Professional Documents
Culture Documents
ARI
17 June 2007
10:33
Key Words
Abstract
The use of phages for disease control is a fast expanding area of plant
protection with great potential to replace the chemical control measures now prevalent. Phages can be used effectively as part of integrated disease management strategies. The relative ease of preparing
phage treatments and low cost of production of these agents make
them good candidates for widespread use in developing countries
as well. However, the efcacy of phages, as is true of many biological control agents, depends greatly on prevailing environmental
factors as well as on susceptibility of the target organism. Great
care is necessary during development, production and application of
phage treatments. In addition, constant monitoring for the emergence of resistant bacterial strains is essential. Phage-based disease
control management is a dynamic process with a need for continuous adjustment of the phage preparation in order to effectively ght
potentially adapting pathogenic bacteria.
245
ANRV319-PY45-11
ARI
17 June 2007
SAR: systemic
acquired resistance
246
10:33
CHALLENGES FOR
CONTROLLING BACTERIAL
DISEASES ON PLANTS
Plant diseases caused by bacteria are a major
economic liability to agricultural production.
Disease control has been a major challenge
for many bacterial diseases (21). This challenge is a direct result of pathogen variability,
high probability for mutation or gene transfer
in the pathogen when confronted with resistance genes or bactericides, high pathogen
multiplication rate during optimal conditions
for disease development, and lack of adequate
chemical-based approaches for control.
Disease control is best achieved using an integrated management approach by combining
proper cultural practices, chemicals such as
bactericides or plant activators where applicable, introgression of plant resistance genes,
and biological control strategies (75, 76).
Copper-based bactericides introduced in
the 1880s are still used extensively to combat many bacterial plant diseases, although
copper resistance has been reported in many
bacterial pathogens, including plasmid-borne
resistance and chromosomal resistance (7, 13
15, 55, 86). Bacterial diseases of plants have
been difcult to contain because few effective,
economical bactericides have been developed.
Streptomycin, an aminoglycoside antibiotic,
has been utilized in agriculture since the 1950s
to control phytopathogenic bacteria (95). Extensive use of this antibiotic for control of
various bacterial diseases resulted in increased
prevalence of streptomycin-resistant strains in
bacterial populations and reduced efcacy of
control of bacterial spot of tomato and pepper (95), re blight of apple and pear (60), as
well as many other bacterial plant pathogens
(25). Resistance develops as a result of both
selection pressure and the widespread distribution of plasmid-encoded streptomycin resistance genes (20, 68, 74, 90).
Systemic acquired resistance (SAR) plant
inducers have shown activity against bacterial
diseases of tomato and pepper (58, 75, 81),
Xanthomonas leaf blight on onion (32), and re
Jones et al.
ANRV319-PY45-11
ARI
17 June 2007
10:33
247
ANRV319-PY45-11
ARI
17 June 2007
Xcp: Xanthomonas
campestris pv. pruni
10:33
248
Jones et al.
ANRV319-PY45-11
ARI
17 June 2007
10:33
ADDRESSING HOST
RESISTANCE TO PHAGE
A major limiting factor in using phages for
control of plant diseases was the probability
of developing bacterial strains resistant to the
phage. This risk was addressed early on by
249
ANRV319-PY45-11
ARI
17 June 2007
10:33
4
X
1
E1
E1r
2
6
Annu. Rev. Phytopathol. 2007.45:245-262. Downloaded from arjournals.annualreviews.org
by U.S. Department of Agriculture on 01/16/08. For personal use only.
5
h-mutant
Figure 1
Development of phage-resistant bacterial strains and host-range mutant phages (h-mutant) in nature.
1, wild-type phage; 2, wild-type, specic bacterial host (E1); 3, 1 per 106 mutate to phage-resistance
(E1r); 4, wild-type phage cannot kill phage-resistant mutant (E1r); 5, 1 per 107 to 109 spontaneously
mutate to h-mutant; h = host-range (extended host range); 6, h-mutant kills both wild-type parent
bacteria and phage-resistant mutants.
h-mutant: host
range mutant phage
Xcpl: Xanthomonas
campestris pv.
pelargonii
250
CHALLENGES IN USING
PHAGES FOR DISEASE
CONTROL
The success of any particular biocontrol treatment is inuenced by agent and target densities (48). In the case of phage therapy, it is critical that the phage comes in contact with its
ARI
17 June 2007
10:33
host before it is destroyed (35) and the probability of phage-bacterium contact depends
on several factors: initial phage concentration,
rates of virion decay, phage replication ability in the target environment, concentration
and location of target bacteria, and presence
of adequate water as a medium for phage diffusion (33). Additionally, disease control efcacy may be inuenced by timing of phage
application, relative tness of phage-resistant
bacterial mutants (33), and the surrounding
environment.
