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Review

Biological Control of the Cucumber Downy Mildew Pathogen Pseudoperonospora cubensis

by
Zhanbin Sun
1,*,
Shufan Yu
1,
Yafeng Hu
1 and
Yanchen Wen
2,*
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
*
Authors to whom correspondence should be addressed.
Horticulturae 2022, 8(5), 410; https://doi.org/10.3390/horticulturae8050410
Submission received: 23 March 2022 / Revised: 2 May 2022 / Accepted: 2 May 2022 / Published: 6 May 2022
(This article belongs to the Section Plant Pathology and Disease Management (PPDM))
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Abstract

:
Cucumber downy mildew (CDM) is a destructive plant disease caused by the air-borne oomycete pathogen Pseudoperonospora cubensis. CDM causes severe yield reduction of cucumber and significant economic losses. Biocontrol is a promising method to control CDM with the advantage of being beneficial to sustainable agricultural development. However, until now, no reviews of biocontrol of CDM have been reported. The objective of this review is to more comprehensively understand the biocontrol of CDM. In this review, the biological characteristics of P. cubensis are introduced, and strategies for screening biocontrol agents to suppress CDM are recommended. Then the current biocontrol agents, including fungi such as Trichoderma and biocontrol bacteria such as Bacillus, which possess the ability to control CDM, and their control characteristics and ability against CDM are also summarized. The potential mechanisms by which these biocontrol agents prevent CDM are discussed. Finally, several suggestions for future research on the biocontrol of CDM are provided.

1. Introduction

Cucumber downy mildew (CDM), caused by the oomycete Pseudoperonospora cubensis (Berk. et Curt.) Rostov., is an airborne foliar disease with characteristics of rapid spread and crop destruction [1,2,3]. CDM severely affects the quality and yield of cucumber in all growing areas and results in significant economic losses [4,5,6,7,8]. CDM is distributed worldwide and occurs in both the seedling and adult plant stages of cucumber [9,10,11,12,13]. When the cucumber plant is infected by P. cubensis, the upper side of the leaf surface exhibits yellowish-brown lesions with irregular form, and gray sporangium layers appear on the lower side of the leaf surface under high humidity. Multiple lesions merge after serious infection, which causes the leaves to turn yellow and wither [14,15,16,17,18]. The reduction in cucumber yield caused by CDM is detrimental if no control countermeasures are applied in the early infection stage of P. cubensis. The damage of CDM to cucumber yield and quality increases over time, and CDM has become an important factor limiting the yield and quality of cucumbers [19,20,21,22,23].
Effective control methods are important to reducing the damage caused by CDM. Currently, common methods used to control CDM include chemical control, planting of CDM-resistant cucumber varieties, and biocontrol. Chemical control is one of the most widely used and effective methods to control CDM. Different kinds of fungicides, including azoxystrobin, fenamidone, dimethomorph, pyraclostrobin, and cyazofamid, are commonly used to control CDM [24,25,26,27,28]. However, frequent use of fungicides is costly and may result in environmental and food-safety concerns [29,30,31]. Moreover, the long-term use of fungicides may result in resistance of P. cubensis, which could be solved by developing or rotating new types of fungicides [32,33,34,35,36]. One additional approach to control CDM is to plant resistant varieties [37,38,39,40,41]. However, developing resistant varieties is time-consuming, and the existing resistant cultivars are limited and cannot satisfy market requirements. Biocontrol is another potential way to manage CDM. Biocontrol mainly utilizes mechanisms such as competition, antagonism, or the production of secondary metabolites by microorganisms to control CDM. Several kinds of biocontrol microorganisms have been reported to exhibit control efficacy against CDM. At present, many reviews of managing CDM by chemical control and cultivation of resistant cultivars have been reported. However, no reviews for biocontrol of CDM exist.
The aim of this review was to summarize and analyze the research by using biocontrol methods to suppress CDM. First, we introduce the biological characteristics of the CDM pathogen P. cubensis. Second, the review presents a strategy of how to effectively screen biocontrol agents to control CDM. Then biocontrol agents with the ability to control CDM are also introduced, as well as their potential control mechanisms. Finally, some suggestions are presented for improving the control ability of CDM by using biocontrol. Overall, this review provides a basis for the broader application of biocontrol to manage CDM.

