The functionality of plant-microbe interactions in disease suppression

2.1 Plant-associated microbes

Plants interact with their environments, including the different microbiota, which confers diverse useful traits to the plants which include stress tolerance, enhancement of nutrient uptake, and disease resistance. In contrast, host plants provide carbon to the associated microbes. Microbes associated with plants are either beneficial, like the plant growth-promoting rhizobacteria, biocontrol rhizobacteria, or detrimental, causing diseases in plants by destroying tissues, wilting, lesions, drying and/or eventual death. These plant-associated microorganisms can also be found in the rhizosphere, where they form association with plants as biocontrol agents and increase plant growth. Some of them are found on the phyllosphere, in plant tissue (endosphere), and sometimes on the stems. Plant-associated microbes have been known to work symbiotically with plants where they impact the development and functionality of plants (Hassani et al., 2018). These impacts include the release of metabolites and hormones from bacteria that improve crop growth and production (Kumar et al., 2017; Olanrewaju et al., 2019) and protection of host plants against pathogen infection by disease suppression, parasitism, induced systemic resistance (ISR) and metabolite production (Adeleke et al., 2019). Bacteria from the phyllosphere can affect plants’ species distribution over time and ecosystem function by influencing plant production under various environmental factors (Hassani et al., 2018).

2.2 Plant defense mechanisms

In nature, plants have two main mechanisms of defense against pathogens which are resistance and tolerance. Tolerance is achieved because of a pathogen establishment in the system of the host and the damage it causes. Resistance, usually of chemical nature is observed when the host suppresses or reduces the growth of the pathogen (Burdon et al., 2016; Olanrewaju et al., 2019). Resistance lowers the risk of infection and pathogen multiplication, while tolerance does not. If plants develop resistance, pathogen prevalence will decrease, whereas tolerance has the opposite effect (Montes et al., 2020).

The plant's ability to recognize pathogens and protect itself from infection is essential. Plants have developed many ways to protect themselves, such as being able to recognize chemicals or molecular patterns that are unique to pathogens. When these patterns or chemicals are sensed, the plant's innate immunity is activated (Olanrewaju et al., 2019; Gourion and Ratet, 2021). Furthermore, the presence of foreign molecules sets off several defense mechanisms, such as structural hardening, biochemical deterrents, and the production of pathogenesis-related (PR) proteins (Pathak et al., 2022). The main way a plant protects itself from pathogens is by having an impenetrable shield made of the bark and a hydrophobic cuticle. However, mechanical damage can weaken this defense, making plants easier to invade. The production of antimicrobial chemicals, the release of signaling molecules to attract helpful microbes, and the creation of systemic acquired resistance (SAR) are other ways that plants fight pathogens. The basic mechanisms of innate immunity plants use are microbe-associated molecular pattern (MAMPs) or pathogen-associated molecular pattern (PAMPs)-triggered immunity (MTI or PTI) using pattern recognition receptors (PRR) and effector-triggered immunity (ETI) (Samad et al., 2019; Olanrewaju and Babalola, 2022). Other molecular patterns recognized are the Nematode-Associated Molecular Patterns (NAMPs) which is a group of molecules that are secreted by nematodes (Choi and Klessig, 2016) and the Damage-Associated Molecular Pattern (DAMP) (Olanrewaju and Babalola, 2022). These molecular patterns are highly conserved molecules in microbes, such as flagellin, that are only detected when pathogens interact directly with host plant receptors. (Olanrewaju and Babalola, 2022; Pathak et al., 2022). Examples of MAMPs include bacterial lipopolysaccharide, flagellin which is recognized by the FLS2 receptor in plant cells, lipoproteins, peptidoglycans that interacts with NOD-like receptors, and fungal chitin (Wang et al., 2022). The binding of PRR to MAMP helps plants to recognize beneficial microbes and pathogens.

The detection of MAMPs/PAMPs by plants results in SAR/ISR pathways, which boost host resistance through the activation of PTI or ETI. Pathogens can sometimes evade the plant MTI and still cause diseases; in such cases, ETI using leucine-rich-repeat receptors is triggered by plants against pathogens. Khoshru et al., (2023) and Wang et al., (2022) have written very good reviews on this subject.

To make a plant and microbe partnership work, the plant must avoid setting off its immune response, ETI. Reportedly, certain genes and proteins control beneficial effects of plant microbes (Zhang et al., 2021). If the microbe and plant are not compatible i.e., pathogenic microbes, the plant will not allow the pathogenic microbe in, but beneficial microbes can still enter (Gourion and Ratet, 2021). This can help the plant resist diseases. It is important for a plant to balance its protection and allowing beneficial microbes in for a successful partnership.

