of natural products—namely, plant essential oils (EOs)—displayed equally impressive anti-QS bioactivities. In 2013, Saeed et al. (Hosseinzadeh et al., 2013) first demonstrated the anti-QS activity of plant EOs against the plant pathogenic bacteria R. solanacearum, who obtained experimental evidence that cinnamon, THY, lavender, and eucalyptus EOs inhibited swimming motility and virulence factors of R. solanacearum at sublethal concentrations, and also inhibited pathogenicity by inhibiting bacterial biofilm formation and twitching. As a consequence, the potential of plant EOs in combating QS mechanisms not only enhances our comprehension of these processes but also opens novel avenues for developing novel, natural anti-QS agents.

In 2016, Li et al. (Li et al., 2016) found that protocatechualdehyde isolated from Salviae miltiorrhizae roots significantly reduced R. solanacearum biofilm formation and significantly inhibited R. solanacearum growth and swarming movements, while also reducing the incidence of tobacco R. solanacearum. In the same year, Yang et al. (Yang et al., 2016) showed for the first time that the inhibitory effects of coumarins at different substitution positions on R. solanacearum, where hydroxy coumarins at different positions (e.g., umbelliferone, hesperidin, and ricin) inhibited R. solanacearum biofilm formation, possibly by downregulating certain flagellar genes (fliA and flhC) and suppressing swimming motility.

4.1.3

4.1.3 Plant-derived extracts anti-Agrobacterium tumefaciens

In Agrobacterium tumefaciens, the TraI and TraR proteins have been discovered as homologs of LuxI and LuxR proteins, respectively, representing a significant finding in the field of bacterial QS research. Zhang and Piper et al. (Piper et al., 1993; Zhang et al., 1993) identified the function of the TraR protein and the structure of the QS signaling molecule and found that the conjugation transfer of the Ti plasmid is also a type of QS. Subsequently, Hwang et al. (Hwang et al., 1994) proved that the traI gene was responsible for signaling factor synthesis.

The virulence of Agrobacterium tumefaciens is mainly expressed by secreting exoenzymes, which degrade the host cell wall and provide nutrients to the bacteria (Clague and Urbe, 2003). Two genes encoding AiiA lactase, attM and aiiB, were identified in Agrobacterium tumefaciens C58, suggesting that both lactase encoding genes could inactivate acyl-HSL, and when the inactivation effects of the enzymes are examined, it is found that attM inactivates acyl-HSL more effectively than aiiB (Carlier et al., 2003). In 2006, Chevrot et al. (Chevrot et al., 2006) experimentally demonstrated that γ-aminobutyric acid (GABA) inactivates the N-(3-oxooctanoyl)homoserine lactone (OC8-HSL) QS signal by stimulating the Agrobacterium lactamase AttM. In 2009, Bodini et al. (Bodini et al., 2009) reported significant QSI activity of both compounds against the TraR-based Agrobacterium tumefaciens NTL4 in the presence extracts of garlic and p-coumaric acid at low concentrations.

4.1.4

4.1.4 Plant-derived extracts anti-Xanthomonas spp

Xanthomonas is a class of Gram-negative plant pathogens that can infect monocotyledonous and dicotyledonous food crops, including Xanthomonas albilineans, Xanthomonas fragariae, Xanthomonas oryzae, Xanthomonas campestris, etc. In a paper by Feng et al. (Feng et al., 2023), the QS pathway in Xanthomonas was introduced in detail. The signaling molecule DSF was synthesized and released by the biological synthetase RpfF. RpfF sensed and transmitted signals, thus triggering the regulation pathway of the whole QS process. In 2017, Singh (Singh et al., 2017) imposed that the expression of the rpfF gene, which plays a key role in plant pathogen virulence, was significantly reduced in Xanthomonas oryzae pv. oryzae cells treated with thyme (THY) oil. In addition, it was confirmed that the DSF and BDSF signaling molecules were significantly reduced after THY oil treatment. In 2018, Singh et al. (Singh et al., 2018) confirmed that citronellal (3, 7-dimethyloct-6-eneale) significantly inhibits the biofilm formation and virulence of Xanthomonas oryzae pv. oryzae, as well as its swimming and clustering potential (Fig. 8).