2. Pseudoperonospora cubensis

Pseudoperonospora cubensis was first described by Berkeley in Cuba in 1868 [42]. Current taxonomic classification indicates that P. cubensis belongs to Stramenopiles (kingdom), Oomycota (phylum), Oomycetes (Class), Peronosporales (order), Peronosporaceae (family), and Pseudoperonospora (genus) [43]. Sporangiophores, sporangia, and zoospores are produced by P. cubensis through asexual reproduction and are essential for infection [44,45,46,47]. In addition, P. cubensis can also generate oospores according to sexual reproduction, but the role of oospores in the P. cubensis disease cycle remains unknown [48,49,50,51,52,53]. Sporangia of P. cubensis can be dispersed by wind, rain, insects, or farm implements [54,55,56,57]. Pseudoperonospora cubensis can infect more than 20 Cucurbit genera and 60 species [58,59,60]. As a strict obligate parasite, P. cubensis depends on living host tissue to grow, survive, reproduce, and disperse [61,62,63].
The infection cycle of P. cubensis starts when the sporangia touch the surface of the cucumber leaf (Figure 1). Sporangia can produce zoospores to achieve infection [64,65,66]. Zoospores can germinate and form germ tubes to infect cucumber leaves via stomata [67]. The mycelium grows intercellularly in cucumber leaves and, if environmental conditions are favorable, forms sporangiophores. Then sporangia are generated at the terminus of the sporangiophore branch [68]. Finally, the generated sporangia can continue to proceed with the infection cycle through wind or other dispersion mechanisms [69]. Temperature and humidity are the main factors that influence the infection efficiency of P. cubensis. Germination and infection occur at 5 to 28 °C, with 15 °C being the optimal infection temperature. A relative humidity higher than 90% is suitable for the occurrence of CDM [16,70,71,72,73,74].
Understanding the infection mechanism of P. cubensis is critical for further improving the control ability of CDM. A transcriptome analysis of P. cubensis–infected cucumber in different stages showed that numerous genes were differentially expressed during the process of P. cubensis infection. Among these differentially expressed genes, genes encoding hydrolytic enzymes, including proteinases, lipases, and carbohydrate active enzymes, might be involved in the damage of P. cubensis to the cucumber host [75]. In addition, genes encoding RXLR-type effectors, which play important roles in the virulence of P. cubensis, were also found [76]. Research showed that the RXLR effector protein-encoding gene PscRXLR1 was upregulated at the early infection stages of P. cubensis [77]. Moreover, P. cubensis suppressed cucumber defense responses by reducing the expression levels of host-defense-response-related genes, such as lipoxygenase, cationic peroxidases, and cinnamate 4-hydroxylases in cucumber [75,78].

3. Strategy of Screening Biocontrol Agents

In contrast to other phytopathogens, as a strict obligate parasite, P. cubensis cannot survive on artificial growth media. Therefore, screening biocontrol agents that are effective against P. cubensis cannot directly use the traditional plate confrontation assay. Investigating the control ability of biocontrol agents against P. cubensis can only be performed on living plants, including leaf disc assays, detached leaf assays, and field trials. A sporangium release inhibition method was also used to evaluate the control effect of biocontrol agents against P. cubensis. Compared with the convenience advantage brought by plate confrontation screening, it is difficult to screen biocontrol agents on a large scale by using living plants. Therefore, the selection of an appropriate screening strategy for biocontrol agents against P. cubensis is very important for improving screening efficiency.
Currently, there are two main strategies for screening biocontrol agents against P. cubensis. The first method is to isolate a range of microorganisms from environmental materials without restrictions. Then a criterion is established to narrow the quantity and species for the control assay of P. cubensis. The criterion for screening biocontrol microorganisms could be set as follows: investigating the production ability of enzymes or metabolites that are harmful to P. cubensis or evaluating the antagonistic effects on alternative oomycete pathogens, which have a close evolutionary relationship and similar pathogenesis mechanism, as does P. cubensis. Zheng et al. [79] isolated 163 bacterial strains from different microenvironments, including the leaf interior, phyllosphere, rhizosphere, and bulk soils, from healthy and diseased plants. Finally, 19 bacterial isolates were selected to further investigate the control efficacy of CDM. The selection criteria could be summarized as follows: these bacterial strains were representative, for which they were derived from all isolated samples, and the relationship among these bacterial strains had high genetic diversity. Furthermore, these bacterial strains produced extracellular hydrolytic enzymes, such as chitinase, protease, and cellulase, which may be involved in controlling P. cubensis.
Another method is to choose a field where CDM is present at a high incidence. Then microorganisms in plant tissues or soils from asymptomatic plant areas are screened. This is mainly because P. cubensis is an airborne pathogen, and most plants should be infected if no biocontrol agents existed. Therefore, uninfected plants or the surrounding soil might contain microorganisms that potentially control CDM. Sun et al. [80] isolated 81 leaf endophytic bacteria from healthy cucumber plants in areas where most plants were infected by P. cubensis. Then these isolates were used to evaluate their ability to control CDM. Similarly, Bacillus licheniformis HS10 originated from a healthy cucumber rhizosphere, from which the surrounding plants were seriously infected.
In this review, “Cucumber downy mildew” and “Pseudoperonospora cubensis” were set as keywords in searching the Web of Science and PubMed. Manuscripts about the biological characters, infection cycle, and mechanism of P. cubensis symptoms, damage, epidemiology, and control methods were reviewed, especially all the articles related to biocontrol of CDM, were included.

