Bacterial Bioprotectants: Comparison
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Plant growth and nutrition are adversely affected by various factors such as water stress, high temperature, and plant pathogens. Plant-associated microbes play a vital role in the growth and development of their hosts under biotic and abiotic stresses. The use of a rhizosphere microbiome for plant growth stimulation and the biological control of fungal disease can lead to improved crop productivity. Mechanisms used by plant-growth-promoting rhizobacteria (PGPR) to protect plants from soilborne pathogens include antibiosis, the production of lytic enzymes, indole-3 acetic acid production, decreasing ethylene levels by secreting 1-aminocyclopropane-1-carboxylate deaminase, competition for nutrients and niches, parasitism and induced systemic resistance. 

  • root-associated microbes
  • biological control
  • plant-beneficial traits

1. Production of Phytohormone

Rhizosphere bacteria have the ability to produce the phytohormones that play important roles in processes such as cell division in symbiotic as well as non-symbiotic plant roots [51][1]. Phytohormones are mainly classified as gibberellins, cytokinins, ethylene and auxins that affect plant–microbe associations [52,53][2][3]. They can enter plants through different mechanisms. One is through direct contact with the plant roots, whereas microbial hormones diffuse into the root cells and are transported throughout the plant [54][4]. Additionally, some microbes can produce hormones that are released into the soil, where they can be taken up by the roots of nearby plants. This is known as allelopathy, where one plant produces chemicals that affect the growth of other plants [55][5]. The microbial phytohormones stimulate plant development and enhance plant tolerance to abiotic and biotic stresses [35,56][6][7]. Moreover, previous studies have reported that phytohormones stimulate the innate immunity of plants against pathogens such as bacteria and fungi [18,51,57][1][8][9]. Kapoor et al. [58][10] reported the inhibition of Verticillium dahliae and Fusarium oxysporum growth and development by up to 70% by an IAA-producing endophytic fungi. In another study, Bacillus amyloliquefaciens induced disease tolerance against the pathogen Rhizoctonia solani through the modulation of phytohormone signaling [59][11]. A similar observation was reported by Zebelo et al. [60][12], where the inoculation of cotton with Bacillus sp. increased jasmonic acid synthesis and suppressed the beet armyworm Spodoptera exigua. Zhao et al. [61][13] observed the biological control ability of IAA-producing bacteria against Phytophthora sojae, which indicates that the use of phytohormones could be one of the mechanisms to increase plant immunity against pathogens. Bacterial cytokinins are also known to induce plant immunity against pathogen infections [62][14]. Karimi et al. [63][15] reported increased plant growth and the biological control of F. oxysporum f. sp ciceris in chickpea by B. subtilis, which produce IAA.
The ethylene phytohormone acts as a signaling molecule in defense against pathogens and signals systemic resistance caused by rhizobacteria [64][16]. For example, Dixit et al. [65][17] observed an amendment of ethylene levels in inoculated plants with ACC deaminase-producing Paenibacillus lentimorbus, which are infected by S. rolfsii. The plant-beneficial bacteria were able to control southern blight disease through the modulation of the ethylene pathway and antioxidant enzyme activities.
The production of these phytohormones by microbes can have beneficial effects on plant growth, development, and stress responses. Overall, phytohormones are important signaling molecules that can activate various defense mechanisms in plants against biotic stress. The modulation of phytohormone signaling pathways could be a promising strategy for developing new plant protection methods against pathogens. It is important to note that the effects of microbe-produced phytohormones on plants can depend on various factors, such as the type of hormone, the type of microbe, and the environmental conditions.

