Next Article in Journal
Concordance of Chest Radiography and Chest Computed Tomography Findings in Patients with Hematologic Malignancy and Invasive Mucormycosis: What Are the Prognostic Implications?
Previous Article in Journal
Morpho-Molecular Identification of Fusarium equiseti and Fusarium oxysporum Associated with Symptomatic Wilting of Potato from Pakistan
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
JoF
Volume 10
Issue 10
10.3390/jof10100702
jof-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
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

The Potential of Microorganisms for the Control of Grape Downy Mildew—A Review

by
Zhan-Bin Sun
1,
Han-Jian Song
1,
Yong-Qiang Liu
2,
Qing Ren
1,
Qi-Yu Wang
1,
Xiao-Feng Li
1,
Han-Xu Pan
1,* and
Xiao-Qing Huang
2,*
1
School of Light Industry Science and Engineering, Beijing Technology and Business University, Beijing 100048, China
2
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
*
Authors to whom correspondence should be addressed.
J. Fungi 2024, 10(10), 702; https://doi.org/10.3390/jof10100702
Submission received: 3 September 2024 / Revised: 27 September 2024 / Accepted: 6 October 2024 / Published: 8 October 2024
(This article belongs to the Section Fungi in Agriculture and Biotechnology)
Browse Figures
Versions Notes

Abstract

:
Plasmopara viticola (Berk.et Curtis) Berl. Et de Toni is the pathogen that causes grape downy mildew, which is an airborne disease that severely affects grape yield and causes huge economic losses. The usage of effective control methods can reduce the damage to plants induced by grape downy mildew. Biocontrol has been widely used to control plant diseases due to its advantages of environmental friendliness and sustainability. However, to date, only a few comprehensive reviews on the biocontrol of grape downy mildew have been reported. In this review, we summarize the biological characteristics of P. viticola and its infection cycle, followed by a detailed overview of current biocontrol agents, including bacteria and fungi that could be used to control grape downy mildew, and their control effects. Furthermore, potential control mechanisms of biocontrol agents against grape downy mildew are discussed. Lastly, suggestions for future research on the biocontrol of grape downy mildew are provided. This review provides the basis for the application of grape downy mildew biocontrol.

1. Introduction

As an important economic fruit, grapes possess significant nutritional value and are rich in minerals, vitamins, and amino acids. Grapes also hold crucial economic value and serve as primary sources in many local agricultural economies. However, grape cultivation is often influenced by a number of different diseases, including grape downy mildew, grape anthracnose, grape gray mold, grape white rot, and other diseases [1,2,3,4]. Among these grape diseases, grape downy mildew is a significant threat. Grape downy mildew is caused by the obligate parasitic oomycetes Plasmopara viticola (Berk.et Curtis) Berl. Et de Toni [5]. Infection with grape downy mildew can lead to reductions in grape yield, with severe cases resulting in 70–80% yield losses, or in some cases, no harvest produced [6]. In addition to impacting grape yields, grape downy mildew can also cause serious economic losses [7].
At present, methods for controlling grape downy mildew include chemical control, the development of resistant varieties, and biological control. Chemical control is a commonly used control method with the advantage of quickly and efficiently preventing the occurrence and development of grape downy mildew. Several pesticides, including azoxystrobin, dimethomorph, and picoxystrobin, have been reported to be involved in controlling grape downy mildew [8,9,10]. However, the use of chemical pesticides can cause severe environmental pollution. Moreover, the long-term use of pesticides can also enhance pathogens’ resistance to pesticides, which limits the application of chemical control agents. The development of disease-resistant grape varieties can improve the resistance of plants to grape downy mildew. A number of grape downy mildew-resistant varieties have been developed [11,12]. However, due to geographical differences in the cultivation of disease-resistant grape varieties, the development of disease-resistant varieties that are suitable for different geographical environments is limited. As a green and sustainable control method, biological control (biocontrol) has attracted considerable attention.
Biocontrol commonly refers to the control of plant diseases by using beneficial biological agents. Compared with chemical control, the advantage of biocontrol is that it does not pollute the environment, in addition to its sustainable usage. With regard to the biocontrol of plant diseases, several microorganisms, including bacteria and fungi, have exhibited excellent plant disease-control capabilities. Once biocontrol microorganisms are inoculated into plants or the surrounding soil, they can continue to prevent disease through their own growth and passage. Bacillus is the most widely reported bacterial agent used for biocontrol. Several Bacillus species—B. subtilis, B. thuringiensis, B. velezensis, B. amyloliquefaciens, and B. aryabhattai—exhibit effective control capabilities against different types of plant diseases [13,14,15,16,17]. Other bacterial species, such as Pseudomonas, Streptomyces, and Paenibacillus, are also reported as biocontrol agents against plant diseases [18,19,20]. Trichoderma is the most commonly reported species of biocontrol fungus. Species such as T. harzianum, T.virens, T. atroviride, T. hamatum, and T. longibrachiatum are reported to be involved in plant disease control [21,22,23,24,25]. In addition to Trichoderma, other fungal species such as Clonostachys rosea, Coniothyrium minitans, Beauveria bassiana, and Metarhizium anisopliae also act as biocontrol agents and play important roles in the control of plant diseases [26,27,28,29]. In addition to the biocontrol effect, many biocontrol microorganisms can also promote plant growth, thereby playing a dual effect in disease prevention and growth promotion [30,31].
Biocontrol microbial agents mainly exhibit their plant disease-control capabilities through the following mechanisms: competition for space and nutrients with pathogens, the secretion of enzymes such as cell wall-degrading enzymes, the production of metabolites such as toxins or antibiotics, inducing plant systemic resistance against plant diseases, and directly parasitizing the host pathogen in some special biocontrol agents. To date, a number of biocontrol microorganisms, such as Bacillus and Trichoderma, have been reported to be involved in controlling grape downy mildew, in addition to reports on their control mechanisms [32,33]. However, only a few systematic reviews on the biological control of grape downy mildew have been reported.
Therefore, in this review, we mainly focus on advances in the biocontrol of grape downy mildew. The biological characteristics and infection cycle of P. viticola are introduced first, in addition to the symptoms of grape downy mildew. Secondly, biocontrol agents currently employed against grape downy mildew are discussed. Thirdly, and most importantly, we provide a detailed introduction to the biocontrol agents, including bacteria and fungi, used for controlling grape downy mildew, and their control efficacy. Fourthly, the potential mechanisms of biocontrol agents in controlling grape downy mildew are discussed. Lastly, an analysis of the problems present in the biocontrol of grape downy mildew, along with corresponding countermeasures and potential further directions for grape downy mildew biocontrol, are discussed. This review provides the basis for the application of grape downy mildew biocontrol.

2. Biological Characteristics of Plasmopara viticola

In the asexual stage, P. viticola produces sporangiophores. The sporangium is generated on the top of the sporangiophore. The sporangium germinates to produce zoospores. At the end of the growing season of grape plants, P. viticola produces oospores through sexual reproduction. Oospores germinate and a germ tube is formed, from which the sporangium is generated at its top and zoospores are produced through germination [34,35].
The occurrence of grape downy mildew is affected by temperature and humidity [36]. Oospores of P. viticola exhibit high stress resistance and can overwinter in plant survival or soil. They can germinate in water or moist soil to form sporangia, releasing zoospores under suitable conditions. Zoospores can disperse to grape leaves via wind, rain, or dew and then invade through stomata, resulting in primary infection [37]. After infecting grape leaves, P. viticola forms mycelia, which can propagate and spread in the intercellular spaces of grape tissue cells and enter grape leaf cells to absorb nutrients through the haustorium. The sporangiophore and sporangium appear at grape leaf disease spots. Sporangium can germinate and release zoospores, which are spread by wind and rain to cause the secondary infection of grape downy mildew. The infection process of P. viticola in grapes mainly involves three stages: sporangium germination, zoospore release, and invasion into grape tissue cells. During the entire growing season of grapes, if environmental conditions are favorable, P. viticola can carry out multiple repeated infections of grape leaves, resulting in the severe epidemic of grape downy mildew. At the end of the grape growth stage, P. viticola forms oospores during the sexual reproduction stage, which are the primary infection source in the following year [38,39,40] (Figure 1 and Figure 2).
P. viticola can infect any green young tissue of grapes, among which young leaves are most susceptible to infection [41]. During the early infection stage, young, infected leaves exhibit light-yellow and watery lesions with unclear edges. Thereafter, the lesions expand rapidly and gradually develop into brown, irregular or polygonal spots.
In severe cases, several spots merge to form large, irregular spots. Under humid weather conditions, the sporangiophore and sporangium of the P. viticola are formed on the back surface of the lesions and appear as a white, frosty mildew layer, which is the most obvious feature of grape downy mildew. Apart from young leaves, other tissues such as the young tips, inflorescence, stems, or fruits of grapes can also easily be infected by P. viticola under high-humidity conditions, resulting in a white mildew layer in the lesions [42,43,44,45]. Because P. viticola is capable of infecting different types of grape tissues, causing huge damage to the production of grapes, understanding the molecular mechanisms of P. viticola infection in grape plants is therefore of great significance for exploring potential targets for its control and further improving the control efficacy of grape downy mildew.
Effector-encoding genes have been widely studied in P. viticola infection. In a study, the results of a transcriptomic analysis revealed that multiple effector-encoding genes were highly differentially expressed in P. viticola following inoculation on a grapevine cultivar [46]. PvRxLR18 and PvRxLR28 effector genes were strongly upregulated in a high-virulence P. viticola strain compared to a low-virulence strain [47]. The RxLR effector-encoding gene PvAvh77 was strongly upregulated during the initial stage of P. viticola infection in grape plants [48]. In addition to RXLR effector-encoding genes, carbohydrate-active enzymes and pathogenicity genes have also been found to be significantly upregulated during P. viticola infection [49].