4. Biocontrol Agents

As a potentially sustainable control method, biological control has attracted widespread attention. To date, only a few fungal genera, including Trichoderma, Pestalotiopsis, and Fusarium, and numerous bacterial genera, including Bacillus, Paenibacillus, Enterobacter, Streptomyces, Pseudomonas, Derxia, and Aneurinibacillus, have exhibited biocontrol ability against CDM (Table 1).

4.1. Biocontrol Fungi

Trichoderma spp. are excellent biocontrol agents that are effective against numerous plant pathogens. The mechanism of action of Trichoderma against pathogens mainly depends on the secretion of cell-wall-degrading enzymes, including chitinase, chitosanase, glucanase, and proteases; the production of secondary metabolites; and the induction of plant resistance [81,82,83,84,85]. Many studies have shown that different Trichoderma species have the ability to control CDM. Trichoderma harzianum was the most reported species that could effectively control CDM. In some studies, the biocontrol ability of T. harzianum against CDM was similar to the chemical treatment in different cucumber growth stages. A single application of T. harzianum at the seventh week decreased the percentage of infection of cucumber plants with CDM (11.0%) compared with the control treatment (99.7%) [86]. Moreover, the growth and yield parameters of cucumber in the T. harzianum treatment were increased compared with the control, including plant length, leaf weight, leaf area, total chlorophyll, fruit number (19.3 vs. 33.3 per plant), and plant yield (1.5 vs. 3.4 kg) [87]. El-Khalily et al. investigated the ability of two Trichoderma species, T. harzianum and T. viride, to control CDM. Both agents exhibited control ability against CDM at 90 days after planting [88]. Differences in disease incidence were observed between the two fungi, ranging from 44.3 to 66.7%. Alvarado-Aguayo et al. recommend a 500 g/ha dose of T. harzianum for suitable control of CDM compared with other doses [89]. The application of T. harzianum/P. fluorescens decreased the percentage of CDM infection in cucumber plants. Treated plants showed only 7.4% CDM severity compared with 95% recorded in the untreated control at the seventh week and increased the yield (843.3 g in control and 1565.7 g in T. harzianum/P. fluorescens treatment), vegetative fresh weight (302.0 vs. 396.0 g), and plant length (143.3 vs. 148.7 cm) [86].
Other Trichoderma species also exhibited control ability against CDM. Applications of T. asperellum reduced the damage caused by P. cubensis [90]. Trichoderma atroviride TRS25 diminished the incidence of CDM and elicited a host defense response in cucumber plants. In addition, the usage of TRS25 was beneficial to cucumber growth, including increasing germination (65.9 ± 4.2 seeds per plot in control; 84.6 ± 2.5 in TRS25 treatment), and shoot fresh weight (19.2 ± 0.6 vs. 39.1 ± 1.4 g per plant) compared with the untreated control [91]. The mixture of T. hamatum and T. harzianum improved the control of CDM and enhanced the number of fruit (19 in mixture application; 18.3, 17, and 18 per plant in single use of each species, respectively) and weight of fruits (3.4 kg in mixture application; 3.1, 2.9, and 3.0 kg per plant in single use of each species, respectively) at 6 weeks after sowing [92].
Two endophytes, Pestalotiopsis and Fusarium, were isolated from the leaves of Pyrethrum cineraryiifolium Trev. Their fermentation products were then used to investigate the control ability of CDM both in protective and therapeutic application. The results showed that both species exhibited protective and therapeutic control ability against CDM [93,94]. Two Fusarium strains, FO47 and FO47B10, exhibited 64.0 and 61.8% control efficacy against CDM at the preliminary disease stage. In addition, FO47B10 improved the growth and development of cucumber, including seeding survival, root length, chlorophyll content, and aboveground fresh weight of individual plants and single plant yield [95].

