Control Strategies of the Major Soilborne Fungal/Oomycete Diseases: History
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Minxiao Ma
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Paul W. J. Taylor
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Deli Chen
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Niloofar Vaghefi
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Ji-Zheng He

Globally, tomato is the second most cultivated vegetable crop next to potato, preferentially grown in temperate climates. Processing tomatoes are generally produced in field conditions, in which soilborne pathogens have serious impacts on tomato yield and quality by causing diseases of the tomato root system. Major processing tomato-producing countries have documented soilborne diseases caused by a variety of pathogens including bacteria, fungi, nematodes, and oomycetes, which are of economic importance and may threaten food security. Surveys in the Australian processing tomato industry showed that plant growth and yield were significantly affected by soilborne pathogens, especially Fusarium oxysporum and Pythium species. Globally, different management methods have been used to control diseases such as the use of resistant tomato cultivars, the application of fungicides, and biological control. Among these methods, biocontrol has received increasing attention due to its high efficiency, target-specificity, sustainability and public acceptance. The application of biocontrol is a mix of different strategies, such as applying antagonistic microorganisms to the field, and using the beneficial metabolites synthesized by these microorganisms. 

  • biocontrol
  • fungus
  • oomycete
  • soilborne pathogen
  • tomato

1. Tomato Corky Root Rot

1.1. Conventional Control Methods

Cultural Control

The disease development of corky rot is at optimum at 15.5–20 °C [1]. Thus, it is better to plant tomatoes in spring when the soils start to become warm.
Though effective against many other pathogens, crop rotation alone may not be effective in controlling corky root rot, for P. lycopersici has a wide host range including cucumber, eggplant, lettuce, melons, and pepper [2].

Physical Control

Soil solarization by covering the field with plastic film for a long period is a practical method for the control of corky root rot. In Italy, Vitale et al. [3] found that solarization performed with ethylene-vinyl-acetate film has an identical level of control effect on corky rot symptoms as compared with fumigation with methyl bromide, which was better than that of metham sodium and metham potassium fumigation. However, the level of success of solarization depends on the combination of high ambient temperatures, maximum solar radiation, and optimum soil moisture as well as the existing inoculum and disease levels [4][5]. Therefore, solarization usually has varying effectiveness, and is generally less effective in climates where high summer temperatures coincide with the rainy season due to the cooling effect of rainfall and extensive clouds blocking the solar radiation [4].

Chemical Control

In fields previously reported to have corky root rot, a preplant treatment with soil fumigation was shown to reduce disease in the subsequent tomato crop [3]. Methyl bromide (MBr) used to be a preferred chemical, but it was proved to be an ozone-depletion agent which is more destructive to stratospheric ozone than chlorine [6], thus its use has been phased out in developed countries by 2005 and in 2015 by the less developed countries as required by Montreal Protocol [7]. Potential alternative chemicals such as chloropicrin, metam sodium, metam potassium, and dazomet [3][8][9] can only provide a lower control level of corky root rot compared with MBr treatment. For example, Vitale et al. [3] found that metham sodium fumigation (MS, 353 litres a.i. ha−1) and metham potassium fumigation (MK, 350 litres a.i. ha−1) did not reduce the disease incidence of corky root rot in their trial. Therefore, with reduced efficiency of chemical controls, the management of corky root rot may require the addition of more effective methods such as the use of resistant cultivars and biocontrol.

Resistance Breeding

Though breeding for resistant cultivars is a common strategy for the control of crop disease, commercial variants of both processing and fresh consumption tomatoes are susceptible to corky root disease [10]. So far, only one single recessive gene (pyl) was shown to confer resistance to corky root rot and was introgressed into Lycopersicon esculentum from L. peruvianum [11]. The pyl gene is later found to possibly be a recessive allele of a susceptibility gene [12] and it has not been cloned yet.

