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Review

Insight into the Microbiological Control Strategies against Botrytis cinerea Using Systemic Plant Resistance Activation

by
Jorge Poveda
*,
Marcia Barquero
and
Fernando González-Andrés
Institute of Environment, Natural Resources and Biodiversity, University of León, 24071 León, Spain
*
Author to whom correspondence should be addressed.
Agronomy 2020, 10(11), 1822; https://doi.org/10.3390/agronomy10111822
Submission received: 14 October 2020 / Revised: 12 November 2020 / Accepted: 18 November 2020 / Published: 20 November 2020
(This article belongs to the Section Pest and Disease Management)
Versions Notes

Abstract

:
Botrytis cinerea is a polyphagous necrotrophic fungus and is the causal agent of grey mold diseases in more than 1400 different hosts. This fungus causes serious economic losses in both preharvest and post-harvest—mainly in grape, strawberry, and tomato crops—and is the second most important pathogen worldwide, to our knowledge. Beneficial bacteria and fungi are efficient biocontrol agents against B. cinerea through direct mechanisms, such as parasitism, antibiosis, and competition, but also indirectly through the activation of systemic plant resistance. The interaction between plants and these microorganisms can lead to the development of defensive responses in distant plant organs, which are highly effective against foliar, flower, and fruit pathogens, such as B. cinerea. This review aimed to explore the systemic plant defense responses against B. cinerea by compiling all cases reported (to the best of our knowledge) on the use of beneficial bacteria and fungi for agriculture, a subject not yet specifically addressed.

1. Introduction

Botrytis is a highly diverse fungal genus including numerous species that differ in their biology, ecology, morphological features, and host range. Progress in molecular genetics and the development of relevant phylogenetic markers in particular has resulted in the characterization of approximately 30 species. Species of Botrytis are responsible for relevant losses in a number of economically important horticultural and floral crops [1].
Botrytis cinerea Pers.:Fr is the most commonly studied polyphagic fungus. Although B. cinerea is the name of the asexual stage (anamorph) and Botryotinia fuckeliana is the name of the sexual stage, the Botrytis community agreed in 2013 at the Botrytis Symposium in Bari to use Botrytis cinerea as the generic name [1]. The life cycle of this fungus includes sclerotia developing within dying host tissues, representing an important survival mechanism. Sclerotia commences its growth in the early spring in temperate regions to produce conidiophores and multinucleate conidia. The sexual lifecycle of this fungus involves the spermatization of sclerotia, leading to the production of apothecia and asci with eight binucleate ascospores serving as the primary source of inoculum within a crop [2,3].
The infection process of B. cinerea is usually described with the following stages: penetration of the host surface, killing of the host tissue/primary lesion formation, lesion expansion/tissue maceration, and sporulation [4]. This necrotrophic fungus is responsible for a very wide range of symptoms, which cannot easily be generalized across plant organs and tissues. Soft rots, accompanied by collapse and water soaking of the parenchyma tissues and followed by a rapid appearance of grey masses of conidia, are the most typical symptoms on leaves and soft fruits. For many fruits and vegetables, the infection commonly begins on attached senescent flowers and then spreads as a soft rot, affecting the adjacent developing fruit (blossom-end rot), such as strawberries and apples. Moreover, seed-borne infections have been reported in over 50 hosts, where grey mold often begins by rotting the herbaceous stems at ground level, with other soft-rot lesions also appearing on leaves and pods [3]. In this sense, B. cinerea is an interesting model system for necrotrophic pathogens; however, it is not easy to study, since there are frequent variations of its karyotypes among natural strains [1].
B. cinerea is a highly polyphagous fungal plant pathogen, causing grey mold on more than 1400 known hosts in 586 plant genera and 152 botanical families, from mosses to gymnosperms and eudicots [5,6]. This pathogen has a disastrous economic impact on various economically important crops, including grape, strawberry, and tomato. Although this fungus causes serious pre-harvest problems, B. cinerea is considered one of the most important post-harvest pathogens in fresh fruits and vegetables. The annual economic losses of B. cinerea easily exceed $10 billion worldwide, possibly reaching as high a $100 billion. Due to both its economic and scientific importance, B. cinerea has been classified as the second most important plant pathogen. Controlling this fungus is difficult because it has a broad host range, various attack modes, and both asexual and sexual stages allowing it to survive. To date, the principal means to control grey mold rot caused by B. cinerea remains the application of synthetic fungicides, with a global investment that exceeds $1 billion. However, the use of conventional fungicides is not an adequate control strategy due to development of resistant strains and risks on human health and the environment [7]. Therefore, new effective and safe control strategies must be sought, such as those based on biocontrol.