Phages are utilized for controlling plant
pathogens either in the rhizosphere or phyllosphere. Gill & Abedon (33) identied several factors that can hinder success of disease
control in the rhizosphere. The rate of diffusion through the heterogeneous soil matrix is
low and changes as a function of available free
water. Phages can become trapped in biolms
(88), reversibly adsorb to particles of soil, such
as clay (98), and be inactivated by low soil
pH (92). Physical refuges can protect bacteria
from coming into contact with phages. Because of low rates of phage diffusion and high
rates of phage inactivation, only a low number
of viable phages is available to lyse target bac-
10
ANRV319-PY45-11
Skim milk
5
4
3
2
1
0
12
16
20
24
251
ANRV319-PY45-11
ARI
17 June 2007
10:33
6 AM
10
Effect of
application time on
the persistence of
bacteriophage
Xacm 2004-16 in
the tomato canopy
under eld
conditions. Phages
were applied at
6 a.m., 10 a.m.,
2 p.m. and 7 p.m.
on May 25, 2005,
in Citra, Florida.
Error bars indicate
the standard error.
Figure 3
10 AM
2 PM
7 PM
4
3
2
1
0
10
20
25
30
15
Jones et al.
DEVELOPMENT OF
PROTECTIVE FORMULATIONS
Various materials have been characterized to
determine if they could extend the life of
viruses following exposure to various physical factors. A number of materials were identied that increased residual activity of insect
viruses and other microbial pesticides by providing protection against sunlight UV and/or
rain leaching, including antioxidants and oxidative enzymes (41), aromatic/heterocyclic
amino acids (40), light adsorbing or reecting dyes (43, 93), activated charcoal (43),
starch- and our- (64, 65), alkaline gluten(10), casein- (11), and lignin-based formulations (12).
Several of these materials were evaluated
for extending phage persistence on tomato foliage and three formulations were identied
that had pronounced effects (3). These included (a) 0.5% pregelatinized corn our and
0.5% sucrose (PCF), (b) 0.5% Casecrete NH400 (a water-soluble casein polymer), 0.25%
pregelatinized corn our and 0.5% sucrose
(Casecrete), and (c) 0.75% skim milk powder
and 0.5% sucrose (skim milk) (3). These formulations increased phage persistence from
several hours to one to two days under
eld conditions compared to phage preparations applied without adding any protective
ANRV319-PY45-11
ARI
17 June 2007
10:33
materials (Figure 2) (3). The effect was signicant under greenhouse conditions as well.
Phages applied in PCF, Casecrete, and skim
milk formulations had 4700-, 38,500- and
100,000-fold higher populations, respectively,
than nonformulated phage two days after application (3). These same formulations were
evaluated for disease control efcacy in greenhouse and eld trials. Under greenhouse conditions they provided only minimal improvement in disease control, as phage treatments
applied in Casecrete and in skim milk formulations reduced disease severity compared
to nonformulated phage only in 1 of 3 experiments, whereas PCF formulation did not
have any signicant effect. Under eld conditions, however, the effect was more evident:
Casecrete-formulation improved disease control in 3 of 3 trials, PCF in 1 of 3 trials, and
the skim milk in the single trial in which it was
evaluated (5).
Although the formulations above enhanced phage persistence on leaf surfaces,
they also enhanced disease development: All
three of these formulations contributed to
signicant increases in tomato bacterial spot
severity when applied in the greenhouse without phages (5). Furthermore, the skim milk
formulation negated disease control of citrus
canker achieved with phage treatment in the
greenhouse (2). Proteins and sugars in the formulations most likely provided a nutritional
source for the pathogen and also may have facilitated ingress by breaking down surface tension and forming a continuous aqueous layer
on the leaf surface. There is clearly a need for
identifying biologically inert formulations to
improve efcacy of phages without enhancing
ingress.
PHAGE PROPAGATION IN
THE TARGET ENVIRONMENT
Another approach for maintaining high phage
populations is to coapply them with bacteria that are able to persist in the plant environment and that are sensitive to the phages.
Thus if the bacterial populations are main-
EFFECT OF PHAGE
DURABILITY AND IN VIVO
MULTIPLICATION ABILITY
ON DISEASE CONTROL
Two opposing factors determine phage population changes: decrease due to virion decay
and increase as a result of multiplication on
the host bacterium. Phages with lower rates
of virion decay and/or better multiplication
ability will maintain higher populations in the
phyllosphere and will likely be more effective in controlling populations of the target
pathogen. Phages differ in their ability to tolerate sunlight irradiation and persist on leaf
surfaces (2). Ability to survive the dry and wet
periods also can increase phage survival on leaf
surfaces. Although the majority of phages are
unable to survive desiccation, a desiccationtolerant phage has been isolated from the
plant phyllosphere (45).
