Microbial Biocontrol Agents in Fight against Alder Diseases: Comparison
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Please note this is a comparison between Version 2 by Fanny Huang and Version 1 by Emma Fuller.

Common Alder (Alnus glutinosa (L.) Gaertn.) is a tree species native to Ireland and Europe with high economic and ecological importance. The presence of Alder has many benefits including the ability to adapt to multiple climate types, as well as aiding in ecosystem restoration due to its colonization capabilities within disturbed soils. However, Alder is susceptible to infection of the root rot pathogen Phytophthora alni, amongst other pathogens associated with this tree species. P. alni has become an issue within the forestry sector as it continues to spread across Europe, infecting Alder plantations, thus affecting their growth and survival and altering ecosystem dynamics. Beneficial microbiota and biocontrol agents play a crucial role in maintaining the health and resilience of plants. Studies have shown that beneficial microbes promote plant growth as well as aid in the protection against pathogens and abiotic stress. 

  • biocontrol agents
  • Phytophthora
  • Alder
  • microbiome

1. Introduction

Biocontrol agents tend to be any beneficial organism, including PGPR and PGPF, which have the ability to provide biological control against harmful pathogenic disease, as well as assisting in acquiring nutrients and amplifying resistive traits within a plant species [1]. Furthermore, the use of PGPR/F can act as a biocontrol agent by enhancing the health of a tree species, thus, a stronger tree can fight/withstand pathogenic infections. Moreover, A. glutinosa has many antioxidant, anti-inflammatory, antitumour, and inhibition properties due to the presence of anthraquinones, betulinic acid, diarylheptanoids, flavonoids, phenols, terpenes, tannins, steroids, and saponins; thus, these substances have the potential as BCAs within forestry [2][3][4]. Emerging diseases within forestry are a cause for concern, therefore, the advancement of BCAs within this sector is desirable. BCAs and bio-fertilisers have been used in agriculture for many years for sustainable crop production to minimise the use of harmful pesticides and fertilisers and reduce pathogenic infections, as well as to promote the health and growth of crops [5][6]. This approach is used intermittently within forestry with a few successful applications. Through research, several potential BCAs have been identified within forest ecosystems to reduce pathogenic spread and associated symptoms including dieback and root rot. Utkhede et al. (1997) analysed the antagonistic effects of the bacterium Enterobacter aerogenes against the pathogen P. lateralis, which tends to affect tree roots within soil and water, causing root rot disease of Lawson cypress trees [7]. D’Souza et al. (2005) investigated several potential BCAs including Acacia extensa, A. stenoptera, A. alata, and A. pulchella against the root rot disease caused by P. cinnamomi, to observe that these genera have the potential to provide protection to susceptible species [8]. With the Alnus species being under threat from the harmful effects of Phytophthora, such studies could potentially aid in determining the association between P. alni and the Alnus species and thus determining potential BCAs to prevent infections.
Several bacterial strains could potentially provide BCAs against emerging tree pathogens [9]. For example, for the pathogen Hymenoscyphus fraxineus, a study performed on the microbial community associated with ash tree leaves (Fraxinus excelsior) discovered elevated amounts of isolates within the genera Luteimonas, Aureimonas, Pseudomonas, Bacillus, and Paenibacillus present within tolerant trees, which potentially inhibit the invasion and spread of ash dieback disease (H. fraxineus) by direct competition or inducing systemic resistance, as well as the potential production of antagonistic metabolites and/or antifungal compounds [10][11]. Similarly, Becker et al. (2022) explored the microbiome of tolerant ash trees, and it was determined that the bacterium Aureimonas altamirensis had the ability to reduce H. fraxineus infections by niche exclusion and inducing mechanisms such as exopolysaccharides production and protein secretion [12]. The plant growth-promoting