3. Biocontrol Agents

3.1. Screening Biocontrol Agents

Because P. viticola is an obligate parasite, it is not possible to cultivate it on artificial media [49]. Therefore, the screening of biocontrol microorganisms for controlling grape downy mildew mainly relies on leaf disk, detached leaf, greenhouse or pot, and field assays. In particular, preliminary screening cannot be carried out on artificial media, which increases the overall workload. Therefore, in order to improve the efficiency of preliminary screening, fungi that are closely related to P. viticola were selected as target pathogens for preliminary screening, such as Phytophthora sp., which belongs to the same family (Peronosporaceae) as P. viticola. Guo et al. [50,51] isolated 153 bacteria and 87 fungi from grapevine leaves and used Phytophthora capsici as the target pathogen for preliminary screening. Lastly, five bacteria and four fungi with evidently antagonistic effects on Phytophthora capsica were screened, with their P. viticola control capabilities further evaluated using the leaf disk method.
Moreover, traditional screening methods for biocontrol agents involve initially isolating numerous strains from the soil, rhizosphere, or grape plants and then evaluating the potential biocontrol capabilities of the isolated strains. Although biocontrol agents capable of controlling grape downy mildew can eventually be obtained through this method, the workload is extremely high. A more efficient screening method is isolating potential biocontrol agents from healthy grapevine tissues from grape plants that are severely diseased by grape downy mildew. This effect is mainly due to grape downy mildew being an airborne disease and the incidence among the same grape variety being similar. Therefore, microorganisms with potential control capabilities against grape downy mildew might exist in healthy grape tissues surrounded by severely infected plants. The use of this method can improve the efficiency of screening biocontrol agents against grape downy mildew. Liu et al. [52] isolated 56 endophytic bacteria from healthy grapevine leaves in a grape downy mildew-infected vineyard and found nine bacteria with biocontrol capabilities against grape downy mildew using the detached leaf method.
There are a number of types of biocontrol microorganisms; however, only a few biocontrol agents, including bacteria (e.g., Bacillus sp., Streptomyces sp., Pseudomonas sp., Paenibacillus, and Lysobacter sp.) and fungi (e.g., Trichoderma sp., Beauveria sp., Fusarium sp., Penicillium sp., and Saccharomyces sp.), exhibit strong control capabilities against grape downy mildew.

3.2. Bacteria as Control Agents for Grape Downy Mildew

Bacillus and Streptomyces are the main biocontrol bacteria exhibiting a strong ability to control grape downy mildew. Multiple Bacillus species, including B. subtilis, B. pumilus, B. megaterium, B. velezensis, B. amyloliquefaciens, and B. methylotrophicus, have been reported to be involved in the control of grape downy mildew (Table 1).
B. subtilis are the most widely reported Bacillus species in controlling grape downy mildew. In a study, B. subtilis GLB191 was isolated from grapevine leaves and exhibited a dramatic reduction in the number of infection sites in P. viticola zoospores through the use of its supernatant. Field assay results demonstrated that the spraying of GLB191 could significantly decrease grapevine disease severity caused by P. viticola [53]. The results of in-depth studies showed that the biocontrol ability of GLB191 is mainly attributed to inducing the plant defense response and the production of metabolites. The application of the supernatant of GLB191 improves the expression level of plant defense response-related genes in grape plants, including genes encoding stilbene synthase, PR protein 3 chitinase 4c, and PR protein 2 β-1,3-glucanase. Moreover, GLB191 is able to produce the cyclic lipopeptides fengycin and surfactin. The disruption of fengycin and surfactin synthesis-encoding genes in GLB191 mutants results in a decrease in the amount of fengycin and surfactin in the supernatant. The sporulation of GLB191 mutants was significantly higher than in the wild strain [54]. Other B. subtilis strains, such as KS1 isolated from grape berry skins, B-FS01 isolated from oilseed rape stalk, and HMB-20428 isolated from grapevine leaves, have also exhibited excellent biocontrol efficiency against grape downy mildew under field conditions [55,56,57].
In addition to B. subtilis, other Bacillus species have shown biocontrol capabilities against grape downy mildew. B. megaterium BMJBN02 was isolated from leek farmland soil. Spraying plants with BMJBN02 can significantly decrease the incidence rate and disease index of grape downy mildew, with a similar efficiency to 0.1% nicotinyl morpholine. The results of in-depth studies showed that BMJBN02 could induce a defense response in grape plants, resulting in dramatically increased salicylic acid content, as well as higher expression of the plant defense response-related genes PR1, PR2, PR5, and PR10.2 in grape plants through the application of BMJBN02 [58]. Similarly, another Bacillus species, B. velezensis KOF112, isolated from a grapevine shoot xylem, is also able to induce a plant defense response. Genes encoding class IV chitinase and β-1,3-glucanase were significantly upregulated in grape leaves following the usage of KOF112. Furthermore, KOF112 was found to be able to reduce the disease severity of grape downy mildew through the leaf disk assay and inhibit the zoospore release of P. viticola [59].
B. amyloliquefaciens strains YTB1407 and CS5, isolated from American ginseng root and grapevine leaf, respectively, showed strong control capabilities against grape downy mildew [52,60]. Another B. amyloliquefaciens strain, N22, exhibited a control efficiency of 76.94% against grape downy mildew under field conditions [61]. Kang et al. isolated B. methylotrophicus T3 from soil and completely inhibited the incidence of grape downy mildew through the use of the detached leaf assay [62].
In addition to Bacillus strains, Streptomyces strains also play an important role in controlling grape downy mildew. In a study, S. atratus PY-1, isolated from soil, exhibited a strong ability to reduce disease severity caused by P. viticola in both the detached leaf (92.13%) and field assay (83%). The results of in-depth studies showed that the fermentation culture of PY-1 could damage the sporangia and sporangiophores of P. viticola. Moreover, 5-acetoxycycloheximide and cycloheximide were purified from PY-1, showing effective capabilities against P. viticola [63]. Khatmiamycin, a novel compound derived from Streptomyces sp. ANK313, has complete motility inhibitory and lytic effects (83 ± 7%) on zoospores of P. viticola [64]. S. microflavus QH94 and S. lydicus A02, isolated from soil, displayed control efficiencies of 89.8% and 95.7% against grape downy mildew, respectively [65,66]. In addition, the supernatant of S. corchorusii NF0919 effectively inhibited the spore germination of P. viticola [67]. The application of S. viridosporus HH1 and S. violates HH5 could significantly reduce the disease severity of grape downy mildew [68].
Pseudomonas aeruginosa HB135 and Ps. azotoformans L-B-4, isolated from leaves, showed 91.27% and 97.2% control efficiency, respectively, against grape downy mildew when the detached leaf assay was used [69]. Additionally, L-B-4 was found to inhibit the sporangium germination of P. viticola [70]. Lakkis et al. isolated P. fluorescens PTA-CT2 from a healthy, field-grown grapevine and found that PTA-CT2 could dramatically reduce the disease severity of grape downy mildew under greenhouse conditions. The results of in-depth studies showed that the main control mechanism of PTA-CT2 is the induction of plant systemic resistance [71].
Paenibacillus polymyxa PB-2, together with its sterile filtrate, was found to be able to strongly inhibit P. viticola [72]. Hao et al. reported that another Paenibacillus sp. strain, B2, could induce the expression of plant defense genes, such as PR-3 (proteinase inhibitor), CHI (chitinase), and LOX (lipoxygenase). An antagonistic peptide, paenimyxin was purified from B2 with the ability to inhibit zoospore motility and reduce the number of infection sites of P. viticola [73]. Microbacterium testaceum N6 and Ochrobactrum sp. SY286 were both isolated from grapevine leaves and exhibited strong control capabilities against grape downy mildew [50,74]. The fermentation fluid of SY286 caused distortions in the mycelium and crimpled or ruptured the sporangium of P. viticola [75]. Lysobacter capsic AZ78 was isolated from the tobacco rhizosphere and showed equal control efficiency to fungicides in controlling grape downy mildew under field conditions [76,77].
Table 1. Overview of biocontrol bacteria control grape downy mildew.
Table 1. Overview of biocontrol bacteria control grape downy mildew.
Biocontrol MicroorganismsStrain NameIsolation SourceApplication ScaleApplication
Manner		Application TypesApplication ConcentrationControl Efficiency
Ochrobactrum sp.SY286 [74]Grapevines leavesFieldSprayLive organisms108 cfu/mL91.05%
Paenibacillus polymyxaPB-2 [72]-FieldSprayLive organisms109 cfu/g46.91%
Paenibacillus sp.B2 [73]Sorghum mycorrhizosphereLeaf discs-Metabolites0, 5, 10, 50 μg/mL-
Pseudomonas aeruginosaHB135 [69]Grapevines leavesDetached leaf-Live organisms107 cfu/mL91.27%
Pseudomonas fluorescensPTA-CT2 [71]Healthy filed-grown grape-vineGreenhouseSprayLive organisms107 cfu/mL-
Pseudomonas azotoformansL-B-4 [70]Grapevines leavesDetached leaf-Live organisms1 × 108 cfu/mL97.2%
Microbacterium testaceumN6 [50]Grapevines leavesLeaf discs-Live organisms1 × 107 cfu/mL74.2%
Lysobacter capsiciAZ78 [76]Tobacco rhizosphereFieldSprayLive organisms108 cfu/mL-
Streptomyces atratusPY-1 [63]SoilFieldSprayFermentation solution-90.08%
Streptomyces microflavusQH94 [65]Soil FieldSprayFermentation solution-82.53%
Streptomyces lydicusA02 [52]SoilFieldSprayMetabolites-95.7%
Streptomyces viridosporusHH1 [68]--SprayLive organisms3 × 107/mL-
Streptomyces violatusHH5 [68]--SprayLive organisms3 × 107/mL-
Streptomyces corchorusiiNF0919 [67]--SprayFermentation supernatant-71.55%
Streptomyces sp.ANK313 [64]Soil--Metabolites--
Bacillus subtilisKS1 [55]Grape berry skinsFieldSprayLive organisms1 × 108 cells/mL-
Bacillus subtilisGLB191 [53]Grapevines leavesFieldSprayLive organisms108 cfu/mL-
Bacillus subtilisB-FS01 [56]Oilseed rape stalkFieldSprayLive organisms107/mL88.25%
Bacillus subtilisHMB-20428 [57]Grapevines leavesFieldSprayLive organisms1 × 108 cfu/mL54.66%
Bacillus subtilisJL4 [78]Grapevines leavesGreenhouseSprayLive organisms8 × 108 cfu/mL88%
Bacillus subtilisDJ-6 WP [67]-FieldSprayLive organisms1 × 1011 cfu/g70.71%
Bacillus pumilusGLB197 [53]Grapevines leavesFieldSprayLive organisms108 cfu/mL-
Bacillus megateriumBMJBN02 [58]SoilPlotSprayMetabolites crude extract--
Bacillus velezensisKOF112 [59]Grapevine shoot xylemLeaf discs-Live organisms1 × 108 cfu/mL100%
Bacillus amyloliquefaciensYTB1407 [60]American ginseng rootLeaf discs-Fermentation liquor-58.05%
Bacillus amyloliquefaciensN22 [61]-FieldSprayLive organisms1 ×107/mL76.94%
Bacillus amyloliquefaciensCS5 [53]-Detached leaf-Live organisms108 cfu/mL96.23%
Bacillus methylotrophicusT3 [62]SoilFieldSprayLive organisms2 × 108 cfu/mL55.4%
Bacillus sp.BCJB01 [79]-FieldSprayLive organisms3 × 109 cfu/mL84.05%
Note: “-” represents not applicable.