1.2. Biological Control

Some fungivorous nematodes have been recorded as potential biocontrol agents for corky root rot. Hasna et al. [13] tested two fungivorous nematodes, Aphelenchus avenae and Aphelenchoides spp. against P. lycopersici, and concluded only A. avenae was able to significantly reduce the severity of tomato root rot in greenhouse trials with a population of 3 or 23 nematodes mL−1 soil. However, in a later on-farm trial covering two tomato seasons in Sweden, Hasna et al. [14] found even at a higher inoculation rate of 50 nematodes mL−1 soil, the application of A. avanae into infested soil did not reduce corky root disease severity. Thus, the potential of nematodes to control corky root rot may not be dismissed, but the application method may still need improvements.
In greenhouse trials, bacterial antagonists such as Streptomyces spp. have been found to effectively suppress corky root disease of tomatoes and enhance plant growth, resulting in higher yields. Bubici et al. [15] evaluated the antagonism of twenty-six Streptomyces spp. against corky root rot on tomatoes in both glasshouse and field conditions and found the most effective strain can reduce disease severity up to 64% in the glasshouse and 48% in the field.
Antagonistic fungi may also be used in the biocontrol against corky root rot. Fiume and Fiume [10] conducted glasshouse trials against corky root rot using Trichoderma viride, Bacillus subtilis, and Streptomyces spp., and concluded that the application of all three microorganisms significantly reduced the corky root symptoms in terms of disease index, with T. viride having the best results, followed by Streptomyces spp. Besoain et al. [16] performed UV on native T. harzianum to obtain mutants and found the mutants ThF1-2 and ThF4-4 inhibited the growth of P. lycopersici in vitro by 1.3 and 5 fold, respectively. Sánchez-Téllez et al. [17] further tested the mutant ThF1-2 in greenhouse tomato trials and found applying solid formulation ThF1-2 resulted in a significantly lower root damage caused by P. lycopersici compared with a previous trial using MBr. The control of T. harzianum against P. lycopersici seems to be correlated to the differential expression of extracellular fungal cell wall hydrolytic enzymes between isolates [18].
Organic amendments may also help in the control of corky root rot. Workneh et al. [19] found that the application of green manure and compost reduced the corky root rot severity in organic farm tomatoes by stimulating microbial activities in a field survey. However, P. lycopersici responds differently to different amendments. Hasna et al. [20] tested composts consisting of green manure, garden waste, and horse manure against corky root rot in greenhouse tomatoes and found that garden waste compost significantly reduced the disease, whereas horse manure compost significantly stimulated disease, while the green manure compost had no effect on the disease despite the increased microbial activity. It was concluded that the disease severity of corky root rot can be suppressed by composts with a low concentration of ammonium nitrogen and a high concentration of calcium, but further studies may be necessary to further prove this perspective.

2. Fusarium Crown and Root Rot (FCRR) of Tomato

2.1. Conventional Control Methods

Cultural Control

Hygiene and sanitation of the seeds and transplant seedlings are important for Forl management. For example, Muslim et al. [21] found that plants not challenged with the pathogen still become infected by FCRR, which is probably due to incomplete soil sterilization. It is also strongly recommended that all equipment coming in direct contact with soil is cleaned and disinfected [22]. The pathogen may also use colonized and infected plants as carrying vectors, thus the infected plants and their roots should be removed immediately.
Crop rotation with a non-host crop may also prevent FCRR. Crops susceptible to Forl such as eggplants and peppers should be avoided in the rotation [23], while non-hosts such as lettuce may be useful to reduce inoculum levels in the soil [24]. However, the efficiency of crop rotation may be limited for FCRR control, because the pathogen can survive as chlamydospores in the soil for a long time [25].

Physical Control

FCRR is favored by cooler temperatures, thus planting in warm periods and using warm water in irrigation is recommended to restrict the development of disease [26]. Soil solarization has also been demonstrated to control FCRR. In studies testing several solarization methods, soil solarization generally reduced populations of Forl down to a depth of 5 cm [22].

Chemical Control

Before the 2010s, the most effective method for FCRR control was soil disinfection using methyl bromide (MBr) [27][28]. However, MBr has been phased out globally since 2015. The ban on MBr prompted the study of alternative chemicals for the control of soilborne pests including Forl. So far, the tested alternatives include 1,3-dichloropropene, chloropicrin, dozamet, fosthiazate, and metam sodium, with similar effects on Forl compared with MBr [22][29][30]. For example, McGovern et al. [29] tested the application of metam sodium in field tomatoes and found that rotovation of metam sodium at 935 L/ha into preformed beds consistently reduced FCRR incidence equal to those achieved by methyl bromide-chloropicrin. Also, 1,3-dichloropropene+chloropicrin (60.5% and 33.3%, w/w) was tested on Italian field tomatoes [30] and was able to achieve a good tomato yield using drip application in sandy loam soils with slight Forl infections and severe infections of Fol and galling nematodes, which was similar to those of the plots treated with MBr.
However, there are still several factors that may reduce the efficiency of Forl chemical control. For example, Forl chlamydospores were found to survive in the soil at a depth beyond 50 cm, which is unreachable by soil fumigation [26]. Also, Forl can efficiently colonize sterilized soil [31]. Therefore, soil fumigation may instead create favorable soil conditions for Forl colonization by reducing microbial competition.