3.1 Plants and disease challenges

Massive losses of planted crops are incurred in agricultural outputs globally due to pathogenic microbes and plant pests. This reduction in productivity leads to huge losses economically and affects food security globally, nationally and at household levels (De Silva et al., 2019; Savary et al., 2019).

One prevalent approach to addressing this issue involves the application of synthetic agrochemicals. Nonetheless, this method proves costly and has detrimental effects on the environment, as well as the health of animals and humans. Moreover, the persistent use of these chemicals fosters the development of pathogen resistance and the emergence of new pathogens and pests. Additionally, the use of synthetic agrochemicals can disrupt the balance of existing beneficial soil microbiota (French et al., 2021), leading to increase in the susceptibility of plants to pathogens in the soil. A sustainable and eco-friendly alternative is the deployment of antagonistic microbes that can suppress disease-causing pathogens. These diseases and pests suppressing organisms are generally called biological control agents (BCA). These biocontrol agents, depending on their beneficial applications, could be termed biopesticides or biofertilizers.

The benefits of BCAs over synthetic agrochemicals applications include no need for re-application at every cropping season as they could persist in the ecological environment by establishing, replicating, and colonizing the above and below ground plant regions (Zeilinger et al., 2016) unlike synthetic fungicides.

3.2 Plant microbiota allied with disease suppression

Plant microbiota play a pivotal role as key suppressors of plant diseases, while the holobiont ensures fitness through the maintenance of health and the suppression of microbial dysbiosis (Berg et al., 2017). They achieve this feat through enhancing plant vigor by mobilizing nutrients, directly antagonizing phytopathogens through parasitism or antibiosis, and competing for available resources through niche colonization. Another mechanism employed by these microbes is the induction of immune activity (Teixeira et al., 2019).

Numerous microbiota are actively involved in disease-suppressive soils. Newer high throughput sequencing techniques and omics technologies have exposed researchers to insights that communities of diverse microbes are involved in interactions between microbial biocontrol agents and the suppression of phytopathogens (rather multi-species/ consortia of beneficial microbial control agents against multi-species pathogens). Insights from disease-suppressive soils have revealed that pathogens encounter an unsuitable environment for growth due to the presence and influence of beneficial microbiome communities. These communities exert both specific and general suppressiveness on disease-causing pathogens (Mazzola and Freilich, 2017). Mousa and Raizada (2016) reported that Gaeumannomyces graminis var. tritici disease infection in wheat plant was suppressed with consortia of Pseudomonas and Fusarium species acting synergistically in producing metabolites and inducing physiological changes in the soil that led to disease suppressive attributes.

4.1 Bacterial – Assisted disease suppression

As earlier said, this is a kind of interaction that is seen between bacteria (biocontrol agent) and a bacterial pathogen. Here, the bacteria having a biocontrol capability is applied to plant roots to contain bacterial-causing diseases in plants. An example is the involvement of Bacillus subtilis MBI 600 in the control of gray mold in cucumber plants caused by Botrytis cinerea (Samaras et al., 2021). This interaction involves biocontrol, where microbes in the rhizosphere compete for space and nutrients, exhibit induced systemic resistance (ISR), or engage in antibiosis. A recent study highlighted the utilization of beneficial induced systemic resistant bacteria in the rhizosphere for controlling leaf infections caused by the biotrophic bacterial pathogen, Pseudomonas syringae (Berendsen et al., 2018). In another study, Trong et al., (2022) observed a significant reduction in the incidence of tumors, commonly referred to as crown gall disease, in grapevine crops caused by the pathogenic Allorhizobium vitis using Paraburkholderia phytofirmans PsJN. However, the process of bacterial-based biocontrol may also encompass other mechanisms, such as the development of antibiotics, contributing to this phenomenon. Samaras et al., (2021) examined whether treating plants with the biocontrol agent B. subtilis MBI 600 can induce defense responses and enhance control efficacy against B. cinerea. The authors analyzed the transcription patterns of five marker genes at different time points and found that all tested genes were highly induced in B. subtilis MBI 600 inoculated plants compared to mock-inoculated plants. The findings showed that the bacterial strain studied had the ability to activate the plant’s basal immune responses. Furthermore, this result suggests that plant treatment with B. subtilis MBI 600 can not only control B. cinerea effectively but also stimulate the plant's immune system. This is a significant finding, as it indicates that the use of biocontrol agents like B. subtilis MBI 600 can be an effective strategy to manage plant diseases sustainably. The induction of basal immune responses also suggests that the plants are better equipped to defend themselves against future pathogen attacks. Other studies have proven that plants under pathogenic attack engage microbes in their rhizospheres for protection (Perea-Molina et al., 2022; Yang et al., 2023). The recruitment of beneficial microbes in the rhizospheres of attacked plants have also been demonstrated in wheat monocultures which developed disease suppressiveness because of the production of 2,4-dicetylphoroglucinol by Pseudomonads, after an outbreak of take-all disease (Weller et al., 2002).