3.3. Fungi as Control Agents for Grape Downy Mildew

Trichoderma and Fusarium are the main biocontrol fungi with the ability to control grape downy mildew. T. harzianum is the most widely reported Trichoderma species involved in grape downy mildew biocontrol. Banani et al. [80] found that the application of T. harzianum T39 significantly reduces the disease severity of grape downy mildew, in addition to improving the expression levels of defense-related genes, such as pathogenesis-related protein 2 (PR-2), pathogenesis-related protein 4 (PR-4), and osmotin 1 (OSM-1) in grape plants. Similar findings have been reported in T. harzianum TriH_JSB36, which elicited defense responses in grape plants and enhanced the activity of defense-related enzymes, including 1,3-glucanase, peroxidase, and phenylalanine ammonia-lyase [81]. In a study, the application of T. harzianum HL1 and HL14 led to a dramatic decrease in the disease severity of grape downy mildew [68,82]. Other Trichoderma species, such as T. viride HL5, have been found to be able to significantly increase the activity of oxidative enzymes and contain peroxidase and polyphenol oxidase [68]. The usage of T. asperellum ICC012 and T. gamsii ICC080 triggered the production of jasmonic acid, which is an important factor in inducing plant defense response [83].
Fusarium proliferatum strain G6 was isolated from atypical grape downy mildew lesions and significantly reduced the disease severity of grape downy mildew under field conditions. Through microscope observations, it was found that G6 could coil around and inside the sporangiophores of P. viticola [84]. Another F. proliferatum strain, F3, isolated from abnormal lesions of grape downy mildew, displayed strong control capabilities against grape downy mildew when the detached leaf assay was used. The conidial suspension and sterile fermentation fluid of F3 showed 86.8% and 83.1% inhibition rates for the sporangium germination of P. viticola. Microscope observation demonstrated that F3 could coil around or cover the sporangiophores of P. viticola [85]. Other Fusarium species, including F. delphinoides M1, F. brachygibbosum M2, F. pseudonygamai M10, F. pseudonygamai M12_1, and Fusarium sp. M12_2, isolated from the sporangiophore of P. viticola, could lyse and inhibit the production of sporangia in P. viticola. The metabolite fusaric acid, produced by these Fusarium species, could inhibit the growth of P. viticola [86,87].
Some fungal species exhibit their biocontrol capabilities through the production of metabolites. An aqueous extract from Penicillium chrysogenum, known as Pen, was found to significantly reduce the disease severity of grape downy mildew under field conditions [88]. Phomopsis sp. CAFT69 was isolated from the leaves and stem bark of Endodesmia calophylloides, producing excelsional, 9-hydroxyphomopsidin, and alternariol, which could inhibit the motility and lysis of P. viticola zoospores [89]. Musetti et al. [90,91] found that Alternaria alternata is able to produce three diketopiperazine metabolites—cyclo (L-leucine-trans-4-hydroxy-l-proline), cyclo (L-phenylalanine-trans-4-hydroxy-l-proline), and cyclo (L-alanine-trans-4-hydroxy-l-proline)—for the complete control of grape downy mildew.
Some fungal species can induce grape plant resistance to P. viticola infection. Four different sources of Beauveria bassiana, strains—ATP01, ATP05, EABb 04/01-Tip—and ATCC 74040 were found to be able to significantly reduce the severity of grape downy mildew. The results of in-depth studies showed that the application of strain ATCC 74040 could increase the expression level of the defense-related PR-1-like gene in grape plants [92,93]. Moreover, Pythium oligandrum Po37 isolated from grapevine roots could induce the expression of genes from the jasmonate and ethylene pathways when the grape plants were infected with P. viticola [94]. Rhizophagus irregularis AMF could alter the expression level of PvRxLR28, a pathogenicity effector of P. viticola, thereby reducing the ability of P. viticola to infect grape plants [95].
Various fungal species, such as Acremonium byssoides A21, isolated from grapevine leaves, were able to completely inhibit the sporangia of P. viticola when the culture filtrates and crude extract of A21 were used [96]. Other Acremonium species, such as A. sclerotigenum A59 and A. persicinum A3, exhibited high inhibition rates against the sporangia germination of P. viticola [97]. In a study involving Epicoccum nigrum isolated from the surface of P. viticola-infected leaves, it was observed that the mycelia were surrounded by sporangiophores of P. viticala [98]. Leptosphaerulina australis Y29, isolated from grapevine leaves, displayed a control efficiency of 72.9% against grape downy mildew when the leaf disk assay was used [51]. In addition, the usage of Aureobasidium pullulans could reduce the number of lesions on leaves caused by P. viticala compared with the control [99]. It has also been reported that the yeast strain Saccharomyces cerevisiae is able to significantly reduce the disease severity of grape downy mildew [100] (Table 2).
Table 2. Overview of biocontrol fungi control grape downy mildew.
Table 2. Overview of biocontrol fungi control grape downy mildew.
Biocontrol MicroorganismsStrain NameIsolation SourceApplication ScaleApplication
Manner		Application TypesApplication ConcentrationControl Efficiency
Acremonium byssoidesA21 [96]Grapevines leaves--Culture filtrates, crude extracts--
Acremonium sclerotigenumA59 [97]Grapevines seed--Culture filtrates--
Acremonium persicinumA3 [97]Grapevines leaves--Culture filtrates--
Penicillium chrysogenum- [88]-FieldSprayMetabolites45 g/L90%
Alternaria alternata- [90]Grapevines leavesGreenhouseSprayMetabolites10−3, 10−4, 10−5, 10−6 M100%
Fusarium delphinoidesM1 [86]P. viticola sporangiophoreLeaf discs-Culture extract10 μg/mL-
Fusarium brachygibbosumM2 [86]P. viticola sporangiophoreLeaf discs-Culture extract10 μg/mL-
Fusarium pseudonygamaiM10 [86]P. viticola sporangiophoreLeaf discs-Culture extract10 μg/mL-
Fusarium pseudonygamaiM12_1 [86]P. viticola sporangiophoreLeaf discs-Culture extract10 μg/mL-
Fusarium sp.M12_2 [86]P. viticola sporangiophoreLeaf discs-Culture extract10 μg/mL-
Fusarium proliferatumG6 [84]Atypical grape downy mildew lesionsFieldSprayLive organisms1 × 106 microconidia/mL-
Fusarium proliferatumF3 [85]Abnormal lesions of grape downy mildewDetached leaf-Live organisms1.7 × 107 spores/mL88.9%
Pythium oligandrumPo37 [94]Grapevine rootsFoliar discs-Live organisms2 × 104 oospores/mL-
Beauveria bassianaATP01 [94]Maize stem borerGreenhouseSprayLive organisms1 × 108 conidia/mL-
Beauveria bassianaATP05 [92]Sorghum chaferGreenhouseSprayLive organisms1 × 108 conidia/mL-
Beauveria bassianaEABb04/01-Tip [92]Dead Timaspis papaveris (Kieffer) larvaeGreenhouseSprayLive organisms1 × 108 conidia/mL-
Beauveria bassianaATCC 74040 [92]- GreenhouseSprayLive organisms1.4 × 107 conidia/mL89.03%
Saccharomyces cerevisiae- [100]--SprayLive organisms1.5 L/ha-
Saccharomyces cerevisiae- [68]--SprayLive organisms1 × 109 cell/mL-
Aureobasidium pullulans- [99]-GreenhouseSprayLive organisms1.0%-
Leptosphaerulina australisY29 [51]Grapevines leavesLeaf discs-Live organisms1 × 107 spores/mL72.9%
Epicoccum nigrum- [98]P. viticola infected leaves--Live organisms--
Phomopsis sp.CAFT69 [89]Leaves or stems bark of Endodesmia calophylloides--Metabolites10, 30, 50 μg/mL-
Rhizophagus irregularis- [95]---Live organisms--
Trichoderma harzianumTriH_JSB36 [81]SoilField-Live organisms108 spores/mL82.9%
Trichoderma harzianumHL1 [68]Soil-SprayLive organisms3 × 107/mL-
Trichoderma harzianumHL14 [82]Bean rhizosphereFieldSprayLive organisms108 spores/mL69.7%
Trichoderma harzianumT39 [80]-GreenhouseSprayLive organisms1 × 107 conidia/mL-
Trichoderma virideHL5 [68]Soil-SprayLive organisms3 × 107/mL-
Trichoderma asperellumICC012 [83]-LaboratorySprayLive organisms2.5 kg/hl-
Trichoderma gamsiiICC080 [83] Laboratory SprayLive organisms2.5 kg/hl-
Note: “-” represents not applicable.