Resistance Breeding

Resistant tomato varieties can also be used to control FCRR. The resistance of tomatoes to FCRR is found to be controlled by a single dominant locus (Frl) on chromosome 9 [32][33]. This gene has been successfully crossed into commercial tomato lines, with many Forl-resistant cultivars currently available. However, no additional resistant genes have been identified.

2.2. Biocontrol

Forl is believed to have poor competitive fitness against other microorganisms [26], thus biocontrol via organic amendments or biocontrol agents may be effective for the management of Forl.
Several antagonistic microorganisms have been tested for their properties to control FCRR. Sivan et al. [34] applied Trichoderma harzianum as seed coating or wheat-bran/peat in tomatoes grown in FCRR-infested field and recorded a 26.2% increase in yield of treated plots compared with the control, with the control of Forl at the highest effect on root tips. Datnoff et al. [35] also applied T. harzianum and Glomus intraradices into tomato fields with FCRR history and recorded a significant reduction in disease severity and disease incidence of FCRR by applying the fungi both combined and separately. Several hypervirulent binucleate Rhizoctonia strains were also found to reduce the vascular discoloration caused by FCRR on tomatoes up to 100% in greenhouse conditions and up to 70% in the field [21]. Moreover, a non-pathogenic endophytic F. solani strain was reported to reduce disease incidence of Forl when applied alone in glasshouse tomato by 47%, the effects of which improved when combined with certain fungicides [36]. Pythium oligandurm was also found to trigger the host defence of greenhouse tomatoes when challenged by Forl in the form of deposition of newly formed barriers beyond the infection sites [37].
Several bacteria species may also control FCRR. Pseudomonas fluorescens was found to synthesize the antibiotic 2,4-diacetylphloroglucinol, which suppressed the growth of Forl in vitro [38]. A further study found that P. fluorescens WCS365 used chemotaxis towards Forl hyphae, enabling it to efficiently colonize Forl and achieve control effects [39]. In a later screening by Kamilova et al. [40], strong competitive biocontrol strains P. fluorescens PCL1751 and P. putida PCL1760 were found to successfully suppress FCRR under the soil and hydroponic conditions. In addition, Baysal et al. [41] assessed in a greenhouse trial the effect of two Bacillus subtilis bacteria strains QST713 and EU07, and concluded that EU07 had a better disease inhibitory effect (disease incidence reduced by 75%) compared with QST713 (disease incidence reduced by 52%), and the inhibition may be achieved by YrvN protein coded in the genome of EU07 as a subunit of protease enzyme. Lytic enzymes, cellulases, proteases, 1,4-b-glucanase, and hydrolases from the secreted proteins from B. subtilis EU07 and FZB24 and concluded these essential proteins of Bacillus bacteria play an important role in the control of Forl [42].
Organic amendments promoting microbial activity may also be used in FCRR management, but they do not have consistent effects in field conditions. Straw was incorporated into the soil to manage FCRR by Jarvis [26], but the Forl soil population increased around and inside the straw, which only started to fall when the straw decomposed. However, Kavroulakis et al. [43] concluded that a compost mix made from grape marc wastes and extracted olive press cake can enhance tomato defensive capacity under Forl stress by making the pathogen unable to penetrate and colonize the host root, resulting in a 40% reduction in the disease incidence compared to the control. However, the plants in this trial were grown completely in the compost, making large-size commercial applications likely unrealistic.