2. Direct Biocontrol against B. cinerea

In recent years, the use of microbial biofungicides based on microbial biocontrol agents has increased continuously due to public concerns regarding the risk of pesticide residues in food and their negative impacts on the environment. For microbiological biocontrol, several fungal and bacterial strains have been successfully tested against grey mold on a variety of crops.
The bacterial genus Bacillus includes species widely studied and used as biocontrol agents against phytopathogenic fungi in agriculture due to their diverse secondary metabolism and ability to produce a wide variety of structurally different antagonistic substances, a mechanism of action known as antibiosis [8]. In this way, inhibition of the grey mold disease in tomato leaves between 75% and 90% has been achieved, thanks to metabolites released into the environment by B. subtilis and B. licheniformis [9,10], such as in strawberry plants [11,12]. This is due to compounds, such as the lipopeptides iturin, bacillomycin, fengycin, and surfactin, in which the efficiency was determined both in vitro by B. velezensis [13] and, in post-harvest apples, by B. subtilis [14]. Moreover, B. subtilis and B. amyloliquefaciens have been described as species with the capacity to produce and release antifungal volatile organic compounds (VOCs) against B. cinerea, thereby inhibiting the germination of their spores and the growth of their hyphae, both in vitro and in planta [15,16]. Finally, bacteria can compete in the phyllosphere for space, preventing the establishment of and attacking the necrotrophic fungus, as verified with B. amyloliquefaciens in tomato leaves, thanks to the formation of biofilms [17].
Antibiosis is also used by other bacteria to control B. cinerea, such as the release of antifungal compounds by Pesudomonas sp., Serratia plymuthica, and Streptomyces philanthi (e.g., antibiotic pyrrolnitrin or different VOCs), capable of totally inhibiting the germination of the spores of the fungus in vitro and decreasing the incidence of the disease in tomato and cucumber by greater than 75% [18,19,20]. In grapevine and strawberry leaves and fruits, it has been possible to verify how the bacteria Pantoea ananatis and Lactobacillus plantarum, respectively, compete effectively for space by rapidly colonizing wounds before the establishment of B. cinerea and suppressing the mycelial growth and disease symptoms [21,22]. In addition, bacteria, such as Paenibacillus elgii, are capable of releasing chitinolytic enzymes [23], a mechanism possibly linked to the ability of Rahnella aquatilis to parasitize the spores of the necrotrophic fungus on the surfaces of post-harvest apples [24].
For yeasts, few studies have been carried out in planta, but the use of yeasts as antagonistic microorganisms in the coating of fruits for the post-harvest control of B. cinerea represents one of the most widespread alternatives in biocontrol. The most commonly used yeast species against B. cinerea is Aureobasidium pullulans due to its ability to compete effectively for space and nutrients, both on the plant surface and in wounds, and for the release of different antifungal compounds, with successful applications in the post-harvest industry in grapes and kiwifruits [25,26,27]. In this regard, effective antagonism has also been described through the release of VOCs in strawberries by Galactomyces candidum [28] and the competition for space in wounds by Rhodotorula glutinis [29]. In addition, in planta, for both tomato leaves and post-harvest grapes, it has been possible to significantly inhibit the development of the fungus and the appearance of the disease, thanks to the ability of Candida oleophila and Pichia membranifaciens, respectively, to produce chitinase and glucanase enzymes that degrade the fungal cell wall [30,31].
Within filamentous fungi, the genus Trichoderma stands out as the main biological control agent against B. cinerea. Various species within this genus are widely used as biological control agents in agriculture due to their direct-action mechanisms, such as mycoparasitism, antibiosis, and competition for space and nutrients in the rhizosphere [32]. These mechanisms are also effective for the control of B. cinerea, with up to 75 species within the genus capable of actively mycoparasitizing the fungus, penetrating its cell wall through the production of different glucanases and chitinases. In addition, there is a very wide diversity of secondary metabolites produced by different Trichoderma species capable of inhibiting the growth and development of B. cinerea and even irreversibly damaging its cells. Some of these secondary metabolites are pyrones, butenolides, azaphylones, anthraquinones, trichothecenes, terpenoids, steroids, and peptaibols [33]. For this reason, Trichoderma has been also used as a source of genes for the development of transgenic plants resistant to B. cinerea [34]. Other species of filamentous fungi are capable of producing and releasing chemical compounds that effectively antagonize the development of grey mold. Inhibition in the growth of hyphae close to 90% has been reported, together with total inhibition of the germination of their spores, both through the diffusion of metabolites and through the production of VOCs by Albifimbria verrucaria, Metarhizium anisopliae, and Ulocladium atrum [35,36,37].