The ability to increase populations by effectively multiplying on the leaf surfaces also
253
ARI
17 June 2007
10:33
leads to prolonged survival of the phage population. Balogh (2) found that two of three
phages that in vitro were able to lyse the host
bacterium Xanthomonas axonopodis pv. citri and
multiply to high populations were not able to
multiply on the same bacterial host in vivo on
grapefruit leaf surfaces and declined rapidly
within hours. These phages were also unable
to control citrus canker. A third phage, however, which was isolated from aerial plant tissue originally, was able to efciently multiply
in vivo and increased in numbers more than
threefold within nine hours. This phage exhibited effective control of the disease. It appears that selection of phages that are better
adapted to targeted environment contributes
to disease control and should be an important
consideration.
ANRV319-PY45-11
EFFECT OF APPLICATION
TIMING ON DISEASE
CONTROL EFFICACY
Timing of bacteriophage applications relative to arrival of the pathogen inuenced efcacy of disease control in several instances.
Civerolo & Keil (24) achieved a marked reduction of peach bacterial spot only if phage
treatment was applied one hour or one day
before inoculation with the pathogen. There
was a slight disease reduction when phage
was applied one hour after inoculation and
no effect if applied one day later. Civerolo
(23) suggested that bacteria were inaccessible to phage in the intercellular spaces, or
there were not enough phages reaching the
pathogen. Schnabel et al. (83) achieved a signicant reduction of re blight on apple blossoms when the phage mixture was applied at
the same time as the pathogen, E. amylovora.
In contrast, disease reduction was not significant when phages were applied a day before inoculation. Bergamin Filho (16) investigated the effect of timing on efcacy of
phage treatment in greenhouse trials with two
pathosystems: black rot of cabbage, caused by
X. campestris pv. campestris, and bacterial spot
of pepper, caused by X. campestris pv. vesicato254
Jones et al.
INTEGRATED STRATEGIES
A number of approaches have been used for
incorporating phage applications into part
of an integrated management strategy of
plant bacterial diseases. Tanaka et al. (94)
reduced tobacco bacterial wilt incited by R.
solanacearum by coapplication of an avirulent
strain of R. solanacearum and its phage that was
active against both the virulent and avirulent
strains. They reduced the ratio of wilted plants
with applications of an avirulent strain and
phage compared to the avirulent strain alone.
Recently, another approach to phage application has been reported (91). Field trials
were conducted with phages selected for their
broad host range on E. amylovora and their
ability to control the pathogen in forced pear
blossom bioassays. P. agglomerans, a biological
ANRV319-PY45-11
ARI
17 June 2007
10:33
control agent for E. amylovora, was used to deliver and sustain phages on the blossom surface. Using an integrated approach by combining two biological control agents (i.e., lytic
bacteriophages and P. agglomerans) effective
control of re blight was achieved that was
comparable to streptomycin (91).
In the past few years, considerable attention has been directed to development
of more sustainable strategies for reducing bacterial spot of tomato. Various combinations of biocontrol agents, including
strains of plant growth-promoting rhizobacteria (PGPR), bacterial antagonists, phages,
and SAR inducers (harpin, acibenzolar-Smethyl), were compared in greenhouse experiments (76). Tomato has been used as a model
system for developing an integrated management strategy for combining phages and other
alternative control strategies in an effort to
reduce severity of foliar tomato bacterial diseases given the extensive research done on
plant activators (58, 80), PGPR (47), and antagonistic bacteria (19, 99) to control bacterial spot of tomato. The idea was to integrate
the positive aspects of these practices in order to optimize benets in control of tomato
bacterial spot in the greenhouse and in eld
production.
Although a previous study proved effectiveness of phages in control of bacterial spot of tomato (29), greenhouse experiments showed inconsistent performance of
phage treatments (76). A single application
of unformulated phages used in this study
probably contributed to this inconsistency.
However, when phage was applied to plants
previously treated with SAR inducers, disease
control signicantly improved. The combination of harpin and phage signicantly reduced disease severity compared to harpin
alone. The SAR compound acibenzolar-Smethyl (ASM) effectively initiated plant defense mechanisms against X. campestris pv.
vesicatoria and prevented the occurrence of
disease symptoms under greenhouse conditions. However, in this experiment, plants
treated with ASM developed HR-like necrotic
spots when challenged with high concentrations of the pathogen. Application of phage
in combination with ASM resulted in elimination of HR-type lesions. Phage applications
were shown to decrease pathogen populations
on the leaf surface and concomitantly reduced
pathogen ingress. This in turn resulted in reduced intensity of the plant defense reaction
induced by ASM (76). Based on results from
greenhouse experiments (76), several combinations of SAR inducers and host-specic
phages were compared in eld trials. Although
ASM was not as effective in controlling bacterial spot in the eld as it was in greenhouse
experiments, it signicantly reduced disease
severity compared to untreated control. The
combination of ASM and phage provided an
additional reduction in disease pressure and
resulted in more effective foliar disease control than ASM, phage, or copper-macozeb
alone (75). Application of formulated hostspecic phages can be an effective alternative
to chemical bactericides for treatment of bacterial plant diseases. Phage treatment, integrated with other practices, is currently widely
used in greenhouses and production elds in
Florida as a part of a standard integrated management program for tomato bacterial spot
control.