3. Fusarium wilt Disease of Tomato

3.1. Conventional Control Methods

Cultural Control

Crop rotation can be used to manage Fusarium wilt, and it is recommended not to plant the same or related type of crop for at least four years if one crop is severely infected by Fusarium wilt [44]. The recommended crops for rotation are grasses and cereals [45].
Hygiene should also be practiced for Fol control. Disease-affected plants should be removed immediately. Used farming tools should be disinfected and cleaned before reuse. The use of sanitized footwear and clothes on the farm may help prevent the transportation of infected soils between paddocks [44]. Fallowing is another strategy for Fol control. Briefly, the land is left uncultivated for a period, and for Fol, it is recommended to practice fallowing during the summer months to let the high temperature and excessive drying reduce soil levels of Fol [46].

Physical Control

Soil solarization can also be used to control Fol residing in soil, preferably performed in the summertimes. However, since the development of Fusarium wilt favors warm temperatures (27–28 °C) [47], this strategy may not work in zones with cool climates.

Chemical Control

Soil fumigation with MBr was an effective method for Fol management however, with the phase-out of MBr the value of chemical control on Fol has drastically reduced. Though alternative chemicals such as chloropicrin, dimethyl disulfide, metam sodium, and 1,3-dichloropropene are available, they all lack the broad-spectrum volatile characteristics of MBr, which made it highly effective [48]. Systemic fungicides such as benomyl, thiabendazole, and thiophanate have also been used to control tomato Fusarium wilt [46], but it was believed that there are no fungicides especially effective for the control of this disease [44].

Resistance Breeding

The application of tomato cultivars resistant to Fusarium wilt is currently the most feasible management method.
The resistance to Fol was first identified by Bohn and Tucker in 1939 [49], who identified one single, dominant resistance locus later named I gene from one wild tomato accession of S. pimpinellifolium, Missouri accession 160 [50]. This gene was crossed into the first commercial Fol-resistant tomato cultivar and was located at tomato chromosome 11 [51].
Later, the second race of Fol, named Fol2 was reported to spread widely in Florida in the 1960s [52], which led to another screening for the corresponding resistant gene. The resistant gene was again found in wild tomato relatives- a natural hybrid PI126915, which was name I-2 and mapped to chromosome 11 [53].
In 1979, the third race of Fol–Fol3 was reported in Australia in fresh tomato production [54]. McGrath et al. [55] were the first to identify resistance to Fol3 in the S. pennellii accession PI414773 in 1987, and Scott and Jones [56] later identified a dominant Fol3 resistance locus in the S. pennellii accession LA716. This newly discovered gene was later named I-3 and used as the primary source of Fol3 resistance in commercial varieties. Gene I-3 was mapped to chromosome 7 [57], and McGrath et al. located another gene I-7 gene in chromosome 8 [58].
Three additional genes with partial resistance to Fol2 were also found by Sela-Buurlage et al. [51]. These researchers studied 53 introgression lines with chromosomes from LA716 and identified alleles I-4 and locus I-5 on chromosome 2, with locus I-6 on chromosome 10 of S. pennellii. However, none of these genes have their effects validated nor used for commercial purposes so far.

3.2. Biological Control

Potential biocontrol agents against Fol on tomatoes have been actively tested in a large number of studies. The most commonly used biocontrol agents belonged to various microbial genera including fungi (Aspergillus spp., Chaetomium spp., Glomus spp., non-pathogenic Fusarium spp., Trichoderma spp. and Penicillium spp.) and bacteria (Bacillus spp., Pseudomonas spp., Streptomyces spp., and Serratia spp.) [59].
Among the different genera of biocontrol microorganisms, non-pathogenic Fusarium strains are of high interest. In 1993, Alabouvette et al. [60] concluded that among the many groups of microorganisms tested for biocontrol activity, only non-pathogenic Fusarium species and fluorescent Pseudomonads showed consistent responses. In a later review by Ajilogba et al., these strains were found to be involved in most research conducted on plant biological enhancement using fungal endophytes [44]. One representative strain, F. oxysporum Fo47, was successfully tested against Fol [61][62][63], with the major mode of function being the induction of systemic resistance and priming of the plant defence reaction.
Another review by Raza et al. [59] analyzed biocontrol trials conducted between 2000 and 2014 and concluded that non-pathogenic Fusarium species and Pseudomonas species were supported by most research to be more effective in controlling Fusarium wilt in natural soil, while Penicillium, Streptomyces, and Aspergillus strains were more effective in growth media. However, the authors also found that 79% of the tests on tomatoes were conducted in greenhouse conditions, with 12% conducted in the field condition. Thus, for processing tomatoes grown predominately in field conditions, further field tests on the efficiency of different biocontrol agents are necessary.
Organic amendments are another group of biocontrol agents. For example, Borrego-Benjumea et al. [64] tested poultry manure, olive residue compost, and pelletised poultry manure for tomatoes grown in natural sandy soil and concluded that the combination of pelletized poultry manure with heating or solarization achieved the greatest reduction in Fusarium wilt severity. In a later study by Zhao et al. [65] testing chicken manure, rice straw, and vermicompost in a long-term tomato monocultural soil, vermicompost addition significantly increased soil pH, ammonium nitrogen, soil organic matter, and dissolved organic carbon, which promoted beneficial bacteria suppressing Fol. Organic amendments are often applied in combination with biocontrol microorganisms for better effects in different studies [59][66][67]. It was also suggested that the combined application of biocontrol organisms and amendments can increase the biocontrol efficiency of various genera of fungi and bacteria, with the exceptions of Pseudomonas and Penicillium [59].