2. Lytic Enzymes

Microbial enzymes, also called cell-wall-degrading enzymes, such as cellulases, chitinases, glucanases, lipases, pectinases, and proteases, have drawn attention for their inhibition of phytopathogens [66,67][18][19]. They also play an important role in nutrient cycling in the ecosystem, through decomposing organic matter. These enzymes degrade the structural component of the fungi cell wall and thus inhibit spore germination and germ-tube elongation [68][20]. Egamberdieva et al. [69][21] isolated bacterial endophytes from horseradish, Armoracia rusticana, and they displayed some o lytic enzyme activities, such as lipase, protease, chitinase, and glucanase. Most of the bacterial strains have been shown to suppress plant pathogens such as Fusarium culmorum, F.solani, and Rhizoctonia solani. In another study, Muniroh et al. [70][22] observed a reduced basal stem rot of oil palm caused by G. boninense by plant-beneficial bacteria Pseudomonas aeruginosa. The strain produced hydrolytic enzymes such as chitinase, cellulase and 1, 3, β-glucanase. Similar results, reported by Woo et al. [71][23], highlight the degradation of cell wall of fungal pathogen by biocontrol Trichoderma spp. through the production of β-1,3-glucanases, chitinase, cellulose, and proteases. Overall, lytic enzymes produced by microbes can degrade the cell walls of plant pathogens and prevent their growth and spread. This can help to protect plants from various diseases and promote their overall health and growth.

3. Antifungal Compounds

Endophytes with biocontrol abilities produce secondary metabolites, such as antibacterial and antifungal compounds, which assist in the inhibition of phytopathogens [66][18]. There are many reports on the antifungal production abilities of endophytic fungi and bacteria, which can be related to the induction of systemic resistance in plants [67,72][19][24]. Microbial antifungal compounds play a critical role in plant defense systems and the biological control of emerging plant pathogens [17,73,74][25][26][27]. According to previous reports, the most well-known antibiotic-producing endophytes are Bacillus, Aspergillus, Penicillium, Trichoderma and Streptomyces species [17,75][25][28]. Streptomyces sp. was reported to produce dimethyl sulfide and trimethyl sulfide, which play an important role in reducing tomato bacterial wilt caused by Ralstonia solanacearum and red pepper leaf spot caused by Xanthomonas euvesicatoria [76][29]. The Bacillus sp. that showed biocontrol ability against Phytophthora sojae and isolated from soybean produced two types of antifungal compounds [61][13]. In another study, iturin A synthesized by Bacillus sp. CY22 was responsible for the inhibition of Rhizoctonia solani, the causal agent of root rot of balloon flower [77][30].
Endophytic fungi have yielded numerous antifungal natural compounds with potential use in the development of biopesticides [78][31]. These compounds have been found to exhibit a range of bioactivities, including antifungal activity against various plant pathogenic fungi [79,80][32][33]. For example, a new natural sesquiterpene compound with antifungal activity has been isolated from Lophodermium sp., an endophytic fungus derived from Pinus strobus. The compound, 5-(hydroxymethyl)-2-(20,60,60-trimethyltetrahydro-2H-pyran2-yl)phenol, exhibited antifungal activity against the phytopathogen Microbotryum violaceum, with a minimum inhibitory concentration (MIC) of 2 µM [81][34]. Two new halogenated cyclopentenones, bicolorins B and D, were isolated from the endophytic fungus Saccharicola bicolor obtained from Bergenia purpurascens. Bicolorins B and D showed strong antifungal activities against P. dissimile with MIC values of 6.2 and 8.5 μg/mL, respectively, compared with the positive control cycloheximide (MIC of 8.6 μg/mL). Moreover, bicolorin D has been found to exhibit potent antifungal activity against the plant pathogenic fungus Sclerotinia sclerotiorum, both in vitro and in vivo [82][35]. In another study conducted by Chen et al., [83][36], two tetranorlabdane diterpenoids, 13,14,15,16-tetranorlabd-7-en19,6β:12,17-diolide and botryosphaerin H, were isolated from the endophytic fungus Botryosphaeria sp. P483 was obtained from Huperzia serrata. These compounds showed strong antifungal activity against several plant pathogenic fungi, including F. solani, F. oxysporum, G. graminis, F. moniliforme, and Pyricularia oryzae at a concentration of 100 µg/disk. According to Talontsi et al. [84][37], three polyketides, epicolactone and epicoccolides A and B, were isolated from an endophytic fungus, Epicoccum sp. CAFTBO, derived from Theobroma cacao. These compounds showed significant inhibitory effects on the mycelial growth of two peronosporomycete phytopathogens, Pythium ultimum and Aphanomyces cochlioides, and the basidiomycetous fungus Rhizoctonia solani.
Microbial antifungal compounds can be used as potential alternatives to chemical fungicides in agriculture, which can have negative impacts on the environment and human health. They can inhibit the growth and spread of fungal pathogens, helping to protect plants from various diseases.