PGPR: plant
growth-promoting
rhizobacteria
ASM: acibenzolarS-methyl
COMMERCIALIZATION
The rst commercial company to produce
phages specically for control of bacterial
plant diseases was AgriPhi, Inc., established by
L. E. Jackson (46). To minimize development
of bacterial strains resistant to the phage, mixtures of wild-type phages and h-mutants were
used. Only lytic phages isolated from plant
parts (leaves, stems, etc.) soil, and water (eld
runoff, river, and stream water and sewage
efuents) were utilized. To insure that temperate phages were not selected, phages were
never obtained from their respective bacterial
hosts. Although an h-mutant will attack and
kill both its specic wild-type host and bacterial phage-resistant mutants selected from this
parent, a secondary bacterial mutant resistant
255
ARI
17 June 2007
10:33
ANRV319-PY45-11
SUMMARY
Bacteriophages are viruses that infect bacteria.
Since their discovery in the early part of the
twentieth century, they have been evaluated
extensively for control of all kinds of bacterial
incited diseases, including plant diseases. In
the recent past, phages have been under evaluation for controlling re blight on apple and
pear, bacterial wilt on tobacco, citrus bacterial
canker, citrus bacterial spot, bacterial blight
on geranium, bacterial blotch of mushroom,
and Xanthomonas blight of onion.
Bacteriophages have great potential because they are widely present in nature; are
self-replicating; can be targeted against bacterial receptors that are essential for pathogenesis; are nontoxic to eukaryotes; and are
specic to certain bacterial species or strains
without damaging other, possibly benecial
members of the indigenous ora. Phages are
fairly easy and inexpensive to isolate, produce,
and store. They may also have application for
use in technologically less developed regions.
There are several challenges associated
with the use of phages. The bacteria can easily mutate and become resistant to an individual phage. Therefore, using a single phage
for control is risky. The environmental factors including exposure to sunlight radiation
and in particular UV, desiccation, temperature, and leaching may reduce phage populations. UV in particular will cause a dramatic
reduction. To increase longevity phages can
be applied with protective formulations or a
carrier bacterium in which they may multiply.
The reduction can also be countered by applying the phage in the evening or early morning
rather than during periods of high sunlight
irradiation. These approaches contribute to
the longer presence of high phage populations
in the target area increasing the likelihood of
control.
Phages have potential for use in integrated disease management strategies, especially with other biocontrol agents. The
combination of ASM and phage provided
additional reduction in disease and resulted
in more efcient foliar disease control than
ASM, phage, or copper-macozeb alone. In
two other instances, phages were coapplied
with bacteria that served as phage hosts as well
as biological control agents providing two levels of biological control simultaneously.
LITERATURE CITED
1. Adams MH. 1959. Bacteriophages. New York: Interscience
2. Balogh B. 2006. Characterization and use of bacteriophages associated with citrus bacterial
pathogens for disease control. PhD thesis. Univ. FL: Gainesville
3. Balogh B. 2002. Strategies of improving the efcacy of bacteriophages for controlling bacterial
spot of tomato. MS thesis. Univ. FL: Gainesville
256
Jones et al.
ANRV319-PY45-11
ARI
17 June 2007
10:33
4. Balogh B, Jones JB, Momol MT, Olson SM. 2005. Persistence of bacteriophages as
biocontrol agents in the tomato canopy. Proc. Int. Symp. Tomato Dis., 1st, Orlando, FL.
ISHS Acta Hortic. 695:299
5. Balogh B, Jones JB, Momol MT, Olson SM, Obradovic A. 2003. Improved efcacy of
newly formulated bacteriophages for management of bacterial spot on tomato. Plant Dis.
87:94954
6. Balogh B, Jones JB, Stall RE, Dilley J, Yonce H, et al. 2006. Control of Asiatic citrus
canker and citrus bacterial spot with bacteriophages in Florida. Proc. Int. Symp. Biol.
Cont.Bac. Plant Dis., 1st, Seeheim/Darmstadt, Germany. MBBLF 408:4647
7. Basim H, Stall RE, Minsavage GV, Jones JB. 1999. Chromosomal gene transfer by
conjugation in the plant pathogen Xanthomonas axonopodis pv. vesicatoria. Phytopathology
89:104449
8. Basit HA, Angle JS, Salem S, Gewaily EM. 1992. Phage coating of soybean seeds reduces
nodulation by indigenous soil bradyrhizobia. Can. J. Microbiol. 38:126469
9. Beckerich A, Hauduroy P. 1922. Le bacteriophage dans le traitment de la `evre typhode
C.R. Soc. Biol. 86:168
10. Behle RW, McGuire MR, Gillespie RL, Shasha BS. 1997. Effects of alkaline gluten on
the insecticidal activity of Bacillus thuringiensis. J. Econ. Entomol. 90:35460
11. Behle RW, McGuire MR, Shasha BS. 1996. Extending the residual toxicity of Bacillus
thuringiensis with casein-based formulations. J. Econ. Entomol. 89:1399405
12. Behle RW, Tamez-guerra P, Mcguire MR. 2003. Field activity and storage stability of
Anagrapha falcifera nucleopolyhedrovirus (af MNPV) in spray-dried lignin-based formulations. J. Econ. Entomol. 96:106675
13. Bender CL, Cooksey DA. 1987. Molecular cloning of copper resistance genes from Pseudomonas syringae pv. tomato. J. Bacteriol. 169:47074
14. Bender CL, Cooksey DA. 1986. Indigenous plasmids in Pseudomonas syringae pv. tomato:
conjugative transfer and role in copper resistance. J. Bacteriol. 165:53441
15. Bender CL, Malvick DK, Conway KE, George S, Cooksey DA. 1990. Characterization
of pXv10A, a copper resistance plasmid in Xanthomonas campestris pv. vesicatoria. Appl.
