Management of Phytopathogens by Antagonistic Bacillus spp in Tomato Crop

Abstract

Bacillus is a genus of gram-positive bacteria that is widely distributed in the environment. The species of this genus present in the endosphere, phyllosphere and rhizosphere in the plant and perform as a beneficial biocontrol agent and promote plant health. These strains exhibit diverse capabilities, including the potentiality to directly suppress the germination of microbial, stimulate plant development, reduce pathogen infections, degrade different types of hydrocarbons, function effectively across a wide temperature range, and induce immune resistance in host plants. The species/strains of Bacillus genus have proven promising biocontrol agents against a large number of fungal and bacterial causal organism, as well as plant-damaging insects. They induce a wide range of composites with antifungal properties, such as iturin, surfactin, cyclic lipopeptides, bacillomycin, bacteriocins, polyketide, lentibiotics, phospholipid, polyketide microlectine, isocosmarin and amino sugar. These compounds play a crucial role in preventing and controlling diseases in plants. The synthesis of these compounds is initiated in response to the presence of bacterial and fungal pathogen biomass and their cell walls. The purpose of this review is to offer a thorough exploration of the disease suppression mechanisms utilized by Bacillus, with a specific emphasis on their function as plant growth-promoting rhizobacteria (PGPR).

1. Introduction

Tomato (Solanum lycopersicum L.) is a highly significant and economically valuable agricultural crop cultivated worldwide, in both field and greenhouse conditions [1]. Tomatoes hold a prominent position in the agricultural sector, with a cultivated area spanning over 5 million hectares. This substantial acreage places tomatoes as the second most widely grown crop after potatoes. The global production of tomatoes is truly remarkable, exceeding an astounding 182 million tons [2, 3]. Despite its widespread cultivation, tomato crops are vulnerable to a range of challenges, including abiotic and biotic stresses [4]. Biotic stresses, arising from factors such as fungi, bacteria, phytoplasmas, viruses, and viroids, significantly impact crop productivity in both greenhouse and field environments [5]. Among these stresses, fungi present one of the most devastating problems, as they affect tomato plants with numerous fungal pathogens [6]. In fact, [7] demonstrated that fungal pathogens are responsible for more than 50% of diseases in tomato plants. Although various methods, such as soil solarization, fungicide seed dressing, spraying of fungicides and bactericides, crop rotation, field sanitation, and soil fumigation, are utilized to control plant diseases, their success is limited [8]. Moreover, treatments like soil fumigation do not provide long-term protection throughout the growing season. High infections often turnout in troublesome areas where soil fumigation was implemented prior the planting season, indicating contamination sources that can be traced back to the growers [9]. While chemical fungicides offer acceptable control of plant diseases in the field, excessive use of these fungicides has been reported to cause environmental pollution and have a destructive impact on human health [10]. In addition, biocontrol management of plant diseases extend a promising and surrogate method to hazardous chemical fungicides for controlling various plant diseases in both field and greenhouse settings. The growing interest in this emerging field can be attributed to a widespread desire to decrease dependence on agrochemicals, owing to their adverse impacts on human health and the environment. As a result, there is an increasing focus on alternative methods and strategies that promote sustainable and environmentally-friendly agricultural practices. The well-known main fungal and bacterial bio-control agents, such as Trichoderma spp., Paecilomyces spp., Bacillus spp., and Pseudomonas spp., have exhibited remarkable abilities in managing a wide range of plant diseases while also promoting plant growth [11]. Moreover, these biological control agents (BCAs) possess a host of additional favorable traits, including rhizosphere competence, fungicide tolerance, saprophytic competitiveness, temperature tolerance, edaphic adaptability, beneficial searching potential, host selectivity, increased reproduction rate, short life cycle, adaptability, and the ability to persist even after reducing the host population [12].

Out of these fungal and bacterial genera, Bacillus is the most well-known and extensively studied bacterial genus. Since the late 1800s, the study of Bacilli has encompassed traditional microbiology and biochemistry methods, as well as more advanced techniques like genomic and proteomic analysis [13]. Bacillus refers to a type of bacterium that is rod-shaped, gram-positive, and can exist in either aerobic or facultative anaerobic conditions [14]. In response to various environmental or nutritional pressures, Bacillus can produce highly resilient endospores that remain dormant for extended periods [15, 16]. Numerous Bacillus species have revealed their role in enhancing plant growth parameters and have proven to be promising biocontrol agents against various plant diseases. Furthermore, they play a role in enhancing plant resilience to both abiotic and biotic stress factors [17, 18]. Several studies have shown that species within this genus promote plant growth through the production of antibiotics, phytohormones, lipopeptides, antimicrobial compounds, nutrient acquirement (such as N and P), and endospores formation, leading to a longer shelf life as well as enhanced plant growth [19, 20, 21, 22]. Specific strains of various Bacillus species have proven effective in controlling fungal pathogens, including Fusarium, Rhizoctonia, Oidium, Septoria, Macrophomina, Botrytis, Pythium, Verticillium, Phytophthora, Sclerotium, and Alternaria. They have also demonstrated efficacy against bacterial phytopathogens, including Erwinia, Pseudomonas syringae, Ralstonia, and Xanthomonas (Figure 1). Notably, certain strains of B. cereus, B. subtilis, B. megaterium, B. velezensis, B. amyloliquefaciens, and other Bacillus species have revealed high effectiveness in controlling numerous plant diseases, such as Fusarium wilt, damping off, grey mold, crown, powdery mildew, verticillium wilt, late and early blight, septoria leaf spot, bacterial wilt, bacterial soft rot, bacterial spot, bacterial speck, and various foliage diseases (Table 1). Therefore, this review aims to explore the promising biocontrol abilities of different Bacillus species/strains against major groups of fungal and bacterial pathogens.

