Next Article in Journal
Comparison of Shuttleworth–Wallace and Dual Crop Coefficient Method for Estimating Evapotranspiration of a Tea Field in Southeast China
Previous Article in Journal
The Effect of Tillage Systems and Weed Control Methods on the Yield and Quality of Spelt Grain (Triticum aestivum ssp. spelta L.)
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agriculture
Volume 12
Issue 9
10.3390/agriculture12091391
agriculture-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Biocontrol of Three Severe Diseases in Soybean

by
Shu-Fan Yu
1,†,
Chu-Lun Wang
1,†,
Ya-Feng Hu
1,
Yan-Chen Wen
2 and
Zhan-Bin Sun
1,*
1
School of Light Industry, Beijing Technology and Business University, Beijing 100048, China
2
Key Laboratory of Plant Nutrition and Fertilizer, Ministry of Agriculture, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agriculture 2022, 12(9), 1391; https://doi.org/10.3390/agriculture12091391
Submission received: 5 August 2022 / Revised: 30 August 2022 / Accepted: 31 August 2022 / Published: 4 September 2022
(This article belongs to the Section Crop Protection, Diseases, Pests and Weeds)
Browse Figures
Versions Notes

Abstract

:
Three damaging soybean diseases, Sclerotinia stem rot caused by a fungus Sclerotinia sclerotiorum (Lid.) de Bary, Phytophthora root rot caused by a fungus Phytophthora sojae, and soybean cyst nematode (Heterodera glycines Ichinohe), are destructive to soybean growth and yield and cause huge economic losses. Biocontrol is an effective way to control soybean diseases with the advantage of being environmentally friendly and sustainable. To date, few reviews have reported the control of these three soybean diseases through biocontrol measures. In this review, the biological characteristics of the three pathogens and the incidence features of the three soybean diseases were first introduced. Then, biocontrol agents containing fungi and bacteria capable of controlling the three diseases, as well as their control abilities, were emphasized, followed by their mechanisms of biocontrol action. Bacillus and Streptomyces were found to possess the ability to control all three soybean diseases under greenhouse or field conditions. Finally, suggestions about screening new biocontrol species and deeply studied biocontrol molecular mechanisms are provided for further research on the biocontrol of soybean diseases.

1. Introduction

The soybean (Glycine max (L.) Merr.) is one of the most important crops in the world and has extremely high social and economic value. However, several pathogens can infect the soybean during its planting process. These diseases caused by the above pathogens can cause a substantial reduction in soybean yield and result in serious economic losses [1]. Therefore, selecting a suitable control method is an effective way to overcome soybean diseases. Currently, the commonly used control methods include chemical control, screening disease-resistant soybean varieties, and biocontrol [2,3,4].
Chemical control is the most used, effective, and extensive method for overcoming soybean diseases. However, the long-term application of chemical pesticides can cause grievous environmental pollution and is harmful to human health [5]. Moreover, pesticide resistance could be generated for pathogens after the long-term use of chemical pesticides [6]. Screening disease-resistant soybean varieties is another effective way to control soybean diseases; however, the current disease-resistant soybean varieties cannot satisfy the requirements of the market [4]. Biocontrol is also a promising way to control soybean diseases. Several mechanisms, including the production of secondary metabolites, such as toxins or antibiotics, secretion of cell wall-degrading enzymes, and induced soybean resistance, are involved in the biocontrol of soybean diseases [7]. Compared with chemical control, the advantages of biocontrol are that it is green, safe, and sustainable [8]. Studies have shown that the control efficacies of some biocontrol agents are similar to those of chemical pesticides and sometimes even higher than those of chemical controls [9]. Moreover, many biocontrol agents possess dual effects, and biocontrol and plant growth promotion. Therefore, as an environmentally friendly control method, biocontrol has drawn much attention [8]. Currently, biocontrol is one of the most important methods to control soybean diseases and is helpful for the sustainable development of agriculture; therefore, biocontrol will have extensive application prospects in the future.
This review focuses on three common and serious soybean diseases, soybean Sclerotinia stem rot, soybean Phytophthora root rot, and soybean cyst nematode, caused by Sclerotinia sclerotiorum, Phytophthora sojae, and Heterodera glycines, respectively. All three soybean diseases are destructive to soybean yield and cause huge economic losses [4,5,10]. This review summarizes and analyses the latest advances in the control of the above three soybean diseases by biocontrol methods. In this review, the characteristics of the three soybean diseases are introduced, and the biocontrol abilities of the above three soybean diseases are analyzed in detail. Finally, suggestions for future directions of soybean disease biocontrol are provided. This review provides useful information for the preferential control of soybean diseases using biocontrol.

2. General Characteristics of Soybean Diseases

2.1. Soybean Sclerotinia Stem Rot

Sclerotinia stem rot (SSR) in the soybean is a destructive fungal disease caused by Sclerotinia sclerotiorum (Lid.) de Bary. It belongs to Ascomycotina (Subphylum), Pezizomycetes (Class), Helotiales (Order), Sclerotiniaceae (Family), and Sclerotinia (Genus) [11]. The mycelia of S. sclerotiorum are tightly intertwined to form sclerotia, which are considered a hypopus structure of S. sclerotiorum with strong stress resistance [12]. Sclerotia can survive in the soil for several years, and when the temperature and humidity are suitable, sclerotia in the soil or soybean debris can germinate into the apothecium. Then, many ascospores are released from the apothecium, spread through wind or rain, and finally infect soybean plants [4]. Sometimes, sclerotia can directly germinate into mycelium to infect soybean plants [13]. After infection, sclerotia can be formed on the diseased tissues of infected soybean plants, and then the formed sclerotia drop out into the soil or are present in the soybean debris, becoming the primary source of the next infection cycle [14] (Figure 1).
Soybean SSR can occur during the whole growth and development period of soybean plants. The main infected tissues of SSR in soybeans are leaves, stems, and fruits. Humidity and temperature are two crucial factors that influence the incidence of SSR in soybeans [12]. Once the tissues of soybean plants are infected by S. sclerotiorum, water-soaked spots first appear and then develop into light brown to dark lesions. The diseased tissues finally become soft, with the surface exhibiting fluffy white mycelium and large numbers of sclerotia when the soybean plant is seriously infected, which is also the typical symptom of SSR in soybeans [15].

2.2. Phytophthora Root Rot

Phytophthora root rot (PRR) in the soybean is another damaging fungal disease that is caused by Phytophthora sojae (Kaufmann and Gerdemann) and belongs to Oomycota (Phylum), Peronosporales (Order), Peronosporaceae (Family), and Phytophthora (Genus) [16]. Oospores are sexual spores of P. sojae that can survive in soil or plant residues for a long time [17]. Oospores can germinate into mycelia when the temperature and soil moisture are favorable [18]. Then, the mycelia can generate zoosporangia through asexual propagation and then release zoospores. Finally, the zoospores can directly infect soybean tissues after germination [5]. Oospores can be formed in diseased tissues of soybean under unfavorable conditions, which can be regarded as the initiation of the next infection cycle [16] (Figure 2).
PRR can occur during all the growth and development stages of soybean plants. PRR has a great influence on the seeds, seedlings, and adult plants of soybean. Soybean seeds decay with the incidence of PRR [5]. Water-soaked lesions appear on the stems of soybean seedling plants after infection with P. sojae [19]. As the disease progresses, the leaves become yellow, the soybean plants wilt, and finally, whole soybean plants die after serious infections [5].

2.3. Soybean Cyst Nematode

Soybean cyst nematode (SCN) in the soybean is a typical soil-borne nematode that is destructive to soybean yield. SCN is Heterodera glycines Ichinohe and belongs to Nematoda (Class), Tylenchina (Suborder), Heteroderidae (Family), and Heterodera (Genus) [20]. The cysts of H. glycines have powerful environmental resistance, and eggs within the cyst can survive on soils for several years [21]. When the environmental conditions are favorable, the eggs of H. glycines develop into second-stage juveniles, which is crucial for the penetration of soybean roots [10]. After the fourth stage, the body of H. glycines expands, and the white cyst nematode body becomes exposed to the surface of soybean roots. Reproduction occurs between males and females, and cysts are formed and prepared for the next infection cycle when the environmental conditions are suitable [7,22] (Figure 3).
SCN can be found during all the growth and development stages of soybean plants. The main soybean tissue for the infection of H. glycines is the root. SCN can influence the growth and development of soybean plants. The soybean plants become stunted and chlorotic after infection with H. glycines. White spheroids can be found on the infected root surface, which is an important symptom for identifying SCN. Severe infections by H. glycines can result in the death of soybean plants and cause huge losses in soybean yield [23,24].
As an environmentally friendly and sustainable control method, biocontrol has drawn widespread attention. To date, a large number of biocontrol agents have been isolated and have exhibited excellent control efficacy against soybean diseases. In the next section, we summarize, as comprehensively as possible, the biocontrol agents, including bacteria and fungi, to control the three soybean diseases.