4. Siderophore Production

Endophytes produce volatile compounds that can directly inhibit pathogen development [85][38]. Siderophores are low-molecular-weight compounds produced by some beneficial microbes that play an important role in plant protection by enhancing iron uptake and inhibiting the growth of some plant pathogens. Iron is an essential nutrient for plant growth and development, but it is often limited in soil. Siderophores can enhance iron uptake in plants by chelating ferric ions and making them more available for plant absorption. [86][39]. Siderophore secretion by endophytes enhances plant growth making plant pathogens compete with iron and protecting the host plant [87][40]. Moreover, some pathogenic microbes, such as fungi and bacteria, require iron for their growth and survival. Siderophores produced by beneficial microbes can compete with these pathogens for iron, limiting their growth and survival. This can help to protect plants from various diseases caused by iron-dependent pathogens.
The usage of siderophore-producing endophytes as biocontrol agents is considered as a promising solution to overcome plant diseases. For instance, in a study by Yu et al. [88][41], the siderophore-producing Bacillus subtilis CAS15, with ability to control Fusarium wilt and improved the growth of pepper, was reported. In another study, Pseudomonas species showed the ability to produce siderophores to control F. oxysporum f. sp. dianthi by improving competition for nutrients and niches [27][42]. Chowdappa et al. [89][43] reported that the endophytic fungi Penicillium chrysogenum, Aspergillus terreus and Aspergillus sydowii from Cymbidium aloifolium had siderophore-producing ability. The isolates were able to control plant pathogens such as Ralstonia solanacearum and Xanthomonas oryzae pv. oryzae. In summary, siderophores produced by beneficial microbes can enhance iron uptake in plants, compete with iron-dependent pathogens, and even have direct antibiotic activity against plant pathogens.

5. Induction Systemic Resistance (ISR)

Induced resistance has been identified as a promising tool to overcome plant diseases in sustainable agriculture applications [66,90][18][44]. Most of the endophytic microorganisms have the ability to protect their host plants against pathogens via two common mechanisms: induced systemic resistance (ISR) and systemic acquired resistance (SAR) [91,92,93][45][46][47]. ISR improves pathogen resistance in host plants through the activation of pathogen-related proteins, polyphenols, and phytoalexins or the induction of signal transduction pathways triggered by jasmonate (JA)/salicylic acid (SA) or ethylene (ET) [94,95][48][49]. The PR proteins decrease plant pathogen effects and simplify the protection against the plant pathogens to stimulate biotic stressors. The PR proteins include enzymes such as chitinases and 1, 3-glucanases. These enzymes have a critical role in the lysing of invading fungal cells and recruitment of cell wall lines to resist infection and cell death [96][50]. For example, P. polymyxa elicited ISR in pepper, which protects plants against the bacterial spot pathogen Xanthomonas axonopodis pv. vesicatoria and reduces disease severity [97][51]. In another study, Penicillium citrinum enhanced the resistance of Helianthus annuus L. to stem rot caused by Sclerotium rolfsii through the SA and JA signaling networks [98][52]. Kavroulakis et al. [99][53] reported an increased ISR in tomato against the pathogen Septorialyco persici by activating the PR7 and PR5 genes. The inoculation of Aradiopsis with Bacillus velezensis reduced the reproduction of green peach aphid Myzus persicae by expressing senescence-promoting gene phytoalexin deficient4 (PAD4) [100][54].