Figure 1.

Antibiotic compounds produced by Bacillus against fungal and bacterial phytopathogens.

Diseases	Causal organism	Species	Reference
Bacterial wilt	Ralstonia solanacearum, Fusarium oxysporum f. sp. radicis-lycopersici, Ralstonia Pseudosolanacearum,	Bacillus Amyloliquefaciens, B. subtilis, B. cereus, B. pumilus, B. licheniformis B. methylotrophicus, B. velezensis	[8, 23, 24, 25, 26, 27, 28]
Gray mold	Botrytis cinerea	Bacillus cabrialesii, B. cereus, B. firmus, B. megaterium, B. endophyticus, B. aryabhattai, B. velezensis, B. subtilis, B. licheniformis, B. amyloliquefaciens, B. methylotrophicus, B. halotolerans	[17, 29, 30, 31, 32, 33, 34, 35, 36]
Fusarium wilt	Fusarium solani, Fusarium oxysporum f. sp. lycopersici	Bacilllus megaterium, B. amyloliquefaciens, B. cereus, B. velezensis, B. methylotrophicus, B. huringiensis, B. pumilus, B. subtilis	[9, 18, 37, 38, 39, 40, 41, 42, 43, 44]
Bacterial soft rot	Erwinia carotovora	B. firmus, B. megaterium, B. endophyticus, B. aryabhattai, B. velezensis, B. subtilis, Bacillus cereus	[35, 45, 46]
Bacterial speck	Pseudomonas syringae	Bacillus cereus, B. firmus, B. megaterium, B. endophyticus, B. aryabhattai, B. velezensis, B. subtilis	[35, 47, 48]
Bacterial spot	X. perforans, X. campestris, X. vesicatoria and X. gardneri, Xanthomonas euvesicatoria	B. subtilis, B. amyloliquefaciens B. velezensis, B. pumilus, B. cereus, B. methylotrophicus	[49, 50, 51, 52, 53, 54]
Damping-off	Rhizoctonia solani, Pythium aphanidermatum, Fusarium solani, Fusarium oxysporium	Bacillus subtilis, B. firmus, B. megaterium, B. endophyticus, B. aryabhattai, B. velezensis, B. polymyxa, B. thracis, B. circulans and B. polymyxa and B. sphaericus, B. amyloliquefaciens	[16, 35, 55, 56, 57, 58, 59, 60]
Verticillium wilt	Verticillium dahliae & V. longisporum	B. amyloliquefaciens, B. firmus, B. megaterium, B. endophyticus, B. aryabhattai, B. velezensis, B. subtilis, B. thuringiensis and B. weihenstephanensis, B. cereus	[30, 42, 61, 62]
Late blight	Phytophthora infestans	B. subtilis, B. firmus, B. megaterium, B. endophyticus, B. aryabhattai, B. velezensis, B. pumilus, B. cereus	[35, 63, 64, 65, 66, 67]
early blight	Alternaria solani & Alterneria alternata	B. amyloliquefaciens, B. cereus, B. firmus, B. megaterium, B. endophyticus, B. aryabhattai, B. velezensis, B. subtilis	[64, 65, 66, 68, 69]
Septoria leaf spot	Septoria lycopersici	B. cereus, B. amyloliquefaciens, B. subtilis, B. thuringiensis	[65, 66, 68, 70]
Powdery mildew	Oidium lycopersicum & Oidium neolycopersici	Bacillus subtilis, B. amyloliquefaciens	[65, 71, 72]
Crown and root rot	Pseudomonas solanacearum, R. solani, Phytophthora capsici, F. oxysporum f. sp. lycopersici & radicis-lycopersici (Forl)	B. subtilis, B. pumilus, B. siamensis, B. thuringiensis, B. amyloliquefaciens	[1, 26, 73, 74, 75, 76]

Table 1.

The antagonistic effect of Bacillus sp., for controlling of various diseases in tomato crop caused by phytopathogens.