3. Biocontrol of Soybean Sclerotinia Stem Rot

3.1. Biocontrol Fungi against Soybean Sclerotinia Stem Rot

Several fungal and bacterial agents have been reported to exhibit promising efficacy in controlling SSR in soybeans (Table 1). Among these fungal agents, Trichoderma (Ascomycota; Sordariomycetes; Hypocreales; Hypocreaceae; Trichoderma) [25] strains are the most widely studied, and varieties of Trichoderma species have been reported to be involved in the biocontrol of SSR in soybeans in America. Spraying with T. harzianum T-22 strain could effectively suppress the growth of S. sclerotiorum, inhibited the carpogenic and myceliogenic germination of sclerotia, and reduced the disease severity index of SSR in soybeans under field conditions. Moreover, T-22 could improve the biomass of shoots and roots [26,27]. Another T. harzianum strain, BAFC 742, mixed with S. sclerotiorum in soil, showed biocontrol efficacy against SSR in soybeans under greenhouse and field conditions, increasing the survival of soybean plants after application [28]. In addition to T. harzianum, other Trichoderma species also exhibited promising biocontrol capacity for SSR in soybeans. Spraying with T. asperelloides strains T25 and T42 originated from soil reduced the disease incidence of SSR in soybeans compared with the control in the field [29]. T. asperelloides, T. atroviride, T. koningiopsis, and T. virens strains improved the germination of soybean seeds infected by S. sclerotiorum in the greenhouse [30].
Clonostachys rosea (Ascomycota, Sordariomycetes, Hypocreales, Bionectriaceae, and Clonostachys) [45] and Coniothyrium minitans (Ascomycota; Dothideomycetes; Pleosporales; Didymosphaeriaceae; Paraphaeosphaeria) [46] are two other important biocontrol fungi against SSR in hypopus structure soybean. C. rosea 67-1 was sprayed on the soybean leaves and exhibited biocontrol efficacy against SSR in soybeans, and several biocontrol-related genes encoding hsp70, transcription factors, and mitogen-activated protein kinase are involved in 67-1 controlling SSR in the soybean [31,47,48]. C. rosea strains BAFC3874 and BAFC1646 were mixed with soil prior to the addition of S. sclerotiorum, which could reduce the soybean death rate after infection with S. sclerotiorum [32,33]. Usage of C. minitans strain CON/M/91-08 reduced the sclerotia number in soil and the disease severity index of SSR in soybeans [26,27]. Pycnidiospores suspension of another C. minitans strain, N09, was sprayed into sclerotia-infected soil and had a significant impact on the viability of S. sclerotiorum sclerotia [49].
In addition to the above-mentioned biocontrol agents, other fungi still exhibit efficacy in controlling SSR in soybeans. Metabolites, such as cyclosporine A isolated from Fusarium oxysporum S6, and griseofulvins isolated from Stachybotrys levispora, could influence the growth of S. sclerotiorum [35,50]. Studies have shown that inoculating S6 into steam-pasteurized soil planted with pregerminated soybean seeds could dramatically improve the surviving plants following SSR infection in soybeans [35]. Other fungi, including Sporidesmium sclerotivorum, Phialomyces macrosporus, Volutella minima, and Myrothecium sp. also reduced the incidence of SSR in soybeans [36,51,52].

3.2. Biocontrol Bacteria against Soybean Sclerotinia Stem Rot

In addition to biocontrol fungi, numerous bacteria have been reported to be involved in the biocontrol of SSR in soybeans. Among these biocontrol bacteria, Bacillus strains are the most widely reported. Application of B. subtilis QST 713 suspension could reduce the number of apothecia and sclerotia of S. sclerotiorum [27]. Under greenhouse and field conditions, the application of the B. subtilis strains SB01, SB24, ZH-2, and B. cereus BA88R, and the B. amyloliquefaciens strains ARP23 and MEP218 significantly reduced the incidence of SSR in soybeans [34,38,39,41]. Metabolites from biocontrol bacteria play important roles in inhibiting S. sclerotiorum. Volatile organic compounds from B. velezensis VM11 and Xenorhabdus spp. affected the mycelial growth and sclerotial production of S. sclerotiorum through the culture plate method [53,54]. Mycelial growth of S. sclerotiorum was fully inhibited by the culture supernatant of Bacillus strain A5F, and then antifungal compounds were isolated from A5F [55].
Streptomyces is another group that is effective against S. sclerotiorum. Streptomyces strain NEAU-S7GS2 and S. lydicus WYEC 108 inhibited mycelial growth and sclerotial germination and reduced the numbers of apothecia and sclerotia of S. sclerotiorum, respectively [26,27,43]. Meanwhile, both Streptomyces strains could reduce the incidence of SSR in soybeans. The cell suspensions of three other Streptomyces strains, S. somaliensis SSD41 and SSD49 and S. hydrogenans SSD60 were sprayed onto the whole soybean seedling and significantly reduced the disease index in soybeans caused by S. sclerotiorum and promoted the shoot length of soybean. Streptomyces was capable of producing antifungal metabolites, and several compounds were detected from four Streptomyces strains and could significantly protect against S. sclerotiorum [44]. Other biocontrol bacteria, such as Burkholderia strains, Paenibacillus polymyxa, and Lysobacter enzymogenes C3, could effectively inhibit the growth of S. sclerotiorum [42,56,57]. Soybean seeds were bioprimed with C3, Pseudomonas putida BA15R, Enterobacter sp. BA48R, or Enterobacter asburiae BA123R, and exhibited a control effect on SSR in soybeans [38,42].

4. Biocontrol of Soybean Phytophthora Root Rot

4.1. Biocontrol Fungi against Soybean Phytophthora Root Rot

Reports of biocontrol fungi controlling PRR in soybeans are very rare (Table 2). Conidial suspension of several Trichoderma species, including T. virens, T. orientalis, T. ceramicum, T. atroviride, T. koningii, T. brevicompactum, T. spirale, T. viridescens, T. pseudokoningii, T. harzianum, T. asperellum, and T. koningiopsis were immersed with soybean seeds and significantly reduced the disease severity of PRR, of which T. brevicompactum was the most effective strain [58]. Mixing the Aspergillus effusus strain with organic fertilizer significantly decreased the incidence of PRR in soybeans caused by P. sojae and increased the biomass of soybean plants compared with the control. The activities of antioxidant enzymes in soybean leaves, including catalase, peroxidase, and superoxide dismutase, were improved after the application of the A. effusus strain [59]. Similarly, germinated soybean seeds inoculated with the arbuscular mycorrhizal fungus Glomus intraradices BGC BJ09 significantly decreased the content of hydrogen peroxide and increased jasmonic acid in soybean leaves after infection by P. sojae [60].

4.2. Biocontrol Bacteria against Soybean Phytophthora Root Rot

Biocontrol bacteria, especially Bacillus strains, are the most studied in controlling PRR in soybeans. B. altitudinis JSCX-1 and Bacillus sp. A4 inhibited spore germination and mycelial growth of P. sojae. Suspension of JSCX-1 was applied to soybean plants and exhibited excellent biocontrol efficacy of PRR in soybeans [66,67]. Moreover, other Bacillus strains, including B. subtilis BY-2 and RSS-1, B. velezensis SN337 and FZB42, B. amyloliquefaciens JDF3, and B. pumilus B048, could effectively reduce the incidence of PRR in soybeans [62,63,64,65,73]. Studies found that bacilysin is crucial against P. sojae in B. velezensis FZB42 because deficient bacilysin biosynthesis would cause FZB42 to lose its antagonistic ability against P. sojae [73]. In addition to the biocontrol ability, B. subtilis BY-2 and B. velezensis SN337 exhibited growth-promoting ability, in which the root length of soybean increased after application [62,63].
Numerous Streptomyces species have an impact on the growth of P. sojae and the incidence of PRR in soybeans. S. humidus 1-17, S. albosporeus XS1-5, S. hygroscopicus S11 and Streptomyces spp. JAX-14 inhibited the growth of P. sojae [70,74,75,76]. In addition to the inhibition ability, XS1-5 could improve the chlorophyll content, soybean growth, and root vitality of soybean plants. When soybean plants were infected by P. sojae, Streptomyces strains JAX-14, S11, 15, 93, PonSSII, GS2-21, and GS43-5 exhibited promising control ability and could reduce the incidence of PRR in soybeans [71]. Induced plant resistance has been found in some Streptomyces strains. Application of XS1-5 increased the activities of catalase, superoxide dismutase, and peroxidase in soybean leaves. Other bacterial strains, including Enterobacter cloacae DD198, Acinetobacter calcoaceticus DD161, and Pseudomonas sp. BS1 had strong inhibitory activity on P. sojae [68,76].

5. Biocontrol of Soybean Cyst Nematode

5.1. Biocontrol Fungi against Soybean Cyst Nematode

Numerous fungal and bacterial agents have exhibited excellent efficacy in controlling SCN (Table 3). Hirsutella strains were the most reported fungi for effective SCN caused by H. glycines in soybeans. H. rhossiliensis isolate OWVT-1 mixed with eggs of H. glycines were inoculated into the soil and found that OWVT-1 markedly reduced the densities of egg and second-stage juveniles (J2) of H. glycines compared with the control [77]. Another Hirsutella species, H. minesotensis, also exhibited the ability to control SCN. The application of H. minesotensis strains 1-10 and HLJ07-21-3 could significantly reduce the densities of eggs, the numbers of soil cysts, and root females of H. glycines [78,79]. Moreover, both strains promoted the fresh weight of soybean plants. Similarly, GFP-labelled H. minesotensis strain AS3G1 inhibited the population density of H. glycines, and AS3G1 increased the biomass and height of soybean plants [80].
Aspergillus and Penicillium strains also exhibited control ability against H. glycines. The A. niger isolate NBC001 originated from a cyst of Heterodera spp. And showed a strong inhibition rate of egg hatching and high lethality to J2 of H. glycines. Soybean seeds were dressed with the culture filtrate of NBC001 and the numbers of cysts of H. glycines were significantly decreased in a field experiment [103]. Studies found that the expression levels of plant defense-related genes, including GmPR1a, which is SA-responsive, and GmEREBP, which is ET-responsive, were markedly improved after the application of NBC001 in soybean plants [104]. Suspension of the other three Aspergillus strains, D1, A. fumigatus D7, and A. parasiticus A1, could effectively inhibit egg hatching and increase the mortality rates in the J2 of H. glycines [105]. Scopoletin isolated from P. janthinellum Snef1650 was coated with soybean seeds and reduced the juveniles of H. glycines in the roots and cysts in the soil in the field assay. Meanwhile, scopoletin promoted the growth and yield of soybean plants [89]. Similarly, two P. oxalicum strains, NBC008 and NBC012, reduced the cyst number and improved the height and root length of soybean plants compared with the control [85].
Application of Verticillium lecanii AaF23 significantly reduced the number of eggs in pale yellow females and yellow–brown cysts of H. glycines compared with the control [106]. Suspensions of other Verticillium species, V. chlamydosporeium V-25, together with Paecilomyces lilacinus P-E, could reduce the densities of cysts, eggs, and females of soybean roots and benefit the growth and fresh weight of soybean plants [88,107]. Fermentation filtrates of F. graminearum F-9 and Beauveria isolates B703147 and B23 had an impact on H. glycines. F-9 could significantly inhibit the egg hatching of H. glycines compared with the control and suppress J2 up to 90% after treatment for 1 h [108,109]. In the greenhouse experiment, Purpureocillium spp. isolate E could effectively control the reproduction of H. glycines compared with the control [90]. Inoculation of two Glomus species, G. mosseae, and G. etunicatum, prior to inoculation with H. glycines, could reduce the number of H. glycines in soybean roots and cysts in rhizospheric soil and roots. Meanwhile, both strains could induce the activity of plant defense enzymes such as peroxidase in soybeans [83,84,110]. Other fungi, including Piriformospora indica, Diversispora eburnean, Claroideoglomus claroideum, Rhizophagus intraradices, Dentiscutata heterogama, and Funneliformis mosseae, also had the ability to reduce the number of cysts on the roots and H. glycines of soybean compared with the control [86,111].