Environ. Microbiol. 56:17075
16. Bergamin Filho A, Kimati H. 1981. Estudos sobre um bacteriofago isolado de Xanthomonas campestris. II. seu emprego no controle de X. campestris e X. vesicatoria. Sum.
Phytopathol. 7:3543
17. Boyd RJ, Hildebrandt AC, Allen ON. 1971. Retardation of crown gall enlargement after
bacteriophage treatment. Plant Dis. Rep. 55:14548
18. Brunoghe R, Maisin J. 1921. Essais de therapeutique au moyen du bacteriophage du
staphylocoque. C. R. Soc. Biol. 102921
19. Byrne JM, Dianese AC, Ji P, Campbell HL, Cuppels DA. 2005. Biological control of
bacterial spot of tomato under eld conditions at several locations in North America.
Biol. Control 32:40818
20. Chiou C, Jones AL. 1993. Nucleotide sequence analysis of a transposon (Tn5393) carrying streptomycin resistance genes in Erwinia amylovora and other gram-negative bacteria.
J. Bacteriol. 175:73240
21. Civerolo EL. 1982. Disease management my cultural practices and environmental control. In Phytopathogenic Prokaryotes, ed. MS Mount, GH Lacy, 2:34360. New York:
Academic
22. Civerolo EL. 1973. Relationship of Xanthomonas pruni bacteriophages to bacterial spot
disease in prunus. Phytopathology 63:127984
www.annualreviews.org Bacteriophages for Plant Disease Control
257
ARI
17 June 2007
10:33
23. Civerolo EL. 1972. Interaction between bacteria and bacteriophages on plant surfaces
and in plant tissues. Proc. Int. Conf. Plant Pathog. Bact., 3rd, Wageningen. Wageningen:
Cent. Agric. Publ. Doc.
24. Civerolo EL, Keil HL. 1969. Inhibition of bacterial spot of peach foliage by Xanthomonas
pruni bacteriophage. Phytopathology 59:196667
25. Cooksey DA. 1990. Genetics of bactericide resistance in plant pathogenic bacteria. Annu.
Rev. Phytopathol. 28:20119
26. Coons GH, Kotila JE. 1925. The transmissible lytic principle (bacteriophage) in relation
to plant pathogens. Phytopathology 35770
27. Davison WC. 1922. The bacteriolysant therapy of bacillary dysentery in children.
Therapeutic application of bacteriolysants; dHerelles phenomenon. Am. J. Dis. Child.
23:531
28. Flaherty JE, Harbaugh BK, Jones JB, Somodi GC, Jackson LE. 2001. H-mutant bacteriophages as a potential biocontrol of bacterial blight of geranium. HortScience 36:98
100
29. Flaherty JE, Jones JB, Harbaugh BK, Somodi GC, Jackson LE. 2000. Control of bacterial spot on tomato in the greenhouse and eld with H-mutant bacteriophages. HortScience
35:88284
30. Frey P, Prior P, Marie C, Kotoujansky A, Trigalet-Demery D, Trigalet A. 1994. Hrp
mutants of Pseudomonas solanacearum as potential biocontrol agents of tomato bacterial
wilt. Appl. Environ. Microbiol. 60:317581
31. Gassmann W, Dahlbeck D, Chesnokova O, Minsavage GV, Jones JB, Staskawicz BJ.
2000. Molecular evolution of virulence in natural eld strains of Xanthomonas campestris
pv. vesicatoria. J. Bacteriol. 182:705359
32. Gent DH, Schwartz HF. 2005. Management of xanthomonas leaf blight of onion with
a plant activator, biological control agents, and copper bactericides. Plant Dis. 89:631