2. Diseases, symptoms, causal organism and nature of pathogen in tomato crop

Tomato is the most popular vegetable crop cultivated worldwide [70]. It serves as an excellent source of nutrition, containing essential components such as vitamin C, potassium, carotenoids, and various phytochemical compounds [77, 78]. However, crops belonging to the Solanaceae family, including tomato, are highly susceptible to various fungal diseases that significantly reduce both the quality and yield of the crop [63]. These diseases like damping off, grey mold, fusarium wilt, powdery mildew, crown, fruit and root rot, verticillium wilt, late and early blight, bacterial soft rot, septoria leaf spot bacterial wilt, bacterial spot, and bacterial speck, can cause yield losses ranging from 10 to 90% [3, 29, 37, 38, 47, 61].

2.1 Crown and root rot disease

F. oxysporum f. sp. radicis-lycopersici (FORL) is the causal agent of crown and root rot disease in tomato crops. This disease for first time in 1974 was reported in Japan and has since become widespread in various regions across the world [79, 80]. It stands as a significant soil-borne ailment affecting tomato cultivation [73]. The fungus exhibits the capability to infect both tomato seedlings within transplant houses and fully grown plants in the open field [1]. F. oxysporum severely infects the root and collar of a plant during the early stages’ growth, leading to decreased productivity in field and greenhouse conditions [81]. The symptoms exhibited by affected tomato plants include stunted growth, leaf chlorosis and premature shedding lower true leaves. As the disease progresses, a distinct brown lesion develops around the root and shoot junction, by showing root rot, wilting, and leading toward plant death [82]. In both greenhouse and field environments, the disease has been observed to result in crop yield reductions spanning from 20 to 60% [83].

2.2 Damping-off

Tomato damping-off, which is triggered by pathogens like Pythium aphanidermatum and Rhizoctonia solani [55], F. solani [56], and F. oxysporum [16, 57], is one of the most aggressive and destructive diseases of tomato crop. This disease leads to the deterioration of germinating seeds and juvenile seedlings, resulting in a significant reduction in crop productivity. Damping-off poses a major problem for cultivators, whether they are operating in greenhouses or in the field [84]. In the literature, the definition of damping-off is challenging due to varying perspectives among researchers. Some consider it a sickness, while others view it as a symptomatic condition [85, 86]. Damping-off can be categorized into two types: pre-emergence and post-emergence. Soil-borne pathogens are commonly responsible for the spread of damping-off, and play a major role in post emergence of the disease [87]. The disease symptoms of damping-off in tomato plants manifest in two distinct ways. Firstly, after emergence, the seedling’s hypocotyl becomes discolored and water-soaked at the soil surface, ultimately leading to plant death [88]. Secondly, under favorable conditions, the typical symptoms include stunted growth, the presence of brown and small water-soaked lesions around the leaves, and infection of the entire root system. Often, seedlings die before they can even emerge [89]. In the field, losses of up to 100% have been recorded [90].

2.3 Fusarium wilts diseases

Fusarium wilt disease of tomatoes, caused by Fusarium species such as F. oxysporum f. sp. lycopersici and F. solani, is a highly destructive constraint in tomato production [18, 39, 40]. The disease was first reported by W.C. Snyder and H.N. Hansen in 1940 [91]. Fusarium species can induce a fatal vascular disease known as wilt, primarily affecting plants of the Solanaceae family [92]. This soil-borne fungal disease significantly impacts tomato crop yield in regions like tropical and subtropical, as the pathogen has the potential to persist in the soil medium for maximum periods of time and infiltrate plants through root injuries [38]. The aggressive nature of this disease presents a significant challenge in terms of control, primarily due to the pathogen’s ability to attack vascular tissue and its soil-borne nature [39]. In the presence of the pathogen, the disease manifests as obstruction and degradation of the xylem within the host plant [93]. Typical symptoms include vascular wilting, yellowing, leaves’ wilting, and discoloration of the vascular tissue, which may turn dark brown. The disease may exhibit symptoms like stunted growth and may eventually lead to the death of the entire plant. In greenhouse and field condition, it was estimated that yield losses may be in range of 50% due to Fusarium wilt [1].