3. Systemic Plant Resistance and B. cinerea

When a pathogen, such as B. cinerea, crosses the constitutive plant defensive barriers, the plant must defend itself by activating a specific defensive response. For this, it is necessary for the plant to recognize the attacking pathogen through what is known as the pattern recognition receptors (PRRs) of the plant cells, which will recognize the molecular components of these microorganisms, called the pathogen-associated molecular pattern (PAMP). As a consequence of this recognition, the plant will activate a first-layer defense response called PAMP-triggered immunity (PTI). Plant responses occur in the organ where the plant was originally attacked (local response) and also in the distant plant parts that are unaffected (systemic response) [38,39].
These defensive responses are coordinated by stress hormones, such as salicylic acid (SA), mostly associated with biotrophic pathogens, as well as jasmonic acid (JA) and ethylene (ET), against necrotrophic pathogens and herbivores. After an attack from a biotroph pathogen and the occurrence of a programmed cell death response in a plant, a broad-spectrum immunity to reinfection through the whole plant body is activated in the plant, called systemic acquired resistance (SAR). SAR signaling is mainly mediated by SA-derived compounds, such as methyl salicylate (MeSA). Similarly, against necrotrophic pathogens and herbivores, the response known as induced systemic resistance (ISR) is activated. ISR is regulated by JA/ethylene (ET) signaling, although dependence on SA signaling has also been reported. Both SAR and ISR are indirect modes of action used by different biocontrol agents and involve considerable energy consumption by the plant [39].
In relation to all of the above, a plant’s ability to pre-activate its defensive responses has been extensively verified to occur through priming without the plant have to come into contact with pathogenic microorganisms or receive signals from nearby plants that have done so. Through this mechanism, plants take defensive measures against a potential attacker while also preparing their defensive systems for a faster and/or stronger reaction in the future. Although beneficial microorganisms, such as plant growth-promoting rhizobacteria (PGPRs) and plant growth-promoting fungi (PGPFs), are most commonly involved in the development of priming, different chemical compounds can activate this mechanism, such as SA, JA, β-aminobutyric acid (BABA), probenazole, and benzothiadiazole [39].
During infection, B. cinerea penetrates the plant-cuticle by secreting lytic enzymes and phytotoxins. Consequently, plants accumulate reactive oxygen species (ROS) in the plasma membranes of the host cells to trigger an oxidative burst, leading to plant cell death. As verified in Arabidopsis thaliana, there is a receptor-like cytoplasmic kinase PRR called Arabidopsis Botrytis-induced kinase1 (BIK1) that recognizes the PAMPs associated with B. cinerea, activating the corresponding PTI [40,41,42].
A plant’s defense against necrotrophic pathogens, such as B. cinerea, is greatly dependent on crosstalk among the phytohormones SA, JA, and ET. The role of SA signaling in plant resistance to B. cinerea is still unclear. Although SA appears to negatively regulate defense responses to B. cinerea, its role is quite complex. On the other hand, the JA signaling pathway is crucial in inducing resistance against B. cinerea, while ET may play a “two-faced” role in disease resistance, depending on the plant species, triggering both negative and positive responses in plant defense against this necrotrophic fungus. In this respect, the synergistic activity of the JA and ET signaling pathways has been well-characterized after B. cinerea infection, showing an antagonistic interaction between SA and JA in which ET acts as a fine-tuning modulator. Therefore, the systemic plant response against B. cinerea is necessarily linked to the ISR and JA/ET pathways [41,42].
Systemic plant resistance against B. cinerea is not only activated after the attack of the pathogen but can also be pre-activated by the exogenous application of various chemical compounds and biological elicitors. The exogenous application of plant defense hormones in fresh products during post-harvest has been shown to be capable of activating plant resistance against attacks from different pathogens, which occurs with the exogenous application of compounds derived from JA, such as methyl jasmonate (MeJA) [39]. In planta, various chemical compounds capable of activating a priming-type systemic resistance against B. cinerea have been described, such as BABA in A. thaliana [43] and tomato [44], benzothiadiazole (BTH) in poinsettia [45], hexanoic acid [46] and riboflavin in tomato [47], and elicitors, such as chitosan [48] and laminarin, in grapevine [49]. In this sense, mechanical damage and wounds are also capable of activating a plant’s systemic resistance against B. cinerea [50,51], as well as adverse environmental factors, such as high temperatures [52] and UV radiation [53]. Moreover, the conditions of cultivation may be able to activate a plant’s systemic resistance against B. cinerea. Indeed, priming against the pathogens in hydroponic crops has been described [54] after the addition of biochar [55] and olive mark compost [56]. In this respect, the activation of systemic defense responses against B. cinerea, thanks to beneficial bacteria and fungi has also been described.