4. Mechanisms of Action of Biocontrol Agents against Plasmopara viticola

Several mechanisms are involved in biocontrol agents’ control of grape downy mildew, including the production of metabolites, the secretion of enzymes, inducing plant systemic resistance in plants, mycoparasitism, and competition (Figure 3, Table 3).
Table 3. Mechanisms of biocontrol microorganisms control grape downy mildew.
Table 3. Mechanisms of biocontrol microorganisms control grape downy mildew.
Biocontrol MicroorganismsMechanismsReferences
Beauveria bassiana ATCC74040Competition; induce the expression of defense-related gene PR-1-like in grape plants[92]
Pythium oligandrum Po37Induce the expression of defenses genes (PR1, GLU, PR5, LOX2, PAL and STS)[94]
Fusarium proliferatum F3Mycoparasitism[85]
Fusarium proliferatum G6Mycoparasitism[84]
Fusarium delphinoides M1Mycoparasitism; production of metabolites, fusaric acid, etc.[86,87]
Fusarium brachygibbosum M2Mycoparasitism; production of metabolites, fusaric acid, etc.[86,87]
Fusarium pseudonygamai M10Mycoparasitism; production of metabolites, fusaric acid, etc.[86,87]
Fusarium pseudonygamai M12_1Mycoparasitism; production of metabolites, fusaric acid, etc.[86,87]
Fusarium sp. M12_2Mycoparasitism; production of metabolites, fusaric acid, etc.[86,87]
Alternaria alternataProduction of three dipeptides, belonging to the family of diketopiperazines; competition[90,91]
Penicillium chrysogenumProduction of Pen, an aqueous extract of the dry mycelium[88]
Epicoccum nigrumMycoparasitism[98]
Phomopsis sp. CAFT69Production of metabolites, excelsional etc.[89]
Trichoderma harzianum T39Induce the expression of defenses genes PR-2, PR-4, OSM-1, etc. [80,101]
Trichoderma harzianum TriH_JSB36Induce the activities of the defense enzymes, peroxidase, etc.[81]
Trichoderma asperellum ICC012/Trichoderma gamsii ICC080Induce the production of jasmonic acid[83]
Paenibacillus sp. B2Production of paenimyxin, an antagonistic peptide[73]
Pseudomonas fluorescens PTA-CT2Induce the expression of defenses genes in SA and HR response[71]
Lysobacter capsici AZ78Production of cyclo (L-Pro-l-Tyr)[77]
Streptomyces atratus PY-1Production of metabolites (5-acetoxycycloheximide and cycloheximide)[63]
Streptomyces sp. ANK313Production of metabolites (Khatmiamycin)[64]
Bacillus subtilis GLB191Production of cyclic lipopeptides fengycin and surfactin; secretion of autolysins[54,102]
Bacillus megaterium BMJBN02Induce the content of salicylic acid and expression of defenses genes (PR genes)[58]
Bacillus velezensis KOF112Induce the expression of defenses genes (class IV chitinase and β-1,3-glucanase)[59]

4.1. Mycoparasitism

Some biocontrol agents have the ability to mycoparasitize P. viticola and thereby control grape downy mildew. Through microscope observations, it was found that F. proliferatum G6 could coil around and inside the sporangiophores of P. viticola [84]. The mycelia of another Fusarium strain, F. proliferatum F3, was found to be able to coil around or cover the sporangiophores of P. viticola, including the entire downy mildew layer [85]. Five species of Fusarium species coil and induce the lysis of P. viticola sporophores [87]. Compared with plants not infected with P. viticala, in the P. viticala-infected group, the hyphae of E. nigrum rapidly surrounded the sporangiophores of P. viticala [98].

4.2. Competition

Competition with pathogens for nutrients or ecological niches is also an important control mechanism of biocontrol agents. Jaber [92] found that Beauveria bassiana ATCC 74040 exhibited the strongest colonization ability compared with all other tested strains, which might compete for plant ecological niches or resources with P. viticola and thereby confer protection against grape downy mildew. Musetti et al. [91] found that space and/or nutrient competition might be involved in A. alternata and P. viticola interaction.

4.3. Secretion of Enzymes and Peptides

Degradative enzymes or peptides secreted by biocontrol agents exert direct effects on P. viticola. Wang et al. [102] disrupted the gene LytD in B. subtilis GLB191, which encodes the autolysin N-acetylglucosaminidase—an endogenous cell wall-degrading enzyme in B. subtilis. The gene-disruption mutants reduced the suppression of Plasmopara viticola, in addition to the stimulation of plant defense. An antagonistic peptide, paenimyxin, was isolated and purified from Paenibacillus sp. strain B2, which was found to be able to inhibit the motility of P. viticola zoospores [73]. Other cyclic lipopeptides such as fengycin and surfactin produced by B. subtilis GLB191 have contributed to the control of grapevine downy mildew [53]. Lysobacter capsici AZ78 is able to produce cyclo(L-Pro-l-Tyr), which is toxic to the sporangia of P. viticola. Regarding fungal biocontrol agents, cyclo (L-phenylalanine-trans-4-hydroxy-l-proline), cyclo (L-leucine-trans-4-hydroxy-l-proline), and cyclo (L-alanine-trans-4-hydroxy-l-proline), isolated from A. alternata, were able to reduce the disease severity of grape downy mildew caused by P. viticola [88,90].

4.4. Production of Metabolites

Secondary metabolites produced by biocontrol agents have an effect on P. viticola. In a study, excelsional, alternariol, and 9-hydroxyphomopsidin produced by Phomopsis sp. CAFT69 showed strong motility inhibitory and lytic activities against the zoospores of P. viticola [89]. Metabolites produced from Streptomyces were found to follow a similar mechanism to Phomopsis sp. CAFT69. Khatmiamycin produced by Streptomyces sp. ANK313 was able to exert a complete motility inhibition effect on P. viticola and was also able to lyse the zoospores of P. viticola [64]. In other Streptomyces strains, 5-acetoxycycloheximide and cycloheximide produced by S. atratus PY-1 were significantly effective against P. viticola [63]. For fungal biocontrol agents, secondary metabolites such as fusaric acid produced by several Fusarium species, including F. delphinoides M1, F. brachygibbosum M2, F. pseudonygamai M10 and M12_1, and Fusarium sp. M12_2, were able to inhibit the growth of P. viticola [86,87]. Pen extracted from the dry mycelium of Penicillium chrysogenum was found to be able to reduce the disease severity of grape downy mildew [88].

4.5. Induction of Plant Systemic Resistance

The induction of plant systemic resistance is an important mechanism for controlling grape downy mildew. In a study, several plant defense response-related genes in grape plants were induced and expressed after being treated with biocontrol agents. The content of salicylic acid and the expression levels of defense-related genes (PR1, PR2, PR5, and PR10.2) were induced in grape plants after being treated with B. megaterium BMJBN02 against grape downy mildew [58]. Plant defense response-related genes encoding class IV chitinase and β-1,3-glucanase were upregulated in grape leaves treated with B. velezensis KOF112 [59]. Similar findings have been reported in Pseudomonas fluorescens. The application of Pseudomonas fluorescens PTA-CT2 can induce the systemic resistance of grape plants to P. viticola infection. The expression of defense genes, such as salicylic acid, and hypersensitive response-related genes were induced following the usage of P. fluorescens PTA-CT2 [71]. In fungal biocontrol agents, the expression levels of genes encoding pathogenesis-related protein 2 (PR-2), pathogenesis-related protein 4 (PR-4), and osmotin 1 (OSM-1) were increased in grape plants after the application of T. harzianum T39 [80]. The application of T. harzianum TriH_JSB36 increases the activities of defense enzymes in grape plants, including phenylalanine ammonia-lyase, peroxidase, and 1,3-glucanase [81]. Jasmonic acid production was induced in plants inoculated with P. viticola when the plants were treated with Trichoderma asperellum ICC012/Trichoderma gamsii ICC080 [83]. Yacoub et al. found that Pythium oligandrum Po37 can induce the expression of grapevine defense genes (PR1, GLU, PR5, LOX2, PAL, and STS) against P. viticola attack [94].