4.2. Biocontrol Bacteria

Bacillus is a promising biocontrol agent that can protect against many pathogens via the mechanisms of competition for nutrition and space, secretion of antimicrobial substances, and induced plant resistance [96,97,98,99,100]. Different Bacillus species exhibited biocontrol effects against CDM. Both B. subtilis (37.5 ± 2.6%) and B. pumilus (34.1 ± 2.1%) decreased the disease severity of CDM compared with the control (91.1 ± 1.4%). Moreover, the application of B. subtilis and B. pumilus increased the chlorophyll content and peroxidase and polyphenoloxidase activities of cucumber plants [101]. A similar phenomenon was found in another B. subtilis strain, and the disease severity of CDM was lower by using B. subtilis (17.2%) compared with the control (30.0%) at 5 weeks. Plant growth parameters, including plant length, total chlorophyll, leaf number, leaf weight, and leaf area; and yield parameters, including plant yield (1.5 vs. 3.6 kg), fruit length (13.0 vs. 17.7 cm), fruit diameter (1.9 vs. 2.7 cm), and shelf life, were also higher in response to the application of B. subtilis compared with the control [87].
In addition to B. subtilis, other Bacillus species also exhibited biocontrol ability against CDM. Bacillus licheniformis HS10 was isolated from a healthy cucumber rhizosphere, and its crude protein extract exhibited 60.1% control efficacy against CDM [102]. The activity of the plant defense enzymes PAL and POD was increased after spraying HS10. An antifungal protein was purified from HS10 and suppressed P. cubensis on cucumber leaves [103]. Bacillus pumilus DS22 and B. licheniformis HS10 were isolated from soils of diseased and healthy cucumber plants, respectively. Both isolates reduced the disease severity of CDM at 8 dpt (days post treatment) and 21 dpt and increased the height (DS22: 28.6 ± 1.3 cm, HS10: 33.2 ± 4.2 cm, Control: 26.8 ± 4.5 cm) and dry weight of cucumber plants (DS22: 5.3 ± 0.1 g, HS10: 4.9 ± 0.4 g, Control: 4.2 ± 0.5 g) [79].
For other Bacillus species, both the fermentation broth and fermentation filtrate of B. velezensis achieved higher control levels against CDM than chemical pesticides. The concentration of the fermentation filtrate of B. velezensis without any dilution was more suitable for control of CDM compared with diluted concentrations [104]. Bacillus chitinosporus isolated from cucumber roots reduced the severity of CDM from 10.8 to 5.9% after 35 days. Further studies showed that metabolites from B. chitinosporus caused damage to the development of P. cubensis, including twisting, turgor loss, and sporangiophore collapse [105]. Separate leaf assays, sporangium release inhibition assays, and field experiments were conducted to investigate the biocontrol ability of Bacillus strains CE8, Z-X-3, and Z-X-10 against CDM, and all the strains exhibited control ability that was better than chemical pesticides and the control treatment [80,106].
Pseudomonas, Streptomyces, and Paenibacillus are also very important for controlling plant diseases [107,108,109,110,111]. A single application of Ps. fluorescens exhibited lower percentage of disease severity of cucumber plants with CDM (6%) than the control (95%) in the greenhouse. Pseudomonas fluorescens was beneficial for the improvement of yield and biomass of cucumber plants compared with the control [86]. The application of other Ps. fluorescens strains also reduced the incidence of CDM and improved the growth and yield parameters [87,92,107,108]. Streptomyces can produce fungicidal metabolites that may be harmful to pathogens. A Streptomyces strain was isolated from soil, and the fermentation broth inhibited the germination of P. cubensis sporangia and improved the control ability against CDM (63.9%) [109]. Another spent forest mushroom compost-derived strain, S. padanus PMS-702, reduced the severity of CDM compared with the control, and the 10-fold dilution suspension inhibited the germination of P. cubensis sporangia [112]. In addition, the usage of Pa. polymyxa effectively controlled CDM. The concentration of Pa. polymyxa P1 was positively correlated with the control ability of CDM in the field experiment and was higher (89.9 ± 2.2% for P1 in the highest application dose) than that of chemical pesticides (74.9 ± 2.7%) [111].
Other bacterial biocontrol agents are seldom reported to be involved in CDM control. Aneurinibacillus migulanus reduced disease severity of CDM (54%) compared with the control (94%) [113]. Another A. migulanus strain reached 92% efficacy to control CDM [114]. For Enterobacter cloacae, application improved seed germination at the 3rd day (82% in treatment and 39% in control) and cucumber yield (6200 kg in treatment and 4550 kg in control). Both the single usage of E. cloacae (88%) or a mixture of E. cloacae strains and fungicides (96.6%) had control ability against CDM [115]. Enterobacter strain DP14 controlled CDM in two sequential years. DP14 also promoted cucumber plant growth, including height, leaf area, fresh and dry weight, and single fruit weight [79]. Derxia gummosa reduced the disease severity of CDM (18.1%) compared with the control (30.0%) and increased the growth characteristics of plant length, total chlorophyll, leaf weight and area, and fresh and dry weight, as well as yield parameters of plant yield, fruit length, and diameter [87].

