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. 2020 Aug 7;9(8):493. doi: 10.3390/antibiotics9080493

Table 1.

Relevant examples of phages used in the biocontrol of plant pathogens.

Phage/Phages Cocktails
(Family)
Target Microorganism Plant Disease Relevant Achievements Reference
ΦAS1
(Siphoviridae)
Streptomyces scabies Potato Common scab
  • Isolation of a new phage from a potato field near Albany, Western Australia

  • Phage propagation by an effective mini-biorreactor

  • Efficient disinfection of seed potato tubers: phage-treated seeds significantly reduced the levels of surface lesions of scab compared with untreated tubers

[70]
vB_DsoM_LIMEstone1, vB_DsoM_LIMEstone2
(Myoviridae)
Dickeya solani Potato Soft rot/Blackleg
  • Isolation of new phages from soil samples from a potato field trial (Merelbeke, Belgium)

  • In laboratory assays, the phages reduced the disease incidence and the severity on potato tubers. In a field trial (using potato tubers infected with D. solani), the phage treatment resulted in higher crop yields

[71]
ΦD1, ΦD2, ΦD3, ΦD4, ΦD5, ΦD7, ΦD9, ΦD10, ΦD11
(Myoviridae)
Dickeya solani Potato Soft rot/Blackleg
  • Isolation of new phages from soil samples collected in different regions in Poland

  • In the in vitro and potato slice assay experiments, phages were able to stop the growth and efficiently lyse D. solani cells, protecting the tuber tissue from maceration caused by the bacteria

[72]
ΦPD10.3, ΦPD23.1
(Myoviridae)
Pectobacterium carotovorum ssp. carotovorum
P. wasabiae
Dickeya solani
Potato Soft rot/Blackleg
  • Isolation of new phages from soil, rhizosphere soil, and potato plant and tuber samples obtained from different regions in Poland

  • Phage genomes were characterized and proteomes obtained

  • In potato slice and whole tuber assays, the phages (applied individually or together) were able to reproducibly and significantly reduce soft rot infections when compared to controls (inoculated with a mixture of bacteria)

[73]
P-PSG-1 (Siphoviridae), P-PSG-2, P-PSG-3, P-PSG-7 (Siphoviridae), P-PSG-8, and P-PSG-9 Ralstonia solanacearum Potato Bacterial wilt
  • Isolation of new phages from different water sources in Kenya and China

  • A phage cocktail with speed and efficacy in the lysis of R. solanacearum enhanced was formulated

  • The phage cocktail was very effective protecting the potato plants from bacterial wilt by injection of the phages into the plants. The cocktail was also able to reduce the density of live bacteria in pathogen-contaminated sterilized soils

[74]
vB_PatP_CB1, vB_PatP_CB3, vB_PatP_CB4
(Podoviridae)
Pectobacterium atrosepticum Potato Soft rot/Blackleg
  • Isolation of new phages from soil samples collected from potato grading machinery and potato fields from two farms in Co. Cork, Ireland

  • Phage genomes were characterized and the proteome for CB1 obtained

  • The cocktail containing phages CB1, CB3, and CB4 showed effective protective effect, evaluated on whole tubers, against the infection caused by a mix of two strains of P. atrosepticum (DSM 18077 and DSM 30186)

[75]
Dagda, Dagda_B1, Katbat, Luksen, Mysterion, P694 (Podoviridae) Dickeya solani Potato Soft rot/Blackleg
  • Isolation of new phages from different environments at different time points and at different locations in Denmark

  • A phage cocktail formulated with ability to significantly decrease the incidence of soft rot and the disease severity after 5 days of storage post-infection with D. solani

[76]
Wc5r, Phage cocktail Pectobacterim atrosepticum
P. carotovorum
Potato Soft rot/Blackleg
  • Isolation of new phages from soil and water samples collected in Wuhan, China

  • Phage Wc5r showed cross-activity against P. atrosepticum and two phage-resistant P. carotovorum strains

  • A formulated phage cocktail applied on potato slices (before or within an hour after bacterial inoculation) was able to reduce 90% soft rot symptoms

[77]
Mixture of four h-mutant (Agriphage, Agriphi, Logan, Utah) Xanthomonas campestris pv. vesicatoria Tomato Bacterial spot
  • Foliar applications of phages to field-grown tomatoes decreased disease severity compared with untreated control plants.