39
33. Gill JJ, Abedon ST. 2003. Bacteriophage ecology and plants. APSnet
34. Gill JJ, Svircev AM, Smith R, Castle AJ. 2003. Bacteriophages of Erwinia amylovora. Appl.
Environ. Microbiol. 69:213338
35. Goodridge LD. 2004. Bacteriophage biocontrol of plant pathogens: fact or ction? Trends
Biotechnol. 22:38485
36. Goto M. 1992. Fundamentals of Bacterial Plant Pathology, San Diego: Academic
37. Goyal SM, Gerba CP, Bitton G, eds. 1987. Phage Ecology. New York: Wiley
38. Graham JH, Leite JRP. 2004. Lack of control of citrus canker by induced systemic resistance compounds. Plant Dis. 88:74550
39. Greer GG. 2005. Bacteriophage control of foodborne bacteria. J. Food Prot. 68:110211
40. Ignoffo CM, Garcia C. 1995. Aromatic/heterocyclic amino acids and the stimulated
sunlight-UV inactivation of the Heliothis/Helicoverpa baculovirus. Environ. Entomol.
24:48082
41. Ignoffo CM, Garcia C. 1994. Antioxidant and oxidative enzyme effects on the inactivation of inclusion bodies of the heliothis baculovirus by simulated sunlight-UV. Environ.
Entomol. 23:102529
42. Ignoffo CM, Garcia C. 1992. Combinations of environmental factors and simulated
sunlight affecting activity of inclusion bodies of the heliothis (lepidoptera: Noctuidae)
nucleopolyhedrosis virus. Environ. Entomol. 21:21013
43. Ignoffo CM, Garcia C, Saathoff SG. 1997. Sunlight stability and rain-fastness of formulations of baculovirus heliothis. Environ. Entomol. 26:147074
ANRV319-PY45-11
258
Jones et al.
ANRV319-PY45-11
ARI
17 June 2007
10:33
44. Ignoffo CM, Rice WC, McIntosh AH. 1989. Inactivation of nonoccluded and occluded
baculoviruses and baculovirus-DNA exposed to simulated sunlight. Environ. Entomol.
18:17783
45. Iriarte FB, Balogh B, Momol MT, Smith LM, Wilson M, Jones JB. 2007. Factors affecting
survival of bacteriophage on tomato leaf surfaces. Appl. Environ. Microbiol. 73:170411
46. Jackson LE. 1989. U.S. Patent No. 4828999
47. Ji P, Campbell HL, Kloepper JW, Jones JB, Suslow TV, Wilson M. 2006. Integrated
biological control of bacterial speck and spot of tomato under eld conditions using
foliar biological control agents and plant growth-promoting rhizobacteria. Biol. Control
36:35867
48. Johnson KB. 1994. Dose-response relationships and inundative biological control. Phytopathology 84:78084
49. Jones JB, Iriarte FB, Obradovic A, Balogh B, Momol MT, Jackson LE. 2006. Management of bacterial spot on tomatoes with bacteriophages. Proc. Int. Symp. Biol. Control Bact.
Plant Dis., 1st, Darmstadt, Germany, 408:154. Land-Forstwirtsch: Mitt. Biol. Bundesanst.
50. Katznelson H. 1937. Bacteriophage in relation to plant diseases. Bot. Rev. 3:499521
51. Kotila JE, Coons GH. 1925. Investigations on the blackleg disease of potato. Mich. Agric.
Exp. Stn. Tech. Bull. 329
52. Kousik CS, Ritchie DF. 1996. Disease potential of pepper bacterial spot pathogen races
that overcome the Bs2 gene for resistance. Phytopathology 86:133643
53. Kuo T, Cheng L, Yang C, Yang S. 1971. Bacterial leaf blight of rice plant IV. Effect of
bacteriophage on the infectivity of Xanthomonas oryzae. Bot. Bull. Acad. Sinica 12:19
54. Kutter E. 1997. Phage Therapy: Bacteriophages as Antibiotics. http://www.evergreen.
edu/phage/phagetherapy/phagetherapy.htm
54a. Lang JM, Schwartz HF, Gent DH. 2004. Alternative strategies for onion Xanthomonas
leaf blight management. Phytopathology 94:S6
55. Lee Y, Hendson M, Ponopoulos NJ, Schroth MN. 1994. Molecular cloning, chromosomal mapping, and sequence analysis of copper resistance genes from Xanthomonas
campestris pv. juglandis: homology with small blue copper proteins and multicopper oxidase. J. Bacteriol. 176:17388
56. Leverentz B, Conway WS, Alavidze Z, Janisiewicz WJ, Fuchs Y. 2001. Examination of
bacteriophage as a biocontrol method for salmonella on fresh-cut fruit: a model study. J.