2.4 Verticillium wilt

Verticillium wilt, also known as vascular wilt, poses a serious challenge to sustainable development and cultivation of tomato plant. A number of species of Verticillium fungus such as V. dahliae and V. longisporum, has been reported and that may leads decline yield production in both yield and fruit quality [30, 61]. Verticillium wilt in tomatoes was reported in 1928 by H.C. Pierce and W.C. Snyder [94]. Unfortunately, resistant tomato varieties were not available at that time to combat this destructive disease [62]. The Verticillium fungus obstructing vascular system of a plant and lead to wilt and death of plant consequently, and the affected plants exhibit symptoms such as wilting [95]. By infiltrating the tomato plant via the roots, this fungus establishes itself within the xylem vessels and generates adhesive substances that hinder the transportation of water and nutrients [96, 97]. Furthermore, it produces harmful compounds that stimulate the plant’s defense mechanism, resulting in the generation of reactive oxygen species (ROS) and the reinforcement of the cell wall [98]. Verticillium wilt disease of tomato crops symptoms includes yellowing and curling of the leaves, particularly at the lower portion of the plants, as well as stunted growth and browning or discoloration of the stems, especially near the plant’s base. Dark brown streaks in the vascular tissue may also be present, indicating damage to the plant’s vascular system [89, 99]. Yield losses attributed to verticillium wilt in tomato crops can range from 10 to 50% or even more [100]. Consequently, effective strategies and resistant varieties are needed to combat this devastating disease and protect tomato crop productivity.

2.5 Grey mold

A variety of diseases pose a threat to tomato crops, and among them is gray mold, also referred to as Botrytis gray mold, and caused by Botrytis cinerea airborne necrotrophic fungal pathogen which has impact on the quality and production of tomato globally [29, 30]. The discovery of gray mold affecting tomatoes was initially reported by Whetzel and Hesler in 1923 [101]. Particularly vulnerable to gray mold are fresh-market tomatoes, making it a crucial concern both before and after harvest [31]. The pathogen attacks different parts of the tomato plant including, flowers, leaves, stems and fruits, leading to significant damage [102]. Under cool and humid weather conditions, the fungus flourishes, leading to the formation of a grayish mold on the affected areas of the plant. B. cinerea affects approximately 200 plant species and causes lesions, producing numerous spores on the above-ground sections of plants [103]. Gray mold disease presents distinct symptoms, such as the presence of grayish-brown fuzzy mold on the leaves surface, stems and tomato fruit. Infected leaves and stems may also exhibit a covering of grayish-brown fuzzy mold, while turning brown or black in color. The fruit manifests grayish-brown mold symptoms and may become soft and mushy. Plants affected by this disease experience stunted growth and a decline in fruit quality and yield, whether in greenhouses or fields [29, 32, 33, 34]. Gray mold causes significant losses, ranging from 5 to 20% of the crop in greenhouse and field environment [104].

2.6 Late blight disease

Late blight, a destructive disease affecting tomatoes, is caused by Phytophthora infestans (Mont.) de Bary, which belongs to the family Oomycetes. Oomycetes are a unique group of filamentous eukaryotes [105]. The pathogen devastating impacts on several plant species, comprising those in the Solanaceae family. During the nineteenth century, the pathogen caused widespread devastation to potato crops, leading to the catastrophic event known as the Irish potato famine [106]. Unfortunately, during that time, no resistant cultivars were available for tomatoes or potatoes to combat late blight disease [64]. This pathogen thrives in cool and humid weather conditions and produce visible symptoms on entire parts of the plant at any stage of growth in form of dark lesions [107]. It causes extensive damage to the stems, leaves, and fruits, often leading to complete crop losses within a mere two weeks [108]. The characteristic symptoms of late blight manifest as water-soaked lesion on entire plant parts, which initially appear light green and later turn brown or black [109]. As the disease progresses, it spreads rapidly, transforming into white mold symptoms on the undersides of stems and leaves. Affected leaves develop irregular shapes, accompanied by dark brown lesions which are often encircled by a yellow halo [110]. Additionally, the fruit can start rotting at the stem end or any other part. Infected plants exhibit symptoms of yellowing, wilting, and eventual death [89]. This devastating disease inflicts annual losses exceeding five billion USD on the crop, as reported by various sources [111].

2.7 Early blight disease

Early blight is one the most important fungal disease caused by Alterneria solani (Ellis and Martin) Jones and Grout and A. alternata, that poses a serious threat to tomato crops production [65, 68]. This fungal pathogen is not limited to tomatoes but also affecting other plants like potatoes and eggplants [112]. A. solani a soil-borne as well as airborne pathogen responsible for diseases like leaf blight, collar, and fruit rot in tomatoes, whereas the disease can be spread through fungal spores [113]. It was first reported in early nineteenth centuries in the US, quickly becoming a significant concern for tomato growers [114]. In regions with high levels of dew, rainfall, humidity, and temperatures, can lead to complete defoliation of the leaves and particularly detrimental to tomato plants [115]. The pathogen produces enzymes like cellulases, which dissolve the cell wall of host’s plant by pectin methyl galacturonase, which aids in host colonization. As a result, the disease negatively impacts crop production by causing premature defoliation, may become cause of low quality and quantity of fruit [116]. Initial symptoms of the disease include brown to black lesion appears on the lower leaves during the early stages of disease development, and gradually spreading to the upper parts of the plant over time. These spots typically are in range of 1/8 to 1/4 inch in diameter. In most cases, the disease manifests on the stem with dark and brown discoloration. Subsequently, the leaves exhibit yellowing symptoms, ultimately resulting in plant defoliation. Furthermore, early blight also affects the quality of tomato fruit, causing dark, sunken lesions [117]. The yield losses due to the disease have been reported in a range of 79% in tomato crops [118].