4. Phytophthora Root Rot of Tomato

4.1. Conventional Control Methods

Cultural Control

Crop rotation is often used to manage P. capsici along with many other soilborne pathogens, but its effectiveness is limited by the long survival of oomycetes in the soil and the wide host range of P. capsici. The host range of P. capsici was reported to cover at least 45 species of cultivated plants and weeds from 14 families of flowering plants [68], thus the selection of rotation crops for P. capsici is very narrow. Also, Lamour and Hausbeck [69] found P. capsici can survive as oospores for a 30-month nonhost period during crop rotation. Therefore, long rotations are required even if non-host crops are available, which may make crop rotations economically unfeasible.
It is very difficult to control P. capsici once the pathogen becomes established in the field. Thus, most control strategies are aimed at limiting free water to minimize inoculum spread and crop loss, which includes planting at well-drained sites or on a raised bed with controlled irrigation [70].

Physical Control

Soil solarization was found to be effective against Phytophthora root rot on tomatoes. From a trial in Florida a soil solarization treatment that heated the soil to a maximum of 47 °C at 10-cm depth had similar effects to MBr treatment at the same site in reducing the P. capsici population [4].

Chemical Control

The application of chemicals has been another approach to managing P. capsici. However, the phasing out of MBr has reduced the cost-efficiency of chemical control [71]. Other chemicals frequently applied include cyazofamid, dimethomorph, fluopicolide, fosetyl-Al, mandipropamid and mefenoxam (metalaxyl) [72][73][74][75]. Despite the various choices of chemicals, extensive use of fungicide has led to the emergence of resistant P. capsici strains, which makes it very hard to protect crops from P. capsici. For example, Lamour and Hausbeck [69] collected 141 isolates of P. capsici in Michigan and found around 60% to be intermediately sensitive or insensitive to mefenoxam. Even more recent groups of chemicals such as fluopicolide and cyazofamid have resulted in the fast emergence of pathogen resistance. Jackson et al. [73] concluded that among the 40 P. capsici isolates tested, all were either intermediately sensitive or resistant to cyazofamid at 100 μg/mL application rate. More recently, Siegenthaler and Hansen [75] found that out of 184 P. capsici isolates collected in Tennessee, 84 were resistant to fluopicolide.

Resistance Breeding

Until the 2010s, only several tomato strains moderately resistant to P. capsici were commercially available. Quesada-Ocampo and Hausbeck [71] screened 42 tomato cultivars and wild relatives for their resistance against P. capsici, and found Solanum habrochaites accession LA407, was resistant to all P. capsici isolates tested, with four additional cultivars having moderate resistance. However, the authors analyzed the genes of these cultivars and found a lack of correlation between genetic clusters and susceptibility to P. capsici, indicating that resistance was distributed in several tomato lineages. In a subsequent study, Quesada-Ocampo et al. [76] generated 62 backcross lines using LA407, and tested their resistance against different P. capsici strains and used annotated markers to locate genes related to the resistance. Though the researchers found that the resistance had a good inheritability among the population, they failed to find any annotated markers strongly associated with P. capsici resistance, with genes with annotation linked to disease resistance responses mapped to all chromosomes segregated among the population with the exceptions for 8, 9, 11, and 12. Therefore, the resistance of tomatos to P. capsici has not been related to specific gene/loci so far, and further studies are required.