Food Prot. 64:111621
57. Leverentz B, Conway WS, Camp MJ, Janisiewicz WJ, Abuladze T. 2003. Biocontrol of
Listeria monocytogenes on fresh-cut produce by treatment with lytic bacteriophages and a
bacteriocin. Appl. Environ. Microbiol. 69:451926
57a. Liu T. 1998. Biological control with tomato bacterial spot with hrp mutants of Xanthomonas
campestris pv. vesicatoria. MS thesis. Univ. FL: Gainesville
58. Louws FJ, Wilson M, Campbell HL, Cuppels DA, Jones JB. 2001. Field control of
bacterial spot and bacterial speck of tomato using a plant activator. Plant Dis. 85:48188
59. Mallmann WL, Hemstreet CJ. 1924. Isolation of an inhibitory substance from plants.
Agric. Res. 599602
60. Manulis S, Zutra D, Kleitman F, Dror O, David I. 1998. Distribution of streptomycinresistant strains of Erwinia amylovora in Israel and occurrence of blossom blight in the
autumn. Phytoparasitica 26:22330
61. Marco GM, Stall RE. 1983. Control of bacterial spot of pepper initiated by strains of
Xanthomonas campestris pv. vesicatoria that differ in sensitive to copper. Plant Dis. 67:779
81
www.annualreviews.org Bacteriophages for Plant Disease Control
259
ARI
17 June 2007
10:33
62. Massey RE. 1934. Studies on blackarm disease of cotton III. Empire Cotton Growing Rev.
11:18893
63. Maxson-Stein K, He SY, Hammerschmidt R, Jones AL. 2002. Effect of treating apple
trees with acibenzolar-S-methyl on re blight and expression of pathogenesis-related
protein genes. Plant Dis. 86:78590
64. McGuire MR, Shasha BS, Lewis LC, Bartelt RJ, Kinney K. 1990. Field evaluation of granular starch formulations of Bacillus thuringiensis against Ostrinia nubilalis (Lepidoptera:
Pyralidae). J. Econ. Entomol. 83:220710
65. McGuire MR, Shasha BS, Lewis LC, Nelsen TC. 1994. Residual activity of granular
starch-encapsulated Bacillus thuringiensis. J. Econ. Entomol. 87:63137
66. McKenna F, El-Tarabily KA, Hardy GESTJ, Dell B. 2001. Novel in vivo use of a polyvalent streptomyces phage to disinfest streptomyces scabies-infected seed potatoes. Plant
Pathol. 50:66675
67. McNeil DL, Romero S, Kandula J, Stark C, Stewart A, Larsen S. 2001. Bacteriophages:
a potential biocontrol agent against walnut blight (Xanthomonas campestris pv. juglandis).
NZ Plant Prot. 54:22024
68. Minsavage GV, Canteros BI, Stall RE. 1990. Plasmid-mediated resistance to streptomycin
in Xanthomonas campestris pv. vesicatoria. Phytopathology 80:71923
69. Momol MT, Jones JB, Olson SM, Obradovic A, Balogh B, King P. 2002. Integrated
management of bacterial spot on tomato in Florida. Rep. PP110, EDIS, Inst. Food Agric.
Sci., Univ. FL. Online
70. Moore ES. 1926. dHerelles bacteriophage in relation to plant parasites. South Afr. J. Sci.
23:306
71. Morrison J. 1932. Bacteriophage in the Treatment and Prevention of Cholera. London: Lewis
72. Munsch P, Olivier JM. 1995. Biocontrol of bacterial blotch of the cultivated mushroom
with lytic phages: some practical considerations. Mushroom Sci. 14:595602
73. Munsch P, Olivier JM, Houdeau G. 1991. Experimental control of bacterial blotch by
bacteriophages. In Science and Cultivation of Edible Fungi, ed. MJ Maher, pp. 38996.
Rotterdam, Neth.: Balkema
74. Norelli JL, Burr TJ, Lo Cicero AM, Gilbert MT, Katz BH. 1991. Homologous streptomycin resistance gene present among diverse gram-negative bacteria in New York state
apple orchards. Appl. Environ. Microbiol. 57:48691
75. Obradovic A, Jones JB, Momol MT, Balogh B, Olson SM. 2004. Management of tomato
bacterial spot in the eld by foliar applications of bacteriophages and SAR inducers. Plant
Dis. 88:73640
76. Obradovic A, Jones JB, Momol MT, Olson SM, Jackson LE, et al. 2005. Integration of
biological control agents and systemic acquired resistance inducers against bacterial spot
on tomato. Plant Dis. 89:71216
77. Okabe N, Goto M. 1963. Bacteriophages of plant pathogens. Annu. Rev. Phytopathol.
1:397418
78. Osawa S, Furuse K, Watanabe I. 1981. Distribution of ribonucleic acid coliphages in
animals. Appl. Environ. Microbiol. 41:16468
79. Pernezny K, Collins J, Stall RE, Shuler K, Datnoff LE. 1999. A serious outbreak of race
6 of Xanthomonas campestris pv. vesicatoria on pepper in southern Florida. Plant Dis. 83:
79
80. Qui D, Wei ZM, Bauer DW, Beer SV. 1997. Treatment of tomato seed with harpin
enhances germination and growth and induces resistance to Ralstonia solanacearum.
Phytopathology 87:S80
ANRV319-PY45-11
260
Jones et al.