members of the genus Streptomyces have proven to be a prime choice as BCAs since these are readily available in nature and have the capacity to control pathogenic infections [13][14][15][16]. Liu et al. (2009) discovered that the BCA metabolite daidzein was produced by the bacterial genus Streptomyces and isolated it from a root of A. nepalensis alongside the Streptomyces bacterium, which may have potential antioxidant, anti-inflammatory, and anticancer effects [17][18]. The genus Streptomyces can produce the enzyme chitinase, which has been shown to have antagonistic effects against fungi due to the ability to degrade chitin present in the cell walls of fungi as well as reduce spore germination [19].
Biocontrol modes of action can be direct (interaction between pathogens and BCAs) or indirect (interaction between BCAs and plants to enhance their health and resistance to (a)biotic stressors) [20]. Direct biocontrol factors include antimicrobial metabolites, hydrolytic enzymes, quorum sensing, quenching, and resource competition, as well as siderophores. Indirect biocontrol factors include organisms triggering enhanced immunity for plants, environmental adaption, and hormone modulation. Microorganisms have the ability to produce microbe-associated molecular patterns (MAMPs) or damage-associated molecular patterns (DAMPs) like flagellin, glucan, xylan, or chitin [21]. These patterns are recognised by pattern-recognition receptors (PRRs) or other elicitors such as volatile organic compounds (VOCs) or siderophores, which are detected by specific receptors. Activation of these receptors initiates various signalling mechanisms that serve as precursors for the production of phytohormones, triggering defensive pathways. The kinase pathway can phosphorylate transcription factors that regulate the expression of early and late response genes [21]. There are many genes that have an association with biocontrol agents and defence-related genes [22]. Each BCA has thousands of genes present within its genome (depending on its genome size); therefore, genes with biocontrol traits can differ from one species to another. Nelkner et al. (2019) used transcription and genome mining in order to identify genes that are related to biocontrol traits and biosynthetic genes within a Pseudomonas strain [23]. In this study, biocontrol activity included the production of siderophores, secondary metabolites, and antibiotics (2,4-Diacetylphloroglucinol (DAPG), hydrogen cyanide (HCN) synthesis, pathogen inhibition genes (iron acquisition, exoprotease activity, and chitinase activity), resistance genes (PRRs), exopolysaccharides genes, lipopolysaccharides genes, metabolism genes, detoxification genes, and genes related to ISR and growth-promoting compounds (VOCs, acetoin, 2,3-butanediol, growth regulators/plant hormones, and phosphate solubilisation) [23]. Genes also involved in plant defence include the phenylpropanoid pathway gene-expressing phenylalanine ammonia-lyase (PAL), which facilitates the deamination process when phenylalanine is converted into cinnamate and ammonia, as well as the lipoxygenase pathway gene encoding hydroxyperoxide lyase (HPL) [21]. Mitogen-activated protein kinase (MAPK)- and cyclic adenosine monophosphate (cAMP)-associated molecules represent widespread intracellular signalling pathways that integrate extracellular stimuli, alter the expression and functionality of receptors, and regulate processes such as cell survival and neuroplasticity [24]. TGA transcription factors are vital regulators of diverse cellular processes which link to hormonal pathways, interacting proteins, and regulatory elements [25]. In addition, the phytohormones brassinosteroids (BRs) and jasmonates (JAs) also aid in the regulation of plant growth, development, and defensive response [26].