6. Antioxidant Enzymes

It is known that abiotic stresses can increase reactive oxygen species (ROS) in plant cells and oxidative damage occurs in plant tissues [110][55]. The proteins and DNA may get damaged, whereas OH⋅- produce lipid peroxides, which may modify protein configuration and cause loss of biological function [111][56]. Antioxidant enzymes play an important role in plant protection by scavenging harmful reactive oxygen species (ROS) that are produced during various stress conditions, including pathogen attack [112][57]. Plants synthesize enzymatic and non-enzymatic antioxidants to reduce ROS damage. Among them, superoxide dismutase (SOD), peroxidase (POD), and ascorbate peroxidase (APX) can help to maintain the dynamic balance of reactive oxygen species. Microbes associated with plants may also help stimulate the antioxidative system in the host plants [113][58].
Pathogens can induce the production of ROS in plants as part of their attack strategy. Antioxidant enzymes can help to counteract this by scavenging the ROS produced by the pathogen and limiting their damaging effects on the plant [114][59]. Peroxidases (POD) play a vital role in plant disease resistance [115][60], whereas superoxide dismutase (SOD) is involved in the plant defense against ROS [116][61]. ROS can also act as signaling molecules in plants, activating defense responses against pathogens. Antioxidant enzymes can regulate the level of ROS in the plant and help to fine-tune these signaling pathways.

7. Competition for Nutrient and Niches

Soil and rhizospheres are complex environments with high carbon concentrations, oxygen, nutrients, and microorganisms. Rhizosphere-inhabiting microbes such as beneficial bacteria and pathogenic fungi compete for nutrients and niches [120,121][62][63]. In biocontrol, competition for nutrients and niches can be an important factor in determining the success or failure of a biological control agent. Nutrients are essential for the growth and reproduction of all organisms, and competition for these resources can be intense in natural ecosystems. [122][64].
When introducing a biocontrol agent, it is important to consider the existing microbial community in the target environment. The biocontrol agent must compete with other microorganisms for nutrients and space [123][65]. If the biocontrol agent is not able to compete effectively, it may not be able to establish itself in the environment or may not be able to maintain its population at a level sufficient for effective pest control. It is found that limiting nutrients such as carbon, iron, mineral elements and space will cause the inhibition of the spore germination of fungal pathogens and formation of infection on host tissue [124][66]. The biocontrol bacteria should actively colonize the root system and occupy niches to consume nutrient sources from root exudates and compete for the resources that the pathogen also uses for its proliferation [125,126][67][68].
Therefore, efficient root colonization by bacteria is the delivery system for biological active metabolites, including antifungal compounds, cell-wall-degrading enzymes and HCN, which negatively affect the physiology of fungal pathogens [127][69]. Kamilova et al. [40][70] reported on the biological control strain P. fluorescens strain PCL1751, which effectively colonized the rhizosphere and reduced tomato foot and root rot caused by F. oxysporum f. sp. radicis-lycopersici. The P. extremorientalis strain TSAU20 was reported as an enhanced root colonizer and reduced cucumber root rot caused by F. solani by 10%. The strain was not able to produce antifungal compounds against Fusarium, was negative for the HCN, cellulase, lipase, and glucanase production, and it seems its major mechanism of biocontrol is competition for nutrients and niches [30][71]. It has been indicated that motility, chemotaxis toward root exudates, induces the colonization of Pseudomonas in the rhizosphere and their interaction with plant [128][72].
Understanding the niche requirements of both the BCA and the target pest is therefore essential for successful biocontrol [131][73]. Competition for nutrients and niches can be an important factor in determining the success of a BCA. It is important to carefully consider the existing microbial community and the niche requirements of both the BCA and the target pest when designing a biocontrol strategy or product.

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