5. Conclusions and Future Prospects

Grape downy mildew is a type of airborne disease caused by P. viticola that can cause significant grape yield decline and severe economic losses. As a green, sustainable, and environmentally friendly control method, biocontrol has attracted considerable attention. Despite there being a plethora of studies on biocontrol agents, microbial resources have seldom been reported to be involved in controlling grape downy mildew. At present, the reported biocontrol resources capable of controlling grape downy mildew mainly involve bacteria such as Bacillus, Streptomyces, Pseudomonas, Paenibacillus, and Lysobacter, and fungi such as Fusarium, Beauveria, Saccharomyces, Trichoderma, and Pythium. Therefore, this review focuses on a detailed introduction to the biocontrol agents that could be used to effectively control grape downy mildew, together with their potential control mechanisms. This review provides a basis for the more efficient use of biocontrol agents in controlling grape downy mildew.
Future research can be carried out by exploring biocontrol microbial resources, including screening novel biocontrol agents, improving the control efficiency of existing biocontrol agents, constructing biocontrol genetic engineering strains, developing biocontrol agent products, and elucidating the molecular mechanisms involved in the control mechanism of biocontrol agents and the pathogenic mechanism of P. viticola.
(1)
Screening for novel biocontrol microbial resources: There are currently still too few microbial resources able to control grape downy mildew. Novel biocontrol resources can be isolated from the soil, rhizosphere, or grape tissues using traditional isolation and purification methods, followed by being screened to determine their biocontrol efficacy. Alternatively, known microbial resources with broad-spectrum antimicrobial properties can be used to evaluate their control capabilities against grape downy mildew.
(2)
Improving the control efficiency of existing biocontrol agents: Improvement mainly involves optimizing cultivation or application conditions, in addition to improving the ability of biocontrol agents to produce enzymes and secondary metabolites. Moreover, a synergistic combination of different biocontrol agents, or the integration of biocontrol agents with pesticides, will further improve control efficiency.
(3)
Constructing biocontrol genetic engineering strains: The transformation of effective biocontrol genes into biocontrol agents to construct genetic engineering strains, thereby improving biocontrol efficiency against grape downy mildew.
(4)
Elucidating the control mechanism of biocontrol agents: Clarifying the control mechanism of biocontrol agents is crucial for further improving the control efficiency of biocontrol agents. Transcriptomics can be used to screen biocontrol-related genes in biocontrol agents that are significantly differentially expressed during the process of controlling grape downy mildew. Thereafter, gene knockout, silencing, or overexpression could be used to verify the function of differentially expressed genes in controlling grape downy mildew.
(5)
Elucidating the pathogenic mechanism of P. viticola: Clarifying the pathogenic mechanism of P. viticola could provide potential targets for biocontrol agents. Transcriptomics can be used to screen the differentially expressed genes during the infection process of P. viticola on grape tissues; thereafter, the function of these differentially expressed genes in P. viticola infection can be studied.
(6)
Developing biocontrol products: Although some biocontrol agents have been reported, very few biocontrol agents have been developed into commercial products and widely used in field control. Therefore, the development of more commercial biocontrol products and the improvement of their shelf life will be of great value for the sustainable application of biocontrol agents.