4.2. Biocontrol

With insufficient levels of conventional control measures against Phytophthora root rot of tomatoes, antagonistic microbes and organic amendments have been tested to find feasible biocontrol approaches. Bacteria species are frequently studied for their biocontrol properties against Phytophthora root rot. Moataza [77] tested five Pseudomonas fluorescences strains against Rhizoctonia solani and P. capsici in tomato pot trials, and concluded that two strains, NRC1 and NRC3 had strong lytic activities leading to the destruction of the pathogen, Sharma et al. [78] tested 20 Bacillus strains against P. capsici on tomatoes grown in net house, and found one species, B. subtilis showed the best efficiency in terms of decreased disease severity. Furthermore, Syed-Ab-Rahman et al. [79] tested three bacteria- B. amyloliquefaciens, B. velezensis and Acinetobacter sp. on tomato, and concluded all three bacteria promoted tomato growth while significantly reducing the P. capsici load in their roots. An oomycete, Pythium oligandrum was also tested, and was believed to synthesize two Necrosis- and ethylene-inducing peptide 1 (Nep1)-like proteins PyolNLP5 and PyolNLP7, which induced the expression of antimicrobial tomato defensin genes against P. capsici [80].
The application of organic amendments is another approach to biocontrol. For P. capsici management, Nicol and Burlakoti [81] aerated compost and water and produced four aerobic compost teas. When tested in the glasshouse, the researchers concluded that if these products were drenched in potting mix before and after P. capsici inoculation, the disease progression was reduced by over 70%, with improved plant growth. Other efforts of using composts against P. capsici have generally been attempted on pepper [82][83][84], so the effects of these composts on tomatoes are unknown.

5. Pythium Root Rot and Damping-Off

5.1. Conventional Control Methods

Cultural Control

The application of pathogen-free seedlings and the control of irrigation are found to be effective forms for tomato Pythium disease management [85][86].
For Pythium species, crop rotation is generally not considered to be effective in the control of tomato infections because most Pythium species have a wide host range [87]. However, one study on wheat found that 3–4-year rotation cycles using wheat, canola and legume resulted in a significantly smaller disease incidence compared with less diverse rotations such as two-year wheat-canola [88]. The reason behind this finding may be that different crops have significantly different susceptibilities to Pythium infection, which may restrict the soilborne pathogen inoculum build-up after each crop, and eventually reducing the disease incidence in the next crop.

Physical Control

Soil solarization is an effective method for Pythium control with a long-period (six weeks to 60 days) of solarization during the summertime having been shown to significantly reduce the soilborne population of P. aphanidermatum in tropic zones [89][90]. In a field trial on tomatoes infected by Pythium spp., solarized soil showed a significantly lower mean damping-off incidence compared with un-solarized soil (2.15% compared with 68%) [91].

Chemical Control

Several chemicals have been used to manage Pythium species, including hymexazol, mefenoxam (metalaxyl), phosphonate, thiram and 8-Hydroxyquinoline [92][93][94][95][96]. The chemicals can be applied as seed treatment [97][98] or soil drenching [99] for seedlings of tomato.
In addition to the common economic and environmental concerns of chemical control, several major Pythium species collected from the production of various crops have developed resistance against several chemicals, especially mefenoxam. For example, Porter et al. [100] reported over 50% of the Pythium soil population consisted of mefenoxam-resistant isolates in ten of 64 potato fields from Oregon and Washington. Del Castillo Munera and Hausbeck [101] tested a total of 202 Pythium spp. isolates collected from Michigan, and found 39% of these, mostly P. ultimum and P. cylindrosporum isolates were intermediate to highly resistant to mefenoxam. For another major species P. irregulare, Aegerter et al. [102] tested four P. irregulare isolates from a greenhouse extensively applying mefenoxam and found no inhibition of growth of any isolate occurred at mefenoxam concentrations of 10 μg/mL or less. For other Pythium species such as P. aphanidermatum, resistance to mefenoxam was also reported [103][104]. In a rare case, Garzón et al. [95] even reported that the disease severity of a mefenoxam-resistant P. aphanidermatum on geranium can be stimulated by sublethal doses of mefenoxam.