4.2 Bacterial antagonists: Effective management of soil-borne fungal infections in plants

There are several pathogenic fungi that infect plants, and these pathogens are capable of infecting different plant parts including the leaves, fruits, roots, and stems. However, numerous studies have also exhibited the management of soil borne fungal infections using bacterial communities and this is due to the rising simplicity with the use of molecular approaches that can be applied to determine the occurrence, distribution, parallel significance, and the specific ways in which various bacterial antagonists act (Madkour et al., 2019; Gogoi et al., 2020). Various bacteria can control the emergence and spread of soil-borne fungal diseases by applying them in the soil, and in plant seeds (Ueki et al., 2018). Certain species of bacteria such as Pseudomonas putida, P. aeruginosa, P. aureofaciens, Bacillus subtilis, B. cereus, B. Polymyxa, and Burkholderia cepacia have shown outstanding results in the control of several soil-borne diseases of fungi (Shafi et al., 2017; Murugan, 2019). The application of these bacterial antagonists to most agricultural plants like rice, sugar beet, wheat, cotton and different vegetables can control the growth of fungal pathogens including Fusarium oxysporum, Verticillium dahlia, F. solani, Rhizoctonia solani, Gaeumanannomuces graminis that are capable of causing soil-borne diseases of plants, for instance, the take all, damping off, root rot, vascular wilt, and seed rot (Majeed et al., 2018; Vurukonda et al., 2018; Abbasi et al., 2019). Streptomyces species such as S. lividans, S. griseus, S. coelicolor have also been found to protect plants against fungal pathogens (Vurukonda et al., 2018). Anderson et al., (2004) in their study, indicated the possibility of using biological materials to control the growth of fungal pathogens in the phyllosphere. Therefore, they proposed that the emergence and development of various diseases can be reduced with the use of bacterial antagonists. A taxonomic analysis of sugar beet root microbiome planted in a soil which suppresses the root associated fungal pathogen R. solani showed a consistency in the association of many bacterial genera with the disease suppressive state. Hence, the upregulation of genes associated with stress in bacterial families was more exuberant on the roots of plants grown in the suppressive soil (Cordovez et al., 2019). The authors of this study hypothesized that the fungal pathogen activates responses in the root microbiome, either directly or indirectly, which causes shifts in composition and triggering of special antagonist characteristics that prevent the growth of pathogens (Cordovez et al., 2019). Similarly, some species of Pseudomonas obtained from Greenland soil repressed potato scab infection triggered by R. solani (Gómez Expósito et al., 2017; Cordovez et al., 2019). A study reported an enhanced resistance against Erysiphe pisi, a plant pathogen that causes powdery mildew by rhizobia species in Medicago truncatula (Smigielski et al., 2019).

4.3 Fungal-assisted disease suppression

Numerous researchers have focused on the interactions between fungal biocontrol agents and plant diseases caused by fungi on an equal footing with studies involving bacterial-fungal pathogen interactions that were earlier discussed. Nevertheless, fungi-fungi interactions are a special type of interactions because fungi can grow better than bacteria in the surrounding soils because of hyphal growth. The biocontrol capacity of several fungi has been investigated in recent research works, although majority of the studies seem to be on Trichoderma species which could reflect their easy growth and ability to grow within a wide range of host. Fungal species of particular interest in biocontrol studies include those of P. oligandrum Drechsler (Baturo-Cieśniewska et al., 2018) and Trichoderma species (Degani and Dor, 2021), among others. Plant pathogens that are mostly targeted by these biocontrol fungi are: Rhizoctonia solani, Pythium, and Fusarium species. These fungal pathogens are of immense agricultural and world-wide importance and are easily controlled under protected cropping systems.

4.4 Mechanisms of microbial disease suppression: An overview

Research indicates that various enzymes and bacteria contribute to disease suppression and plant growth promotion (Olanrewaju and Babalola, 2019; Mir et al., 2022). Pseudomonas, Bacillus, Streptomyces, and other beneficial microbes play a role in plant disease suppression through siderophore-mediated competition for iron, antibiosis, production of lytic enzymes, and ISR (Ankati et al., 2021; Agbodjato et al., 2022; Zeng et al., 2023). Additionally, bacteria that produce the enzyme 1-aminocyclopropane-1-carboxylate (ACC) deaminase contribute to plant growth, particularly under environmental stress conditions (Glick and Nascimento, 2021). ACC deaminase breaks down ACC, the precursor of ethylene, into α-ketobutyrate and ammonia. By reducing ethylene production in plants, this enzyme helps sustain plant growth and development during biotic and abiotic stress conditions (Fig. 1).