4. Bacteria as Inductors of Plant Resistance against B. cinerea

Plant-microbe interactions play an important role in nutrient mobilization and protection against pathogens and are crucial for proper growth and development. In the interaction between microbes and plants, microbes release different elicitors that trigger physiological and biochemical changes in plants. These changes lead to disease resistance in plant for several months [57]. In this regard, the ability of beneficial plant bacteria, such as PGPRs, to induce systemic plant resistance to pathogens and pests in different crops has been widely reported in recent decades [58], as reported in Table 1.
In plant defense against B. cinerea, the recognition of microbe-associated molecular patterns (MAMPs) by plant cells, such as bacterial flagellin or different N-acylated-homoserine lactones, is capable of pre-activating systemic resistance, whereby the plant prepares before a pathogen attack [65,97].
Many Bacillus species have proven to be effective against a broad range of plant pathogens. They have been reported as plant growth promoters and systemic resistance inducers and are used for production of a broad range of antimicrobial compounds (lipopeptides, antibiotics, and enzymes) and competitors for growth factors (space and nutrients) with other pathogenic microorganisms through colonization. In general, by colonizing the roots, Bacillus is capable of inducing plant systemic resistance involving phenolic compounds, genetic and structural modifications, plant resistance activators, and the activation of enzymatic weapons [98]. Against B. cinerea, several Bacillus species have been described to have the ability to pre-activate systemic resistance through different mechanisms. Without identifying the hormonal pathway involved, studies have reported that B. amyloliquefaciens and B. cereus are capable of promoting the plant growth of tomato seedlings and controlling B. cinerea by increasing the expression of pathogenesis-related genes, such as PR2a and Chi3 [61]. This could be due to the production of microbial elicitors, such as VOC dimethyl disulfide, from B. cereus, which has been shown to significantly protect tobacco and maize plants against necrotrophic pathogens [64]. In B. cinerea control, the biocontrol agent can use direct control and activation of plant defenses in conjunction. For example, B. amyloliquefaciens, when applied to the roots and leaves of tomato plants, synergistically increases the control capacity against B. cinerea [17].
Through the SA pathway, the increase in the expression of PR1 and β-1,3-glucanase genes was determined to be effective against B. cinerea in the leaves of strawberry and tomato plants. This defensive response against B. cinerea is a consequence of the root inoculation of B. amyloliquefaciens and B. thuringiensis, respectively, which activates a priming before the attack of the pathogen [62,68]. Similarly, the inoculation of B. velezensis in pepper roots is capable of causing hydrogen peroxide accumulation and superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD) activity in leaves [69]. On the other hand, the JA/ET pathway reduced disease incidence and severity by 50% and 60% in tomato and strawberry leaves, respectively, due to the reduction in oxidative damage and the induction of callose deposition by B. velezensis root inoculation [70], as well as by B. cereus in A. thaliana roots [65,99]. This systemic resistance can be activated by the recognition of bacterial lipopeptides, such as surfactins and fengycins, which are recognized in bean and tomato plants when B. subtilis is applied radicularly, systemically increasing lipoxygenase (LOX) and lipid hydroperoxidase (LHP) activity against the necrotrophic pathogen [66]. Moreover, the produced systemic defense response can be mediated by both the SA and JA/ET pathways, activating the expression of genes independently, such as PR1 (SA) and PDF1.2 (JA) [60,67], as well as common genes, such as β-1,3-glucanase [63].
Pseudomonas is a bacteria genus widely studied as a root colonizer and has been the subject of several reviews on its plant growth-promoting capacity and biocontrol potential, with high interest in an agricultural setting [100]. In the 1990s, several species within the genus were described to have the ability to induce systemic plant resistance by colonizing the roots, and there are currently many studies on different plant species and against different biotic stresses [101]. Against B. cinerea, the ability to activate systemic resistance via P. fluorescens has been reported in both the leaves and fruits of grapevine plants in the field due to an increase in chitinase and β-1,3 glucanase activity [59] and in the production of phytoalexins [85]. This is due to the perception of MAMPs by plant cells, mainly within the group of lipopolysaccharides [88], such as rhamnolipids, used by P. aeruginosa as biosurfactants that induce the expression of the Chit4c gene in the leaves of grapevine plants [81]. An increase in chitinolytic activity was also reported in Chinese cabbage leaves after P. syringae pv. phaseolicola colonized the plant tissues systemically [90]. In this sense, it was proven that, when colonizing roots, P. aeruginosa releases SA and the elicitors pyochelin and phenazine, which cause the systemic activation of plant defenses through the SA-pathway in tomato [80], inducing a response of the priming type via the accumulation of phytoalexins in grapevine leaves [82]. Despite this, most of the systemic defensive responses reported for Pseudomonas against B. cinerea were carried out through JA/ET-pathway. These responses are related to an increase in JA-related gene expression in leaves, such as PDF1.2 by P. fluorescens [83], the increase in LOX and LHP activity by P putida [86,87,89], and the accumulation of phytoalexins by both bacterial species [84,89].
Streptomyces are an aerobic and filamentous bacterial genus in which the species colonize plant tissues from the roots to the aerial parts. These bacteria are active producers of antibiotics and volatile organic compounds, both in soil and in planta, and this feature is helpful for identifying active antagonists of plant pathogens; these bacteria can also be used in several cropping systems as biocontrol agents [102]. This includes crops, such as chickpea, in which the ability to systemically increase the activity of different antioxidant enzymes and increase the total phenolic content against B. cinerea has also been reported [95,96]. This activity was also reported in forest crops, such as eucalyptus [94], and Norway spruces [93].
Pantoea agglomerans has been identified as an antagonist of many plant pathogens belonging to bacteria and fungi as a result of antibiotic production [103]. P. agglomerans is found on grapevine roots, and is capable of inducing systemic resistance against attacks from B. cinerea, both in vitro and in the field, on both its leaves and fruits due to an increase in the synthesis of phytoalexins and chitinase and β-1,3 glucanase activity [77,78]. This defensive induction can be carried out by means of the JA/ET-pathway, as happens with P. eucalyptii in A. thaliana, which is capable of reducing the size of the necrotic lesions caused by B. cinerea by up to 60% due to the foliar deposition of callose [79].
Other systemic defensive responses have been reported with the application of other bacterial species. B. cinerea secretes oxalic acid as a pathogenicity factor with a broad action, against which SA-mediated systemic action has been observed after inoculation of A. thaliana roots with Cupriavidus campinensis [74]. This has also been observed in tomato through the JA-pathway after root inoculation with Micromonospora spp., thereby increasing the expression of genes coding for LOX and proteinase inhibitors (PIN) [75].