2.8 Powdery mildew disease

Powdery mildew disease of tomato caused by Oidium lycopersicum and O. neolycopersici are the major constrains in tomato production that affects all parts of the tomato plant [71, 72, 119]. This disease was observed for first time in England in 1986 and 1987, and it has then spread world-wide [120, 121]. Consequently, the new mildew pathogen on tomato plants was variously termed O. lycopersicum, Erysiphe orontii or E. cichoracearum) or was simply described as Erysiphe sp.. The first appropriate description of the fungus, Oidium lycopersicum, appeared to come from Australia, and the name was re-designated, in 1999, as Oidium lycopersici, in accordance with the International Code of Botanical Literature [122]. However, confusion remained over classification based on morphological characteristics. Consequently, we analysed the internal transcribed spacer regions of the nuclear rRNA genes from the new tomato powdery mildew pathogen and were able to differentiate Oidium (neo)lycopersici from E. orontii and E. cichoracearum. Moreover, we found O. (neo) lycopersici to be a sister taxon of E. aquilegia var. ranunculi. Importantly, it was recognized that all recent outbreaks of tomato powdery mildew reported outside Australia were caused by a species that formed conidia singly, or, in high relative humidity, in pseudo-chains of 2–6 conidia, and so created a new species, O. neolycopersici, for this pathogen. The Australian isolates, which always formed conidia in chains, retained the name Oidium lycopersici. However, its true identity was uncertain due to the lack of a sexual stage and varying reports of its structure, particularly whether conidia were formed singly or in chains. O. lycopersicum (Erysiphales) differs from L. taurica based on a number of characteristics, including conidiophore and conidia morphology, and from E. cichoracearum, which produces conidia in long chains [123]. It has the ability to infect the crop at any stage of growth in a greenhouse or in the field, leading to a reduction in fruit quality and yield. Consequently, a huge number of tomato cultivars are susceptible to Oidium spp. [124]. This disease can manifest at any stage of the crop by producing symptoms likes spots on the leaves, stems, and fruits, and may lead to cover the entire plant parts [119]. Subsequently, the leaves become distorted and stunted, exhibiting curling and twisting [125]. These dark spots or blotches appeared on the infected fruits, damaging their shape and color of the fruit and ultimately lead to loss of fruit in the form of its quality. In most cases, premature leaf drop occurs, leading to a decrease in photosynthesis that contributes to yield reduction [126] and the estimated yield was around 50% in fruit and yield, in control environment as well as in field conditions [127].

2.9 Septoria leaf spot disease

Septoria leaf spot (also named as septoria blight) is caused by Septoria lycopersici, most aggressive and destructive pathogen of vegetables. It contributes huge losses to tomato production in market and poses a major threat to tomato production worldwide [66]. The earliest report of Septoria leaf spot in the United States came from Byron D. Halsted, an American plant pathologist, who observed it in New Jersey during the years 1894 to 1895. Since then, the disease has spread to tomato-growing areas worldwide, presenting continuous challenges for tomato growers [128]. Disease incidence tends to increase significantly during the summer when temperatures reach their peak and precipitation is high. When temperatures exceed 25°C and leaves remain wet for extended periods, tomato yields can decrease by more than 50% [129]. The pathogen primarily spreads through contaminated seeds, but it can also survive in crop debris for extended periods [130]. Septoria leaf spot affects plants at any stage when temperatures range between 20 and 25°C, combined with high humidity and rain showers [131]. Under such conditions, the fungus initially targets older leaves, causing circular spots with dark brown margins and tan to gray centers. These spots are accompanied by black pycnidia, leading to extensive damage across the entire leaf area [132, 133]. The disease also manifests as small, dark lesions measuring approximately 1–8 mm in diameter on stems, peduncles, and calyxes [134]. This ultimately results in a significant reduction in fruit yield, not only due to the loss of photosynthetic area but also because the fruit becomes more susceptible to sunburn. In severe cases, tomato crops have experienced estimated disease losses of up to 100% [135].

2.10 Leaf mould

Leaf mould of tomato caused by Cladosporium fulvum syn. Passalora fulva, is one of the most devastating diseases in tomato crop [80]. The disease was first time reported in Netherlands [136]. Typically, the fungus primarily affects the foliage of tomato plants, although there are instances where stems, blossoms, petioles, and fruit can also be targeted. Successful infection occurs when the fungus conidia settle on the lower side of a leaf, germinate, and enter the plant through open stomata [137]. Symptoms of the disease become apparent approximately one week after infection, manifesting as pale green or yellowish diffuse spots on the upper surface of the leaves. Over time, these spots enlarge and become distinctive yellow patches due to cell death in the palisade parenchyma. The most noticeable symptoms are observed on the lower side of the leaf, where patches of white to olive-green mould develop, eventually turning brown when sporulation begins [138]. In the initially stage of the disease, the stomata become blocked by clusters of conidiophores, which use the stomata to exit the leaf and release conidia, further contributing to the spread of the disease. Stomatal blockage severely impedes plant respiration, leading to leaf wilting, partial defoliation, and, in severe infections, the death of the affected plant [139]. In the favorable condition the disease cause up to 50% yield losses [140].