Author Contributions

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

Funding

This study was funded by the National Key Research and Development Program of China (2023YFD1401405); the China Agricultural Research System (CARS-29); the Expert Workstation Project in Yunnan Province (202305AF150129).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Chen, M.; Brun, F.; Raynal, M.; Makowski, D. Timing of grape downy mildew onset in bordeaux vineyards. Phytopathology 2019, 109, 787–795. [Google Scholar] [CrossRef]
  2. Li, Z.; Dos Santos, R.F.; Gao, L.; Chang, P.; Wang, X. Current status and future prospects of grapevine anthracnose caused by Elsinoe ampelina: An important disease in humid grape-growing regions. Mol. Plant Pathol. 2021, 22, 899–910. [Google Scholar] [CrossRef] [PubMed]
  3. Zhang, H.; Godana, E.A.; Sui, Y.; Yang, Q.; Zhang, X.; Zhao, L. Biological control as an alternative to synthetic fungicides for the management of grey and blue mould diseases of table grapes: A review. Crit. Rev. Microbiol. 2020, 46, 450–462. [Google Scholar] [CrossRef]
  4. Su, K.; Guo, Y.; Zhao, Y.; Gao, H.; Liu, Z.; Li, K.; Ma, L.; Guo, X. Candidate genes for grape white rot resistance based on SMRT and Illumina sequencing. BMC Plant Biol. 2019, 19, 501. [Google Scholar] [CrossRef] [PubMed]
  5. Fu, Q.; Yang, J.; Zhang, K.; Yin, K.; Xiang, G.; Yin, X.; Liu, G.; Xu, Y. Plasmopara viticola effector PvCRN11 induces disease resistance to downy mildew in grapevine. Plant J. 2024, 117, 873–891. [Google Scholar] [CrossRef] [PubMed]
  6. Li, B.Y.; Ran, L.X.; Shi, L.M.; Zhang, K.C.; Ge, B.B. Research progress of grape downy mildew. Chin. Agric. Sci. Bull. 2023, 39, 125–131. [Google Scholar]
  7. Capriotti, L.; Baraldi, E.; Mezzetti, B.; Limera, C.; Sabbadini, S. Biotechnological approaches: Gene overexpression, gene silencing, and genome editing to control fungal and oomycete diseases in grapevine. Int. J. Mol. Sci. 2020, 21, 5701. [Google Scholar] [CrossRef] [PubMed]
  8. Tan, Y.X.; Feng, J.; Yi, T.Y. Toxicity determination of azoxystrobin and dimethomorph against Plasmopara viticola. J. Agric. 2016, 6, 20–23. [Google Scholar]
  9. Xin, Z.M.; Xu, D.K.; Zhang, M.; Wu, B.; Jiang, S.S.; Xin, X.Q. Allied toxicity determination of azoxystrobin and polyhexamethylene biguanidine hydrochloride combined with dimethomorph on Plasmopara viticola. Shandong Agric. Sci. 2016, 48, 117–120. [Google Scholar]
  10. Cheng, Y.P.; Pan, S.F.; Li, Y.L.; Zhang, W.L.; Gao, C.L.; Cheng, Y. Comparison on effect of six fungicides on grape downy mildew (Plasmopara viticola) in laboratory and field. J. Anhui Agric. Sci. 2018, 46, 109–111. [Google Scholar]
  11. Djennane, S.; Gersch, S.; Le-Bohec, F.; Piron, M.C.; Baltenweck, R.; Lemaire, O.; Merdinoglu, D.; Hugueney, P.; Nogué, F.; Mestre, P. CRISPR/Cas9 editing of downy mildew resistant 6 (DMR6-1) in grapevine leads to reduced susceptibility to Plasmopara viticola. J. Exp. Bot. 2024, 75, 2100–2112. [Google Scholar] [CrossRef] [PubMed]
  12. González-Centeno, M.R.; Chira, K.; Miramont, C.; Escudier, J.L.; Samson, A.; Salmon, J.M.; Ojeda, H.; Teissedre, P.L. Disease resistant bouquet vine varieties: Assessment of the phenolic, aromatic, and sensory potential of their wines. Biomolecules 2019, 9, 793. [Google Scholar] [CrossRef] [PubMed]
  13. Xie, D.; Cai, X.; Yang, C.; Xie, L.; Qin, G.; Zhang, M.; Huang, Y.; Gong, G.; Chang, X.; Chen, H. Studies on the control effect of Bacillus subtilis on wheat powdery mildew. Pest. Manag. Sci. 2021, 77, 4375–4382. [Google Scholar] [CrossRef]
  14. Kiani Dehkian, Z.; Taheri, H.; Pakdaman Sardrood, B.; Farkhari, M. Controlling tomato Fusarium wilt disease through Bacillus thuringiensis-mediated defense primining. Iran. J. Biotechnol. 2024, 22, e3690. [Google Scholar]
  15. Sawant, S.S.; Song, J.; Seo, H.J. Characterization of Bacillus velezensis RDA1 as a biological control agent against white root rot disease caused by Rosellinia necatrix. Plants 2022, 11, 2486. [Google Scholar] [CrossRef]
  16. Yamamoto, S.; Shiraishi, S.; Kawagoe, Y.; Mochizuki, M.; Suzuki, S. Impact of Bacillus amyloliquefaciens S13-3 on control of bacterial wilt and powdery mildew in tomato. Pest. Manag. Sci. 2015, 71, 722–727. [Google Scholar] [CrossRef]
  17. Akram, W.; Waqar, S.; Hanif, S.; Anjum, T.; Aftab, Z.E.; Li, G.; Ali, B.; Rizwana, H.; Hassan, A.; Rehman, A.; et al. Comparative effect of seed coating and biopriming of Bacillus aryabhattai Z-48 on seedling growth, growth promotion, and suppression of Fusarium wilt disease of tomato plants. Microorganisms 2024, 12, 792. [Google Scholar] [CrossRef] [PubMed]
  18. Hariprasad, P.; Chandrashekar, S.; Singh, S.B.; Niranjana, S.R. Mechanisms of plant growth promotion and disease suppression by Pseudomonas aeruginosa strain 2apa. J. Basic. Microbiol. 2014, 54, 792–801. [Google Scholar] [CrossRef] [PubMed]
  19. Khan, S.; Srivastava, S.; Karnwal, A.; Malik, T. Streptomyces as a promising biological control agents for plant pathogens. Front. Microbiol. 2023, 14, 1285543. [Google Scholar] [CrossRef]
  20. Son, S.H.; Khan, Z.; Kim, S.G.; Kim, Y.H. Plant growth-promoting rhizobacteria, Paenibacillus polymyxa and Paenibacillus lentimorbus suppress disease complex caused by root-knot nematode and fusarium wilt fungus. J. Appl. Microbiol. 2009, 107, 524–532. [Google Scholar] [CrossRef]
  21. Mahmoud, G.A.; Abdel-Sater, M.A.; Al-Amery, E.; Hussein, N.A. Controlling Alternaria cerealis MT808477 tomato phytopathogen by Trichoderma harzianum and tracking the plant physiological changes. Plants 2021, 10, 1846. [Google Scholar] [CrossRef] [PubMed]
  22. Tomah, A.A.; Alamer, I.S.A.; Khattak, A.A.; Ahmed, T.; Hatamleh, A.A.; Al-Dosary, M.A.; Ali, H.M.; Wang, D.; Zhang, J.; Xu, L.; et al. Potential of Trichoderma virens HZA14 in controlling Verticillium wilt disease of eggplant and analysis of its genes responsible for microsclerotial degradation. Plants 2023, 12, 3761. [Google Scholar] [CrossRef] [PubMed]
  23. Rao, Y.; Zeng, L.; Jiangm, H.; Mei, L.; Wang, Y. Trichoderma atroviride LZ42 releases volatile organic compounds promoting plant growth and suppressing Fusarium wilt disease in tomato seedlings. BMC Microbiol. 2022, 22, 88. [Google Scholar] [CrossRef] [PubMed]
  24. Li, X.; Leng, J.; Yu, L.; Bai, H.; Li, X.; Wisniewski, M.; Liu, J.; Sui, Y. Efficacy of the biocontrol agent Trichoderma hamatum against Lasiodiplodia theobromae on macadamia. Front. Microbiol. 2022, 13, 994422. [Google Scholar] [CrossRef]
  25. Liu, Z.; Xu, N.; Pang, Q.; Khan, R.A.A.; Xu, Q.; Wu, C.; Liu, T. A salt-tolerant strain of Trichoderma longibrachiatum HL167 is effective in alleviating salt stress, promoting plant growth, and managing Fusarium wilt disease in cowpea. J. Fungi 2023, 9, 304. [Google Scholar] [CrossRef]
  26. 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]
  27. Partridge, D.E.; Sutton, T.B.; Jordan, D.L.; Curtis, V.L.; Bailey, J.E. Management of Sclerotinia blight of peanut with the biological control agent Coniothyrium minitans. Plant Dis. 2006, 90, 957–963. [Google Scholar] [CrossRef]
  28. Ownley, B.H.; Griffin, M.R.; Klingeman, W.E.; Gwinn, K.D.; Moulton, J.K.; Pereira, R.M. Beauveria bassiana: Endophytic colonization and plant disease control. J. Invertebr. Pathol. 2008, 98, 267–270. [Google Scholar] [CrossRef]
  29. Sarven, M.S.; Hao, Q.; Deng, J.; Yang, F.; Wang, G.; Xiao, Y.; Xiao, X. Biological control of tomato gray mold caused by Botrytis Cinerea with the entomopathogenic fungus Metarhizium Anisopliae. Pathogens 2020, 9, 213. [Google Scholar] [CrossRef]
  30. Hashem, A.; Tabassum, B.; Abd_Allah, E.F. Bacillus subtilis: A plant-growth promoting rhizobacterium that also impacts biotic stress. Saudi. J. Biol. Sci. 2019, 26, 1291–1297. [Google Scholar] [CrossRef]
  31. Vurukonda, S.S.K.P.; Giovanardi, D.; Stefani, E. Plant growth promoting and biocontrol activity of Streptomyces spp. as endophytes. Int. J. Mol. Sci. 2018, 19, 952. [Google Scholar] [CrossRef] [PubMed]
  32. Zeng, Q.; Xie, J.; Li, Y.; Gao, T.; Zhang, X.; Wang, Q. Comprehensive genomic analysis of the endophytic Bacillus altitudinis strain GLB197, a potential biocontrol agent of grape downy mildew. Front. Genet. 2021, 12, 729603. [Google Scholar] [CrossRef]
  33. Palmieri, M.C.; Perazzolli, M.; Matafora, V.; Moretto, M.; Bachi, A.; Pertot, I. Proteomic analysis of grapevine resistance induced by Trichoderma harzianum T39 reveals specific defence pathways activated against downy mildew. J. Exp. Bot. 2012, 63, 6237–6251. [Google Scholar] [CrossRef]
  34. Gouveia, C.; Santos, R.B.; Paiva-Silva, C.; Buchholz, G.; Malhó, R.; Figueiredo, A. The pathogenicity of Plasmopara viticola: A review of evolutionary dynamics, infection strategies and effector molecules. BMC Plant Biol. 2024, 24, 327. [Google Scholar] [CrossRef] [PubMed]
  35. Gessler, C.; Pertot, I.; Perazzolli, M. Plasmopara viticola: A review of knowledge on downy mildew of grapevine and effective disease management. Phytopathol. Mediterr. 2011, 50, 3–44. [Google Scholar]
  36. Jürges, G.; Kassemeyer, H.H.; Dürrenberger, M.; Düggelin, M.; Nick, P. The mode of interaction between Vitis and Plasmopara viticola Berk. & Curt. Ex de Bary depends on the host species. Plant Biol. 2009, 11, 886–898. [Google Scholar]
  37. Buonassisi, D.; Colombo, M.; Migliaro, D.; Dolzani, C.; Peressotti, E.; Mizzotti, C.; Velasco, R.; Masiero, S.; Perazzolli, M.; Vezzulli, S. Breeding for grapevine downy mildew resistance: A review of “omics” approaches. Euphytica 2017, 213, 103. [Google Scholar] [CrossRef]