5. Fungi as Inductors of Plant Resistance against B. cinerea

As with bacteria, there are numerous groups of beneficial fungi described with the ability to activate systemic plant resistance against biotic stresses. These fungi belong to the so-called PGPFs, which include mycorrhizal fungi and other rhizospheric and/or endophytic fungi that belong, for example, to the genera Aspergillus, Fusarium, Penicillium, Piriformospora, Phoma, and Trichoderma [104]. In the B. cinerea control, reduction of the disease due to the activation of systemic plant resistance by groups of filamentous fungi and yeasts has been reported in several studies (Table 2).
The filamentous-fungal genus Trichoderma includes several species that colonize the outer layers of the roots [138]. Thanks to this interaction, Trichoderma favors the acquisition of nutrients by modifying the root architecture and releasing different molecules to the rhizosphere, which leads to a significant increase in crop productivity [139]. Moreover, Trichoderma is capable of increasing plant tolerance to abiotic stresses, such as salinity and drought [140]. Regarding the activation of systemic resistance in plants, when in contact with the roots, Trichoderma is capable of activating a defensive response in all plant organs, which has been widely described in many different crops and against a wide variety of pathogens [141]. Against B. cinerea, different Trhichoderma species are capable of promoting plant growth while inducing a priming-type systemic defensive response by inhibiting ROS production [120], increasing the pectin content of cell walls [137], or increasing the gene expression of the enzymatic activity of POD, PPO, PAL, SOD, and CAT [136].
This systemic activation has been described as SA-mediated, with 35% less disease severity in tomato leaves by T. asperellum [121]. The SA-mediated response is elicited when Trichoderma comes into contact with the roots and releases molecules, such as cyclophilins, thereby increasing thaumatin-like protein activity in bean leaves [124] and PR-2 and PINII expression in tomato [134]. For the JA/ET-mediated systemic response, reductions in the severity of the disease greater than 60% have been reported as a consequence of the induction in the expression of genes, such as Chi9 [133], VSP2, PDF1.2 [83,122], and PINII [132], as well as the leaf-accumulation of phenylpropanoids [130]. This mediated JA/ET defensive activation is due to the plant-perception of VOCs emitted by Trichoderma, which results in a priming-type response and greater absorption of iron by the roots [122]. However, a significant number of studies were carried out on Trichoderma plant–B. cinerea interactions with A. thaliana and tomato plants, in which the systemic defensive responses were shown to be SA- and JA/ET-mediated. Thus, the systemic induction of the expression of genes related to both routes, such as PR, PDF, LOX, and PIN genes, was verified [126,127], in addition to hydrogen peroxide and camalexin leaf-accumulation [125] due to an increase in the expression of genes encoding for peroxidases and α-dioxygenases [128]. Therefore, Trichoderma is an efficient tool for the biocontrol of B. cinerea through different mechanisms, including the activation of systemic resistance. Moreover, it has been observed that, in tomato plants attacked by necrotrophic fungus, there is an increase in the rhizosphere populations of T. asperellum due to the directed secretion of compounds by the roots [142].
Mainly used as biofertilizers, mycorrhizal fungi are obligate symbionts of the roots in 97% of the vascular plants. Mycorrhizal hyphae are able to colonize places in the soil where plant roots could never reach. Moreover, hyphae have the ability to absorb nutrients through active transporters. The fungus contributes mostly to the supply of phosphorus to the plant, but other nutrients with low mobility, such as ammonium, potassium, copper, iron, sulfur, molybdenum, and zinc, also contribute. In response, the plant must provide carbohydrates to the fungus to meet its needs, although this does not have a negative impact on the plant due to photosynthetic compensation with the fungal supply of nutrients and reduced root development. Moreover, it is widely believed that the inoculation of mycorrhizal fungi provides tolerance to host plants against various stresses, like heat, salinity, drought, pollution, and extreme temperatures. Once symbiosis is established, mycorrizal fungi-induced resistance and priming regulated by JA become activated, similar to the responses controlled by the JA and ET pathways against necrotrophic pathogens [141]. As far as plant systemic resistance against B. cinerea is concerned, a reduction in disease index of up to 50% was achieved in tomato plant roots inoculated with the mycorrhizal fungus Funneliformis mosseae [109]. This was due to a JA-mediated plant defensive response through localized callose deposition [118] alongside the accumulation of indolic derivates and phenolic compounds [116] and/or lignans and oxylipins [117], observed in tomato plants interacting with Rhizophagus irregularis.
Endophytic filamentous fungi include fungi that can be isolated from plant tissues once they have been superficially disinfected and do not cause visible damage to plants. This group plays an important role in ecosystems, returning nutrients to the soil once plants die and protecting plants against biotic and abiotic stresses. In this regard, endophytic fungi are able to induce SAR and ISR in plants against the attacks of pests and/or pathogens, but they also need to suppress, at least partially, the defenses of the plants to colonize their tissues [141]. In B. cinerea biocontrol, several species of filamentous endophytic fungi have been reported with the ability to systemically activate plant defenses. In tomato and pepper, plants root colonized by Fusarium oxysporum achieved a reduction in the percentage of diseased plants and the appearance and intensity of symptoms, thanks to an increase in the foliar expression of PR genes [110,111] and chitinase activity [112]. The JA-mediated response also reported under colonization by Clonostachys rosea is capable of systemically increasing PAL and PPO activity [105]. However, for Colletotrichum acutatum and C. fragariae, this is an SA-mediated response, causing a systemic increase in PR-1 expression, hydrogen peroxide accumulation, and callose deposition in A. thaliana and strawberry plants [106,108]. In addition, as verified in chickpea plants with the endophyte Piriformospora indica, greater control of the disease is directly related to greater root colonization [114].
Yeasts are single-celled microbes classified as members of the kingdom fungi. Today, the role of yeasts as plant growth-promoters and biocontrol agents in agriculture is increasingly understood [143]. The ability of different yeasts to activate post-harvest defenses is widely known [39]; for example, the application of Aureobasidium pullulans in strawberry fruits significantly reduced infection by B. cinerea [144], which was reported in tomato fruits to be a consequence of the perception of chitin present in the Saccharomyces cerevisiae cell walls, leading to an increase in the activity of SOD, CAT, POD, PAL, β-1,3-glucanase, and chitinase enzymes through the SA-pathway [145]. In this sense, the abilities of different yeasts to activate systemic plant resistance against the necrotrophic pathogen have been described. All the studies carried out to date have used A. thaliana as a model plant, reporting a significant in the systemic expression of JA/ET-related genes, such as ACS6, PR4, and PDF1.2, after the application of yeasts, such as Hanseniaspora opuntiae and Pseudozyma aphidis, on leaves [113,115]. The plant response elicited by the components of the fungal cell wall, like that under the foliar application of autoclaved S. cerevisiae cells, increases the systemic expression of PR genes and the accumulation of the phytoalexin camalexin via the SA-pathway [119].
Finally, although they are not found within the fungi kingdom, several examples of oomycetes have been reported to have the ability to induce systemic plant resistance against B. cinerea by colonizing the roots. Specifically, Pythium oligandrum has been described to increase tomato yield by colonizing its roots. This is due to several mechanisms, including the ability to activate plant systemic defenses against pathogens, such as B. cinerea, thanks to an increase in the expression of PR genes [110,146] and due to the root perception of oomycete-secreted proteins, like oligandrin [147].