2.11 Bacterial soft rot disease

The presence of bacterial soft rot disease poses serious threat to tomato crops production, resulting in substantial yield losses in both greenhouse and open field environments, surpassing the impact of other bacterial diseases [35]. The initial occurrence of this disease was observed on tomato fruit in a greenhouse in the Buenos Aires province in 1995 [45]. The pathogen responsible for this disease is known as Erwinia carotovora subsp. carotovora (Ecc) [141]. Ecc, a rod-shaped bacterium, affects a wide range of vegetable crops, including potatoes, carrots, onions, cucumbers, lettuce, and tomatoes. It can also infect ornamental plants under favorable environmental conditions [142]. The pathogen has the ability to infect all parts of the plant and exhibits severe symptoms in tomato plants. Initially, yellowing symptoms on the lower side of leaves, led by brown-yellowing of the pith and stem xylem vessel [143]. As the disease progresses, the entire tomato plant wilts, showing water-soaked lesion all over the stem, vascular tissue turn brown, pith become hollow, and rotting of stems and fruits. The symptoms typically begin in the root or crown region of seedlings in greenhouses or fields [144]. It has been reported that yield losses up to 100% may be reached due to the bacterial soft rot disease [145].

2.12 Bacterial speck

Pseudomonas syringae (Okabe) Alstatt is the causal agent of Bacterial speck of tomato, is the most prevalent bacterial disease infecting tomato plants worldwide [146]. The first recorded instance the disease in tomato plants was reported by J.C. Walker in New York in 1922 [147]. Since then, the disease has been spread to rest of the world and identified in various tomato-growing regions worldwide and continues to pose a significant threat to tomato production, whether in greenhouses or open fields. The pathogen is commonly introduced through infected seeds or may already be present in the surrounding environment [148]. The disease manifests as small black spots with a sunken appearance on green tomato fruits, accompanied by darker green halos that eventually develop into cankers. Ripe tomato fruits exhibit dark brown to black spots, ranging from 1 to 2 mm in diameter. Additionally, bacterial speck disease often presents with large black spots on older leaves, stems, and petioles [149, 150]. These symptoms contribute to various losses, including reduced fruit yield and quality, diminished plant vigor, and heightened susceptibility to other diseases [151]. In severe cases, bacterial speck can lead to defoliation and even death of the plant. The extent of these losses depends on the severity of the infection, the susceptibility of the tomato cultivar, and environmental factors such as temperature and moisture [152, 153]. It is estimated that bacterial speck disease causes a staggering 52% loss in tomato crops [154]. Given its detrimental impact, effective management strategies are crucial to mitigate the economic and agricultural consequences associated with this disease.

2.13 Bacterial wilt

Bacterial wilt of tomato, caused by Ralstonia pseudosolanacearum and R. solanacearum [155], are the major constrain in tomato losses in temperate, tropical and subtropical regions in the worldwide [23]. These pathogens have the ability to infect around 200 plant species, including those in the Solanaceae family [24]. The typical symptoms exhibited an infected tomato plants may include stunted growth, yellowing of leaves, vascular discoloration, wilting and ultimate cause death, all of which are associated with the presence of the bacterial wilt pathogens R. solanacearum and R. pseudosolanacearum [25]. When stems affected by the disease are submerged in water, bacteria continuously seep out from the cut ends. Transmission of R. solanacearum occurs through various means, including root contact, irrigation water, insects, and machinery [8, 26, 71]. In tomato crops, this disease can result in yield losses of up to 91% [156].

2.14 Bacterial spot disease

Bacterial spot of tomato is a significant foliar disease that affects the plant at any stage and hampers the growth of both fruit and plant [49]. The disease is caused by five species of the bacterial genus Xanthomonas: X. euvesicatoria, X. perforans, X. campestris, X. vesicatoria, and X. gardneri. These bacteria result in substantial losses in tomato production [49, 50, 51, 52, 53, 54]. This disease was first observed in tomato plants in the United States in the early 1900s, specifically in the southern states of Georgia and South Carolina [157]. The pathogen responsible for this disease can spread through contaminated seeds, live as epiphytes on tomato leaves, and infect various parts of the plant by inducing spots, lesions, and defoliation. It can also persist on weeds and infected plant debris [158, 159]. Furthermore, heavy rainfall, contaminated mechanical tools, and insects serve as additional vectors for spreading the pathogen [160]. The pathogen produces numerous bacteriocin-like substances that pose a risk to fruit and plant growth [161]. Due to heavy rainfall, the disease exhibits early symptoms on the leaves, stem, and fruits, thereby reducing the quality and yield of the fruit [125]. As the disease progresses, small, water-soaked, round dark brown spots appear on the affected parts of the leaves, later turning black with a near-yellow halo [162]. These water-soaked spots increase in size and undergo a color transformation from dark green to purplish-gray, accompanied by the emergence of a recognizable black center. Over time, the leaf spots expand and merge, creating a scorching appearance [163]. This destructive disease has been recorded to cause losses of up to 50% in greenhouse tomato crops and overall yield [164].