The main components of thymol oil and Kaffir lime oil and their molecular docking diagram respectively with RpfF protein.
Fig. 8
The main components of thymol oil and Kaffir lime oil and their molecular docking diagram respectively with RpfF protein.

4.1.5

4.1.5 Other

As other bacterial species including Pectobacterium spp., Pseudomonas spp. and Pectobacterium spp., some natural products also showed the ability to inhibit the quorum sensing. For instance, Pectobacterium spp., as the member of Enterobacteriaceae spp., had the a broad host range (Yasuhara-Bell et al., 2016). In 2013, Leonid et al. (Lagonenko et al., 2013) proposed that SA at sub-inhibitory concentrations inhibited biofilm formation, motility, and N-acyl homoserine lactone production in Pectobacterium carotovorum. Interestingly, SA ha the same inhibitory activity toward Pseudomonas syringae, Erwinia amylovora, Pseudomonas corrugata, Pseudomonas syringae pv. syringae, and Xanthomonas campestris pv. campestris. Furthermore, two plant phenolic acids (cinnamic acid and SA) further affected the virulence factors of two Pectobacterium species (Pectobacterium aroidearum and Pectobacterium carotovorum spp. brasiliense) by interfering with their QS system. (Barnard and Salmond, 2007). In 2012, Pollumaa et al. further found that cinnamic acid and SA could inhibit AHL signaling molecule production (3-oxo-C6-AHL and 3-oxo-C8-AHL) in Pectobacteria, and ExpR transcriptional regulators undergo conformational changes (Fig. 9), which in turn reduce the expression levels of rsmA genes and ultimately inhibits PCWDE synthesis (Pollumaa et al., 2012), affecting Pectobacteria virulence (Joshi et al., 2016). Moreover, Joshi et al. (Joshi et al., 2015) showed significant activity against small plant molecules in the phenylpropane pathway (SA, cinnamic, coumaric, and syringic acids, as well as vanillin, catechol, and tyrosol) against three different Pectobacterium species (P. aroidearum, P. carotovorum, and P. brasiliensis) and concluded that these phenolic acid-treated Pectobacterium showed decreased biofilm formation, increased motility, and inhibited exoenzyme synthesis (pectate lyase, polygalacturonase, and protease). Implying that cinnamic acid and SA had the excellent quorum sensing inhibitory ability towards various pathogenic bacteria.

Molecular docking scores of carvacrol and eugenol with ExpR and Expl.
Fig. 9
Molecular docking scores of carvacrol and eugenol with ExpR and Expl.

Erwinia spp. was pathogenic bacteria, which caused the postharvest disease of Chinese cabbage and lettuce. To prevent these postharvest diseases, some natural products were chosen to verify the quorum sensing inhibitory efficiency. 10 of essential oil including trans-cinnamaldehyde (72.81 %), benzyl alcohol (12.5 %) and eugenol (6.57 %), obtained from plant C. verum were assay their QSI effect on E. carotovora. (Zhang et al., 2018b) Interestingly, hexanal was first discovered as QS inhibitor by inhibiting biofilm formation, with inhibition ratio of 20.18 %. Salicylic acid and thymol also possessed the optimal inhibitory ability toward biofilm formation of E. carotovora (47.24 %). At sub-MICs, hexanal could inhibit E. carotovora’s biofilm movement and extracellular polysaccharide (EPS) production (Zhang et al., 2018a; Zhang et al., 2018b; Zhang et al., 2022a). To further understand the relationship between QSI effect of hexanal on AI-2, biofilm formation, and enzyme activity, the action mechanism in-depth was further explored by Zhang in 2021 and 2022. Results implied that the QSI effect of hexanal on biofilm might attribute to the inhibition of AI-2 signal molecule secreted by E. carotovora. Overall, these EO could be regarded as novel active components to ensure the safety and quality of vegetables (Zhang et al., 2021, 2022b).

4.2

4.2 Microbial-derived natural product quorum sensing inhibitors

Interestingly, a large number of compounds with QSI activity have been discovered among microorganisms’ secondary metabolites in addition to plant-derived extracts or secondary metabolites. Microorganisms are community species that modify themselves to live in their surroundings. It is possible that during their evolutionary process, they would create secondary metabolites that block the QS systems of rival bacteria (Fig. 10). Natural products of microbial origin with the following characteristics: 1) structural and functional diversity; 2) massive synthesis, a generation of bacteria that can reproduce in a few minutes to a few hours under eutrophic conditions; 3) unique source; 4) widely distributed are potential QSIs (Zhao et al., 2019). Microorganisms live wherever there are higher organisms, even in extreme environments where plants and animals cannot live, and they possess many metabolic types and are highly active. The high efficiency of microbial culture makes it an important resource for developing population induction inhibitors (Table 3).