6. Conclusions

Botrytis cinerea is a necrotrophic phytopathogenic fungus that causes serious economic and agronomic losses worldwide. The use of chemical fungicides cannot alleviate the persistence of this fungus, in addition to the serious damage it causes to the environment and human health. For this reason, in recent decades, many biological control strategies have been developed against this pathogen, with antagonist bacteria and fungi as the main interest groups.
Different groups of beneficial bacteria and fungi, such as Bacillus, Pseudomonas, Aureobasidium, and Trichoderma, have been described as efficient direct antagonists of the growth and development of B. cinerea through parasitism, antibiosis, and competition. Thus, future lines of research should be developed to identify new antifungal compounds (also those within VOCs) and search for new groups of antagonistic microorganisms.
Moreover, beneficial bacteria and fungi are both capable of activating a systemic defensive response against B. cinerea when recognized by plant cells. This defensive response leads to significant reductions in the incidence of the disease in different crops, thus providing a good alternative to the use of agricultural chemicals. In addition, these microorganisms can be effective against necrotrophic fungus both directly and through the activation of systemic plant resistance (as occurred with many of the reviewed examples), which significantly increased the effectiveness of the use of bacteria and fungi in the biocontrol of B. cinerea.
For the phytohormonal pathway activated by bacteria and fungi against B. cinerea, SA-mediated, JA/ET-mediated, and SA- and JA/ET-mediated responses have been reported. In this sense, the plant defense responses against necrotrophic pathogens through JA/ET pathway and the responses against biotrophic pathogens through the SA pathway, mainly through ISR and SAR, respectively, are becoming increasingly less clearly differentiated. Understanding the crosstalk complexes between both hormonal pathways and the rest of the plant hormones is essential for the development of targeted and effective biocontrol strategies against B. cinerea. For this reason, the development of new research that delves into transcriptomics, proteomics, and metabolomics linked to the microbial activation of systemic resistance against necrotrophic fungus is necessary.

Author Contributions

J.P. conceptualized and designed the manuscript. J.P. performed the bibliographic search and analyzed the information. J.P. wrote the first version of the manuscript. M.B. and F.G.-A. contributed to the manuscript correction and critical reading, as well as to the knowledge on the bacteria field. All authors have read and agreed to the published version of the manuscript.

Funding

Ministerio de Ciencia e Innovación (Spain), RETOS-COLABORACIÓN Program; Grant number RTC-2017-6007-2. The Open Access publication fees have been borne by the University of León.

Conflicts of Interest

The authors declare no conflict of interest.