5. Biocontrol Mechanisms against CDM

Understanding the biocontrol mechanism is critical for further improving the control ability of CDM. Currently, several mechanisms have been reported to be involved in the biocontrol of CDM (Figure 2). The production of hydrolytic enzymes or metabolites, and induced plant resistance are two main mechanisms involved in controlling CDM. The biocontrol agents T. harzianum and Ps. fluorescence secrete degrading enzymes such as glucanase or produce secondary metabolites, which are crucial for antifungal effects [86]. Bacillus licheniformis HS10 has the ability to produce the hydrolytic enzymes protease, chitinase, and cellulase, which are important for controlling CDM [103]. Metabolites from B. chitinosporus resulted in the collapse of sporangiophores of P. cubensis [105]. Similarly, secondary metabolites produced by S. padanus affected the germination of P. cubensis sporangia [112].
Trichoderma atroviride TRS25 exhibited control ability against CDM. The activities of plant defense enzymes such as guaiacol peroxidase, ascorbate peroxidase, and phenylalanine ammonia lyase in cucumber leaves were increased after the application of TRS25 [91]. One reason for the high control ability of TRS25 might be the stimulation of host resistance by TRS25. The activity of phenylalanine ammonia lyase was increased by the usage of B. licheniformis HS10 in cucumber plants, which might enhance plant defenses, thus reducing the damage caused by P. cubensis [79]. Similar results were reported for B. subtilis, Ps. fluorescens, T. harzianum, D. gummosa, and B. pumilus, the application of which increased the activities of some defense enzymes in cucumber, peroxidase, and polyphenoloxidase [101,108].
Competition for space or nutrients with P. cubensis is another important mechanism for biocontrol agents to suppress CDM. The ability of B. subtilis to control CDM is mainly caused by its strong space-occupying capacity on plants, thereby preventing pathogen colonization [92,116]. In addition, Ps. fluorescens has a powerful competitive ability to utilize iron, which is important for pathogen growth and pathogenic capacity [92,117]. Moreover, the supernatant of A. migulanus accelerated the drying period of leaves, along with the inhibition of zoospore release and dispersion of pathogens [113]. Sometimes, a mixture of different biocontrol agents provided higher control ability against CDM, which might be due to synergistic effects. Functions from different biocontrol agents include inducing host resistance, producing antifungal compounds, or mycoparasitism [92].