3. Control of fungal and bacterial disease through Bacillus sp., in tomato crop

Chemical fungicides are commonly utilized to prevent various pests and diseases, but they have limited effectiveness and pose harm to crop physiology, human health and also harmful impact on environment [1]. In order to manage these diseases and decrease pathogen populations in crops, novel and alternative approaches like the utilization of fungi and bacteria as biocontrol agents have been implemented [24]. The possession of both antagonistic and plant growth-promoting characteristics by biocontrol agents is considered significant for managing plant diseases and improving fruit yield. Numerous rhizobacteria including Bacillus, Streptomyces, Pseudomonas, Flavobacterium, Brevibacillus, Mesorhizobium and Rhizobium found in plants exhibit growth-promoting properties, capable of mitigating pathogen infections and enhancing plant development [165]. Among them, Bacillus sp., are well-known for their superior bacterial antagonistic properties compared to other genera because they can survive at higher temperatures and resist desiccation by producing endospores within the cell. Additionally, Bacillus sp., can promote plant growth to some extent under unfavorable conditions [166]. Bacillus species possess the capability to decrease populations of fungal pathogens through the production of a substantial quantity of antibiotics. They achieve this by lysing cells, promoting plant growth, and triggering resistance against a range of diseases. Bacillus species are capable of producing a variety of antibiotics, including iturin, surfactin, cyclic lipopeptides, bacillomycin, bacteriocins, polyketide, lentibiotics, phospholipid, polyketide microlectine, isocosmarin and amino sugar. These antibiotics play a crucial role in inhibiting the growth and spread of bacterial and fungal pathogens, which are responsible for causing diseases in plants. By producing these diverse compounds, Bacillus species effectively suppress the harmful microorganisms, thus protecting the health and vitality of plants. Out of the 21 isolates tested, only B. amyloliquefaciens (FZB24) showed maximum growth inhibition of F. oxysporum through dual assay test. The study also revealed that B. amyloliquefaciens was further efficacious in reducing the occurrence of Fusarium wilt disease in tomato plants due to its abundance of antibiotics and enzymes, including polyphenol oxidase, ammonia lyase, phenylalanine catalase, superoxide dismutase and peroxidase [41]. Bacillus velezensis, recover from the crown root tissue of tomatoes, produced various compounds such as lipopeptides, polyketides, dipeptide bacilysin, and volatile substances including fengycin, bacillomycin, surfactin, benzaldehyde, bacillaene, macrolactin, difficidin, tetradecane, dipeptide bacilysin, benzeneacetic acid, benzaldehyde, phenylethyl alcohol and 1-decene. Additionally, the specie exhibited the ability to generate lytic enzymes (chitinase, protease, and β-glucanase), indole-3-acetic acid, solubilize inorganic phosphate and siderophore. B. velezensis achieved a maximum growth suppression on the mycelial development of V. dahliae and decrease the prevalence of wilt disease in tomatoes by 70.43% in both greenhouse and open field conditions [42]. Two selected isolates of Bacillus produced antibiotics, cyanide, and solubilized phosphate, resulting in a 44% growth inhibition against F. oxysporum, responsible for the root and crown rot disease in tomatoes [73]. Due to the presence of polyphenol oxidase, superoxide, catalase, dismutase, and peroxidase activities produced by Bacillus subtilis CBR05 the treated tomato plants exhibited a minimum occurrence (36%) of soft rot disease [46]. In another study, B. subtilis suppress the root and crown rot disease incidence by up to 75% in a greenhouse [9]. A total of 200 different strains of Bacillus were obtained from the rhizosphere soil of tomatoes and potatoes. These strains were carefully examined and tested to determine their ability to antagonist or inhibit the growth and activity of the bacterial wilt pathogen Ralstonia solanacearum. Out of these strains, only four strains showed promising results in combating bacterial wilt disease. Specifically, two strains of B. amyloliquefaciens (AM1 and D29), one strain of B. subtilis (D16), and one strain of B. methylotrophicus (H8) displayed significant decreases in the prevalence of bacterial wilt disease. The reduction in disease incidence ranged from 81.1 to 89.0%, indicating a strong antagonistic effect against the pathogen Ralstonia solanacearum. Furthermore, these four strains demonstrated additional beneficial effects on the growth and development of the plants. They were found to enhance plant height by up to 20–45% and also increase the dry weight of plant by up to 45–92%. These positive effects were attributed to the production of certain compounds such as indole-3-acetic acid, phosphate solubilization and siderophores by the Bacillus strains. These compounds are known to promote plant growth and nutrient uptake. The greenhouse experiments revealed the potential of these specific strains of Bacillus in improving plant health and productivity, providing a promising solution for managing bacterial wilt disease in tomato and potato crops [8]. Lamsal et al. [167] obtained seven Bacillus strains from the rhizosphere of tomato crops. These isolated strains exhibited a significant inhibitory effect, with more than 80% suppression of mycelial growth of the targeted pathogen. Moreover, they demonstrated a remarkable reduction of 74% in the incidence of late blight disease in a greenhouse environment. Additionally, the Bacillus strains were found to positively influence plant growth. Furthermore, the researchers explored the potential of a B. subtilis formulation as a seed treatment method. They discovered that this treatment was particularly effective in combating damping off disease, which is caused by the pathogen Pythium aphanidermatum [56]. Hentriacontane and 2,4-di-tert-butylphenol are metabolic compounds of B. cereus (MH778713). These compounds have demonstrated strong inhibitory properties against various fungal plant pathogens, including F. oxysporum and Colletotrichum orbiculare, which cause fusarium wilt in tomatoes [18]. Im et al. [27] successfully isolated two metabolites, namely oxydifficidin and difficidin derivatives, from the strain methylotrophicus (DR-08). These compounds were proven to possess significant effectiveness against the bacterial wilt pathogen R. solanacearum. Through pot and field experiments, the strain DR-08 demonstrated its ability to effectively suppress the development of bacterial wilt in tomatoes, as well as bacterial leaf spot symptoms on peach and red pepper plants. The desired outcome was achieved using a concentration of 30%. These findings highlight the potential of DR-08 as a biocontrol agent for managing bacterial diseases in various crops, including tomatoes, peaches, and red peppers.