References

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Table
Table 1. Systemic resistance-inducing bacteria against B. cinerea.
Table 1. Systemic resistance-inducing bacteria against B. cinerea.
SpeciesPlantExperimental ConditionsHormonal Pathway InvolvedPlant Defensive ResponsesReference
Acinetobacter lwoffiiGrapevineFieldRoot inoculationUnidentifiedInduction of chitinase and β-1,3 glucanase activity[59]
Bacillus amyloliquefaciensTobaccoGreenhouseLeaf inoculationSA and JAEnhancement of PR-1a, PR1b PR-5, PAL, NPR1, PDF1.2, and COI1 expression[60]
TomatoGreenhouseRoot inoculationUnidentifiedEnhancement of PR2a and Chi3 expression[61]
StrawberryGreenhouseRoot inoculationSAEnhancement of PR1 and β-1,3-glucanase expression[62]
TomatoGreenhouseRoot inoculationUnidentifiedNot described[17]
ArabidopsisGrowth chamberRoot inoculationSA and JA/ETEnhancement of β-1,3-glucanase expression[63]
Bacillus cereusTobaccoMaizeGreenhouseRoot inoculationUnidentifiedNot described[64]
ArabidopsisGrowth chamberRoot inoculationJA/ETEnhancement of PR1 expression, hydrogen peroxide accumulation and callose deposition[65]
Bacillus subtilisBeanTomatoGreenhouseRoot inoculationJAInduce LOX and LHP activity[66]
ArabidopsisGrowth chamberRoot inoculationSA and JAEnhancement of PR1 and PDF1.2 expression[67]
TomatoGreenhouseRoot inoculationUnidentifiedEnhancement of PR2a and Chi3 expression[61]
Bacillus thuringiensisTomatoGreenhouseRoot inoculationSAEnhancement of PR1 expression[68]
Bacillus velezensisPepperGreenhouseRoot inoculationSAInduction of hydrogen peroxide accumulation and SOD, CAT, and POD activity[69]
TomatoStrawberryGreenhouseRoot inoculationJA/ETReduce oxidative damage and induce callose deposition[70]
Brevibacillus laterosporusTobaccoGrowth chamberLeaf inoculationUnidentifiedInduction of SOD and POD activity[71]
Burkholderia cepaciaGrapevineGrowth chamberRoot inoculationUnidentifiedNot described[72]
Burkholderia phytofirmansGrapevineGrowth chamberRoot inoculationSAInduction of callose deposition, H2O2 production and prime expression of PR1, PR2, and PR5[73]
Cupriavidus campinensisArabidopsisGreenhouseRoot inoculationSAReduce oxalate concentration[74]
Micromonospora spp.TomatoGreenhouseRoot inoculationJAEnhancement of LOXa and PinII expression[75]
Paenibacillus terraeTomatoGreenhouseRoot inoculationSA and JANot described[76]
Pantoea agglomeransGrapevineGrowth chamberRoot inoculationUnidentifiedInduction of phytoalexin accumulation[77]
GrapevineFieldRoot inoculationUnidentifiedInduction of chitinase and β-1,3 glucanase activity[78]
Pantoea eucalyptiiArabidopsisGrowth chamberRoot inoculationJA/ETEnhancement of callose deposition[79]
Pseudomonas aeruginosaTomatoGreenhouseRoot inoculationSANot described[80]
GrapevineGrowth chamberLeaf inoculationUnidentifiedEnhancement of Chit4c expression [81]
GrapevineGrowth chamberLeaf inoculationSAInduction of phytoalexin accumulation[82]
Pseudomonas fluorescensGrapevineFieldRoot inoculationUnidentifiedInduction of chitinase and β-1,3 glucanase activity[59]
GrapevineGrowth chamberLeaf inoculationSAInduction of phytoalexin accumulation[82]
ArabidopsisGrowth chamberRoot inoculationJA/ETEnhancement of PDF1.2 expression[83]
GrapevineGrowth chamberRoot inoculationJA/ETInduction of phytoalexin accumulation[84]
GrapevineFieldRoot inoculationUnidentifiedInduction of phytoalexin accumulation[85]
Pseudomonas putidaBeanGrowth chamberRoot inoculationJA/ETNot described[86]
BeanGrowth chamberRoot inoculationJA/ETInduction of LOX and LHP activity[87]
TomatoBeanGrowth chamberRoot inoculationUnidentifiedNot described[88]
TomatoGreenhouseRoot inoculationJA/ETInduction of phytoalexin accumulation and LOX activity[89]
Pseudomonas syringae pv. phaseolicolaChinese cabbageGreenhouseSeeds inoculationUnidentifiedInduction of CHI activity[90]
Saccharothrix algeriensisArabidopsisGrowth chamberRoot inoculationJA/ETNot described[91]
Serratia plymuthicaCucumberGreenhouseRoot inoculationUnidentifiedNot described[92]
Streptomyces sp.Norway spruceGrowth chamberRoot inoculationUnidentifiedInduction POD activity[93]
Eucalyptus grandisGrowth chamberRoot inoculationUnidentifiedInduction of PPO and POD activityInduction of total phenolic accumulation[94]
ChickpeaGreenhouseRoot inoculationUnidentifiedInduction of PAL, CAT, SOD, PPO, APX, and GPX activityInduction of total phenolic accumulation[95,96]
APX: ascorbate peroxidase; CAT: catalase; CHI or CHIT: chitinase; COI: coronative insensitive; GPX: glutatión peroxidase; LHP: lipid hydroperoxidase; LOX: lipoxygenase; PDF: plant defensin; PAL: phenylalanine ammonia lyase; PIN: proteinase inhibitor; POD: peroxidase; PPO: polyphenol oxidase; PR: pathogenesis related; SA: salicylic acid; SOD: superoxide dismutase.
Table
Table 2. Systemic resistance-inducing fungi against B. cinerea.
Table 2. Systemic resistance-inducing fungi against B. cinerea.
SpeciesPlantExperimental ConditionsHormonal Pathway InvolvedPlant Defensive ResponsesReference