  • The incidence of bacterial spot on greenhouse-grown seedlings was also reduced in bacteriophage-treated plants

[78]
Formulated phage cocktails Xanthomonas campestris pv. vesicatoria Tomato Bacterial spot
  • The formulations analyzed significantly increased the longevity of the phage on the plant surface

  • Protective formulations significantly improved the efficacy of phage treatments both in the greenhouse and in the field. Skim milk and Casecrete gave the best results in greenhouse and field assays, respectively

[79]
6 Phages (Agriphage, OmniLytics, Inc., Salt Lake Cith, UT) combined with plant activator (ASM) Xanthomonas campestris pv. vesicatoria Tomato Bacterial spot
  • Formulation of a phage mixture containing six different phages specific to X. campestris pv. vesicatoria race T3 strain 91–118

  • In field experiments, application of host-specific phages was effective against the bacterial spot pathogen, showing better disease containment than with copper-Mancozeb or the untreated controls

[80]
ΦRSL1
(Myoviridae)
Ralstonia solanacearum Tomato Bacterial wilt
  • Alternative phage biocontrol method using a unique phage instead of a phage cocktail

  • During the experimental period, tomato plants treated with ΦRSL1 phage showed no symptoms of wilting, whereas all untreated plants had wilted by 18 days post-infection.

  • Active ΦRSL1 particles can be recovered from the roots of treated plants and from soils 4 months post-infection

[81]
PE204
(Podoviridae)
Ralstonia solanacearum Tomato Bacterial wilt
  • Simultaneous application of phage PE204 and R. solanacearum on tomato rhizosphere completely inhibited the occurrence of bacterial wilt.

  • Addition of Silwet L-77 to the phage suspension did not impair the disease control activity of the phage, allowing the control of the bacterial wilt

[82]
Stsc1, Stsc3 (Siphoviridae) Streptomyces scabies Radish Common scab
  • Isolation of new phages from soil samples

  • Phages Stsc1 and Stsc3 infected 88% and 75% of the pathogenic S. scabiei strains tested, respectively

  • Both phages prevented symptoms of S. scabiei on radish seedlings

[83]
Bacteriophage mixture (AgriPhage, OmniLytics, Salt Lake City, UT) Xanthomonas axonopodis pv. allii Onion Xanthomonas leaf blight
  • Under field conditions, applications of the mix of phages reduced disease severity in an equivalent or better manner than weekly applications of copper hydroxide plus Mancozeb.

  • Phage populations remained on onion leaves for at least 72 to 96 h under field and greenhouse conditions, respectively

[84]
PP1
(Podoviridae)
Pectobacterium carotovorum ssp. carotovorum Lettuce Soft rot/Blackleg
  • Isolation of a new phage from soil samples (Chinese cabbage fields)

  • A rapid and strong lytic activity against its host bacteria was shown by the new phage

  • Treatment with phage PP1 significantly reduced the disease caused by P. carotovorum subsp. carotovorum

[85]
vB_PsyM_KIL1, vB_PsyM_KIL2, vB_PsyM_KIL3, vB_PsyM_KIL4, and vB_PsyM_KIL5, vB_PsyM_KIL3b (Myoviridae) Pseudomonas syringae pv. porri Leek Bacterial blight
  • Isolation of new phages from infected fields in Flanders

  • Phage genomes were characterized and proteomes obtained

  • Classified into a novel clade

  • Development of a phage cocktail effective against 41 tested strains

  • Specific bio-assays showed the in planta effectiveness of phages and attenuation of symptoms development in a field experiment

[86]
ΦXOT1, ΦXOT2, ΦXOM1, ΦXOM2, ΦXOF1, ΦXOF2, ΦXOF3, ΦXOF4 (Siphoviridae) Xanthomonas oryzae Rice Leaf blight disease (BLB)
  • Isolation of new phages from diseased plant leaves and soil samples

  • The phage ΦXOF4 showed the broadest host range, killing all the pathogenic X. oryzae strains tested