6. Conclusions and Prospects

CDM is a destructive oomycete plant disease that causes a serious reduction in cucumber production and economic loss. Biocontrol may be an effective way to control CDM because it has the advantage of being environmentally friendly and contributing to sustainable agricultural development. Numerous biocontrol agents, such as Trichoderma, Bacillus, Paenibacillus, Enterobacter, Streptomyces, and Pseudomonas, exhibited control of CDM. To comprehensively understand the biocontrol of CDM, this review focuses on the strategy of screening biocontrol agents, control characteristics, and efficacy against CDM by different biocontrol agents, as well as the potential biocontrol mechanisms. This review should provide useful information for the further application of biocontrol agents to suppress CDM.
Although the application of biocontrol agents to prevent fungal and oomycete plant diseases has been widely reported, controlling CDM by using biocontrol methods has seldom been studied. Future suggestions are provided as follows for further extensive application of biocontrol agents to prevent CDM:
(1)
Study the molecular mechanism by which biocontrol agents prevent CDM. This could include investigating the transcriptome of biocontrol agents and analyzing the differentially expressed genes in biocontrol agents during the process of controlling CDM. The functions of differentially expressed genes in biocontrol agents preventing CDM can be studied through gene knockout, silencing, or overexpression.
(2)
Expand the variety and amount of biocontrol agents that effectively control CDM. Compared with controlling fungal plant diseases, the variety and amount of biocontrol agents that suppress CDM are small. The selection of a suitable screening method could be an effective way to expand the variety and amount of biocontrol agents. Another way is to investigate the control ability of CDM by known biocontrol agents with significant control ability against other fungal and oomycete plant diseases, e.g., other Bacillus strains, Clonostacys rosea, and Coniothyrium minitans [118,119,120].
(3)
Improve the control efficacy of existing biocontrol agents suppressing CDM. Several methods could be applied. One approach is to optimize the culture and inoculation conditions. In addition, genetic manipulations such as mutagenesis or genetic engineering could be used to improve the control ability of biocontrol agents suppressing CDM.
(4)
Study the synergistic effect of integrating multiple biocontrol agents or combining biocontrol agents and fungicides. We can expect to reach an ideal control efficacy for CDM by optimizing the proportion of each component.
(5)
Develop biocontrol agent products. Although many potential biocontrol agents were screened, commercially available products are very few. Therefore, developing biocontrol agent products is crucial for the wide application of biocontrol agents to control CDM.