5.2. Biocontrol Bacteria against Soybean Cyst Nematode Disease

Biocontrol bacteria, especially Bacillus strains, have been the most reported to control SCN. The suspension of B. megaterium Sneb207, which originated from soybean nodules, was coated with soybean seeds, and could significantly decrease the numbers of eggs, juveniles, and cysts of H. glycines. The application of Sneb207 increased soybean root length and chlorophyll content. Studies found that the activities of the plant defense enzymes phenylalanine ammonia-lyase, polyphenoloxidase, and peroxidase were increased after the application of Sneb207 [94,112,113]. Other Bacillus strains, B. velezensis Bve2, B. mojavensis Bmo3 and B. aryabhattai Sneb517, reduced the number of cysts and the population of H. glycines under greenhouse and field trials [92,93]. A mixed strain group named SN101 contains B. simple, B. megaterium and Sinarhizobium fredii at a proportion of 3:1:1. Coted soybean seeds with SN101 reduced the reproduction of H. glycines and markedly promoted the growth and yield of soybean plants under greenhouse and field experiments [95]. Moreover, the application of B. thuringiensis could also effectively control H. glycines and increase the yield of soybean plants [96]. Other Bacillus strains, including B. subtilis NXXJ0624, B. aryabhattai Ba1-7, B. laterosporus BL-21, and B. subtilis HND-F2, could increase the mortality rates of H. glycines [97,114,115,116].
Sinorhizobium fredii is another important biocontrol agent against H. glycines. Suspension of isolate Sneb183 was inoculated to soybean plants and reduced the numbers of juveniles and cysts and inhibited the egg hatching of H. glycines [117,118]. Another isolate, L396, also inhibited egg hatching and improved the mortality rate of H. glycines [119]. Microbacterium maritypicum Sneb159 and Klebsiella pneumoniae SnebYK reduced the number of H. glycines [98,120]. Moreover, the application of Sneb159 could induce the expression levels of the plant defense genes PR2, PR3b, and JAZ1 [100]. S. venezuelae Snea253 could inhibit the cyst numbers of H. glycines [102], and another S. zaomyceticus strain, XFS-4, was coated with soybean seeds and showed the ability to suppress the hatching rate of soybean cysts [101]. Other biocontrol bacteria, including P. fluorescens NXXJ1225, L. enzymogenes C3, and Photorhabdus sp. NJ exhibited the ability to control H. glycines [96,116,121].

6. Biocontrol Mechanisms of Controlling Soybean Diseases

Understanding the mechanism of biocontrol agents against soybean disease is pivotal for further improving their biocontrol abilities. Several mechanisms are involved in the control of soybean diseases from two perspectives (Figure 4). One side of the mechanism is from biocontrol agents. The production of secondary metabolites or cell wall-degrading enzymes is the main mechanism that directly acts on pathogens. Secondary metabolites produced by biocontrol agents could inhibit the growth of pathogens or even kill them. An antifungal metabolite cyclosporine A was isolated from F. oxysporum S6, which could inhibit the growth of S. sclerotiorum and sclerotia formation [35]. Metabolite compounds from Streptomyces strains also exhibited remarkable effects against S. sclerotiorum [122]. Scopoletin was isolated from P. janthinellum Snef1650 and could decrease the number of cysts in the soil and juveniles in the soybean roots [89]. The L. enzymogenes C3 mutant was defective in antimicrobial secondary metabolite complex production and reduced the inhibitory effect on the reproduction of H. glycines [99]. Another bacterium, the B. velezensis FZB42 mutant, was disrupted in bacilysin biosynthesis and lost antagonistic ability against P. sojae [73].
In addition to metabolite compounds, cell wall-degrading enzymes also play crucial roles in soybean disease management. Cell wall-degrading enzymes such as chitinase, glucanase and protease secreted by biocontrol agents could hydrolyze the cell wall of pathogens. Transformation of the endochitinase gene Chi67-1 in C. rosea 67-1 increased the chitinase activity and biocontrol efficacy of SSR of soybean in a greenhouse assay [123]. An endochitinase-encoding gene chi46 was cloned from Chaetomium globosum and expressed in Pichia pastoris GS115. The expressed CHI46 enzyme had a degrading effect on the cell wall of P. sojae [124]. An extracellular alkaline protease (Hasp) was obtained from H. rhossiliensis OWVT-1. Hasp has the ability to degrade proteins of the H. glycines cuticle and is lethal to juveniles of H. glycines [125].
Moreover, some biocontrol agents can induce resistance of soybean plants to pathogens. Biocontrol agents could induce activities of defense enzymes such as peroxidase and phenyl ammonia-lyase in the plants, which had resistance to pathogen infection. The application of T. harzianum T-aloe markedly increased the activities of peroxidase and superoxide dismutase in soybean leaves after infection with S. sclerotiorum [126]. The use of S. hygroscopicus S11 increased the expression levels of the salicylic acid-dependent defense gene ICS1 and the jasmonic acid pathway defense genes LOX1 and AOC1 in soybeans after infection with P. sojae [72].
The activities of the plant defense enzymes phenyl ammonia-lyase, polyphenoloxidase, and peroxidase were increased in soybean roots after the application of B. megaterium Sneb 207 under H. glycines infection [94]. The expression levels of the plant defense genes PR2, PR3b, and JAZ1, which belong to the salicylic acid and jasmonic acid pathways in soybeans, were significantly improved by the use of M. maritypicum Sneb159 under H. glycines infection [100].

7. Conclusions and Prospects

Soybean Sclerotinia stem rot, soybean Phytophthora root rot, and soybean cyst nematode commonly occur in soybean plants and cause huge economic losses. From 1996 to 2016, the soybean economic losses caused by SSR, PRR, and SCN reached USD 4663, 8755, and 31,954 million, respectively, across 28 states in the United States [127]. Although many biocontrol agents have been studied and have been confirmed to have the ability to control the above soybean diseases, until now, few reviews have reported the control of these three soybean diseases. This review focuses on the species of biocontrol agents, as well as their control efficacies and mechanisms in soybean diseases. In particular, certain biocontrol agents, such as Bacillus and Streptomyces, possess the ability to control all three soybean diseases under greenhouse or field conditions.
The following suggestions are provided for the future better application of biocontrol agents against soybean diseases.
(1) More microorganisms that could effectively control PRR in soybeans should be screened. Compared with controlling SSR and SCN, there are few species of biocontrol agents controlling PRR, but the damage caused by PRR is not less severe than that caused by the other two soybean diseases.
(2) The microorganism species that could control all three soybean diseases should be extended. The three diseases could be incident at one time; therefore, the application of biocontrol agents with wide disease control spectra is effective and economical.
(3) The molecular mechanisms of biocontrol agents against soybean diseases should be studied in depth. Although the transcriptomes and proteomes during the process against soybean diseases have been analyzed and the expression levels of biocontrol-related genes have been detected, the molecular functions of biocontrol-related genes against soybean diseases have rarely been studied. Understanding the molecular functions of genes in biocontrol is crucial for further improving the biocontrol ability of biocontrol agents.
(4) Excellent biocontrol genes could be transformed into biocontrol agents to improve their biocontrol ability against soybean diseases. Currently, genetic modification strains used for the biocontrol of soybean diseases are rare and could be further developed.
(5) More biocontrol agent products that meet the requirements of the market should be developed. Although a number of biocontrol agents have been reported, few marketable products have been reported. The objective of the studied biocontrol agents is to solve the incidence of soybean diseases; therefore, it is necessary to develop biocontrol agent products for market applications.