Quorum sensing inhibitors derived from microorganisms.
Fig. 10
Quorum sensing inhibitors derived from microorganisms.
Table 3 Quorum sensing inhibitors of natural products from microorganisms against plant pathogens.
Microbial-derived QSIs Phytopathogen QS signal/related gene Targeted function Reference
Red algae D. pulchra The furanone Erwinia carotovora 3-oxo-C6-HSL Virulence factors and antibiotic production (Manefield et al., 2001)
Bacillus sp. 240B1 AiiA Erwinia carotovora AHL (Dong et al., 2001) Virulence factors (Dong et al., 2000)
Bacillus sp. AHL-lactonase Erwinia carotovora HSL Virulence factors (Dong et al., 2001)
Bacillus thuringiensis AHL-lactonase Erwinia carotovora AHL Virulence factors (Dong et al., 2004)
Bacillus thuringiensis AiiA Erwinia carotovora AHL Virulence factors (Lee et al., 2002)
Rhodococcus strains LS31 and PI33 Erwinia carotovora AHL, OHHL Decrease in the number of AHLs, PL (Park et al., 2006)
Arthrobacter sp. IBN110 AhlD Erwinia carotovora AHL Decrease in the number of AHLs, PL (Park et al., 2003)
Streptomyces xanthocidicus KPP01532 Piericidin A and glucopiericidin A Erwinia carotovora subsp.atroseptica AHL Virulence factors (Kang et al., 2016)
Acinetobacter sp. strain C1010 Intracellular enzyme Erwinia carotovora ssp. carotovora 1238 AHL Degrade AHL (Kang et al., 2004)
Ginger root GG2, GG4, Se14 Erwinia carotovora AHL Virulence factors (Chan et al., 2011)
Ti plasmid AttM and AiiB Erwinia. carotovora subsp. atroseptica CFBP 6276 acyl-HSL Virulence factors (Carlier et al., 2003)
Agrobacterium tumefaciens C58 γ-butyrolactone Agrobacterium tumefaciens C58 acyl-HSL Interfere with acyl-HSL signalling (Carlier et al., 2004)
Korean red algae Floridoside, betonicine and isethionic acid Agrobacterium tumefaciensde OHL / (Escobar and Dandekar, 2003; Kim et al., 2007)
Pseudomonas spp. strain G carAB Xanthomonas campestris pv. campestris DSF Breakdown of DSF (Newman et al., 2008)
The marine alga Delisea pulchra Halofuranone Bacillus subtilis The formation of the biofilm (Ren et al., 2002)
Ralstonia solanacearum The polyamine putrescine Dickeya zeae. / Swimming, swarming and biofilm formation (Shi et al., 2019)
Bacillus amyloliquefaciens SQR-9 Volatile organic compounds (VOCs) Ralstonia solanacearum and Xanthomonas campestris pv. campestris eps Production of EPS; formation of biofilm; Production of polygalacturonase (Raza et al., 2016)
Bacillus megaterium CYP102A1 Cytochrome P450 / AHL Oxidation of AHLs (Chowdhary et al., 2007)
Phomopsis liquidambari 4-hydroxycinnamic acid Agrobacterium tumefaciens traI and traR Biofilm formation, motility, and flagellar formation (Zhou et al., 2022)
Bacteria D-amino acids Pantoea agglomerans YS19 / Biofilm formation (Vahdati et al., 2022)
Penicillium sp. PM031 Endo-metabolites Ralstonia solanacearum Virulence factors (Dey et al., 2022)

4.2.1

4.2.1 The secondary metabolites of microorganisms anti-Erwinia carotovora

Erwinia is a bacterium similar to E. coli that is parasitic on plants and causes spoilage. It mainly generates pectin lyase (PL), polygalacturonase, cellulase, and protease. These extracellular enzymes infiltrate and lyse plant tissues, helping bacteria colonize into internal vegetable tissues and further reproduce; in particular, PL has a dominant position (Barras et al., 1994).A large number of studies show that the signaling factor N-(3-oxo-hexanoyl)-L-homoserine lactone (3-oxo-C6-HSL) in Erwinia carotovora has two functions: i) The increased production of extracellular degradative enzymes with increasing levels of 3-oxo-C6-HSL (Jones et al., 1993). ii) 3-oxo-C6-HSL regulates the production of a broad-spectrum L-lactam carbapenem antibiotic (McGowan et al., 1995).