ANRV319-PY45-11
ARI
17 June 2007
10:33
81. Romero AM, Kousik CS, Ritchie DF. 2001. Resistance to bacterial spot in bell pepper
induced by acibenzolar-S-methyl. Plant Dis. 85:18994
82. Saccardi A, Gambin E, Zaccardelli M, Barone G, Mazzucchi U. 1993. Xanthomonas
campestris pv. pruni control trials with phage treatments on peaches in the orchard. Phytopathol. Mediterr. 32:20610
83. Schnabel EL, Fernando WGD, Meyer MP, Jones AL, Jackson LE. 1999. Bacteriophage
of Erwinia amylovora and their potential for biocontrol. Acta Hortic. 489:64954
84. Slopek S, Weber-Dabrowska B, Dabrowski M, Kucharewica-Krukowska A. 1987. Results
of bacteriophage treatment of suppurative bacterial infections in the years 19811986.
Arch. Immunol. Ther. Exp. 35:56983
85. Solodovnikov YP, Pavlova LI, Emelyanov PI. 1970. Prophylactic application of dry polyvalent dysentery bacteriophage with pectin in childrens preschool. Z. Mikrobiol. Epidemiol.
Immunobiol. 47:13137
86. Stall RE, Loschke DC, Jones JB. 1986. Linkage of copper resistance and avirulence loci
on a self-transmissible plasmid in Xanthomonas campestris pv. vesicatoria. Phytopathology
76:24043
87. Stanier T, McSharry J, Speitel T. 1967. Agrobacterium tumefaciens conn IV. bacteriophage
PB2 and its inhibitory effect on tumor induction. J. Virol. 1:26873
88. Storey MV, Ashbolt NJ. 2001. Persistence of two model enteric viruses (B408 and
MS-2 bacteriophages) in water distribution pipe biolms. Water Sci. Technol. 43:133
38
89. Summers WC. 2005. Bacteriophage research: early history. In Bacteriophages: Biology and
Applications, ed. E Kutter, A Sulakvelidze, pp. 527. Boca Raton, FL: CRC Press
90. Sundin GW, Bender CL. 1993. Ecological and genetic analysis of copper and streptomycin resistance in Pseudomonas syringae pv. syringae. Appl. Environ. Microbiol. 59:1018
24
91. Svircev AM, Lehman SM, Kim W, Barszcz E, Schneider KE, Castle AJ. 2006. Control
of the re blight pathogen with bacteriophages. Proc. Int. Symp. Biol. Control Bact. Plant
Dis., 1st, Seeheim/Darmstadt, Germany, 259. Berlin: Dtsch. Bibl., CIP-Einh.aufn.
92. Sykes IK, Lanning S, Williams ST. 1981. The effect of pH on soil actinophage. J. Gen.
Microbiol. 122:27180
93. Tamez-Guerra P, McGuire MR, Behle RW, Shasha BS, Wong LJG. 2000. Assessment
of microencapsulated formulations for improved residual activity of Bacillus thuringiensis.
J. Econ. Entomol. 93:21925
94. Tanaka H, Negishi H, Maeda H. 1990. Control of tobacco bacterial wilt by an avirulent
strain of Pseudomonas solanacearunm M4S and its bacteriophage. Ann. Phytopathol. Soc. Jpn.
56:24346
95. Thayer PL, Stall RE. 1961. A survey of Xanthomonas vesicatoria resistance to streptomycin.
Proc. Fla. Hortic. Soc. 75:16365
96. Thomas RC. 1935. A bacteriophage in relation to Stewarts disease of corn. Phytopathology
25:37172
97. Vidaver AK. 1976. Prospects for control of phytopathogenic bacteria by bacteriophages
and bacteriocins. Annu. Rev. Phytopathol. 14: 45165
98. Williams ST, Mortimer AM, Manchester L. 1987. Ecology of soil bacteriophages. In
Phage Ecology, ed. SM Goyal, CP Gerba, G Bitton, pp. 15779. New York: Wiley
99. Wilson M, Campbell HL, Ji P, Jones JB, Cuppels DA. 2002. Biological control of
bacterial speck of tomato under eld conditions at several locations in North America.
Phytopathology 92:128492
www.annualreviews.org Bacteriophages for Plant Disease Control
261
ANRV319-PY45-11
ARI
17 June 2007
10:33
100. Woods TL, Israel HW, Sherf AF. 1981. Isolation and partial characterization of a bacteriophage of Erwinia stewartii from the corn ea beetle, Chaetocnema pulicaria. Prot. Ecol.
3:22936
101. Zaccardelli M, Saccardi A, Gambin E, Mazzucchi U. 1992. Xanthomonas campestris pv.
pruni bacteriophages on peach trees and their potential use for biological control. Phytopathol. Mediterr. 31:13340
262
Jones et al.
AR319-FM
ARI
13 July 2007
17:17
Annual Review of
Phytopathology
Contents
AR319-FM
ARI
13 July 2007
17:17
vi
Contents