Chitinase has been used in agriculture during crop cultivation for disease management, improved growth, and greater yields [27]. Kumar et al. (2018) highlighted various ways in which chitinase gene expression has been used in agriculture to combat fungal diseases [27]. Auxins such as IAA and phenylacetic acid (PAA) are well-known bio-agents within agriculture due to their plant growth-promoting abilities and provide potential control against Fusarium pathogens, which have been found within soils, causing root rot [28][29]. IAA has been abundantly produced from PGPR isolates associated with forest trees; therefore they may have the potential for BCAs within this sector since they are proven to be advantageous in agriculture [30]. Trinh et al. (2022) discovered that the rhizobacteria Bacillus subtilis, isolated from the rhizosphere roots of black pepper, has potential as a bio-agent for Fusarium antagonism [28]. Fungal endophytes could potentially provide BCAs against emerging tree pathogens [31]. For example, Kosawang et al. (2017) performed in vitro antagonistic assays of Sclerostagonospora sp., Setomelanomma holmii, Epicoccum nigrum, Boeremia exigua, and Fusarium sp. against the dieback-causing fungus, H. fraxineus, and it was observed that these endophytes are potential BCAs [32]. Halecker et al. (2020) analysed the antagonistic effects of the fungal endophyte Hypoxylon rubiginosum on H. fraxineus, and it was determined that this endophyte has potential as a BCA due to the production of metabolites that are toxic to the pathogen [10][33]. This investigative approach is beneficial to determine potential pathogen-fighting microbes present within tolerant tree species that can aid in the protection of trees that are susceptible to certain diseases. See Table 1 for a summary of BCAs.
The most commonly used biocontrol agents belong to the genera Pseudomonas, Bacillus, and Trichoderma [34]. For example, Pseudomonas (P. pudida 06909) was used as a biocontrol agent against Phytophthora root rot within citrus orchids [35], P. chlororaphis has antagonistic effects against the cacao rot pathogen Ph. Palmivora [36], and Bacillus amyloliquefaciens isolated from ginseng rhizosphere induced systemic resistance to Ph. cactorum [37]. In addition, Trichoderma virens, Trichoderma harzianum, Trichoderma asperellum, and Trichoderma spirale isolated from cocoa show antagonistic effects against Ph. Palmivora [38], and Trichoderma saturnisporum also showed antagonistic effects against the Phytophthora spp. [34][39]. Abbas et al. (2022) conducted an extensive review regarding the identification of multiple biocontrol encoding genes within the Trichoderma spp. against R. solani including secondary metabolite genes, siderophores genes, signalling molecular genes, cell wall degradation enzymatic genes, and plant growth regulatory genes [40]. Furthermore, G-protein coupled receptor (GPCR) genes, adenylate cyclase genes, protein kinase-A genes, and transcription factor proteins are important genes found in Trichoderma for biocontrol against R. solani [40]. Moreover, Trichoderma has the ability to generate chitinase, which can minimise the survival of R. solani through the activation of the expression of chitinase genes [41]. Hernando José et al. (2021) discuss several isolated endophytic bacteria, fungi, and metabolites that have shown antagonistic and biocontrol activities as well as induced mechanisms against Phytophthora pathogens [42]. Some bacterial examples include Pseudomonas fluorescence isolated from the flowering vine saw greenbrier, which showed antagonistic effects against P. parasitica, P. cinnamomi and P. palmivora, as well as Burkholderia spp. isolated from the herb huperzine showing the ability to inhibit the growth of P. capsici. The isolate Acinebacter calcoaceticus from soybeans showed antagonistic effects against P. sojae. An isolate from a tomato plant (Bacillus cereus) helped to reduce the infection severity of P. capsici associated with cacao trees. Several strains of bacteria isolated from cucurbits including Bacillus, Cronobacer, Enterobacteriaceae, Lactococcus, Pantoea, and Pediococus showed antagonistic activity against P. capsici using various biocontrol mechanisms. Some fungal examples include species of Trichoderma, Pestalotiopsis, and Fusarium which were isolated from cacao trees and illustrated antagonism against P. palmivora. The fungus Muscodor crispans was isolated from a pineapple plant and showed inhibition properties against P. cinnamomi and P. palmivora. Hernando José et al. (2021) discuss numerous other bacterial and fungal strains that showed biocontrol activities and mechanisms against P. capsici, P. infestans, P. citricola, P. cactorum, and P. pini [42]. It is evident that there are various studies associated with the biocontrol of several Phytophthora species, but there are minimal studies regarding P. alni.