Author Contributions

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

Funding

This study was supported by Science and Technology general project of Beijing municipal education commission (KM202110011002).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Infection cycle of Pseudoperonospora cubensis.
Figure 1. Infection cycle of Pseudoperonospora cubensis.
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Figure 2. Mechanisms of biocontrol agents to suppress cucumber downy mildew caused by Pseudoperonospora cubensis.
Figure 2. Mechanisms of biocontrol agents to suppress cucumber downy mildew caused by Pseudoperonospora cubensis.
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Table
Table 1. Overview of biocontrol agents showing control ability against cucumber downy mildew.
Table 1. Overview of biocontrol agents showing control ability against cucumber downy mildew.
Biocontrol MicroorganismsStrain NameApplication TypesApplication ScaleApplication MannerApplication FrequencyInvestigated TimeDisease Severity 2Disease Severity 1Disease Index ScaleDisease Index 2Disease Index 1
Fungi
Trichoderma harzianum1 [92]Live organismGreenhouseSprayEvery three weeks—1265.7———
2 [92]Live organismGreenhouseSprayEvery three weeks—12.765.7———
— [86]Live organismPlastic houseSpraySuccessiveSeven weeks7.795———
— [87]Live organismGreenhouseSprayEvery week Five weeks after application17.230———
— [88]Live organismGreenhouseSprayEvery week 90 days from planting19.3100———
Trichoderma atrovirideTRS25 [91]Live organismFieldSeed treatmentOnceHarvest40% lower than CK————
Trichoderma viride— [88]Live organismGreenhouseSprayEvery week90 days from planting40.8100———
Trichoderma hamatum2 [92]Live organismGreenhouseSprayEvery three weeks—11.765.7———
Fusarium oxysporumFO47 [95]Live organismGreenhouseSoil mixOnce7 days after inoculation of P. cubensis——0–46.718.6
FO47B10 [95]Live organismGreenhouseSoil mixOnce7 days after inoculation of P. cubensis——0–47.118.6
Y2 [94]Fermentation supernatantGreenhouseSprayOnce7 days after application——0–427.867.3
Pestalotiopsis microsporaY1 [93]Fermentation supernatantGreenhouseSprayOnce———0–413.942.6
Bacteria
Bacillus subtilis4 [92]Live organismGreenhouseSprayEvery three weeks—15.765.7———
— [87]Live organismGreenhouseSprayEvery week Five weeks after application17.230———
— [101]Live organismGreenhouseSprayEvery 10 days One week after the last spray32.888.3———
Bacillus pumilusDS22 [79]Live organismFieldSprayEvery 10 days 15 days after application4.620.2———
— [101]Live organismGreenhouseSprayEvery 10 days One week after the last spray35.288.3———
Bacillus licheniformisHS10 [79]Live organismFieldSprayEvery 10 days 15 days after application5.520.2———
Bacillus asahiiCE8 [80]Live organismFieldSprayOnce7–12 days after application——0–941.170.9
Bacillus velezensisHMQAU19044 [104]Live organismPot experimentSprayOnce7 days after application——0–931.377.8
HMQAU19044 [104]Fermentation filtratePot experimentSprayOnce7 days after application——0–915.9877.8
Bacillus chitinosporus— [105]MetabolitesPlastic houseSprayEvery week 35 days after application5.910.8———
Bacillus sp.HP4 [79]Live organismFieldSprayEvery 10 days 15 days after application11.620.2———
Z-X-3 [106]Fermentation supernatantGreenhouseSprayEvery 6 days ———0–40.50.8
Z-X-10 [106]Fermentation supernatantGreenhouseSprayEvery 6 days ———0–40.50.8
Streptomyces sp.NO.24 [109]—Pot experimentSprayOnce7 days after application———13.838.3
Pseudomonas fluorescens4 [92]Live organismGreenhouseSprayEvery three weeksFive weeks after application20.765.7———
Pf1 [107]Filtrate productFieldSpray————0–58.944.6
— [86]Live organismPlastic houseSpraySuccessiveSeven weeks695———
— [87]Live organismGreenhouseSprayEvery week Five weeks after application16.730———
Enterobacter cloacae— [115]Live organismGreenhouseSpray—————10.385.6
Enterobacter sp.DP14 [79]Live organismFieldSprayEvery 10 days15 days after application5.620.2———
Paenibacillus polymyxaP1 [111]Live organismFieldSprayEvery 7 days 7 days after the last application——0–92.524.7
Derxia gummosa— [87]Live organismGreenhouseSprayEvery week Five weeks after application18.130———
Note: “—” represents not available. Disease Index 1 and Index 2 mean disease index in CK group and treatment group, respectively. Disease Severity 1 and Disease Severity 2 mean disease severity (%) in CK group and treatment group, respectively. Representative data from each work in the literature are shown.
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MDPI and ACS Style

Sun, Z.; Yu, S.; Hu, Y.; Wen, Y. Biological Control of the Cucumber Downy Mildew Pathogen Pseudoperonospora cubensis. Horticulturae 2022, 8, 410. https://doi.org/10.3390/horticulturae8050410

AMA Style

Sun Z, Yu S, Hu Y, Wen Y. Biological Control of the Cucumber Downy Mildew Pathogen Pseudoperonospora cubensis. Horticulturae. 2022; 8(5):410. https://doi.org/10.3390/horticulturae8050410

Chicago/Turabian Style

Sun, Zhanbin, Shufan Yu, Yafeng Hu, and Yanchen Wen. 2022. "Biological Control of the Cucumber Downy Mildew Pathogen Pseudoperonospora cubensis" Horticulturae 8, no. 5: 410. https://doi.org/10.3390/horticulturae8050410

APA Style

Sun, Z., Yu, S., Hu, Y., & Wen, Y. (2022). Biological Control of the Cucumber Downy Mildew Pathogen Pseudoperonospora cubensis. Horticulturae, 8(5), 410. https://doi.org/10.3390/horticulturae8050410

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