4. Conclusion

In this review, we emphasize the capacity of microbial antagonists to efficiently control infectious plant diseases originating from fungal and bacterial pathogens in tomato crops. Various species/strains of Bacillus, including B. subtilis, B. cereus, B. megaterium, B. endophyticus, B. velezensis, B. amyloliquefaciens, and B. methylotrophicus, have been identified as having favorable characteristics as plant growth-promoting rhizobacteria (PGPR) and biocontrol capabilities. The identification of potent Bacillus strains typically involves extensive sampling from the rhizosphere of the specific host plant, followed by dual assay method and in vivo testing against the target plant pathogen(s). In some instances, more than a hundred Bacillus strains have proved antagonistic antifungal activity against fungal and bacterial pathogens through in vitro methods, with certain strains exhibiting high growth inhibition. The effective Bacillus strains produce various compounds such as iturin, surfactin, cyclic lipopeptides, bacillomycin, bacteriocins, polyketide, lentibiotics, phospholipid, polyketide microlectine, isocosmarin and amino sugar. These compounds performance well to suppressing bacterial and fungal pathogens responsible for numerous plant diseases. Each Bacillus strain produces unique metabolites and compounds, resulting in variations in type and quantity. Consequently, these compounds display strain-specific effects in inhibiting the growth and infection of specific phytopathogens. Studies have shown that mutant strains lacking specific compounds are ineffective in controlling the targeted pathogens. Generally, Bacillus bacteria inhabit the root rhizosphere and endosphere of host plants, forming mutually beneficial relationships with them. These bacteria colonize the root rhizosphere and endosphere and provide several benefits to the host plant, including nutrient acquisition, disease suppression, and stress tolerance. Therefore, Bacillus species have been widely utilized for controlling various diseases in plants, including fungal soil-borne, root infecting, seed-borne, crown, fruit and root rot, Fusarium wilt, Verticillium wilt, Septoria leaf spot, damping-off, grey mold, late and early blight, and powdery mildew. Moreover, they effectively combat some bacterial diseases viz., bacterial wilt, bacterial speck, bacterial spot, and bacterial soft rot. The addition of Bacillus cell cultures or cultural filtrates containing effective compounds to the soil surrounding the roots, as well as seed treatment with these compounds, offer comparable benefits in preventing plant pathogen infestations. In some cases, more efficient disease control can be achieved by combining Bacillus with other bacterial antagonists (e.g., Pseudomonas) or fungal antagonists (e.g., Trichoderma spp.) or by using compatible fungicides. Overall, the appearance of Bacillus in the root rhizosphere and endosphere significantly influences the health and productivity of host plants.

Acknowledgments

I thank Professor Abdul Mubeen Lodhi and Professor Chengyun Li for their inspiration and help to carry out this work.

Conflict of interest

The authors declare that there is no conflict of interest.