  38. Burruano, S. The life-cycle of Plasmopara viticola, cause of downy mildew of vine. Mycologist 2000, 14, 179–182. [Google Scholar] [CrossRef]
  39. Wang, L.L.; Sun, Y.K.; Xu, X.; Zhou, J.; Wang, Q.M.; Zhu, X.Z. Research progress on pathogensis and control of grape downy mildew. Hortic. Seed 2022, 42, 31–33. [Google Scholar]
  40. Velasquez-Camacho, L.; Otero, M.; Basile, B.; Pijuan, J.; Corrado, G. Current trends and perspectives on predictive models for mildew diseases in vineyards. Microorganisms 2022, 11, 73. [Google Scholar] [CrossRef]
  41. Fröbel, S.; Zyprian, E. Colonization of different grapevine tissues by Plasmopara viticola-a histological study. Front. Plant Sci. 2019, 10, 951. [Google Scholar] [CrossRef] [PubMed]
  42. Musetti, R.; Stringher, L.; Borselli, S.; Vecchione, A.; Zulini, L.; Pertot, I. Ultrastructural analysis of Vitis vinifera leaf tissues showing atypical symptoms of Plasmopara viticola. Micron 2005, 36, 73–80. [Google Scholar] [CrossRef] [PubMed]
  43. Peng, J.; Wang, X.; Wang, H.; Li, X.; Zhang, Q.; Wang, M.; Yan, J. Advances in understanding grapevine downy mildew: From pathogen infection to disease management. Mol. Plant Pathol. 2024, 25, e13401. [Google Scholar] [CrossRef] [PubMed]
  44. Koledenkova, K.; Esmaeel, Q.; Jacquard, C.; Nowak, J.; Clément, C.; Ait Barka, E. Plasmopara viticola the causal agent of downy mildew of grapevine: From its taxonomy to disease management. Front. Microbiol. 2022, 13, 889472. [Google Scholar] [CrossRef] [PubMed]
  45. Zhang, W.; Yan, J.Y.; Liu, M.; Peng, J.B.; Xing, Q.K.; Li, X.H. Research progress on prediction and epidemic of grapevine downy mildew. China Fruits 2020, 3, 11–15. [Google Scholar]
  46. Toffolatti, S.L.; De Lorenzis, G.; Brilli, M.; Moser, M.; Shariati, V.; Tavakol, E.; Maddalena, G.; Passera, A.; Casati, P.; Pindo, M.; et al. Novel aspects on the interaction between grapevine and Plasmopara viticola: Dual-RNA-Seq analysis highlights gene expression dynamics in the pathogen and the plant during the battle for infection. Genes 2020, 11, 261. [Google Scholar] [CrossRef]
  47. Gómez-Zeledón, J.; Spring, O. Up-regulated RxLR effector genes of Plasmopara viticola in synchronized host-free stages and infected leaves of hosts with different susceptibility. Fungal Biol. 2018, 122, 1125–1133. [Google Scholar] [CrossRef]
  48. Fu, Q.; Wang, Y.; Yang, J.; Jiao, Y.; Li, W.; Yang, F.; Yin, X.; Shang, B.; Liu, R.; Zhang, Y.; et al. Plasmopara viticola RxLR effector PvAvh77 triggers cell death and governs immunity responses in grapevine. J. Exp. Bot. 2023, 74, 2047–2066. [Google Scholar] [CrossRef]
  49. Yin, L.; An, Y.; Qu, J.; Li, X.; Zhang, Y.; Dry, I.; Wu, H.; Lu, J. Genome sequence of Plasmopara viticola and insight into the pathogenic mechanism. Sci. Rep. 2017, 7, 46553. [Google Scholar] [CrossRef]
  50. Guo, J.P.; Ma, G.; Zhu, H.X.; Liu, C.Y.; Fu, J.F. Isolation, screening and identification of antagonistic bacteria strain N6 against grape downy mildew. Hubei Agric. Sci. 2014, 53, 4063–4065. [Google Scholar]
  51. Guo, J.P.; Ma, G.; Zhu, H.X.; Liu, C.Y.; Fu, J.F. Isolation, screening and identification of antagonistic fungi against grape downy mildew. J. Jilin Agric. Sci. 2014, 59, 72–75. [Google Scholar]
  52. Liu, X.; Yang, X.C.; Tao, Y.; Yu, X.; Li, H. Screening, identification and optimization of fermentation conditions for antagonistic bacteria against Plasmopara viticola on grape. J. Fruit Sci. 2015, 32, 681–688. [Google Scholar]
  53. Zhang, X.; Zhou, Y.Y.; Li, Y.; Fu, X.C.; Wang, Q. Screening and characterization of endophytic Bacillus for biocontrol of grapevine downy mildew. Crop Prot. 2017, 96, 173–179. [Google Scholar] [CrossRef]
  54. Li, Y.; Héloir, M.C.; Zhang, X.; Geissler, M.; Trouvelot, S.; Jacquens, L.; Henkel, M.; Su, X.; Fang, X.; Wang, Q.; et al. Surfactin and fengycin contribute to the protection of a Bacillus subtilis strain against grape downy mildew by both direct effect and defence stimulation. Mol. Plant Pathol. 2019, 20, 1037–1050. [Google Scholar] [CrossRef]
  55. Furuya, S.; Mochizuki, M.; Aoki, Y.; Kobayashi, H.; Takayanagi, T.; Shimizu, M.; Suzuki, S. Isolation and characterization of Bacillus subtilis KS1 for the biocontrol of grapevine fungal diseases. Biocontrol Sci. Techn. 2011, 21, 705–720. [Google Scholar] [CrossRef]
  56. Chen, H.; Hu, L.B.; Tang, C.P.; Hu, J.; Shi, Z.Q. Efficacy of the strain B-FS01 of Bacillus subtilis in suppression of the grape downy mildew caused by Plasmopara viticola. Plant Prot. 2011, 37, 194–197. [Google Scholar]
  57. Bi, Q.Y.; Han, X.Y.; Ma, Z.Q.; Zhao, J.J.; Wang, W.Q.; Jia, H.M. Inhibitory effects of Bacillus subtilis HMB-20428 interacted with chemical fungicides and decrement of chemical fungicides on oomycete pathogen Plasmopara viticola. J. Plant Prot. 2018, 45, 1396–1404. [Google Scholar]
  58. Xie, X.Y.; Han, X.Y.; Zhang, G.Z.; Fan, S.S.; Zhou, H.Z.; Zhang, X.J. Bacillus megaterium BMJBN02 induces the resistance of grapevine against downy mildew. Vitis 2022, 61, 101–109. [Google Scholar]
  59. Hamaoka, K.; Aoki, Y.; Suzuki, S. Isolation and characterization of endophyte Bacillus velezensis KOF112 from grapevine shoot xylem as biological control agent for fungal diseases. Plants 2021, 10, 1815. [Google Scholar] [CrossRef]
  60. Yu, X.L.; Qi, C.; Wang, P.S.; Li, B.Y.; Wang, Y.Z. Screening and identification of antagonistic bacteria against fungal pathogens in fruit trees and their antifungal mechanisms. J. Fruit Sci. 2016, 33, 734–743. [Google Scholar]
  61. Guo, J.P.; Ma, G.; Gao, X.K.; Fu, J.F. Preliminary report on screening and identification of antagonistic bacterium N22 against grape downy mildew and its controlling efficiency. China Plant Prot. 2016, 36, 9–14. [Google Scholar]
  62. Kang, X.J.; Shen, H.M.; Jia, Z.S.; Yang, J.Y.; Ran, L.X.; Zhen, Z.X. Identification of Bacillus methylotrophicus T3 and its control effect on grape downy mildew. Chin. J. Biol. Control 2016, 32, 775–782. [Google Scholar]
  63. Liang, C.H.; Zang, C.Q.; McDermott, M.I.; Zhao, K.H.; Yu, S.Y.; Huang, Y.Q. Two imide substances from a soil isolated Streptomyces atratus strain provide effective biocontrol activity against grapevine downy mildew. Biocontrol Sci. Technol. 2016, 10, 1337–1351. [Google Scholar] [CrossRef]
  64. Abdalla, M.A.; Win, H.Y.; Islam, M.T.; von Tiedemann, A.; Schüffler, A.; Laatsch, H. Khatmiamycin, a motility inhibitor and zoosporicide against the grapevine downy mildew pathogen Plasmopara viticola from Streptomyces sp. ANK313. J. Antibiot. 2011, 64, 655–659. [Google Scholar] [CrossRef]
  65. Jiang, X.T.; Zhao, K.H.; Liu, C.Y.; Liang, C.H.; Zang, C.Q. Screening and identifying of antagonistic actinomycete QH94 against Plasmopara viticola. J. Shenyang Agric. Univ. 2015, 46, 303–308. [Google Scholar]
  66. Liu, T.; Tao, W.Q.; Wang, H.; Hua, Y.P.; Liu, W.C. The antifungal activity of the metabolite of biocontrol strain A02 against some fruit tree diseases. North. Horticult. 2011, 17, 13–16. [Google Scholar]
  67. Ji, M.X.; Yao, K.B.; Miao, K.; Chen, H.Z.; Wu, X.; Zhuang, Y.Q. Toxicity test and field control effects of 4 different fungicides on grape downy mildew. Agric. Sci. Technol. 2016, 17, 1654–1657, 1752. [Google Scholar]
  68. El-Sharkawy, H.H.A.; Abo-El-Wafa, T.S.A.; Aal Ibrahim, S.A. Biological control agents improve the productivity and induce the resistance against downy mildew of grapevine. J. Plant Pathol. 2018, 100, 33–42. [Google Scholar] [CrossRef]
  69. Wang, X.J.; Dong, C.H.; Liu, C.Y.; Zhao, K.H.; Huang, Y.F.; Jiang, X.T. Identification of endophytic bacteria HB135 from grape and primary studies on its extract. J. Shenyang Agric. Univ. 2014, 45, 538–542. [Google Scholar]
  70. Shi, X.M.; Zhang, S.Y.; Wang, Y.C.; Shen, H.M.; Ran, L.X. Resuscitation of grape endophytic bacteria and their inhibitive effects against Plasmopara viticola. Acta Phytopathol. Sin. 2021, 51, 951–961. [Google Scholar]
  71. Lakkis, S.; Trotel-Aziz, P.; Rabenoelina, F.; Schwarzenberg, A.; Nguema-Ona, E.; Clément, C.; Aziz, A. Strengthening grapevine resistance by Pseudomonas fluorescens PTA-CT2 relies on distinct defense pathways in susceptible and partially resistant genotypes to downy mildew and gray mold diseases. Front. Plant Sci. 2019, 10, 1112. [Google Scholar] [CrossRef] [PubMed]
  72. Hu, J.D.; Wu, Y.Z.; Li, J.S.; Wei, Y.L.; Chen, Q.; Yang, H.T. The control effects of antagonistic Paenibacillus polymyxa PB-2 and its preparation against grape downy mildew. Shandong Sci. 2014, 27, 30–33. [Google Scholar]
  73. Hao, Z.P.; Tuinen, D.V.; Wipf, D.; Fayolle, L.; Chataignier, O.; Li, X.L.; Chen, B.D.; Gianinazzi, S.; Gianinazzi-Pearson, V.; Adrian, M. Biocontrol of grapevine aerial and root pathogens by Paenibacillus sp. strain B2 and paenimyxin in vitro and in planta. Biol. Control 2017, 109, 42–50. [Google Scholar] [CrossRef]
  74. Zang, C.Q.; Lin, Q.J.; Xie, J.H.; Lin, Y.; Zhao, K.H.; Liang, C.H. The biological control of the grapevine downy mildew disease using Ochrobactrum sp. Plant Protect. Sci. 2020, 56, 52–61. [Google Scholar] [CrossRef]
  75. Zang, C.Q.; Zhao, K.H.; Liu, C.Y.; Liang, C.H.; Liu, L.; Yu, S.Y. Inhibitory effect of SY286 strain against Plasmopara viticola. J. Shenyang Agric. Univ. 2014, 45, 221–224. [Google Scholar]