In 2001, Michael et al. (Manefield et al., 2001) showed that halogenated furanones extracted from D. pulchra antagonized the activity of the signaling factor 3-oxo-C6-HSL in Erwinia carotovora, and regulated the virulence factor expression and antibiotic production. They also suggested that halogenated furanones with 3-oxo-C6-HSL structural similarity and that halogenated furanones could control bacterial surface colonization by specifically interfering with AHL-mediated gene expression at the level, these offered the possibility of halogenated furanones inhibiting 3-oxo-C6-HSL, and reducing the ability of pathogenic bacteria to infect the host (Manefield et al., 1999).

AiiA, isolated from Bacillus sp. 240B1, with a gene encoding an AI-inactivating enzyme, was the first protein identified to inactivate N-acyl homoserine lactones enzymatically. Moreover, in 2000, Dong et al. introduced an aiiA-containing cosmid clone into E. carotovora strain SCG1 and tested whether AiiA enzyme expression significantly reduced AI release, modulated Erwinia carotovora virulence, reduced extracellular pectinase activity, and attenuated host plant pathogenicity (Dong et al., 2000). The group then investigated AiiA further and found that AiiA is able to hydrolyze the ester bond of the acyl homoserine lactones ring in AHL (Dong et al., 2001). Furthermore, the same research group (Dong et al., 2004) detected that AHL-lactonase in Bacillus thuringiensis can hydrolyze AHL in the plant pathogenic bacterium Erwinia carinii without affecting its growth. The discovery of AiiA has increased the interest among researchers QS in the microbial aspects of QS regulation. In 2002, Lee et al. (Lee et al., 2002) identified homologs of AiiA from Bacillus thuringiensis, and both have the ability to degrade AHL in Erwinia carotovora and reduce pathogenicity.

In 2006, Park et al. (Park et al., 2006) isolated two Rhodococcus strains (LS31 and PI33) from soil and identified that they both degraded different signaling molecules (various AHLs and N-(3-oxo)-octanoyl-L-HL (OOHL)), with strain LS31 being able to degrade AHLs of different lengths and acyl side chain substitutions. They found that LS31 was more effective in reducing the OHHL content and PL activity than PI33. To investigate whether this genus can degrade AHL, six different Rhodococcus-type strains (Rhodococcus coprophilus KCTC 9804, Rhodococcus equi KCTC 1298, Rhodococcus erythropolis KCTC 3483, Rhodococcus jostii KCTC 19938, Rhodococcus opacus KCTC 9811, and Rhodococcus rhodochrous KCTC 9086) were validated and all members of this genus were found to have AHL degrading activity. Previously, the group (Park et al., 2003) suggested that Arthrobacter sp. IBN110 could degrade AHLs of different lengths and acyl side chain substitutions and co-cultures of Arthrobacter sp. IBN110 with the plant pathogen Erwinia carotovora showed a reduction in the amount of AHL and PL activity. The ahlD gene in Arthrobacter sp. IBN110 was later cloned and found to encode a catalytic AHL degrading enzyme. It was also proposed that AhlD is an acyl homoserine lactamase (AHL) that may hydrolyze the lactone ring of N-3-hexanoyl-L-homoserine lactone.

In 2004, Kang et al. (Kang et al., 2004) found that Acinetobacter sp. strain C1010 could degrade AHL produced by E. carotovora ssp. carotovora 1238 further speculated that the AHL degradation activity could also be due to AHL bioinactivation via an intracellular enzyme mode of action in E. carotovora ssp. carotovora 1238.