Author Contributions

Conceptualization, Z.-B.S.; investigation, Z.-B.S. and S.-F.Y.; data curation, S.-F.Y., C.-L.W., Y.-F.H., and Y.-C.W.; writing—original draft preparation, S.-F.Y. and C.-L.W.; writing—review and editing, Z.-B.S.; supervision, Z.-B.S.; funding acquisition, Z.-B.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Science and Technology general project of the Beijing municipal education commission (KM202110011002), the open fund project in the key laboratory of integrated pest management of the Ministry of Agriculture/key laboratory of major crop disease management of Hubei Province (2021ZTSJJ9), and university students’ scientific research and entrepreneurial action project (G022).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. McCaghey, M.; Willbur, J.; Smith, D.L.; Kabbage, M. The complexity of the Sclerotinia sclerotiorum pathosystem in soybean: Virulence factors, resistance mechanisms, and their exploitation to control Sclerotinia stem rot. Trop. Plant Pathol. 2018, 44, 12–22. [Google Scholar] [CrossRef]
  2. Morais, E.M.; Silva, A.A.R.; Sousa, F.W.A.; Azevedo, I.M.B.; Silva, H.F.; Santos, A.M.G.; Beserra Júnior, J.E.A.; Carvalho, C.P.; Eberlin, M.N.; Porcari, A.M.; et al. Endophytic Trichoderma strains isolated from forest species of the Cerrado-Caatinga ecotone are potential biocontrol agents against crop pathogenic fungi. PLoS ONE. 2022, 17, e0265824. [Google Scholar] [CrossRef] [PubMed]
  3. Rodriguez, M.C.; Sautua, F.; Scandiani, M.; Carmona, M.; Asurmendi, S. Current recommendations and novel strategies for sustainable management of soybean sudden death syndrome. Pest Manag. Sci. 2021, 77, 4238–4248. [Google Scholar] [CrossRef]
  4. Willbur, J.; Mccaghey, M.; Kabbage, M.; Smith, D.L. An overview of the Sclerotinia sclerotiorum pathosystem in soybean: Impact, fungal biology, and current management strategies. Trop. Plant Pathol. 2019, 44, 3–11. [Google Scholar] [CrossRef]
  5. Giachero, M.L.; Declerck, S.; Marquez, N. Phytophthora root rot: Importance of the disease, current and novel methods of control. Agronomy 2022, 12, 610. [Google Scholar] [CrossRef]
  6. O’Sullivan, C.A.A.; Belt, K.; Thatcher, L.F.F. Tackling control of a cosmopolitan phytopathogen: Sclerotinia. Front. Plant Sci. 2021, 12, 707509. [Google Scholar] [CrossRef]
  7. Xiang, N.; Lawrence, K.S.; Donald, P.A. Biological control potential of plant growth-promoting rhizobacteria suppression of Meloidogyne incognita on cotton and Heterodera glycines on soybean: A review. J. Phytopathol. 2018, 166, 449–458. [Google Scholar] [CrossRef]
  8. Bejarano, A.; Puopolo, G. Bioformulation of microbial biocontrol agents for a sustainable agriculture. In How Research Can Stimulate the Development of Commercial Biological Control against Plant Diseases; De Cal, A., Ed.; Progress in Biological Control Series; Springer: Berlin, Germany, 2020; pp. 275–293. [Google Scholar]
  9. Cui, L.; Yang, C.; Wang, Y.; Ma, T.; Cai, F.; Wei, L.; Jin, M.; Osei, R.; Zhang, J.; Tang, M. Potential of an endophytic bacteria Bacillus amyloliquefaciens 3-5 as biocontrol agent against potato scab. Microb. Pathog. 2022, 163, 105382. [Google Scholar] [CrossRef] [PubMed]
  10. Niblack, T.L.; Lambert, K.N.; Tylka, G.L. A model plant pathogen from the kingdom animalia: Heterodera glycines, the soybean cyst nematode. Annu. Rev. Phytopathol. 2006, 4, 283–303. [Google Scholar] [CrossRef]
  11. Xu, Z.; Huang, G.; Song, N.; Wang, J.; Cao, L.; Jiang, H.; Ding, T. Complete mitochondrial genome sequence of the phytopathogenic fungi Sclerotinia sclerotiorum JX-21. Mitochondrial DNA B Resour. 2016, 1, 656–657. [Google Scholar] [CrossRef] [Green Version]
  12. Bolton, M.D.; Thomma, B.P.; Nelson, B.D. Sclerotinia sclerotiorum (Lib.) de Bary: Biology and molecular traits of a cosmopolitan pathogen. Mol. Plant Pathol. 2006, 7, 1–16. [Google Scholar] [CrossRef] [PubMed]
  13. Le Tourneau, D. Morphology, cytology and physiology of Sclerotinia species in culture. Phytopathology 1979, 69, 887–890. [Google Scholar] [CrossRef]
  14. Ding, L.N.; Li, T.; Guo, X.J.; Li, M.; Liu, X.Y.; Cao, J.; Tan, X.L. Sclerotinia stem rot resistance in rapeseed: Recent progress and future prospects. J. Agric. Food Chem. 2021, 69, 2965–2978. [Google Scholar] [CrossRef] [PubMed]
  15. Yang, M.L.; Zhang, W.; Wei, Q.H.; Shi, L.M.; Guo, Y.; Zhang, K.C.; Ge, B.B. Sclerotinia stem rot of soybean: A review. Chin. AgrIC. Sci. E Bull. 2021, 37, 90–99. [Google Scholar]
  16. Dai, R.P.; Liu, H. Research advance on soybean Phytophthora root rot. Soybean Sci. Technol. 2011, 1, 20–22. [Google Scholar]
  17. Kato, M. Recent reseach on Phytophthora root and stem rot of soybean in Japan. Plant Protect. 2010, 64, 497–500. [Google Scholar]
  18. Zhang, S.Z.; Ding, G.W.; Li, W.B.; Yang, C.P.; Lin, S.F.; Xu, P.F.; Ning, H.L.; Zhang, D.Y.; Jiang, Z.F.; Wu, X.X. Research progress on Phytophthora sojae root rot. Chin. J. Oil Crop Sci. 2004, 26, 102–107. [Google Scholar]
  19. Sugimoto, T.; Kato, M.; Yoshida, S.; Matsumoto, I.; Kobayashi, T.; Kaga, A.; Hajika, M.; Yamamoto, R.; Watanabe, K.; Aino, M.; et al. Pathogenic diversity of Phytophthora sojae and breeding strategies to develop Phytophthora-resistant soybeans. Breed Sci. 2012, 61, 511–522. [Google Scholar] [CrossRef]
  20. Lilley, C.J.; Atkinson, H.J.; Urwin, P.E. Molecular aspects of cyst nematodes. Mol. Plant Pathol. 2005, 6, 577–588. [Google Scholar] [CrossRef]
  21. Yu, B.L.; Gao, L. Occurrence and management of soybean cyst nematode. Soybean Sci. Technol. 2012, 1, 29–33. [Google Scholar]
  22. Xu, Y.L.; Wang, L.F.; Zhan, L.L. The research advances on soybean cyst nematodes (SCN). Soybean Sci. Technol. 2010, 1, 21–24. [Google Scholar]
  23. Opperman, C.H.; Bird, D.M. The soybean cyst nematode, Heterodera glycines: A genetic model system for the study of plant-parasitic nematodes. Curr. Opin. Plant Biol. 1998, 1, 246–342. [Google Scholar] [CrossRef]
  24. Chen, L.J.; Wang, Y.Y.; Zhu, X.F.; Duan, Y.X. Riview of the biocontrol on soybean cyst nematode (Heterodera glycines). J. Shenyang Agric. Univ. 2011, 42, 393–398. [Google Scholar]
  25. Alfiky, A.; Weisskopf, L. Deciphering Trichoderma-plant-pathogen interactions for better development of biocontrol applications. J. Fungi 2021, 7, 61. [Google Scholar] [CrossRef] [PubMed]
  26. Zeng, W.T.; Kirk, W.; Hao, J.J. Field management of Sclerotinia stem rot of soybean using biological control agents. Biol. Control 2012, 60, 141–147. [Google Scholar] [CrossRef]
  27. Zeng, W.T.; Wang, D.C.; Kirk, W.; Hao, J.J. Use of Coniothyrium minitans and other microorganisms for reducing Sclerotinia sclerotiorum. Biol. Control 2012, 60, 225–232. [Google Scholar] [CrossRef]
  28. Menendez, A.B.; Godeas, A. Biological control of Sclerotinia sclerotiorum attacking soybean plants. Degradation of the cell walls of this pathogen by Trichoderma harzianum (BAFC 742). Mycopathologia 1998, 142, 153–160. [Google Scholar] [CrossRef]
  29. Sumida, C.H.; Daniel, J.F.S.; Araujod, A.P.C.S.; Peitl, D.C.; Abreu, L.M.; Dekker, R.F.H.; Canteri, M.G. Trichoderma asperelloides antagonism to nine Sclerotinia sclerotiorum strains and biological control of white mold disease in soybean plants. Biocontrol Sci. Technol. 2018, 28, 142–156. [Google Scholar] [CrossRef]
  30. Haddad, P.E.; Leite, L.G.; Lucon, C.M.M.; Harakava, R. Selection of Trichoderma spp. strains for the control of Sclerotinia sclerotiorum in soybean. Pesqui. Agropecuária Bras. 2017, 52, 1140–1148. [Google Scholar] [CrossRef]
  31. Sun, Z.B.; Wang, Q.; Sun, M.H.; Li, S.D. The heat shock protein 70 gene is involved for colony morphology, sporulation and mycoparasitism of Clonostachys rosea. FEMS Microbiol. Lett. 2019, 366, 188. [Google Scholar] [CrossRef] [PubMed]