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Fig. 1

Schematic diagram of ACC deaminase-containing beneficial microbes stimulating plant development. Stress boosts IAA and ethylene production, reducing plant growth. ACC deaminases reduce ethylene levels which keeps bacterial IAA thereby promoting plant development. Thus, beneficial microbe that produce both IAA and ACC deaminase reduce plant growth inhibition from many environmental stresses. Beneficial microbes protect plants from ethylene-producing conditions like fungal and bacterial phytopathogens (Olanrewaju et al., 2017).

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Bacillus spp. has been reported to produce indole-3-acetic acid, gibberellic acid, and ACC deaminase that helps in regulating the intracellular phytohormone, initiating the antioxidant and defense systems, and increasing plant stress tolerance (Narayanasamy et al., 2020; Patel et al., 2023).

Siderophores are small molecules that are produced by bacteria and fungi to scavenge iron from the environment (Olanrewaju et al., 2017). Iron is an essential nutrient for the growth and survival of microbes, and siderophores play a key role in high-affinity iron acquisition in both pathogenic and non-pathogenic bacteria and fungi (Fig. 2) (Olanrewaju and Babalola, 2022). Siderophores are also involved in the biocontrol mechanism of beneficial microbes by depriving the pathogen of iron nutrition, thus resulting in increased yields of crops (Nithyapriya et al., 2021). The role of siderophores in natural conditions is still not fully understood. In addition, siderophores can function as virulent factors in pathogenic organisms by facilitating iron uptake from the host. Therefore, the mechanism of siderophore-mediated disease suppression involves the production of siderophores by microbes to scavenge iron from the environment, which deprives pathogens of iron nutrition and reduces their virulence.

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Fig. 2

Schematic representation of three bidentate groups of a siderophore molecule binding to iron (Olanrewaju et al., 2017).

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5.1 Root exudation to recruit microbial partners: Plant’s rescue call

The first study to report root-microbe relationship was carried out on ultrathin sections of wheat rhizosphere microbiome by Foster and Rovira (1976). Many processes occurring in the rhizosphere microbiome are not passive, they are induced by external influences. These external factors serve as mediators linking the various processes (Olanrewaju et al., 2019). They are said to therefore act as signals in the activation or regulation of different processes in the rhizosphere. This is one of the key functions of root exudates in rhizosphere microbial interplay. They help in recruiting beneficial microbes to the rhizosphere thereby connecting communications that occur in the rhizosphere (Fig. 3). During this process, they exert a significant effect on the plant’s health.

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Fig. 3

Soil microbiome response to plant signals. Left panel, plant signals to the soil microbiome arising from pathogen attack, nutrient, or water deficiency; center panel, the response of the various microbes to the exudates released by the plant; right panel, plant growth response to biocontrol mechanisms provided by recruited microbes. There is a positive response as pathogens do not respond to the signals (Olanrewaju and Babalola, 2022).

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Plants secrete root exudates in response to various external factors. We are going to deal only with the release of exudates in response to pathogen attack on plants. The infestation of plants by diseases induces multiple biological, biochemical, and genetic changes and modifications to plant processes and development. These changes invariably induce the exudation of various metabolites majorly through the roots into the rhizosphere. These exudates serve as signal molecules to the plant environment to call for help and support because they attract beneficial microbes to the roots of the plants. These microbes, through various mechanisms, would then help the plants to fight against various diseases. This process of interactions of the microbes with the plants as an effect of the root exudates is still not adequately fathomed (Hayat et al., 2017). However, there have been recent developments in this regard for this purpose. However, common elements of signal pathways in the rhizosphere because of root exudate impact induces a high level of interactions between plants and microbes thus, regulating responses in the rhizosphere (Olanrewaju et al., 2019). Exudates such as monosaccharide sugars (fructose, mannose, and glucose), disaccharide sugars such as maltose, five-carbon sugars such as arabinose, and oligosaccharide sugars. There are also amino acids such as glutamine, aspartate, arginine, cysteine, and asparagine; organic acids (acetic, malic, ferulic, and benzoic acids); phenolics like coumarin. Others include high-molecular-weight compounds like auxins, tannins, alkaloids, terpenoids, flavonoids, fatty acids, vitamins, enzymes, and polyacetylenes (Hayat et al., 2017).