2. Improving Plant Resistance via Microbe Inoculation and Genetic Resistant Breeding

In recent studies, a greater focus has been placed on ways to detect and diagnose tree diseases, understand the interactions between trees and pathogens, develop disease-resistant trees, and ultimately optimise soil and tree microbiomes to improve plant health and behaviour [43][44][45]. The microbial communities associated with forest trees provide vital information relative to species health since numerous beneficial microbes have the ability to increase growth, development, productivity, and ecosystem function, as well as improve soil structure, and provide some resistance to pests and pathogenic diseases [1][46]. Alder trees may be inoculated with beneficial microbes in order to improve disease tolerance and environmental stressors, as well as enhance growth and quality. For example, Chandelier et al. (2015) discuss several inoculation methods in order to screen A. glutinosa resistance to P. alni [47]. These included wound inoculation, stem inoculation, seed and seedling inoculation, inoculation by flooding of root cuttings, and zoospore suspension inoculation. It was determined that the combination of zoospore suspension with flooding root systems was the most reliable since unwounded trees better mimicked natural environmental conditions [48]. Zaspel et al. (2014) investigated a way to increase the resistance of Common Alder against P. alni using in vitro and in planta analysis with a cyclolipopeptide (CLP)-producing Pseudomonas veronii metabolite (PAZ1) [48]. It was observed that inoculation with PAZ1 showed some inhibition effects as well as growth-promoting effects on the Alder species.
In order to aid the protection and integrity of forestry, natural genetic resistance breeding programmes of several species against biotic stressors have been studied [49]. Examples of resistance programmes include white pine and white pine blister rust resistance, Port Orford cedar and P. lateralis, Sitka spruce and white pine weevil resistance, Loblolly pine and fusiform rust resistance, Pinus radiata and Dothistroma pini resistance, Koa and koa wilt resistance, American beech and beech bark disease resistance, and Dutch elm disease [49][50][51]. Wei and Jousset (2017) suggest an alternative foundation to reach economically novel phenotypes by altering genetic information coupled with plant-associated microbiota [1][52]. Since pathogenic organisms have caused significant economic losses within forestry, greater research and screening techniques are required in order to expand bio-control procedures against forestry pathogens. Marco et al. (2022) extensively review microbe-assisted breeding programmes to date, particularly those associated with crops, and how this has improved the agricultural sector [53]. The Institute of Forest Genetics in Waldsieversdorf, Germany, was working on a selective breeding programme to improve the resistance of A. glutinosa to P. alni; however, this project appears to be complete since 2018 [54]. A greater focus on the development of natural genetic resistance breeding programmes specifically focused on the Alnus genus coupled with identifying species-specific biocontrol agents to minimise the infection of the pathogen P. alni will greatly aid in the protection of the Alnus species.
Table 1. Bio-control agents (BCAs) and the plant diseases they suppress via associated biocontrol mechanisms.
Potential BCA Classification Pathogens They Potentially Control Mechanism Expressed Showing Bio-Control Abilities In Vitro/In Planta/In Vivo/Field/