  76. Markellou, M.; Kapaxidi, E.; Karamaouna, F.; Samara, M.; Kyriakopoulou, K.; Anastasiadou, P.; Vavoulidou, E.; Meidanis, M.; Machera, K.; Mandoulaki, A.; et al. Evaluation of plant protection efficacy in field conditions and side effects of Lysobacter capsica AZ78, a biocontrol agent of Plasmopara viticola. Biocontrol Sci. Technol. 2022, 32, 930–951. [Google Scholar] [CrossRef]
  77. Puopolo, G.; Cimmino, A.; Palmieri, M.C.; Giovannini, O.; Evidente, A.; Pertot, I. Lysobacter capsici AZ78 produces cyclo(L-Pro-L-Tyr), a 2,5-diketopiperazine with toxic activity against sporangia of Phytophthora infestans and Plasmopara viticola. J. Appl. Microbiol. 2014, 117, 1168–1180. [Google Scholar] [CrossRef]
  78. Shen, H.M.; Li, Z.N.; Jia, Z.S.; Yang, J.Y.; Ran, L.X. Colonization of grape leaves by endophytic Bacillus subtilis JL4 and its control of grape downy mildew. Chin. J. Appl. Ecol. 2016, 27, 4022–4028. [Google Scholar]
  79. Wang, Y.L.; Li, J.S.; Wang, Y.Z.; Xin, X.Q.; Li, B.Y.; Xie, X.Y. Efficacy of Bacillus spp. BCJB01 and BMJBN02 on grape downy mildew. Northern Horticult. 2017, 17, 67–71. [Google Scholar]
  80. Banani, H.; Roatti, B.; Ezzahi, B.; Giovannini, O.; Gessler, G.; Pertot, I.; Perazzolli, M. Characterization of resistance mechanisms activated by Trichoderma harzianum T39 and benzothiadiazole to downy mildew in different grapevine cultivars. Plant Pathol. 2014, 63, 334–343. [Google Scholar] [CrossRef]
  81. Kamble, M.V.; Joshi, S.M.; Hadimani, S.; Jogaiah, S. Biopriming with rhizosphere Trichoderma harzianum elicit protection against grapevine downy mildew disease by triggering histopathological and biochemical defense responses. Rhizosphere 2021, 19, 100398. [Google Scholar] [CrossRef]
  82. El-Sharkawy, H.H.A.; Abo-El-Wafa, T.S.A.; Mostafa, N.A.; Yousef, S.A.M. Boosting biopesticide potential of Trichoderma harzianum for controlling the downy mildew and improving the growth and the productivity of King Ruby seedless grape. Egypt. J. Biol. Pest. Control 2023, 33, 61. [Google Scholar] [CrossRef]
  83. Parrilli, M.; Sommaggio, D.; Tassini, C.; Di Marco, S.; Osti, F.; Ferrari, R.; Metruccio, E.; Masetti, A.; Burgio, G. The role of Trichoderma spp. and silica gel in plant defence mechanisms and insect response in vineyard. Bull. Entomol. Res. 2019, 109, 771–780. [Google Scholar] [CrossRef] [PubMed]
  84. Falk, S.P.; Pearson, R.C.; Gadoury, D.M.; Seem, R.C.; Sztejnberg, A. Fusarium proliferatum as a biocontrol agent against grape downy mildew. Phytopathology 1996, 86, 1010–1017. [Google Scholar] [CrossRef]
  85. Shen, H.M.; Li, Z.N.; Yang, J.Y.; Zhang, M.; Ran, L.X. Identification of the mycoparasitic strain F3 on Plasmopara viticola and its control effect on grape downy mildew. J. Plant Protect. 2017, 44, 643–649. [Google Scholar]
  86. Ghule, M.R.; Sawant, I.S.; Oulkar, D.; Hingmire, S.; Shabeer, A.; Holkar, S. Identification of secondary metabolites in mycoparasites Fusarium strains and antifungal activity of fusaric acid against Plasmopara viticola. Arch. Phytopathol. Plant Protect. 2022, 55, 1283–1297. [Google Scholar] [CrossRef]
  87. Ghule, M.R.; Sawant, I.S.; Sawant, S.D.; Sharma, R.; Shouche, Y.S. Identification of Fusarium species as putative mycoparasites of Plasmopara viticola causing downy mildew in grapevines. Australas. Plant Dis. Notes 2018, 13, 16. [Google Scholar] [CrossRef]
  88. Thuerig, B.; Binder, A.; Boller, T.; Guyer, U.; Jimenez, S.; Rentsch, C.; Tamm, L. An aqueous extract of the dry mycelium of Penicillium chrysogenum induces resistance in several crops under controlled and field conditions. Eur. J. Plant Pathol. 2006, 114, 185–197. [Google Scholar] [CrossRef]
  89. Talontsi, F.M.; Islam, M.T.; Facey, P.; Douanla-Meli, C.; von Tiedemann, A.; Laatsch, H. Depsidones and other constituents from Phomopsis sp. CAFT69 and its host plant Endodesmia calophylloides with potent inhibitory effect on motility of zoospores of grapevine pathogen Plasmopara viticola. Phytochem. Lett. 2012, 5, 657–664. [Google Scholar] [CrossRef]
  90. Musetti, R.; Polizzotto, R.; Vecchione, A.; Borselli, S.; Zulini, L.; D’Ambrosio, M.; di Toppi, L.S.; Pertot, I. Antifungal activity of diketopiperazines extracted from Alternaria alternata against Plasmopara viticola: An ultrastructural study. Micron 2007, 38, 643–650. [Google Scholar] [CrossRef]
  91. Musetti, R.; Vecchione, A.; Stringher, L.; Borselli, S.; Zulini, L.; Marzani, C.; D’Ambrosio, M.; di Toppi, L.S.; Pertot, I. Inhibition of sporulation and ultrastructural alterations of grapevine downy mildew by the endophytic fungus Alternaria alternata. Phytopathology 2006, 96, 689–698. [Google Scholar] [CrossRef] [PubMed]
  92. Jaber, L.R. Grapevine leaf tissue colonization by the fungal entomopathogen Beauveria bassiana s.l. and its effect against downy mildew. BioControl 2015, 60, 103–112. [Google Scholar] [CrossRef]
  93. Rondot, Y.; Reineke, A. Endophytic Beauveria bassiana activates expression of defence genes in grapevine and prevents infections by grapevine downy mildew Plasmopara viticola. Plant Pathol. 2019, 68, 1719–1731. [Google Scholar] [CrossRef]
  94. Yacoub, A.; Haidar, R.; Mesguida, O.; Gerbore, J.; Hachicha, M.; Attard, E.; Guyoneaud, R.; Rey, P. Deciphering plant-induced responses toward Botrytis cinerea and Plasmopara viticola attacks in two grapevine cultivars colonized by the root biocontrol Oomycete, Pythium oligandrum. J. Fungi 2023, 9, 511. [Google Scholar] [CrossRef]
  95. Cruz-Silva, A.; Figueiredo, A.; Sebastiana, M. First insights into the effect of mycorrhizae on the expression of pathogen effectors during the infection of grapevine with Plasmopara viticola. Sustainability 2021, 13, 1226. [Google Scholar] [CrossRef]
  96. Burruano, S.; Alfonzo, A.; Lo Piccolo, S.; Conigliaro, G.; Mondello, V.C.; Torta, L.; Moretti, M.; Assante, G. Interaction between Acremonium byssoides and Plasmopara viticola in Vitis vinifera. Phytopathol. Mediterr. 2008, 47, 122–131. [Google Scholar]
  97. Lo Piccolo, S.; Alfonzo, A.; Giambra, S.; Conigliaro, G.; Lopez-Llorca, L.V.; Burruano, S. Identification of Acremonium isolates from grapevines and evaluation of their antagonism towards Plasmopara viticola. Ann. Microbiol. 2015, 65, 2393–2403. [Google Scholar] [CrossRef]
  98. Kortekamp, A. Epicoccum nigrum LINK: A biological control agent of Plasmopara viticola (BERK. et CuRT.) BERL. et DE ToNI? Vitis 1997, 36, 215–216. [Google Scholar]
  99. Harm, A.; Kassemeyer, H.H.; Seibicke, T.; Regner, F. Evaluation of chemical and natural resistance inducers against downy mildew (Plasmopara viticola) in grapevine. Am. J. Enol. Vitic. 2011, 62, 184–192. [Google Scholar] [CrossRef]
  100. Gomes, E.C.S.; Leite, R.P.; Silva, F.J.A.; Cavalcanti, L.S.; Nascimento, L.C.; Silva, S.M. Management of mildew and rust in grapes with resistance elicitors: Yield and postharvest quality. Trop. Plant Pathol. 2011, 36, 332–335. [Google Scholar]
  101. Perazzolli, M.; Roatti, B.; Bozza, E.; Pertot, I. Trichoderma harzianum T39 induces resistance against downy mildew by priming for defense without costs for grapevine. Biol. Control 2011, 58, 74–82. [Google Scholar] [CrossRef]
  102. Wang, L.; Huang, J.; Chen, S.; Su, X.; Zhang, X.; Wang, L.; Zhang, W.; Wang, Z.; Zeng, Q.; Wang, Q.; et al. Endogenous cell wall degrading enzyme LytD is important for the biocontrol activity of Bacillus subtilis. Front. Plant Sci. 2024, 15, 1381018. [Google Scholar] [CrossRef] [PubMed]
Jof 10 00702 g001
Figure 1. Infection cycle of Plasmopara viticola. The red arrow represents the direction and starting. point of the primary infection; the blue arrow indicates the direction and starting point of the secondary infection.
Figure 1. Infection cycle of Plasmopara viticola. The red arrow represents the direction and starting. point of the primary infection; the blue arrow indicates the direction and starting point of the secondary infection.
Jof 10 00702 g001
Jof 10 00702 g002
Figure 2. The biological process of Plasmopara viticola infecting grape plants.
Figure 2. The biological process of Plasmopara viticola infecting grape plants.
Jof 10 00702 g002
Jof 10 00702 g003
Figure 3. Mechanisms of biocontrol agents against grape downy mildew.
Figure 3. Mechanisms of biocontrol agents against grape downy mildew.
Jof 10 00702 g003
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Sun, Z.-B.; Song, H.-J.; Liu, Y.-Q.; Ren, Q.; Wang, Q.-Y.; Li, X.-F.; Pan, H.-X.; Huang, X.-Q. The Potential of Microorganisms for the Control of Grape Downy Mildew—A Review. J. Fungi 2024, 10, 702. https://doi.org/10.3390/jof10100702

AMA Style

Sun Z-B, Song H-J, Liu Y-Q, Ren Q, Wang Q-Y, Li X-F, Pan H-X, Huang X-Q. The Potential of Microorganisms for the Control of Grape Downy Mildew—A Review. Journal of Fungi. 2024; 10(10):702. https://doi.org/10.3390/jof10100702

Chicago/Turabian Style

Sun, Zhan-Bin, Han-Jian Song, Yong-Qiang Liu, Qing Ren, Qi-Yu Wang, Xiao-Feng Li, Han-Xu Pan, and Xiao-Qing Huang. 2024. "The Potential of Microorganisms for the Control of Grape Downy Mildew—A Review" Journal of Fungi 10, no. 10: 702. https://doi.org/10.3390/jof10100702

APA Style

Sun, Z.-B., Song, H.-J., Liu, Y.-Q., Ren, Q., Wang, Q.-Y., Li, X.-F., Pan, H.-X., & Huang, X.-Q. (2024). The Potential of Microorganisms for the Control of Grape Downy Mildew—A Review. Journal of Fungi, 10(10), 702. https://doi.org/10.3390/jof10100702

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