  32. Rodriguez, M.A.; Cabrera, G.; Gozzo, F.C.; Eberlin, M.N.; Godeas, A. Clonostachys rosea BAFC3874 as a Sclerotinia sclerotiorum antagonist: Mechanisms involved and potential as a biocontrol agent. J. Appl. Microbiol. 2011, 110, 1177–1186. [Google Scholar] [CrossRef] [PubMed]
  33. Rodríguez, M.A.; Rothen, C.; Lo, T.E.; Cabrera, G.M.; Godeas, A.M. Suppressive soil against Sclerotinia sclerotiorum as a source of potential biocontrol agents: Selection and evaluation of Clonostachys rosea BAFC1646. Biocontrol Sci. Technol. 2015, 25, 1388–1409. [Google Scholar] [CrossRef]
  34. Zhang, S.M.; Wang, Y.X.; Wang, J.L.; Li, J. Biocontrol of soybean Sclerotinia sclerotiorum by Bacillus subtilis. Soybean Bull. 2006, 1, 18–19. [Google Scholar]
  35. Rodriguez, M.A.; Cabrera, G.; Godeas, A. Cyclosporine A from a nonpathogenic Fusarium oxysporum suppressing Sclerotinia sclerotiorum. J. Appl. Microbiol. 2006, 100, 575–586. [Google Scholar] [CrossRef] [PubMed]
  36. Peitl, D.C.; Sumida, C.H.; Gonçalves, R.M.; Pascholati, S.F.; Balbi-Peña, M.I. Antagonism of saprobe fungi from semiarid areas of the Northeast of Brazil against Sclerotinia sclerotiorum and biocontrol of soybean white mold. Semin. Ciências Agrárias 2020, 41, 2597–2612. [Google Scholar] [CrossRef]
  37. Safaei Asadabadi, R.; Hage-Ahmed, K.; Steinkellner, S. Biochar, compost and arbuscular mycorrhizal fungi: A tripartite approach to combat Sclerotinia sclerotiorum in soybean. J. Plant Dis. Prot. 2021, 128, 1433–1445. [Google Scholar] [CrossRef]
  38. Vitorino, L.C.; Silva, F.O.D.; Cruvinel, B.G.; Bessa, L.A.; Rosa, M.; Souchie, E.L.; Silva, F.G. Biocontrol potential of Sclerotinia sclerotiorum and physiological changes in soybean in response to Butia archeri palm rhizobacteria. Plants 2020, 39, 64. [Google Scholar] [CrossRef]
  39. Alvarez, F.; Castro, M.; Principe, A.; Borioli, G.; Fischer, S.; Mori, G.; Jofre, E. The plant-associated Bacillus amyloliquefaciens strains MEP218 and ARP23 capable of producing the cyclic lipopeptides iturin or surfactin and fengycin are effective in biocontrol of sclerotinia stem rot disease. J. Appl. Microbiol. 2012, 112, 159–174. [Google Scholar] [CrossRef]
  40. Simonetti, E.; Hernández, A.I.; Kerber, N.L.; Pucheu, N.L.; Carmona, M.A.; García, A.F. Protection of canola (Brassica napus) against fungal pathogens by strains of biocontrol rhizobacteria. Biocontrol Sci. Technol. 2012, 22, 111–115. [Google Scholar] [CrossRef]
  41. Zhang, J.; Xue, A.G.; Morrison, M.J.; Meng, Y. Impact of time between field application of Bacillus subtilis strains SB01 and SB24 and inoculation with Sclerotinia sclerotiorum on the suppression of Sclerotinia stem rot in soybean. Eur. J. Plant Pathol. 2011, 131, 95–102. [Google Scholar] [CrossRef]
  42. Nian, J.; Yu, M.; Bradley, C.A.; Zhao, Y. Lysobacter enzymogenes strain C3 suppresses mycelium growth and spore germination of eight soybean fungal and oomycetes pathogens and decreases disease incidences. Biol. Control 2021, 152, 104424. [Google Scholar] [CrossRef]
  43. Liu, D.; Yan, R.; Fu, Y.; Wang, X.; Zhang, J.; Xiang, W. Antifungal, plant growth-promoting, and genomic properties of an endophytic actinobacterium Streptomyces sp. NEAU-S7GS2. Front. Microbiol. 2019, 10, 2077. [Google Scholar] [CrossRef] [PubMed]
  44. Liu, X.; Dou, G.; Ma, Y. Potential of endophytes from medicinal plants for biocontrol and plant growth promotion. J. Gen. Plant Pathol. 2016, 82, 165–173. [Google Scholar] [CrossRef]
  45. Sun, Z.B.; Li, S.D.; Ren, Q.; Xu, J.L.; Lu, X.; Sun, M.H. Biology and applications of Clonostachys rosea. J. Appl. Microbiol. 2020, 129, 486–495. [Google Scholar] [CrossRef] [PubMed]
  46. Zhao, H.; Zhou, T.; Xie, J.; Cheng, J.; Chen, T.; Jiang, D.; Fu, Y. Mycoparasitism illuminated by genome and transcriptome sequencing of Coniothyrium minitans, an important biocontrol fungus of the plant pathogen Sclerotinia sclerotiorum. Microb. Genom. 2020, 6, e000345. [Google Scholar] [CrossRef]
  47. Sun, Z.B.; Wang, Q.; Zhang, J.; Jiang, W.Z.; Wang, Q.; Li, S.D.; Ma, G.Z.; Sun, M.H. The transcription factor-encoding gene crtf is involved in Clonostachys chloroleuca mycoparasitism on Sclerotinia sclerotiorum. Microbiol. Res. 2018, 210, 6–11. [Google Scholar] [CrossRef] [PubMed]
  48. Sun, Z.B.; Wang, Q.; Sun, M.H.; Li, S.D. The mitogen-activated protein kinase gene crmapk is involved in Clonostachys chloroleuca mycoparasitism. Mol. Plant Microbe Interact. 2020, 33, 902–910. [Google Scholar] [CrossRef]
  49. Jing, L.; Navi, S.S.; Yang, X. Effects of colonisation by different strains of Coniothyrium minitanson the viability of sclerotia of Sclerotinia sclerotiorum. Biocontrol Sci. Technol. 2014, 25, 460–474. [Google Scholar] [CrossRef]
  50. Ribeiro, A.I.; Costa, E.S.; Thomasi, S.S.; Brandao, D.F.R.; Vieira, P.C.; Fernandes, J.B.; Forim, M.R.; Ferreira, A.G.; Pascholati, S.F.; Gusmao, L.F.P.; et al. Biological and chemical control of Sclerotinia sclerotiorum using Stachybotrys levispora and its secondary metabolite griseofulvin. J. Agric. Food Chem. 2018, 66, 7627–7632. [Google Scholar] [CrossRef]
  51. del Rio, L.E.; Martinson, C.A.; Yang, X.B. Biological control of Sclerotinia stem rot of soybean with Sporidesmium sclerotivorum. Plant Dis. 2002, 86, 999–1004. [Google Scholar] [CrossRef]
  52. Barros, D.C.M.; Fonseca, I.C.B.; Balbi-Peña, M.I.; Pascholati, S.F.; Peitl, D.C. Biocontrol of Sclerotinia sclerotiorum and white mold of soybean using saprobic fungi from semi-arid areas of Northeastern Brazil. Summa Phytopathologica. 2015, 41, 251–255. [Google Scholar] [CrossRef]
  53. Massawe, V.C.; Hanif, A.; Farzand, A.; Mburu, D.K.; Ochola, S.O.; Wu, L.M.; Tahir, H.A.S.; Gu, Q.; Wu, H.J.; Gao, X.W. Volatile compounds of endophytic Bacillus spp. have biocontrol activity against Sclerotinia sclerotiorum. Phytopathology 2018, 108, 1373–1385. [Google Scholar] [CrossRef] [PubMed]
  54. Chacon-Orozco, J.G.; Bueno, C.J.; Shapiro-Ilan, D.I.; Hazir, S.; Leite, L.G.; Harakava, R. Antifungal activity of Xenorhabdus spp. and Photorhabdus spp. against the soybean pathogenic Sclerotinia sclerotiorum. Sci. Rep. 2020, 10, 20649. [Google Scholar] [CrossRef] [PubMed]
  55. Kumar, A.; Saini, S.; Wray, V.; Nimtz, M.; Prakash, A.; Johri, B.N. Characterization of an antifungal compound produced by Bacillus sp. strain A5F that inhibits Sclerotinia sclerotiorum. J. Basic Microbiol. 2012, 52, 670–678. [Google Scholar] [CrossRef] [PubMed]
  56. Lopes, K.B.D.; Carpentieri-Pipolo, V.; Fira, D.; Balatti, P.A.; Lopez, S.M.Y.; Oro, T.H.; Pagliosa, E.S.; Degrassi, G. Screening of bacterial endophytes as potential biocontrol agents against soybean diseases. J. Appl. Microbiol. 2018, 125, 1466–1481. [Google Scholar] [CrossRef]
  57. Wang, B.; Zhou, J.N.; Huang, Z.Q.; Wang, X.; Ding, Z.Q.; Chang, Y.; Su, Z.X.; Zhou, X.G. Biological properties of Paenibacillus polymyxa XZ-2 and its antagonistic effect against 3 soybean pathogens. Southwest China J. Agric. Sci. 2018, 31, 1197–1202. [Google Scholar]
  58. Ayoubi, N.; Zafari, D.; Mirabolfathy, M. Combination of Trichoderma species and Bradyrhizobium japonicum in control of Phytophthora sojae and soybean growth. J. Crop Prot. 2012, 1, 67–79. [Google Scholar]
  59. Liu, H.A.; Wu, H.S.; Li, J.; Ren, Q.Q.; Su, J.K.; Shang, X.X.; Li, Y.F.; Zhou, X.D.; Yan, S.; Liu, X.X. Effects of antagonistic microbes and organic fertilizer mixtures on controlling pathogen Phytophthra sojae of soybean. J. Yangzhou Univ. 2014, 35, 90–94. [Google Scholar]