  • Seedlings raised from phage-treated seeds displayed complete bacterial growth inhibition and reduced incidence of BLB disease

[87]
CP2, ΦXac2005-1, ccΦ7, ccΦ13, ΦXacm2004-4, ΦXacm2004-16, ΦX44, ΦXaacA1 Xanthomonas axonopodis pv. citri Grapefruit Asiatic citrus canker
  • In greenhouse assays, phage treatment significantly reduced the disease severity when applied without skim milk. If skim milk was added, no disease reduction was observed

  • In a citrus nursery no synergistic effect was observed by combining phages and copper-Mancozeb

[88]
ΦEa1337-26 (Podoviridae),
ΦEa2345-6
(Myoviridae)
Erwinia amylovora Pear and apple trees Fire blight
  • Isolation of new phages from apple and pear orchards in the Okanagan and Fraser Valleys of British Columbia

  • Phages ΦEa1337-26 and ΦEa2345-6 reduced the bacterial infection by 84% and 96%, respectively, when applied on detached pear blossoms using as a carrier the epiphyte bacterium Pantoea agglomerans Eh21-5

  • Phage ΦEa2345-6, combined with Eh21-5, reduced infection of fire blight on apple flowers of potted apple trees with an efficacy comparable to the antibiotic streptomycin

[89]
CP2, ΦXac2005-1, ccΦ7, ccΦ13, ΦXacm2004-4, ΦXacm2004-16, ΦX44, ΦXaacA1 Xanthomonas axonopodis pv. citrumelo Orange Citrus bacterial spot
  • In a commercial citrus nursery, phages application significantly reduced the progress of the disease on Valencia oranges (a moderately susceptible culture)

  • In an experimental nursery, under low disease pressure, phage treatment significantly reduced the disease incidence providing similar levels of control than copper-Mancozeb treatment

[88]
Sano, Salvo, Prado, Paz Xylella fastidiosa subsp. fastidiosa Grapevines Pierce’s disease (PD)
  • Development of a cocktail with four lytic phages

  • The phage cocktail significantly reduced X. fastidiosa levels in grapevines and prevented the development of PD symptoms

  • No in planta phage-resistant X. fastidiosa isolates were recovered, and in vitro selected X. fastidiosa mutants did not cause PD symptoms

[90]
KHUΦ34 (Myoviridae), KHUΦ38 (Podoviridae), KHUΦ44 (Myoviridae) Pseudomonas syringae pv. actinidiae Kiwifruit Canker disease
  • Isolation of new phages from soils collected from kiwifruit orchards in South Korea

  • Phages showed activity against strains of P. syringae pv. actinidiae, including Psa2 and Psa3 groups. Some of them were also effective against other P. syringae pathovars

  • The effective lytic activity of phages KHUΦ34, KHUΦ38, and KHUΦ44 allows one to propose their potential use in the control of bacterial canker disease in kiwifruits

[91]
Φ6 (Cystoviridae)
Leibniz-
Institute DSMZ collection
Pseudomonas syringae pv. actinidiae Kiwifruit Canker disease
  • Phage Φ6 was effective against two biovar 3 (a highly aggressive pathogen) Psa strains using both in vitro and ex vivo test

  • The inactivated CRA-FRU 14.10 Psa strain did not re-grow after treatment was concluded

[92]
PN05
PN09
Cocktail of both phages
(Myoviridae)
Pseudomonas syringae pv. actinidiae Kiwifruit Canker disease
  • Isolation of new phages from water samples collected in Hangzhou, China

  • The combined treatment with phages (PN05 and PN09) and carvacrol effectively reduced the Psa concentration, preventing the emergence of phage-resistant mutants and controlling biofilm development

[93]
ΦPto-bp6g Pseudomonas tolaasii Pleurotus ostreatus Brown blotch disease
  • The phage ΦPto-bp6g was characterized at the genomic level

  • Phage ΦPto-bp6g showed strong bactericidal activity against P. tolaasii

  • The mushroom (P. ostreatus) buds treated with the mixture of P. tolaasii and phage ΦPto-bp6g, exhibited over time the same growing pattern that the control, developing normal mushroom fruit bodies

[94]

Entries are grouped according to the agricultural crop, and the works related to the same crop were ordered chronologically.