Resistance Breeding

Though the deployment of resistant cultivars is a common and effective strategy for crop disease management, currently there is no Pythium-resistant tomato. The only potentially useful genetic resource against Pythium is the genes encoding pathogenesis-related (PR) proteins, with PR-1 protein showing antifungal activity against oomycetes [105]. Tomato has two related genes, PR1b1 and PR1a2, each encoding a basic and an acidic PR-1 protein [106], but the resistance of PR proteins is not pathogen-specific, with only limited effects against Pythium species.

5.2. Biocontrol

For biocontrol of Pythium disease on tomatoes, several bacteria strains have been studied. Postma et al. [107] tested four bacteria strains against P. aphanidermatum and found three strains, Pseudomonas chlororaphis, Peanibacillus polymyxa and Streptomyces pseudovenezuelae, significantly controlled P. aphanidermatum in under greenhouse conditions. The effect of Streptomyces bacteria was also supported by the study of Hassanisaadi et al. [87], who found two root-symbiont Streptomyces species significantly decreased disease incidence and improved performance of greenhouse tomato under P. aphanidermatum in stress out of the 116 tested species. For Bacillus bacteria, Martinez et al. [108] tested one B. subtilis strain MBI600 in a peat-based potting mix and concluded the addition of this strain significantly reduce tomato and sweet pepper damping-off and root rot while promoting root growth. Samaras et al. [96] also tested MBI600 on greenhouse tomatoes and concluded that the application of this strain achieved satisfactory control efficacy compared to chemical treatment with 8-Hydroxyquinoline.
For the application of fungal antagonists, the current focus seems to be on the Trichoderma species. Caron et al. [109] tested one local T. harzianum strain MAUL-20 on greenhouse tomatoes and found that it significantly reduced P. ultimum disease incidence, with a better effect compared with Rootshield™, a biofungicide based on T. harzianum KRL-AG2. Cuevas et al. [94] also tested T. parceramosum, T. pseudokoningii and T. harzianum respectively, and found the application of the Trichoderma pellets into the field before seeding can minimize the activity of Pythium spp., with a higher seed germination rate compared with the treatment using chemical fungicide mancozeb. Elshahawy and El-Mohamedy [110] tested the effects of five Trichoderma strains on P. aphanidermatum damping-off of tomatoes and concluded that under field conditions the combined application of the five isolates reduced by half the root rot severity while almost doubling the survival of tomato. This was thought to be through activating tomato defence enzymes and increasing leaf chlorophyll content, with an increased yield.
Interestingly, even arbuscular mycorrhizal fungi suppressing plant growth may also be used to control Pythium species. Larsen et al. [111] pre-treated greenhouse tomato seedlings with Glomus intraradices, G. mosseae, G. claroideum, and then challenged the seedlings with P. aphanidermatum, with the hypothesis that the application of growth-suppressive fungi may trigger plant defence response in terms of PR-1 expression to prepare the plants for Pythium infection. However, the application of arbuscular mycorrhizal fungi did not affect PR-1 gene expression, with only G. intraradices reducing the pathogen root infection level of P. aphanidermatum, thus the hypothesis was not confirmed.
Several organic amendments have also been tested against Pythium, such as canola residues and composts (animal bone charcoal, compost tea, solid green wastes, or green waste +manure) [107][112][113][114]. Also, Jayaraj et al. [115] found that formulating amendments such as lignite with biocontrol agents such as B. subtilis can greatly increase their shelf life, with good effects on Pythium suppression and plant growth promotion.

6. Tomato Verticillium Wilt

6.1. Conventional Control Methods

Cultural Control

Crop rotation with non-host crops is an effective strategy for Verticillium wilt management. The known non-host crops include small grain crops such as wheat and corn [116], and long rotations lasting over four years are recommended [117].
Hygiene is also important for Verticillium wilt control. pathogen-free seed and disease-free transplants should be used [117], with infected crop debris removed and destroyed away from the field. Equipment and foot ware should be washed to prevent the movement of infested soil between fields. Verticillium also prefers humid soil, thus maintaining well-drained soil, and eliminating excessive soil moisture may also limit the development of the pathogen [118].