In 2011, Chan and colleagues (Chan et al., 2011) isolated 10 bacteria genera from the ginger inter-rhizosphere and selected Acinetobacter (GG2), Burkholderia (GG4), and Klebsiella (Se14) to explore the effect for Erwinia carotovora. The GG2 and Se14 strains were shown to exhibit the most extensive AHL degradation activity through lactolysis, while GG4 reduced 3-oxo-AHLs (including 3-oxo-C6-AHL, 3-oxo-C8-AHL, et al) to the corresponding 3-hydroxy compound. GG2 was shown to inactivate both auto-produced AHL and exogenously supplied AHL. Finally, the above-mentioned ginger inter-root isolates influenced Erwinia carotovora virulence factor production.

In 2016, Kang et al. (Kang et al., 2016) isolated piericidin A and glucopiericidin A from Streptomyces xanthocidicus KPP01532, both of which resulted in reduced expression of four virulence genes (pelC, pehA, celV, and nip) in Erwinia carotovora. Both piericidin A and glucopiericidin A had attenuating effects on the virulence factors of Erwinia carotovora.

4.2.2

4.2.2 The secondary metabolites of microorganisms anti-Agrobacterium tumefaciensde

The Ti plasmid of Agrobacterium tumefaciens contains two lactase genes: attM and aiiB. It was also proposed that both lactase genes hydrolyze HSL. Carlier and colleagues (Carlier et al., 2003) introduced plasmid p6010 and its derivatives expressing lactase into E. carotovora subsp. atroseptica CFBP 6276 by electroporation, where it was observed that lactase reduced endogenous acyl-HSL levels and bacterial virulence in the plants. In 2004, Carlier et al. (Carlier et al., 2004) found that AttM enzyme involvement was required in the assimilation pathway of γ-butyrolactone, involved in A. tumefaciens C58, and that active AttM could interfere with acyl-HSL signaling.

In 2007, Kim et al. (Kim et al., 2007) extracted floridoside, betonicine, and isethionic acid from Korean red algae and have shown that a mixture of these three substances significantly inhibits the biological activity of the signaling molecule OHL of Agrobacterium tumefaciensde.

In 2022, Zhou et al. (Zhou et al., 2022) discovered that natural 4-hydroxycinnamic acid, namely HA, which isolated from Phomopsis liquidambari, had the ability to suppress the QS and virulence factors of A. tumefaciens. In detail, increased concentrations of HA are associated with an increase inhibitory effect on β-galactosidase activity and AHL secretion. Consequently, HA further suppressed the transcription levels of genes including traI and traR, and thus disrupting bacterial QS charactered by the reduction of biofilm formation, motility, and flagellar formation.

4.2.3

4.2.3 The secondary metabolites of microorganisms anti-Xanthomonas spp

Newman and colleagues (Newman et al., 2008) concluded experimentally that Pseudomonas spp. strain G could be used as a biocontrol agent against diseases caused by X. campestris pv. campestris and other Xanthomonas species, and also suggested that the degradation was due to Pseudomonas spp. strain G containing carAB, a gene with the ability to degrade DSF. In 2016, Su et al. (Su et al., 2016) found that the enzyme DgcA in c-di-GMP could negatively affect virulence, EPS production, bacterial self-aggregation, and motility but could positively regulate biofilm formation by regulating intracellular c-di-GMP levels, and further inhibit Xanthomonas oryzae pv. oryzae growth.

4.2.4

4.2.4 Other

Bacillus subtilis belongs to Gram-positive bacteria. In 1999, Michcel et al. (Surette et al., 1999) analyzed the database and further speculated that Bacillus subtilis might produce AI-2. Subsequently, in 2002, Ren et al. (Ren et al., 2002) also found that the (5Z)-4-Bromo-5-(bromomethylene)-3-butyl-2 (5H)-furanone (halofuranone) extracted from the marine alga Delisea pulchra could inhibit the formation of the biofilm of Bacillus subtilis by inhibiting AI-2.

CYP102A1, as the unique molecule, has the ability to oxidize the saturated and unsaturated long-chain fatty acids. In 2007, Chowdhary et al. (Chowdhary et al., 2007) found that CYP102A1, affiliated a member of the P450 family in Bacillus megaterium, could oxidize AHL and its breakdown product homoserine lactone, result in producing an inhibitory effect on both self and host QS.

In 2016, Raza et al. (Raza et al., 2016) reported that volatile organic compounds produced by strain Bacillus amyloliquefaciens SQR-9 had a significant negative impact on EPS and polygalacturonase production, biofilm formation and pathogenic bacteria Ralstonia solanacearum on tomato root colonisation as well.