  60. Li, Y.; Liu, Z.; Hou, H.; Lei, H.; Zhu, X.; Li, X.; He, X.; Tian, C. Arbuscular mycorrhizal fungi-enhanced resistance against Phytophthora sojae infection on soybean leaves is mediated by a network involving hydrogen peroxide, jasmonic acid, and the metabolism of carbon and nitrogen. Acta Physiol. Plant. 2013, 35, 3465–3475. [Google Scholar] [CrossRef]
  61. Tai, L.M.; Gao, J.F.; Zuo, Y.H.; Jin, X.H.; Zhang, Y.L.; Li, H.Y. Induction of defense enzymes activities in soyben and control effect of Phytophthora Root Rot in flowerpot by Trichoderma longibrachiaum T115D. Chin. J. Biol. Control 2018, 34, 897–905. [Google Scholar]
  62. Yang, G.H.; Gao, Z.M.; Cao, S.; Jiang, T.; Wang, T. Screening and biocontrol effects of antagonistic against Phytophthora sojae. J. Anhui Agr. Uni. 2012, 39, 677–681. [Google Scholar]
  63. Xi, X.; Fan, J.; Yang, X.; Liang, Y.; Zhao, X.; Wu, Y. Evaluation of the anti-oomycete bioactivity of rhizosphere soil-borne isolates and the biocontrol of soybean root rot caused by Phytophthora sojae. Biol. Control 2022, 166, 104818. [Google Scholar] [CrossRef]
  64. Liu, D.; Li, K.Y.; Hu, J.L.; Wang, W.Y.; Liu, X.; Cao, Z.M. Biocontrol and action mechanism of Bacillus amyloliquefaciens and Bacillus subtilis in soybean Phytophthora blight. Int. J. Mol. Sci. 2019, 20, 2908. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  65. Fu, H.M.; Li, M.; Tan, G.J.; Wang, Z.Y.; Zhao, P.S. Screening and identification of antagonistic strain against Phytophthora sojae. J. Anhui Agric. Sci. 2011, 39, 11482–11484. [Google Scholar]
  66. Lu, X.; Zhou, D.; Chen, X.; Zhang, J.; Huang, H.; Wei, L. Isolation and characterization of Bacillus altitudinis JSCX-1 as a new potential biocontrol agent against Phytophthora sojae in soybean [Glycine max (L.) Merr.]. Plant Soil 2017, 416, 53–66. [Google Scholar] [CrossRef]
  67. Han, X.D.; Hua, M.N.; Feng, Y.J.; Wu, C.V. Isolation and characterization of endophytic bacteria for Phytophthora sojae inhibition from soybean plant. Soybean Sci. 2012, 32, 85–91. [Google Scholar]
  68. Hou, J.M.; Bi, S.N.; Yan, L.; Zuo, Y.H.; Wang, Y.J.; Liu, T.; Zhu, J.W. Biological potential of Pseudomonas sp. BS1 in the control of Phytophthora root rot of soybean. Afr. J. Microbiol. Res. 2012, 6, 3589–3593. [Google Scholar]
  69. Arfaoui, A.; Adam, L.R.; Bezzahou, A.; Daayf, F. Isolation and identification of cultivated bacteria associated with soybeans and their biocontrol activity against Phytophthora sojae. BioControl 2018, 63, 607–617. [Google Scholar] [CrossRef]
  70. Jiu, M.; Li, J.J.; Li, W.S.; Feng, H.; Liu, R.X.; Wei, L.H.; Zhou, D.M. Screening, identification and biocontrol effect of actinomycetes against Phytophthora sojae. Jiangsu J. Agric. Sci. 2021, 37, 1137–1142. [Google Scholar]
  71. Xiao, K.; Kinkel, L.L.; Samac, D.A. Biological control of Phytophthora root rots on alfalfa and soybean with Streptomyces. Biol. Control 2002, 23, 285–295. [Google Scholar] [CrossRef]
  72. Arfaoui, A.; El Hadrami, A.; Adam, L.R.; Daayf, F. Combining Streptomyces hygroscopicus and phosphite boosts soybean’s defense responses to Phytophthora sojae. BioControl 2020, 65, 363–375. [Google Scholar] [CrossRef]
  73. Han, X.S.; Shen, D.X.; Xiong, Q.; Bao, B.H.; Zhang, W.B.; Dai, T.T.; Zhao, Y.J.; Borriss, R.; Fan, B. The pant-beneficial rhizobacterium Bacillus velezensis FZB42 controls the soybean pathogen Phytophthora sojae due to bacilysin production. Appl. Environ. Microbiol. 2021, 87, e0160121. [Google Scholar] [CrossRef] [PubMed]
  74. Wang, K.; Han, Y.Q.; Shi, L.L.; Wang, Y.J.; Wang, W.D.; Xiang, W.S.; Gao, Y.M. Isolation of a actinomycete with inhibitory activity against Phytophthora sojae in soil. Heilongjiang Agric. Sci. 2016, 5, 64–68. [Google Scholar]
  75. Zhang, H.Y.; Gao, Q.; Zhang, L.Y.; Lin, G.L.; Li, R.L. Screening of actinomycetes against Phytophthora root rot of soybean and its growth promotion and disease control. Biotechnol. Bull. 2020, 36, 25–31. [Google Scholar]
  76. Zhao, L.F.; Xu, Y.J.; Zheng, A.Z.; Lai, X.H. Antagonistic endophytic bacteria associated with nodules of soybean (Glycine max L.) and plant growth-promoting properties. Braz. J. Microbiol. 2018, 49, 269–278. [Google Scholar] [CrossRef]
  77. Liu, S.F.; Chen, S.Y. Effectiveness of Hirsutella minnesotensis and H. rhossiliensis in control of the soybean cyst nematode in four soils with various pH, texture, and organic matter. Biocontrol Sci. Technol. 2009, 19, 595–612. [Google Scholar] [CrossRef]
  78. Qian, H.L.; Li, S.X.; Xu, Y.L.; Li, C.J.; Sun, Y.Q. Effects of two Hirsutella minnesotensis on soybean cyst nematode and soybean growth. Soybean Sci. 2011, 30, 266–271. [Google Scholar]
  79. Qian, H.L.; Xu, Y.L.; Sun, Y.Q.; Li, C.J. Effects of Hirsutella minnesotensis metabolites on soybean cyst nematode juvenile. Soybean Sci. 2009, 28, 119–122. [Google Scholar]
  80. Liu, J.B.; Zhu, W.J.; Hamid, M.I.; Chen, X.L.; Wang, N.N.; Sun, J.Z. Population dynamics and biocontrol efficacy of the nematophagous fungus Hirsutella minnesotensis in pot assay. Nematology 2016, 18, 823–830. [Google Scholar] [CrossRef]
  81. Liu, X.Z.; Chen, S.Y. Screening isolates of Hirsutella species for biocontrol of Heterodera glycines. Biocontrol Sci. Technol. 2001, 11, 151–160. [Google Scholar] [CrossRef]
  82. Chen, S.Y.; Liu, X.Z. Control of soybean cyst nematode by the fungi Hirsutella rhossiliensis and Hirsutella minnesotensis in greenhouse studies. Biol. Control. 2005, 32, 208–219. [Google Scholar] [CrossRef]
  83. Li, Y.; Li, J.X.; Xu, L.J.; Zhao, H.H.; Liu, R.J. The effectiveness of arbuscular mycorrhizal fungi to antagonize soybean cyst nematode disease. Microbiol. China 2010, 37, 1610–1616. [Google Scholar]
  84. Li, H.Y.; Liu, R.J.; Shu, H.R. A preliminary report on interactions between arbuscular mycorrhizal fungi and soybean cyst nematode. Acta Phytopathol. Sin. 2002, 32, 356–360. [Google Scholar]
  85. Li, T.; Huang, W.K.; Peng, D.L.; Kong, L.A.; Peng, H. Control efficiencyof three fungal strains’ fermentation broth on soybean cyst nematode (Heterodera glycines). J. Huazhong Agric. Univ. 2017, 36, 42–46. [Google Scholar]
  86. Pawlowski, M.L.; Hartman, G.L. Impact of arbuscular mycorrhizal species on Heterodera glycines. Plant Dis. 2020, 104, 2406–2410. [Google Scholar] [CrossRef] [PubMed]
  87. Lu, J.C.; Xu, Y.L.; Song, J. Effect of soil disturbance to the biological control of fermentation filtrate of parasitic fungi on soybean cyst nematode in glasshouse. Soybean Sci. 2016, 35, 106–111. [Google Scholar]
  88. Xu, Y.L.; Lu, J.C.; Song, J. Virulence and control effect of parasitic fungi on race 3 of soybean cyst nematode. Soybean Sci. 2020, 39, 595–604. [Google Scholar]
  89. Yan, J.C.; Xing, Z.F.; Lei, P.; Sikandar, A.; Yang, R.W.; Wang, Y.Y.; Zhu, X.F.; Liu, X.Y.; Fan, H.Y.; Xuan, Y.H.; et al. Evaluation of scopoletin from Penicillium janthinellum Snef1650 for the control of Heterodera glycines in soybean. Life 2021, 11, 1143. [Google Scholar] [CrossRef]
  90. Haarith, D.; Kim, D.; Chen, S.; Bushley, K.E. Growth chamber and greenhouse screening of promising in vitro fungal biological control candidates for the soybean cyst nematode (Heterodera glycines). Biological Control 2021, 160, 104635. [Google Scholar] [CrossRef]
  91. Silva, D.M.; de Souza, V.H.M.; Moral, R.d.A.; Delalibera Junior, I.; Mascarin, G.M. Production of Purpureocillium lilacinum and Pochonia chlamydosporia by submerged liquid fermentation and bioactivity against Tetranychus urticae and Heterodera glycines through Seed Inoculation. J. Fungi 2022, 8, 511. [Google Scholar] [CrossRef]
  92. Xiang, N.; Lawrence, K.S.; Kloepper, J.W.; Donald, P.A.; McInroy, J.A. Biological control of Heterodera glycines by spore-forming plant growth-promoting rhizobacteria (PGPR) on soybean. PLoS ONE 2017, 12, e0181201. [Google Scholar] [CrossRef] [PubMed]