Physical Control

Verticillium prefers cool temperatures for survival and developing symptoms, thus heating the soil through solarization could be an effective control method. Currently, solarization against Verticillium wilt is practiced generally in Mediterranean, desert, and tropical climates, because these climates allow the accumulation of adequate heat to neutralize the pathogen [119]. However, the data on solarization alone showed poorer performance compared with the MBr application, which can be improved when combined with the fumigation using MBr alternatives [120].

Chemical Control

Soil fumigation is also used to control Verticillium wilt. MBr alternatives such as chloropicrin (CP) (trichloronitromethane) are traditionally used as in formulations together with MBr to achieve a broader spectrum of activity [120]. In a trial by Gullino et al. [121], CP applied by shank injection at rates ≥30 g/m2 induced a satisfactory and consistent control of tomato Verticillium wilt, with no phytotoxicity, but the efficiency was slightly lower than standard MBr application and may have been influenced by soil type and organic matter content. Metam-sodium and 1,3-dichloropropene are other alternative soil fumigants, which have been applied in combination or with metam-sodium alone in the United States to reduce soil populations of V. dahliae [122]. Several other chemicals such as fungicides including azoxystrobin, benomyl, captan, thiram, and trifloxystrobin, and a plant defense activator, acibenzolar-S-methyl were also recommended [15][120][123].

Resistance Breeding

By far, the most feasible and economic control for Verticillium wilt is the application of resistant cultivars. The resistance gene in tomato to V. dahliae was first identified as a single dominant factor in the reciprocal crosses between the wilt-resistant variety W6 (Peru Wild × Century) and Moscow, a susceptible variety, and named as Ve in 1951 [124]. Ve was found to be a locus, which contains two genes, Ve1 and Ve2, with only Ve1 found to mediate resistance in tomato [125]. The strains of V. dahliae resistant to Ve1 and V. albo-atrum were assigned to race 2 [125]. The Ve1 gene has been incorporated into many commercial cultivars. However, all the current verticillium-resistant gene resources are against V. dahliae race 1, thus all race 2 strains of V. dahliae and V. albo-atrum can still infect the resistant cultivars.

6.2. Biocontrol

Biological control may be a promising method to control Verticillium wilt, given that most current management methods have limited efficiency. Various microorganisms have been tested against V. dahliae, such as bacteria Bacillus subtilis and B. velezensis [126], and fungi including Burkholderia gladioli [127], Gliocladium spp., Penicillium sp. [128][129], Trichoderma spp. [130], Talaromyces flavus [131], and even V. klebahnii and V. isaacii with low pathogenicity [132]. Though most of the microorganisms are found to be effective in trials, most of the trials were carried out in greenhouses or with sterilized soil, with only a few verified in field conditions. Larena et al. [129] conducted a field assay using P. oxalicum and concluded that seedlings needed to be treated with 106–107 CFU/g of the biocontrol agent around a week before transplanting to achieve a sufficient level of control, but only in a certain soil type (loam soil, pH = 7.0), and the formulation may not be feasible for tomato mass production due to the high CFU density requirement.
The application of organic amendments is known as another approach for crop disease biocontrol. It has long been known that bloodmeal and fishmeal can eliminate the incidence of Verticillium wilt in tomato [120]. Compared to animal-based amendments (manure), plant-based amendments not only support beneficial microbial activities but also have greater efficiency on pathogens due to deleterious chemicals produced by the plants, in addition to supporting beneficial microbial activities [133]. Giotis et al. [134] concluded that fresh Brassica tissue, household waste compost, and composted cow manure significantly reduced soilborne disease severity of tomato Verticillium wilt, with enhanced plant growth. Similar results were also achieved by Kadoglidou et al. [135], who applied soil incorporated spearmint and oregano-dried plant material, which caused disease suppression resulting in increased fruit yields of tomatoes inoculated with V. dahliae. Moreover, Ait Rahou et al. [136] used compost based on green waste (quackgrass) to greenhouse tomatoes inoculated with Verticillium and concluded that growth regulators directly produced by the microorganisms in the compost improved plant growth significantly. However, when Lazarovits et al. [137] applied compost made from sewage sludge to suppress V. dahliae in tomato plants, phytotoxicity was detected over one month, which may have been due to the excessive accumulation of plant-toxic heavy metals in soils. To conclude, though organic amendments may be useful for Verticillium wilt management, they may also carry toxic compounds which may lead to undesired effects.

This entry is adapted from the peer-reviewed paper 10.3390/microorganisms11020263

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