In 2017, using proteomic analysis technology, Lowe-Power et al. (Lowe-Power et al., 2018) first revealed that R. solanacearum had the new metabolic virulence strategy though producing and excreting the abundant polyamine putrescine for infecting host. To prevent the infection by Ralstonia solanacearum, Dey and colleagues (Dey et al., 2022) in 2022 isolated a fungal endophyte PM031, identified as Penicillium sp. Interestingly, although strain PM031 was no active toward phytopathogen Ralstonia solanacearum, its endo-metabolites could attenuate the virulence factors, like motility and biofilm of Ralstonia solanacearum, and result in facilitating to controlling Ralstonia solanacearum infection.

Shi et al. (Shi et al., 2019) further discovered that putrescine was the vital active molecule during the process of the intraspecies and interkingdom cell–cell communication, which enable to significantly handicap the swimming and swarming motility and drastically attenuate the biofilm formation ability of Dickeya zeae.

Moreover, some bacterial metabolite also could be developed as potential anti-quorum sensing active molecule. For instance, D-amino acids (D-AAs), produced by numerous types of bacteria via the especial reversible reaction between racemase/epimerase enzymes and L-amino acid, could inhibit the P. aeruginosa biofilm at the nanomolar range (Kolodkin-Gal et al., 2010; Vahdati et al., 2022; Zhang et al., 2021).Another case studied by Wang et al. in 2014 revealed that D-Leu had the good ability to diminishes the Xanthomonas citri subsp. citri infection though preventing biofilm formation (Li and Wang, 2014).

Furthermore, a lot of literatures had been showed that the discovery of quorum sensing inhibitors emerges as the new tactic for the prevention and control of plant diseases. The common sensing signals of plant pathogenic bacteria mainly include AHL, DSF of Xanthomonas and DSF analogues of Ralstonia solanacearum. These signal factors further regulate the bacterial social activities and communication though regulating different genes in a variety of ways (Table 4) (Baltenneck et al., 2021). The most special is that quorum sensing inhibitors can control bacterial infection though regulating the bacterial behavior rather than killing them. Therefore, discovering and screen the plentiful quorum sensing inhibitors may highlight the new orientation for finding new and high-efficiency bacteriostatic agent with low pesticide-resistance risk.

Table 4 Quorum sensing molecules produced by phytopathogenic bacteria.
Single structure Signal molecule of QS system Plant pathogen bacteria Pathway

(AHL Signal molecules)		 C10-HSL Pseudomonas syringae AhlI, AhlR
OHHL, OOHL Pseudomonas syringae pv. tabaci PsyI, PsyR
C6-HSL, C8-HSL Ralstonia solanacearum SolI, SolR
OC8-HSL Agrobacterium spp. TraI, TraR
OHHL, HHL Erwinia amylovora EamR, EamI
OHHL Dickeya spp. ExpI, ExpR
OOHL, OHHL: Pectobacterium spp. ExpI, ExpR1/ExpR2; CarR/CarI
OHHL Pantoea stewartii EsaI, EsaR

(DSF Signal molecules)		 DSF; BDSF; CDSF Xanthomonas oryzae pv. oryzae rpf cluster (rpfB, rpfF, rpfC and rpfG)
DSF; DF Xanthomonas campestris pv. campestris rpf cluster; PigB
DSF Xanthomonas axonopodis pv. glycines rpf cluster
DSF Xyllela fastidiosa rpf cluster

(DSF-Derived Signal molecules)		 3-OH-MAME, 3-OH-PAME Ralstonia solanacearum PhcB, PhcS/PhcR

5

5 The relationship of QSIs with antibiotic resistance

According to the rules of evolution, never-ending battle occurs between the pathogen and its host. As once a panacea, antibiotics has stimulated the evolution of resistant mechanisms in bacteria in recent decades due to its abuse. If there will exist the same resistant issues in the treatment of bacterial infection via QSI? There is a distinct possibility that the new resistance mechanisms to QSIs might be similar to antibiotic resistance mechanisms. Some factors including efflux pumps, point mutations endows bacteria to decrease the sensibility towards QSI (Kalia and Kumar, 2014; Koul et al., 2015; Patel et al., 2023).