  93. Zhao, J.; Liu, D.; Wang, Y.Y.; Zhu, X.F.; Chen, L.J.; Duan, Y.X. Evaluation of Bacillus aryabhattai Sneb517 for control of Heterodera glycines in soybean. Biol. Control 2020, 142, 104147. [Google Scholar] [CrossRef]
  94. Duan, Y.X.; Zhang, Y.; Zhu, X.F.; Liu, D.W.; Li, S.; Chen, L.J.; Wang, Y.Y. Biochemical mechanism of resistance against soybean cyst nematode induced by plant growth promoting rhizobacteria in soybean. Soybean Sci. 2011, 30, 442–446. [Google Scholar]
  95. Zhou, Y.Y.; Wang, Y.Y.; Zhu, X.F.; Liu, R.; Xiang, P.; Chen, J.S.; Liu, X.Y.; Duan, Y.X.; Chen, L.J. Management of the soybean cyst nematode Heterodera glycines with combinations of different rhizobacterial strains on soybean. PLoS ONE 2017, 12, e0182654. [Google Scholar] [CrossRef]
  96. Liu, C.J.; Cao, C.X.; Zhou, R.H.; Cheng, X.L. Field Tests of Bacillus thuringiensis for controlling Heterodera glycines Ichinohe. Hubei Agric. Sci. 2011, 50, 520–522. [Google Scholar]
  97. Wang, Y.Y.; Duan, Y.X.; Chen, L.J. Effect of endophytic bacteria from soybean root nodules on soybean cyst nematode and pathogens of soybean root rot. Soybean Sci. 2007, 26, 213–217. [Google Scholar]
  98. Liu, D.; Chen, L.; Zhu, X.F.; Wang, Y.Y.; Xuan, Y.H.; Liu, X.Y.; Chen, L.J.; Duan, Y.X. Klebsiella pneumoniae SnebYK mediates resistance against Heterodera glycines and promotes soybean growth. Front. Microbiol. 2018, 9, 1134. [Google Scholar] [CrossRef] [PubMed]
  99. Yuen, G.Y.; Broderick, K.C.; Jochum, C.C.; Chen, C.J.; Caswell-Chen, E.P. Control of cyst nematodes by Lysobacter enzymogenes strain C3 and the role of the antibiotic HSAF in the biological control activity. Biol. Control 2018, 117, 158–163. [Google Scholar] [CrossRef]
  100. Zhao, J.; Liu, D.; Wang, Y.Y.; Zhu, X.F.; Xuan, Y.H.; Liu, X.Y.; Fan, H.Y.; Chen, L.J.; Duan, Y.X. Biocontrol potential of Microbacterium maritypicum Sneb159 against Heterodera glycines. Pest Manag. Sci. 2019, 75, 3381–3391. [Google Scholar] [CrossRef]
  101. Xiang, P.; Hao, J.G.; Zhang, W.; Li, B.H.; Lu, W.C. Identification and field control efficacy of biocontrol actinomycetes against Heterodera glycines. Chin. J. Oil Crop Sci. 2017, 39, 234–238. [Google Scholar]
  102. Chen, L.J.; Chen, J.S.; Zheng, Y.N.; Dong, J.; Yu, B.S.; Duan, Y.X. Identification of actinomycetes strain Snea253 and its activity against soybean cyst nematode. Chin. J. Biol. Control 2009, 25, 66–69. [Google Scholar]
  103. Jin, N.; Liu, S.M.; Peng, H.; Huang, W.K.; Kong, L.A.; Peng, D.L. Effect of Aspergillus niger NBC001 on the soybean rhizosphere microbial community in a soybean cyst nematode-infested field. J. Integr. Agric. 2021, 20, 3230–3239. [Google Scholar] [CrossRef]
  104. Jin, N.; Liu, S.M.; Peng, H.; Huang, W.K.; Kong, L.A.; Wu, Y.H.; Chen, Y.P.; Ge, F.Y.; Jian, H.; Peng, D.L. Isolation and characterization of Aspergillus niger NBC001 underlying suppression against Heterodera glycines. Sci. Rep. 2019, 9, 591. [Google Scholar] [CrossRef] [PubMed]
  105. Chen, X.J.; Li, H.X.; Xu, Z.P.; Luo, N.; Han, S.M. Nematocidal activities and species identification of three biocontrol fungi. Soybean Sci. 2019, 38, 576–583. [Google Scholar]
  106. Shinya, R.; Aiuchi, D.; Kushida, A.; Tani, M.; Kuramochi, K.; Koike, M. Pathogenicity and its mode of action in different sedentary stages of Heterodera glycines (Tylenchida: Heteroderidae) by Verticillium lecanii hybrid strains. Appl. Entomol. Zool. 2008, 43, 227–233. [Google Scholar] [CrossRef]
  107. Xu, Y.L.; Lu, J.C.; Song, J. The virulence of 3 parasitic fungi fermentation filtrates on race 4 of soybean cyst nematode. Soils Crops. 2020, 9, 22–30. [Google Scholar]
  108. Chen, L.J.; Liu, B.; Duan, Y.X.; Zhang, G.D. Effect of fermentation filtrate of Beauveria on bio-activities of different nematodes. J. Shenyang Agric. Univ. 2008, 39, 305–308. [Google Scholar]
  109. Zhao, X.H.; Xu, Y.L. Inhibition of Fusarium spp. fermented filtrates on soybean cyst nematode. Soybean Sci. 2011, 30, 471–474. [Google Scholar]
  110. Li, J.X.; Li, H.; Wang, W.H.; Zhu, X.C.; Liu, R.J. Effects of arbuscular mycorrhizal fungal arbuscule development on soybean cyst nematode diseases. J. Qingdao Agric. Univ. 2010, 27, 95–99. [Google Scholar]
  111. Bajaj, R.; Hu, W.M.; Huang, Y.Y.; Chen, S.Y.; Prasad, R.; Varma, A.; Bushley, K.E. The beneficial root endophyte Piriformospora indica reduces egg density of the soybean cyst nematode. Biol. Control 2015, 90, 193–199. [Google Scholar] [CrossRef]
  112. Zhou, Y.Y.; Guo, Y.X.; Duan, Y.X.; Li, H.Y.; Chen, L.J. Prevention effect and photosynthetic performance in Bacillus megaterium Sneb207 against soybean cyst nematode. Soybean Sci. 2020, 39, 605–611. [Google Scholar]
  113. Zhou, Y.Y.; Chen, J.S.; Zhu, X.F.; Wang, Y.Y.; Liu, X.Y.; Fan, H.Y.; Duan, Y.; Chen, L.J. Efficacy of Bacillus megaterium strain Sneb207 against soybean cyst nematode (Heterodera glycines) in soybean. Pest Manag. Sci. 2020, 77, 568–576. [Google Scholar] [CrossRef]
  114. Li, X.M.; Du, C.M.; Zheng, N.; Chi, L.; Pu, Z.G.; Han, D.W.; Wang, L.D. Inhibitory effect of Bacillus BL-21, HNDF2 on soybean cyst nematode. Soybean Sci. 2011, 30, 710–712. [Google Scholar]
  115. Fu, Y.; Li, J.; Zhang, Z.A.; Zhou, Y.Y. Separation and identification of Bacillus sp. Antagonistic to soybean cyst nematode. Heilongjiang Agric. Sci. 2022, 2, 36–40. [Google Scholar]
  116. Wang, Y.Y.; Si, B.B. Virulence of soybean rhizosphere bacteria on Heterodera glycines in Ningxia. Agrochemicals 2016, 55, 844–846. [Google Scholar]
  117. Wang, Y.Y.; Yang, R.W.; Feng, Y.X.; Sikandar, A.; Zhu, X.F.; Fan, H.Y.; Liu, X.Y.; Chen, L.J.; Duan, Y.X. iTRAQ-based proteomic analysis reveals the role of the biological control agent, Sinorhizobium fredii strain Sneb183, in enhancing soybean resistance against the soybean cyst nematode. Front. Plant Sci. 2021, 11, 597819. [Google Scholar] [CrossRef]
  118. Tian, F.; Wang, Y.Y.; Zhu, X.F.; Chen, L.J.; Duan, Y.X. Effect of Sinorhizobium fredii strain Sneb183 on the biological control of soybean cyst nematode in soybean. J. Basic Microbiol. 2014, 54, 1258–1263. [Google Scholar] [CrossRef]
  119. Wang, Y.Y.; Duan, Y.X.; Chen, L.J. Antagonim of rhizobium against pathogens of soybean root. Acta Phytopathol. Sin. 2008, 38, 607–612. [Google Scholar]
  120. Zhao, J.; Xing, Z.F.; Tian, M.X.; Liu, X.Y.; Wang, Y.Y.; Liu, D.; Chen, L.J.; Duan, Y.X. Isolation and identification of nematicidal compound from Microbacterium maritypicum Sneb159. Acta Microbiologica Sin. 2020, 60, 2341–2349. [Google Scholar]
  121. Ma, L.L.; Xu, Y.L.; Li, C.J.; Tai, L.M. Effect of Photorhabdus sp. NJ metabolites on Heterodera glycines. Chin. J. Oil Crop Sci. 2008, 30, 370–373. [Google Scholar]
  122. Liu, C.X.; Zhuang, X.X.; Yu, Z.Y.; Wang, Z.Y.; Wang, Y.J.; Guo, X.W.; Xiang, W.S.; Huang, S.X. Community structures and antifungal activity of root-associated endophytic actinobacteria of healthy and diseased soybean. Microorganisms 2019, 7, 243. [Google Scholar] [CrossRef]
  123. Sun, Z.B.; Sun, M.H.; Zhou, M.; Li, S.D. Transformation of the endochitinase gene Chi67-1 in Clonostachys rosea 67-1 increases its biocontrol activity against Sclerotinia sclerotiorum. AMB Express 2017, 7, 1. [Google Scholar] [CrossRef]
  124. Liu, Z.H.; Yang, Q.; Hu, S.; Zhang, J.D.; Ma, J. Cloning and characterization of a novel chitinase gene (chi46) from Chaetomium globosum and identification of its biological activity. Appl. Microbiol. Biotechnol. 2008, 80, 241–252. [Google Scholar] [CrossRef]
  125. Wang, B.; Liu, X.Y.; Wu, W.P.; Liu, X.Z.; Li, S.D. Purification, characterization, and gene cloning of an alkaline serine protease from a highly virulent strain of the nematode-endoparasitic fungus Hirsutella rhossiliensis. Microbiol. Res. 2009, 164, 665–673. [Google Scholar] [CrossRef]