Commercial		 Reference
A. extensa, A. stenoptera, A. alata, A. pulchella Legume (Acacia) Phytophthora cinnamomi Suppression and containment of Phytophthora cinnamomi inoculum in soil-infested areas to protect susceptible species and enhance species diversity In planta [7]
Bacillus amyloliquefaciens Firmicutes Phytophthora cactorum Induces systemic resistance In vitro [37]
Pseudomonas chlororaphis Gammaproteobacteria Phytophthora palmivor Antibiosis and suppression; reduce symptom severity; production of lytic enzymes, siderophores, and bio-surfactants In vitro/in planta [36]
Pseudomonas putida 06909 Gammaproteobacteria Phytophthora spp. Hypovirulence and suppression; colonise pathogenic hyphae and reduce pathogenic populations Field [35]
Enterobacter aerogenes Proteobacteria Phytophthora lateralis Suppression; reduce disease symptoms and promote plant growth Field [6]
Hypoxylon rubiginosum Ascomycetes Hymenoscyphus fraxineus Antibiosis; production of metabolites that are toxic to H. fraxineus In vitro/in planta [33]
Aureimonas altamirensis Alphaproteobacteria Hymenoscyphus fraxineus Colonisation resistance; exopolysaccharide production; protein secretion; stress adaptation genes In vitro/in planta [11]
Bacillus subtilis Firmicutes Fusarium sp. Antibiosis and antagonistic effects In vitro [28]
Pseudomonas fluorescens Pseudomonas Fusarium oxysporum, Rhizoctonia solani, Macrophomira phaseolina, Fusarium sp. Antibiosis, hypovirulence, and suppression; inhibit plant disease, minimise fungal infections, protect seeds and roots from infection; production of secondary metabolites In vitro/field [55][56][57][58]
daidzein Isoflavones No specific pathogen Antibiosis; antioxidant, anti-inflammatory, and anticancer effects In vitro/in vivo [16][17]
Streptomyces Actinobacteria Acidovorax spp., Fusarium sp., Ralstonia solanacearum, Xanthomonas spp., Sclerotinia sclerotiorum, Erwinia amylovora Antibiosis and induced resistance; source of bioactive compounds like antimetabolites, antibiotics, extracellular enzymes, and antitumor agents In vitro/in vivo [12][14][15][16][59]
Chitinase Enzyme Phytophthora cinnamomi Suppression; reduced spread, reduced sporangia production, applied in agriculture during crop cultivation for disease management, improved growth, and greater yields Commercial/in vitro [26][27]
IAA Auxin Plant Hormone Fusarium sp. Systemic resistance; regulate growth and development processes Commercial/in vitro [29][30][60]

3. Microbiome Engineering and Its Potential Phytophthora Control

The practice of microbiome engineering has been applied recently to enhance human well-being, agricultural efficiency and combat challenges of bioremediation and contamination within the environment [61][62]. This involves various methods for the modification of host-associated microbiota to improve its health, resilience, and disease tolerance, as well as to benefit surrounding ecosystems [62]. These methods include enrichment, artificial selection, direct evolution, population control, pairwise interactions, microbiome transfer, synthetic microbes, and engineered interactions which are used to manipulate a microbiome to obtain desired characteristics [61][62]. In agriculture, a method used to manage plant diseases involves root microbiome transfer by combining fertile disease-suppressive soils with less fertile disease-conductive soils [63]. For example, Mendes et al. (2011) showed that by mixing these soil types, sugar beet soil was suppressive to the pathogen R. solani due to the presence of several species of Proteobacteria, Firmicutes, and Actinobacteria, which play a role in disease suppression. Santhanam et al. (2015) showed that synthetic root-associated microbiota transplants using a mixture of native bacterial isolates (species from Arthrobacter, Bacillus, and Pseudomonas) were effective at reducing the wilt disease of tobacco Nicotiana attenuate and that they increased crop resilience [64]. Mukherjee et al. (2022) used a bio-inoculant containing two bacterial strains isolated from chickpeas, Enterobacter hormaechei and Brevundimonas naejangsanensis, to enhance the productivity of inoculated chickpeas seeds, and it was observed that the consortium increased plant-growth attributes, yields, nutritional content, levels of IAA, siderophore, ammonia, phosphate solubilisation, and potassium solubilisation, as well as antagonistic activity against Fusarium sp. due to successful manipulation of the plant microbiome [65]. Wicaksono et al. (2017) inoculated wounds of kiwi fruit plants with Pseudomonas strains isolated from the medicinal plant Mānuka, and it was determined that the bacterial strains aided the pathogenic resistance of P. syringae, indicating that microbe transfer can be successful in reducing disease severity [66]. There is a great potential for the use of microbiome engineering in forestry as it offers an innovative solution to address various challenges in sustainable forest management. The manipulation of tree-associated microbiota can potentially enhance tree growth and pathogenic resistance as well as optimise nutrient cycles and improve tree tolerance to environmental stressors.

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