In fact, the probability of regarding QSIs resistance issues is extremely low in comparison of antibiotics-induced resistance. For instance, Ning et al. in 2021 found that the co-use of QSIs with antibiotics showed the antagonistic or additive joint effects on bacterial growth, and thus result in reducing the antibiotic-induced resistance mutations in bacteria (Ning et al., 2021). Hence, quorum sensing inhibitors are expected to become a new and effective way to control antimicrobial resistance (Naga et al., 2023; Patel et al., 2023).

6

6 Conclusion

There are many important benefits to inhibit plant pathogen proliferation via regulating QS. First, QS is a naturally occurring bacterial communication mechanism, allowing precise intervention in bacterial growth and reproduction processes to effectively inhibit bacterial growth. Second, QSIs comprise mainly natural products that are less toxic and safer for humans and the environment. Finally, the development and application of QSIs offer a new method of biological control in agricultural production. Therefore, the use of QSIs to inhibit the growth of plant pathogenic bacteria has important practical significance and application prospects.

Therefore, the microbial communication system is the command center for the pathogenicity of pathogens and a new entry point for disease prevention and control. QSIs can block the communication system of pathogenic microorganisms, interfere with the “language” communication of microorganisms, and make microorganisms become “deaf and dumb” out of control individuals, thus achieving green prevention and control of microbial diseases and becoming a potential alternative antimicrobial drug with a novel mechanism of action. It is expected that highly effective QSIs from the natural product library will be screened, which will provide an effective way to solve the problem of bacterial infection and drug resistance. Despite the many advantages of QSIs, challenges and limitations to their development and application remain. For example, ensuring inhibitor stability, improving their efficacy, and reducing production costs still need to be investigated and explored further.

In the future, combination with computational, cytogenetic, molecular genetics, proteomic, and other disciplines is a good idea to explore the mechanism of quorum sensing and the screening and discovery of natural products further through multidisciplinary interdisciplinary research. Given the rapid development of computational approaches, de novo molecular design has been successfully operated over the past 30 years and, thus, development of new QSIs with efficient and broad-spectrum inhibitory activity may be stimulated by the advances in machine learning (ML) and artificial intelligence (AI). For example, High-Throughput Mining of natural QSIs (Meena et al., 2024). Furthermore, quorum sensing inhibitors were modified, and/or gifted by materials to achieve a quantitative release, precise control effect, and synergistic antibacterial effect under the low resistance risk (Celik et al., 2020). And this strategy also involves the optimization of delivery systems such as the adopt of nanotechnology to improve bioavailability, stability and absorption facilitating its agriculture application. Moreover, through an in-depth study of the QS mechanism of pathogenic bacteria, more specific inhibitors are expected to be designed and developed to precisely target pathogens and reduce the impact on non-target microorganisms. Fourthly, to avoid pathogenic bacteria becoming resistant, the resistance risk assessment should be concerned (Gupta and Kumar, 2022). Other strategies can be used alternately with different types of QSIs or in combination with other types of bactericides or biological control methods to improve control effectiveness and reduce the risk of resistance. In addition, the environmental stability of QSIs can be improved by optimizing natural product structures to make them more stable or by preparing them as more stable nanomaterial complexes, for example, so that they can maintain a stable effect under different environmental conditions.

CRediT authorship contribution statement

Ai-Qun Chen: Writing – original draft, Visualization. Zhou-Qing Long: Writing – original draft, Visualization, Conceptualization. Ya Xiao: Investigation, Data curation. Yu-Mei Feng: Investigation, Data curation. Ya Zhou: Data curation, Investigation. Shan Yang: Investigation, Data curation. Yan-Mei Liao: Investigation, Data curation. Xiang Zhou: Writing – review & editing, Investigation, Funding acquisition. Li-Wei Liu: Validation. Zhi-Bing Wu: Validation. Song Yang: Writing – review & editing, Supervision, Project administration, Funding acquisition.

Acknowledgements

This research was financially supported by National Natural Science Foundation of China (32372610, U23A20201, 32160661, 32202359), National Key Research and Development Program of China (2022YFD1700300), the Central Government Guides Local Science and Technology Development Fund Projects [Qiankehezhongyindi (2024) 007] and [Qiankehezhongyindi (2023) 001].

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