Clonostachys roseaTomatoGreenhouseLeaf inoculationJAEnhancement of PAL and PPO activity[105]
Colletotrichum acutatumArabidopsisGrowth chamberRoot inoculationUnidentifiedEnhancement of PR1 expression, and callose deposition[106]
StrawberryGrowth chamberRoot inoculationJA/ETNot described[107]
Colletotrichum fragariaeStrawberryGreenhouseRoot inoculationSAHydrogen peroxide accumulation and callose deposition[108]
Funneliformis mosseaeTomatoGreenhouseRoot inoculationUnidentifiedNot described[109]
Fusarium oxysporumTomatoGreenhouseRoot inoculationUnidentifiedEnhancement of PR gene expression[110]
PepperGreenhouseRoot inoculationUnidentifiedEnhancement PR-1 expression[111]
Fusarium oxysporum f. sp. lycopersiciPepperGreenhouseRoot inoculationJA/ETEnhancement chitinase activity[112]
Hanseniaspora opuntiaeArabidopsisGrowth chamberLeaf inoculationJA/ETEnhancement ACS6, PR4, and PDF1.2 expression[113]
Piriformospora indicaChickpeaGrowth chamberRoot inoculationUnidentifiedEnhancement GST activity[114]
Pseudozyma aphidisArabidopsisGrowth chamberLeaf inoculationJA/ETEnhancement PR1 and PDF1.2 expression[115]
Rhizophagus irregularisTomatoGreenhouseRoot inoculationJAIndolic derivative and phenolic compound accumulation[116]
TomatoGreenhouseRoot inoculationJALignan and oxylipin accumulation[117]
TomatoGreenhouseRoot inoculationJAIncreased callose deposition[118]
Saccharomyces cerevisiaeArabidopsisGrowth chamberLeaf inoculationSAEnhancement of PR1, PR2, and PR5 expression, and phytoalexin camalexin accumulation[119]
Trichoderma asperellumTomatoGreenhouseRoot inoculationUnidentifiedInhibit ROS production[120]
TomatoGrowth chamberRoot inoculationSANot described[121]
ArabidopsisGrowth chamberRoot inoculationJAEnhancement of VSP2 and PDF1.2 expression[122]
Trichoderma atrovirideBeanGrowth chamberRoot inoculationUnidentifiedNot described[123]
BeanGrowth chamberRoot inoculationSAEnhancement of thaumatin-like protein activity[124]
ArabidopsisGrowth chamberRoot inoculationSA and JAHydrogen peroxide and camalexin accumulation[125]
ArabidopsisGrowth chamberRoot inoculationSA and JAEnhancement of PR-1a, PR-2, PDF1.2, LOX1, peroxidase, and camalexin-synthesis-enzyme expression[126]
TomatoGreenhouseRoot inoculationSA and JAEnhancement of PR1b1, LOXa, and PINI expression[127]
TomatoGreenhouseRoot inoculationSA and JAEnhancement of peroxidase and α-dioxygenase expression[128]
Trichoderma hamatumGeraniumGreenhouseRoot inoculationUnidentifiedNot described[129]
ArabidopsisGrowth chamberRoot inoculationJAPhenylpropanoids accumulation[130]
Trichoderma harzianumArabidopsisGrowth chamberRoot inoculationJA/ETNot described[131]
TomatoGreenhouseRoot inoculationSA and JAEnhancement of PR1b1, LOXa, and PINI expression[127]
ArabidopsisGrowth chamberRoot inoculationJA/ETEnhancement of PDF1.2 expression[83]
TomatoGreenhouseRoot inoculationJAEnhancement of PINII expression[132]
TomatoGreenhouseRoot inoculationJAEnhancement of Chi9 expression[133]
TomatoGreenhouseRoot inoculationSAEnhancement of PR-2 and PINII expression[134]
ArabidopsisGrowth chamberRoot inoculationJAEnhancement PDF1.2 expression[122]
Trichoderma koningiopsisTomatoGreenhouseRoot inoculationUnidentifiedNot described[135]
Trichoderma pseudokoningiiMoth orchidGrowth chamberRoot inoculationUnidentifiedEnhancement POD, PPO, PAL, SOD and CAT activity[136]
Trichoderma virensArabidopsisGrowth chamberRoot inoculationSA and JAHydrogen peroxide and camalexin accumulation[125]
TomatoGreenhouseRoot inoculationSA and JAEnhancement peroxidase and α-dioxygenase expression[128]
TomatoGreenhouseRoot inoculationUnidentifiedIncrease pectin content of cell walls[137]
ACS: 1-aminocyclopropane-1-carboxylate synthase; CAT: catalase; CHI: chitinase; GST: glutathione S-transferases; LOX: lipoxygenase; PAL: phenylalanine ammonia lyase; PDF: plant defensin; PIN: proteinase inhibitor; POD: peroxidase; PPO: polyphenol oxidase; PR: pathogenesis related; ROS: reactive oxygen species; SOD: superoxide dismutase; VSP: vegetative storage protein.
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Poveda, J.; Barquero, M.; González-Andrés, F. Insight into the Microbiological Control Strategies against Botrytis cinerea Using Systemic Plant Resistance Activation. Agronomy 2020, 10, 1822. https://doi.org/10.3390/agronomy10111822

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Poveda J, Barquero M, González-Andrés F. Insight into the Microbiological Control Strategies against Botrytis cinerea Using Systemic Plant Resistance Activation. Agronomy. 2020; 10(11):1822. https://doi.org/10.3390/agronomy10111822

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Poveda, Jorge, Marcia Barquero, and Fernando González-Andrés. 2020. "Insight into the Microbiological Control Strategies against Botrytis cinerea Using Systemic Plant Resistance Activation" Agronomy 10, no. 11: 1822. https://doi.org/10.3390/agronomy10111822

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