  126. Zhang, F.L.; Ge, H.L.; Zhang, F.; Guo, N.; Wang, Y.C.; Chen, L.; Ji, X.; Li, C.W. Biocontrol potential of Trichoderma harzianum isolate T-aloe against Sclerotinia sclerotiorum in soybean. Plant Physiol. Bioch. 2016, 100, 64–74. [Google Scholar] [CrossRef]
  127. Bandara, A.Y.; Weerasooriya, D.K.; Bradley, C.A.; Allen, T.W.; Esker, P.D. Dissecting the economic impact of soybean diseases in the United States over two decades. PLoS ONE 2020, 15, e0231141. [Google Scholar] [CrossRef] [Green Version]
Agriculture 12 01391 g001 550
Figure 1. Infection cycle of Sclerotinia sclerotiorum.
Figure 1. Infection cycle of Sclerotinia sclerotiorum.
Agriculture 12 01391 g001
Agriculture 12 01391 g002 550
Figure 2. Infection cycle of Phytophthora sojae.
Figure 2. Infection cycle of Phytophthora sojae.
Agriculture 12 01391 g002
Agriculture 12 01391 g003 550
Figure 3. Infection cycle of Heterodera glycines.
Figure 3. Infection cycle of Heterodera glycines.
Agriculture 12 01391 g003
Agriculture 12 01391 g004 550
Figure 4. Mechanisms of biocontrol agents to suppress soybean common diseases. SSR: Sclerotinia stem rot; PRR: Phytophthora root rot; SCN: soybean cyst nematode.
Figure 4. Mechanisms of biocontrol agents to suppress soybean common diseases. SSR: Sclerotinia stem rot; PRR: Phytophthora root rot; SCN: soybean cyst nematode.
Agriculture 12 01391 g004
Table
Table 1. Overview of biocontrol agents showing control ability against SSR.
Table 1. Overview of biocontrol agents showing control ability against SSR.
Biocontrol MicroorganismsStrain Name and ReferenceApplication Scale
Fungi
Trichoderma harzianumBAFC 742 [28]Field
T-22 [26]Field
Trichoderma asperelloidesT25 [29]Field
T42 [29]Field
37/12 [30]Greenhouse
91/12 [30]Greenhouse
Trichoderma atroviride07/01 [30]Greenhouse
30/12 [30]Greenhouse
Trichoderma koningiopsis62/12 [30]Greenhouse
103/12 [30]Greenhouse
Clonostachys rosea67-1 [31]Greenhouse
BAFC3874 [32]Greenhouse
BAFC1646 [33]Greenhouse
Coniothyrium minitansCON/M/91–08 [26]Field
Sporidesmium sclerotivorumCS-5 [34]Field
Fusarium oxysporumS6 [35]Greenhouse
Myrothecium sp.isolate 2 [36]Greenhouse
Phialomyces macrosporus- [36]Greenhouse
Volutella minima- [36]Greenhouse
Funneliformis mosseaeBEG 12 [37]Greenhouse
Bacteria
Bacillus sp.BA122R [38]Greenhouse
Bacillus amyloliquefaciensMEP218 [39]Greenhouse
ARP23 [39]Greenhouse
BNM340 [40]Pots
Bacillus pumilusBA25R [38]Greenhouse
Bacillus cereusBA78R [38]Greenhouse
BA81R [38]Greenhouse
BA88R [38]Greenhouse
Bacillus subtilisSB01 [41]Field
SB24 [41]Field
QST 713 [27]Field
ZH-2 [34]Field
Lysobacter enzymogenesC3 [42]Greenhouse
Pseudomonas fluorescensBNM296 [40]Growth chamber
Pseudomonas putidaBA15R [38]Greenhouse
Pantoea cypripediiBA45R [38]Greenhouse
Enterobacter sp.BA48R [38]Greenhouse
BA103R [38]Greenhouse
BA110R [38]Greenhouse
BA80R [38]Greenhouse
Enterobacter oryzaeBA106R [38]Greenhouse
Enterobacter asburiaeBA123R [38]Greenhouse
BA203R [38]Greenhouse
Streptomyces sp.NEAU-S7GS2 [43]Greenhouse
Streptomyces somaliensisSSD41 [44]Greenhouse
SSD49 [44]Greenhouse
Streptomyces hydrogenansSSD60 [44]Greenhouse
Streptomyces lydicusWYEC 108 [26]Field
Table
Table 2. Overview of biocontrol agents showing control ability against PRR.
Table 2. Overview of biocontrol agents showing control ability against PRR.
Biocontrol MicroorganismsStrain Name and ReferenceApplication Scale
Fungi
Aspergillus effusus- [59]Pot
Glomus intraradicesBGC BJ09 [60]Chamber
Trichoderma virens- [58]Greenhouse
Trichoderma orientalis- [58]Greenhouse
Trichoderma ceramicum- [58]Greenhouse
Trichoderma atroviride- [58]Greenhouse
Trichoderma koningii- [58]Greenhouse
Trichoderma brevicompactum- [58]Greenhouse
Trichoderma spirale- [58]Greenhouse
Trichoderma pseudokoningii- [58]Greenhouse
Trichoderma viridescens- [58]Greenhouse
Trichoderma harzianum- [58]Greenhouse
Trichoderma asperellum- [58]Greenhouse
Trichoderma koningiopsis- [58]Greenhouse
Trichoderma longibrachiaumT115D [61]Pot
Bacteria
Bacillus subtitlisBY-2 [62]Pot
SN342 [63]Greenhouse
RSS-1 [64]Pot
Bacillus cereusSN340 [63]Greenhouse
Bacillus velezensisSN337 [63]Greenhouse
Bacillus licheniformisSN338 [63]Greenhouse
Bacillus pumilusB048 [65]Pot
Bacillus altitudinisJSCX-1 [66]Greenhouse
Bacillus amyloliquefaciensJDF3 [64]Pot
Bacillus sp.A4 [67]Pot
Pseudomonas sp.A2 [67]Pot
BS1 [68]Greenhouse
Pseudomonas aeruginosaSN339 [63]Greenhouse
Paenibacillus polymyxaS1 [69]Pot
Actinomycetales bacteriumJAX-13 [70]Pot
Streptomyces
93 [71]Pot
15 [71]Pot
GS-8-1 [71]Pot
GS-43-5 [71]Pot
GS-2-21 [71]Pot
PonSSII [71]Pot
Streptomyces sp.JAX-14 [70]Pot
Streptomyces hygroscopicusS11 [72]Greenhouse
Table
Table 3. Overview of biocontrol agents showing control ability against SCN.
Table 3. Overview of biocontrol agents showing control ability against SCN.
Biocontrol MicroorganismsStrain Name and ReferenceApplication Scale
Fungi
Hirsutella rhossiliensisOWVT-1 [81]Greenhouse
ATCC46487 [81]Greenhouse
MO1-1 [81]Greenhouse
FR6-1 [81]Greenhouse
JA9-1 [81]Greenhouse
LE5.1-1 [81]Greenhouse
WT8-1 [81]Greenhouse
MA36.4-1 [81]Greenhouse
ST8-1 [81]Greenhouse
MA30-1 [81]Greenhouse
WT4-1 [81]Greenhouse
MA37-1 [81]Greenhouse
Hirsutella minnesotensisRW7-1 [81]Greenhouse
AS3G1 [80]Pot
WA23-1 [82]Greenhouse
FA2-1 [81]Greenhouse
1-10 [78]Greenhouse
HLJ07-21-3 [78]Greenhouse
Glomus mosseae- [83]Greenhouse
Glomus etunicatum- [83]Greenhouse
Glomus fasiculatum- [84]Greenhouse
Glomus intraradices- [84]Greenhouse
Glomus versiforme- [84]Greenhouse
Gigaspora margarita- [84]Greenhouse
Aspergillus nigerNBC001 [85]Field
Clairoideoglomus claroideum- [86]Greenhouse
Dentiscutata heterogama- [86]Greenhouse
Diversispora eburnean- [86]Greenhouse
Funneliformis mosseae- [86]Greenhouse
Fusarium spp.F-9-3 [87]Greenhouse
F-V-1-4 [87]Greenhouse
F-9 [88]Greenhouse
Paecilomyces lilacinusP-V-7-2 [87]Greenhouse
P-E-13-2 [87]Greenhouse
P-E [88]Greenhouse
Pochonia chlamydosporiumV-25-3 [87]Greenhouse
V-21-2 [87]Greenhouse
Penicillium oxalicumNBC008 [85]Pot
NBC012 [85]Pot
Penicillium janthinellumSnef1650 [89]Field
Purpureocillium sp.E [90]Greenhouse
T [90]Greenhouse
Purpureocillium lilacinumESALQ1744 [91]Greenhouse
ESALQ2482 [91]Greenhouse
ESALQ2593 [91]Greenhouse
Rhizophagus intraradices- [86]Greenhouse
Verticillium chlamydosporiumV-25 [88]Greenhouse
Bacteria
Bacillus altitudinisBal13 [92]Field
Bacillus subtilisBsssu2 [92]Field
Bacillus aryabhattaiSneb517 [93]Field
Bacillus mojavensisBmo3 [92]Greenhouse
Bacillus megateriumSneb207 [94]Field
Sneb482 [95]Field
Bacillus safensisBsa27 [92]Field
Bacillus simpleSneb545 [95]Field
Bacillus velezensisBve12 [92]Field
Bve2 [92]Field
Bacillus thuringiensis- [96]Field
Bacillus sp.Snb2 [97]Greenhouse
Klebsiella pneumoniaeSnebYK [98]Field
Sinorhizobium frediiSneb183 [95]Field
Lysobacter enzymogenesC3 [99]Pot
Microbacterium maritypicumSneb159 [100]Field
Streptomyces sp.XFS-4 [101]Field
XFS-5 [101]Field
CL-4 [101]Field
XS-3 [101]Field
BJ-4 [101]Field
XF-5 [101]Field
Streptomyces venezuelaeSnea253 [102]Field
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Yu, S.-F.; Wang, C.-L.; Hu, Y.-F.; Wen, Y.-C.; Sun, Z.-B. Biocontrol of Three Severe Diseases in Soybean. Agriculture 2022, 12, 1391. https://doi.org/10.3390/agriculture12091391

AMA Style

Yu S-F, Wang C-L, Hu Y-F, Wen Y-C, Sun Z-B. Biocontrol of Three Severe Diseases in Soybean. Agriculture. 2022; 12(9):1391. https://doi.org/10.3390/agriculture12091391

Chicago/Turabian Style

Yu, Shu-Fan, Chu-Lun Wang, Ya-Feng Hu, Yan-Chen Wen, and Zhan-Bin Sun. 2022. "Biocontrol of Three Severe Diseases in Soybean" Agriculture 12, no. 9: 1391. https://doi.org/10.3390/agriculture12091391

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop