Plant Viral Disease Management

REVIEW
published: 20 January 2017

doi: 10.3389/fmicb.2017.00034
Bacteriophages and Bacterial Plant

Diseases
Colin Buttimer 1 , Olivia McAuliffe 2 , R. P. Ross 3 , Colin Hill 3 , Jim O’Mahony 1 and
Aidan Coffey 1*
1
Department of Biological Sciences, Cork Institute of Technology, Cork, Ireland, 2 Moorepark Food Research Centre,
Teagasc, Fermoy, Ireland, 3 Alimentary Pharmabiotic Centre, University College, Cork, Ireland
Losses in crop yields due to disease need to be reduced in order to meet increasing
global food demands associated with growth in the human population. There is a
well-recognized need to develop new environmentally friendly control strategies to
combat bacterial crop disease. Current control measures involving the use of traditional
chemicals or antibiotics are losing their efficacy due to the natural development of
bacterial resistance to these agents. In addition, there is an increasing awareness that
Edited by: their use is environmentally unfriendly. Bacteriophages, the viruses of bacteria, have
Stephen Tobias Abedon, received increased research interest in recent years as a realistic environmentally friendly
Ohio State University, USA
means of controlling bacterial diseases. Their use presents a viable control measure
Reviewed by:
Benjamin K. Chan,
for a number of destructive bacterial crop diseases, with some phage-based products
Yale University, USA already becoming available on the market. Phage biocontrol possesses advantages over
Robert Czajkowski, chemical controls in that tailor-made phage cocktails can be adapted to target specific
University of Gdańsk, Poland
disease-causing bacteria. Unlike chemical control measures, phage mixtures can be
*Correspondence:
Aidan Coffey easily adapted for bacterial resistance which may develop over time. In this review, we
[email protected] will examine the progress and challenges for phage-based disease biocontrol in food
crops.
Specialty section:
This article was submitted to Keywords: bacteriophages, plant diseases, biocontrol, biopesticides, phytopathogens
Antimicrobials, Resistance
and Chemotherapy,
a section of the journal
Frontiers in Microbiology
IMPORTANCE OF CROP DISEASES
Received: 01 June 2016 The human population is expected to reach 9.6 billion by 2050 and this will result in increased
Accepted: 06 January 2017
demands for food. It has been estimated that the global food supply may need to grow by as much
Published: 20 January 2017
as 70% in order to meet these demands (UN, 2013). For such growth, it has been predicted that
Citation: crop supply may have to increase as much as 80–110% (Ray et al., 2013). To achieve these yields,
Buttimer C, McAuliffe O, Ross RP,
the impact of crop disease has to be reduced. It has been estimated that at least 10% of global food
Hill C, O’Mahony J and Coffey A
(2017) Bacteriophages and Bacterial
production is lost to plant diseases (Strange and Scott, 2005). The major pathogens of plants are
Plant Diseases. Front. Microbiol. 8:34. parasitic plants, oomycetes, nematodes, viruses, fungi and bacteria. Among the latter, there are over
doi: 10.3389/fmicb.2017.00034 200 plant pathogenic bacterial species (Considine and Considine, 1995). Those considered to be the
Frontiers in Microbiology | www.frontiersin.org 1 January 2017 | Volume 8 | Article 34

Buttimer et al. Bacteriophages and Bacterial Plant Diseases
most important belonging to the genera of Pseudomonas, 1.5% (treated). However, this type of research became neglected
Ralstonia, Agrobacterium, Xanthomonas, Erwinia, Xylella, as understanding of the nature of phage was poor at the
Pectobacterium, and Dickeya (Mansfield et al., 2012). time, and data on their efficacy was limited (Okabe and Goto,
1963).
BACTERIOPHAGES, THEIR LIFE

CYCLES AND THEIR MORPHOLOGY BACTERIOPHAGE TYPES USED FOR
THERAPY/BIOCONTROL
Bacteriophages (phages) are the most abundant biological entity
in the biosphere with an estimated number of 1031 , as total From a terminology perspective, the term bacteriophage therapy
prokaryotic cell numbers are understood to be around 1030 in is usually reserved for human and animal applications. For plants
the biosphere and phage numbers are believed to be at least 10 the term bacteriophage biocontrol is more often used. In recent
times greater than this value (Whitman et al., 1998; Wommack years, several studies have been published on phage biocontrol
and Colwell, 2000). Phages are specific viruses of bacteria that on a number of important bacterial plant pathogens, with many
subvert the metabolism of their bacterial hosts in order to very promising results (see Table 1). The main deciding factor
replicate. Of the phages that have been identified, the majority whether a phage is applicable for biocontrol (and also therapy
belong to the tailed phages; and these form the Taxonomic in humans or animals) is whether a phage is exclusively lytic
Order: Caudovirales (Ackermann, 2007). These phages possess (virulent) or instead temperate in nature. Virulent phages are
icosahedral heads containing genomes comprised of double those which conduct infections that ultimately result in lysis of
stranded DNA. The order Caudovirales is made up of three their host bacterium with the release of progeny phage particles.
phage families; Myoviridae which have rigid contractile tails, Temperate phages can follow the lytic route of infection but
Podoviridae with short, non-contractile tails and Siphoviridae also follow the route of lysogeny, where the phage genome
with long flexible tails. Phages belonging to other families have integrates into the bacterial chromosome or persists as a plasmid.
highly variable morphologies with genomes of varying nucleic In this form the phage is known as a prophage (Łobocka
acid composition. et al., 2004). With this strategy, the phage genome replicates
as part of the bacterial genome of its host until a trigger
switches it into the lytic cycle. These triggers can be chemical
HISTORY OF BACTERIOPHAGES AND or physical (UV light or heat) in nature (Brunner and Pootjes,
THEIR USE AS ANTIBACTERIAL AGENTS 1969; Müller et al., 2012). It is interesting to note that certain
TOWARD PLANT DISEASES plant extracts can also trigger these events (Sato, 1983). Often,
prophage DNA can increase the fitness of the bacterial host
The discovery of bacteriophages is credited to Frederick Twort due to genes present on prophage genome. For example, in
(Twort, 1915) and Felix d’Herelle (d’Herelle, 1917). Similar the case of plant pathogens, the P. atrosepticum prophages
findings of antibacterial agents that hinted on the existence of ECA41 and ECA29 both improve the motility of the bacterial
phage had been made prior to that of Twort and d’Herelle host (Evans et al., 2010). Prophages may also harbor genes
(Abedon et al., 2011). However, they were the first to suggest for toxins, e.g., shiga, cholera, and diphtheria toxins (Abedon
this phenomenon as being viral in origin. The potential of and Lejeune, 2005). Another concern with these phages is the
phages as antibacterial agents was quickly recognized, with spread of virulence genes by transduction, where these phages
d’Herelle in 1919 demonstrating the capability of his phage can excise themselves from their host genomes incorporating
preparations to treat dysentery patients in the Hôpital des host DNA into their own genomes facilitating horizontal transfer
Enfants-Malades in Paris (Wilkinson, 2001). Following this work, of genetic material among bacteria (Griffiths et al., 2000). Also,
many early studies and attempts were made to use phages some lytic bacteriophages are capable of transduction, where they
to treat staphylococcal infections, cholera and bubonic plaque accidently pack bacterial DNA into their own capsid heads during
of humans (Sulakvelidze et al., 2001). This pre-antibiotic era the later stages of lytic cycle (Klumpp et al., 2008). There is
approach became known as bacteriophage therapy. Studies were also a third mechanism of phage-host interaction identified in
also initiated with the aim of using phages to control plant filamentous phages (Inovirus family). Here, phages form a non-
diseases. Mallmann and Hemstreet (1924) showed that the filtrate lethal chronic infection with continuous production of progeny
of decomposing cabbage could be used to inhibit the “cabbage- phages. However, suitability of these phages for biocontrol is
rot organism” Xanthomonas campestris pv. campestris. In 1925, questionable as their infection can have varying effects on host
Kotila and Coons demonstrated with bioassays that they could virulence, as shown with phytopathogen Ralstonia solanacearum
use phage to prevent soft rot by Pectobacterium atrosepticum with its phage φRSS1 causing increased virulence (Yamada,
and Pectobacterium carotovorum ssp carotovorum on slices of 2013), although it has been shown possible to isolate virulent
potato tuber and carrot, respectively (Coons and Kotila, 1925; filamentous phage (Kuo et al., 1994). Another undesirable
Kotila and Coons, 1925). The first field trials were also done by property in a phage intended for biocontrol is the ability to bring
Thomas (1935), who showed that he could reduce the incidence about superinfection exclusion to its host during infection. This
of Stewart’s wilt disease by treating seeds with phage against prevents secondary infection of the host by another phage (Lu
the phytopathogen Pantoea stewartii from 18% (untreated) to and Henning, 1994).

TABLE 1 | Summary of bacteriophage biocontrol experiments which have been conducted since the year 2000 to the present.
Pathogen Host Disease Information Reference
Pectobacterium carotovorum ssp. Potato Soft rot Bioassays with phage 8PD10.3 and 8PD23.1 could Czajkowski et al., 2015
carotovorum, Pectobacterium reduce severity of soft rot of tubers by 80% on potato
wasabiae, slices and 95% with whole tubers from a mixed
Dickeya solani pathogen infection.
Dickeya solani Potato Soft rot/Blackleg Phage vB_DsoM_LIMEstone1 and Adriaenssens et al., 2012
vB_DsoM_LIMEstone2 reduced soft rot of inoculated
tubers in bioassays and in field trials which produced a
potato crop with higher yields.
Dickeya solani Potato Soft rot Bioassays with phage 8D1, 8D2, 8D3, 8D4, 8D5, Czajkowski et al., 2014
8D7, 8D9, 8D10, 8D11 could reduce incidence of
soft rot by up to 30–70% on co-inoculated potato slices
with pathogen and phage.
Streptomyces scabies Potato Common scab Seed tubers treated with phage 8AS1 resulted in McKenna et al., 2001
producing tuber progeny with reduced levels of surface
lesion of scab (1.2%) compared with tubers harvested
from non -treated seed tubers (23%).
Ralstonia solanacearum Tomato Bacterial wilt Tomato plants treated with phage 8RSL1 showed no Fujiwara et al., 2011
symptoms of bacterial wilt during the experimental
period; whereas all untreated plants showed wilting
18 days post infection.
Ralstonia solanacearum Tomato Bacteria wilt Simultaneous treatment of phage PE204 with Bae et al., 2012
R. solanacearum of the rhizosphere of tomato
completely inhibited bacterial wilt. However,
pre-treatment with phage before the inoculation of
pathogen was not effective with control of bacterial wilt,
whereas post treatment of PE204 delayed disease
development.
Xanthomonas campestris pv. Tomato Bacterial spot Greenhouse experiments with formulated phage Balogh et al., 2003
vesicatoria cocktails could reduce disease severity with formulated
phage cocktails providing better protection in
comparison to unformulated. A similar effect was found
in three consecutive field trials.
Xanthomonas campestris pv. Tomato Bacterial spot In field experiments phage treatment was comparable Obradovic et al., 2004
vesicatoria to disease control with copper-mancozeb. Combination
of phage and plant activator (ASM) resulted in
enhanced control.
Xylella fastidiosa Grapevines Pierce’s Disease X. fastidiosa levels in grapevines were significantly Das et al., 2015
reduced on pre and post inoculation of a four phage
(Sano, Salvo, Prado and Paz) cocktail. Pierce disease
symptoms could be stopped using phage treatment
post infection as well as applying phage prophylactically
to grapevines.
Xanthomonas axonopodis pv. allii Onion Xanthomonas leaf Field trial showed that weekly and biweekly applications Lang et al., 2007
blight of onion of phage could reduce disease severity, a result which
was comparable to treatments of weekly applications of
copper-mancozeb.
Pectobacterium carotovorum ssp. Lettuce Soft rot Green house trials showed that phage PP1 could Lim et al., 2013
carotovorum significantly reduce disease development on lettuce
plants.
Streptomyces scabies Radish Common scab Phages Stsc1 and Stsc3 could prevent disease Goyer, 2005
development by treating radish seedlings. Non-treated
radishes had 30% less weight than negative control,
with phage treated radishes having masses similar to
negative control.
(Continued)

TABLE 1 | Continued
Pathogen Host Disease Information Reference
Xanthomonas axonopodis pv. citri Grapefruit Asiatic citrus Five greenhouse experiments utilizing phage treatment Balogh et al., 2008
canker could reduce disease severity by 59%. However, using
a skim milk formulation of phage did not have increased
disease control. Phage treatment was also capable of
reducing disease occurrence in a citrus nursery. Control
was less effective than copper-mancozeb. Combination
did not give increased disease control.
Xanthomonas axonopodis pv. Orange Citrus bacterial Phage treatments reduced citrus spot occurrence by Balogh et al., 2008
citrumelo spot 35 and 48% in two trials in commercial citrus nursery.
Control was equal or less effective than
copper-mancozeb. Combination did not give increased
disease control
Pseudomonas syringae pv. porri Leek Bacterial blight Specific bio-assays demonstrated the in planta efficacy Rombouts et al., 2016
of phages vB_PsyM_KIL1, vB_PsyM_KIL2,
vB_PsyM_KIL3, and vB_PsyM_KIL3b. However, phage
cocktail of six phages (vB_PsyM_KIL1, vB_PsyM_KIL2,
vB_PsyM_KIL3, vB_PsyM_KIL4, and vB_PsyM_KIL5
and vB_PsyM_KIL3b), were tested with two parallel
field trial experiments in three locations which showed
variable results. In one trial, symptom development was
attenuated.
Pseudomonas tolaasii Mushrooms Brown blotch Surface of mushrooms were inoculated with pathogen. Kim et al., 2011
Disease The formation of blotches was completely blocked by
co-incubation of phages with pathogen.
Erwinia amylovora Pear, apple trees Fire blight Phages 8Ea1337-26 and 8Ea 2345 reduced infection Boulé et al., 2011
of detached pear tree blossoms by 84 and 96%,
respectively, with Pantoea agglomerans as a carrier.
Also, infection of potted apple tree blossoms could be
reduced by 54% with phage 8Ea1337-26 and
P. agglomerans. Control was comparable to
streptomycin.
Ideally a phage for biocontrol applications should be where individual members work in synergy to eliminate the target
exclusively lytic and possess a host range which allows productive bacterium (Born et al., 2011).
infection on all strains of the pathogen genus/species being
targeted. Also, current opinion is that phages should be able to
lyse the host quickly while producing high numbers of progeny ADVANTAGES OF PHAGE BIOCONTROL
phage and diffuse easily though the environment to which they OVER OTHER STRATEGIES
are being applied. However, there was a report of a phage (φRSL1)
of the phytopathogen R. solanacearum which was described as Unlike chemical biocides, phages occur naturally in the
not highly lytic but still exhibited great biocontrol effect. The environment and humans are thus exposed to them on a
current standing theory of this phage’s disease prevention ability daily basis without any harm. After application, their numbers
is that it is capable of co-existing without complete removal increase if their target bacterial host species are accessible to
of its host from the soil surrounding crop roots, forming an them. However, they tend to persist in high numbers in any
equilibrium of infection that maintains the phage’s population but environment only long as the host is present (Iriarte et al.,
yet suppresses bacteria pathogenicity (Fujiwara et al., 2011). 2012). Thus, phages are unlike copper-based pesticides which
While a given phage’s infection properties may appear to have can potentially accumulate in the soil (Hirst et al., 1961; Pietrzak
great potential with in vitro studies, this does not necessarily and McPhail, 2004). Phages generally have a narrow host range,
translate into biocontrol potential in the field. Balogh (2006) typically being limited to stains within a particular species of
showed in a study of three phages of X. citri pv citri exhibiting bacteria. This can allow the creation of phage mixtures which
lytic activity in overlay plate assays that two of these phages can target bacterial species within a given genus of bacteria
were unable to lyse their host bacterium on grapefruit leafs, and only. This could be a specific bacterial phytopathogen or it
indeed were later shown to be ineffective for the suppression could be a particular bacterium in a microbial community
of citrus canker in greenhouse trials. Attention should also be whose suppression could help improve crop growth. Basit
paid to the receptors that a given phage recognizes on a bacterial et al. (1992) for example, isolated phage which was unable
target. This can aid in the creation of phage mixtures with a to infect a desired strain of Bradyrhizobium japonicum which
reduced likelihood of host resistance (Frampton et al., 2014), could aid soy bean crop growth due its nitrogen fixation
and as such can lead to the development of phage combinations properties, but could inhibit competing bacteria which did not

possess this feature, thus allowing enhanced nitrogen fixation to hosts. There has always been a constant race between phage and
occur. bacteria in nature. This is indicated by the fact that 10–20% of
Biofilm formation is an important factor in the virulence bacterial populations in certain habitats are lysed daily because of
of phytopathogens such a E. amylovora (Koczan et al., 2011; phage infection (Suttle, 1994). In the context of phage resistance,
Li and Wang, 2014). It is an attribute which has been shown Qiao et al. (2010) found that Pseudomonas syringae phage
to be involved in bacterial phytopathogen resistance to copper phi2954 was dependent on a host protein glutaredoxin 3 for
bactericides (Rodrigues et al., 2008). Phages have evolved to successful infection. Mutant host strains without this protein
overcome this biofilm barrier through the use of depolymerase were shown to be resistant to the phage. Nevertheless, these
enzymes on their capsids but can also be released on host authors showed it was possible to isolate mutants of the phage
lysis, which allows them to degrade biofilm material, allowing that had become independent of this host protein for infection
the phage anti-receptor to gain access to the receptors on the and this observation has been developed and employed in certain
surface of their host bacterium (Born et al., 2014). There is a phages aimed at biocontrol. Flaherty et al. (2001) also showed
growing demand by consumers for food produce that is free that phages could evolve to overcome phage resistance in target
from chemicals biocides and preservatives. This has resulted in bacteria and these were referred to as H-mutants. This allowed
the restricted use of chemicals to produce “organic label” crops. the development of phages with broader host ranges.
The requirements of such food require the absence of chemical In addition to simple mutation-based phage resistance,
residues in crop production and processing (Lohr, 2001). Since bacterial phytopathogens can also possess other more complex
phages are naturally occurring in the environment, they can resistance mechanisms such as the altruistic abortive infection
be registered as biopesticides, making them suitable for more (Abi) systems which give a bacterial host population immunity
consumer-friendly organic farming (OmniLytics, 2006). against a phage by causing phage-infected cells to commit
suicide in order to prevent phage reproduction (Parma et al.,
1992). While a number of these systems have been identified in
POTENTIAL ISSUES CONCERNING THE Lactococcus starter culture strains found in dairy fermentations
USE OF PHAGE IN BIOCONTROL (Coffey and Ross, 2002; Chopin et al., 2005), recently such a
system was identified in the phytopathogen P. atrosepticum and
The main limitation for the application of phages in biocontrol was termed ToxIN. This was characterized as a plasmid encoded
in most settings is bacterial host-range. While this can be an Type III protein-RNA toxin-antitoxin system. The toxic protein
advantage in certain circumstances, developing a phage-biocide ToxN is bound to RNA antitoxin ToxI in its inactive form.
that eliminates every member of a particular bacterial genus or However, when phage infection occured, ToxI RNA antitoxin
species can be a challenge. Frequently the development of phage became unbound from ToxN causing death of the bacterial host
mixtures (cocktails) overcomes this disadvantage. Occasionally cell (Fineran et al., 2009). Indeed, Blower et al. (2012) also
(but nevertheless, rarely) a phage is isolated which has an showed using phage phiTE, that the phage was capable of creating
unexpectedly broad host-range. One example of this is a phage mutants that could overcome this system by producing a pseudo
isolated from sewage and shown to target Pectobacterium and also ToxI RNA antitoxin preventing ToxN toxic activity.
enteric bacteria associated with humans (Pirhonen and Palva, Another mode of phage resistance is CRISPR/Cas systems,
1988). Thus, careful attention should be given to ensure full which are used by bacteria as well as archaea to form an immunity
understanding of likely host-range of a phage to avoid inefficacy to protect from infection by foreign DNA such as phage. These
or indeed to avoid the elimination of non-target potentially systems are comprised of clustered regularly interspaced short
beneficial bacteria. In the latter context, instances of phage palindromic repeat (CRISPR) arrays and CRISPR associated
infecting beneficial bacteria resulting in reduced crop yield have (Cas) proteins. In a recent study of 1,724 bacterial and archaeal
been reported (Basit et al., 1992; Ahmad and Morgan, 1994). genomes it was found that these systems were present in 10%
It is believed that phages do not directly interact with plants. of studied genomes. Previous studies had estimated CRISPR/Cas
However, a number of phage-like genes have been identified prevalence values of 40 and 80% of studied bacteria and
in wheat, corn and Arabidopsis cress (Hedtke et al., 1997; archaeal genomes, respectively (Burstein et al., 2016). These
Chang et al., 1999; Ikeda and Gray, 1999) which would suggest have been detected in phytopathogens such as P. atrosepticum
incorporation of phage DNA into the genomes of these crops and (Przybilski et al., 2011), E. amylovora (Rezzonico et al., 2011), and
thus a possible a role in their evolution. Xantomonas oryzae (Semenova et al., 2009). CRISPR arrays are
comprised of short stretches of DNA (termed spacers), which are
transcribed into short RNAs which interact with Cas proteins to
ADVANTAGES OF PHAGES IN THE detect and cut foreign DNA that match the sequence of the spacer
CONTEXT OF HOST RESISTANCE (protospacer). Spacer sequences are acquired during exposure
to foreign DNA in phage or plasmids, and thus they provide a
Like antibiotics and copper sprays, for which resistance has genetic immunity from invasion by foreign DNA due to previous
been reported, there is also the possibility of bacteria becoming encounters (Marraffini and Sontheimer, 2008). However, it is also
resistant to phage infection following constant exposure. possible for phage to evolve to overcome these systems. Indeed,
However, unlike chemicals, phages are biological entities which Semenova et al. (2009) detected a spacer in X. oryzae which
can evolve and overcome these biological alterations in their matched a protospacer of phage Xop411. However, the phage was

still able to infect this bacterium, due a mutation having occured that persist at relatively stable concentrations for several weeks in
in the protospacer sequence. soil (Fujiwara et al., 2011).
Bacteria developing resistance against phage infection is not
necessarily a negative development in the context of phage
biocontrol. Phage-resistance mutations in bacteria frequently PHAGE IN THE PHYLLOSPHERE
are accompanied by a fitness cost, one example being a
reduction in virulence, resulting in reduced disease severity. The phyllosphere is the portion of the plant which is above the
This results from the fact that molecules involved in phage ground and phages can readily be isolated from this location.
attachment are frequently also involved in the virulence process. How phages get there naturally has not been defined precisely,
Examples include lipopolysaccharide (LPS) (Evans et al., 2010a), although it is possible that they originate in the soil from which
extracellular polysaccharide (EPS) (Ayers et al., 1979), flagella the plant germinated - or alternatively get deposited by insect
(Evans et al., 2010b; Addy et al., 2012) and pili (Ahern et al., 2014). vectors. Indeed, phages for the phytopathogens Pantoea stewartii
Thus, mutations leading to resistance frequently compromise and Erwinia herbicola var. herbicola have been isolated from
virulence. There, are however, a few examples where these corn flea beetles (Woods et al., 1981). Another route is the
mutations in bacteria surface structures did not lead to reduced translocation of phage from the roots to leaves of plants through
virulence as seen with LPS production mutants of Pectobacterium the plant vascular system. And it has been shown that phages
and Dickeya (Schoonejans et al., 1987; Pirhonen et al., 1988). of R. solanacearum, Xanthomonas perforans, and Xanthomonas
euvesicatoria can translocate though tomatoes plants, phage of
Xanthomanas oryzae though the rice seedlings and phages of
BACTERIOPHAGE AND CHEMICALS E. amylovora though apple seedlings and fire thorn (Rao and
Srivastava, 1973; Iriarte et al., 2012; Kolozsváriné Nagy et al.,
Phage have been shown to be stable in certain agrichemicals 2015). However, this translocation may be influenced by the
(Ravensdale et al., 2010). However, precautions need to be phage type, plant age, plant size, plant species, plant health
taken with some chemicals being combined with phage. and possibly soil type in which the plant is growing (Iriarte
Chemical biocides typically contain a range of phage inactivating et al., 2012). It has also been reported that E. amylovora phages
substances such as surfactants and chelators (Yamamoto could pass from the leaves to the roots of apple seedlings
et al., 1968; Chattopadhyay et al., 2002). Also, copper-based (Kolozsváriné Nagy et al., 2015). The phyllosphere is nevertheless
bacteriocides have been shown to inactivate phage, but this a harsh environment for phages to survive and it has been
inactivation can be avoided with the delayed application of phage reported that their numbers can rapidly decline during daylight
(4–7 days) after initial application of copper-based bactericide hours (Balogh et al., 2003; Iriarte et al., 2007). The destructive
(Iriarte et al., 2007). influence of UV light from the sun has been reported to be
a limiting factor for the application of phages for successful
biocontrol. The radiation causes the formation of lesions in
COMPLEXITY OF PHAGE INTERACTION DNA which can block DNA replication and transcription. In
WITH SOIL an vivo study with phage phiXV3-16, Iriarte et al. (2007)
demonstrated a direct relationship between phage reduction on
The rhizosphere is the area of soil which is in close proximity tomato leaves and increasing UVA+B dose. They also showed
to the roots of a plant. There are several factors which can in an in vitro study that UV was capable of inactivating phage
affect phage activity in this environment such as pH, moisture used against Xanthomonas campestris pv. vesicatoria, preventing
levels, presence of organic matter and soil type. A number of it from exerting a biocontrol effect. Phage sensitivity against
these factors either individually or in combination can cause UV light has been shown to occur also with phage of Dickya
phage inactivation. Different soil types affect the survival of solani and E. amylovora phages (Czajkowski et al., 2014; Born
phage. For example, clay loam soils appear better at maintaining et al., 2015). However, there have been phages isolated against the
phage at low soil moisture levels and high soil temperatures than phytopathogen Pseudomonas syringae pv. actinidiae which can
that of sandy loam soils (Straub et al., 1992) As well, low soil tolerate extended UV-B doses (Yu et al., 2015). Other potential
pH can also negativity affect phage survivability (Sykes et al., factors that could cause phage decline on the phyllosphere
1981). are desiccation, temperature, pH as well as certain chemicals
Levels of adsorption of phage are affected differently in produced by plants (Erskine, 1973; Delitheos et al., 1997; Iriarte
differing soil types, with levels of hindrance varying from one et al., 2007).
phage type to another (Goyal and Gerba, 1979). Phage can
become bound to soil components such as clays (kaolinite
and montmorillonite) as these minerals possess positively PHAGE APPLICATION METHODS FOR
and negatively charged surfaces to which phage can adsorb OPTIMAL BIOCONTROL
(Schiffenbauer and Stotzky, 1982). Such adsorption can be PERFORMANCE ON PLANTS
influenced by pH (Goyal and Gerba, 1979; Loveland et al., 1996)
as well as the presence of organic materials (Zhuang and Jin, One of the limitations to effective phage biocontrol on crops is
2003). Under favorable conditions, phages have been identified the possibility of poor persistence on the phyllosphere due to

the factors discussed in the previous section. However, several blight E. amylovora and is being sold under the band name
methods have been found to reduce this problem. Survival of Bloomtime (Mikiciński et al., 2016). However, it has been
R
phage can be improved in the phyllosphere and rhizosphere if reported that combining this bacterium with phage biocontrol
they are accompanied by a viable host. This can be an avirulent can give enhanced protection that is comparable to that achieved
strain of the pathogen being targeted or indeed another species with the antibiotic streptomycin (Svircev et al., 2006; Boulé
of bacteria which occurs naturally in that environment (Svircev et al., 2011). A similar observation of enhanced control was
et al., 2006; Bae et al., 2012; Iriarte et al., 2012). It has also been seen using a bacteriocin-producing strain of R. solanacearum
found that avoiding daylight during application can improve with a phage to combat tobacco bacterial wilt (Tanaka et al.,
phage-based biocontrol. Indeed, it has been demonstrated that 1990). In another study, combining phage with Acibenzolar-S-
applying phage to tomato leaves in the evening resulted in longer methyl (ASM) was shown to have improved protection against
phage persistence in the phyllosphere, giving phage more time to bacterial spot of tomato in the field (Obradovic et al., 2004).
infect and kill their bacterial targets (Balogh et al., 2003; Iriarte However, combinations of phage with copper based pesticides do
et al., 2007). not appear to produce synergistic effects. Treatment with copper-
Born et al. (2015) conducted studies with number of mancozeb as seen with citrus canker and bacterial spot of citrus
substances to investigate if they gave phage protection against fruits did not produce synergy against Xanthomanas axonopodis
UV and reported that natural extracts from carrot, red pepper pv.citri or Xanthomanas axonopodis pv. citrumelo, respectively
and beetroot all gave protection as did casein, soy peptone and (Balogh et al., 2008). As mentioned previously, this could be due
also purfied aromatic amino acids, astaxathin and Tween 80. to phage sensitivity to the components of these copper based
None of these subtances had a compromising effect on phage sprays.
infection and stability (Born et al., 2015). Thus, it appears that
a wide range of substances could enhance phage preformance
in the phyllosphere with the main requirement being that they IMPROVED UNDERSTANDING OF
need to absorb UV thus limiting phage exposure. Biodegradable BACTERIAL HOST DIVERSITY SHOULD
polymers have also been shown to give these protective effects AID PHAGE BIOCONTROL AND
(Khalil et al., 2016). In addition, Balogh et al. (2003) also IMPROVE ITS SUCCESS IN THE FUTURE
showed an enhanced phage activity by combining the following
preparations with phage, namely (i) 0.5% pregelatinized corn Recent years have seen recognition of the increasing diversity and
(PCF) and 0.5% sucrose, (ii) 0.5% Casecrete NH400, 0.5% sucrose complexity of bacterial phytopathogens mainly due to advances
and 0.25% PCF and (iii) 0.75% skim milk and 0.5% sucrose. in molecular techniques (16S rRNA sequencing). For example,
These tests were performed in greenhouse trials and in field trials X. campestris pv. vesicatoria, which was previously a single species
on tomato plants with phages against Xanthomonas campestris has since been divided into four (Jones et al., 2004). Another
pv. vesicatoria. All formulations were used under a variety example is of the soft rot Erwinia group, which has undergone
of different conditions, but generally demonstrated enhanced a significant taxonomic reshuffle with creation of novel species
disease protection. and genera (Hauben et al., 1998; Gardan, 2003; Samson et al.,
Soil based phage delivery is another approach that has been 2005). These developments are very important, as while the
looked at to improve phage presistance in the phylosphere. Iriarte afflictions caused by these bacteria may appear identical on their
et al showed that a proprietary mixture of phage (OmniLytics respective crop targets, the phage sensitivities of the pathogens
Inc.) active against X. perforans strain 97-2 could translocate are likely to differ significantly, but nevertheless are likely to have
to the upper leaves of a tomato plant from its roots. They some correlation with their taxonomic groupings. For example,
demonstrated that these phages which were applied to soil at the soft rot Erwinia group, which affects potato crops, has
levels of 108 PFU/mL could be detected at titres of 104 PFU/g in more recently been reclassified into two new bacterial genera
leaf tissue for 7 days, whereas with a direct foliar application of (Pectobacterium and Dickeya), and these are relatively distinct
the same phage mix, phage were undetectable 1 to 2 days after from the point of view of phage susceptibilities (Czajkowski,
application (Iriarte et al., 2012). This work would suggest that 2016).
the phage control of foliar plant diseases could be controlled by
applying the phages to surrounding soil of a plant rather than by
foliar spraying. PHYTOPATHOGENS TARGETED FOR
PHAGE BIOCONTROL AND HOW THEY
ARE CURRENTLY MANAGED
COMBINATION OF PROTECTIVE
METHODS APPEAR TO BE THE BEST There are a number of important bacterial plant pathogens
DIRECTION FOR PHAGE BIOCONTROL that have received attention for phage biocontrol in recent
years (Table 1) as existing approaches are having limited
There is evidence to support that combining phage with efficacy or their use is restricted in certain regions of the
several methods used to control crop disease results in better world. The following section discusses selected crop pathogens
control. The bacterium Pantoea agglomerans has been used as where phage biocontrol has been evaluated and is showing
a biocontrol agent to suppress growth of the agent of fire promise.

Dickeya and Pectobacterium Pathogenesis typically involves the bacterium entering a

Both Dickeya and Pectobacterium belong to the family of susceptible plant host though the nectarthodes of its flowers, but
Enterobacteriacea, which collectively can be referred to as the it may also enter the plant though other openings such as wounds
Soft Rot Enterobacteriacea (SRE). Both genera characteristically (Bubán and Orosz-Kovács, 2003). Once in the plant, it is capable
produce several cell-wall-degrading enzymes that allow them of moving though the intracellular space of parenchyma, where at
to infiltrate and macerate the plant tissue on which they feed the latter stages it may reach the xylem vessels. Under favorable
(Pérombelon, 2002). The plant host range of both bacterial genera conditions, disease can present itself as wilting, necrosis of tissue
is very broad: species belonging to Dickeya have been reported and dieback of the plant (Vanneste and Eden-Green, 2000). The
to infect 10 monocot and 11 dicot families, while those of bacterium does not produce cell-wall-degrading enzymes but
Pectobacterium are reported to infect eleven monocot and sixteen the exopolysaccharide amylovoran, biofim formation capacity,
dicot families (Ma et al., 2007). motility, a type III secretion system, and quorum sensing are all
P. carotovorum ssp carotovorum has a wide host range and understood to be features in its virulence (Piqué et al., 2015).
global distribution, while P. atrosepticum is primarily found Traditionally, control of fire blight relies on cultural practices
in temperate climates with a host range mainly limited to the involving the removal of diseased tissue as well as preventative
potato (Pérombelon, 2002). P. wasabie and P. carotovurum ssp. sprays containing copper or antibiotics (Norelli et al., 2003).
brasilensis are also found to infect potato in several regions However, issues with these chemical controls is copper tolerance
worldwide (Waleron et al., 2013; Lee et al., 2014). In Europe, of the pathogen and also the long term of use antibiotics (such as
Dickeya dianthicola is reported to be very important in potato streptomycin) as a control strategy may be limited in the future,
disease, although more recently, a new Dickeya species called with growing concern of antibiotic resistance and the resulting
D. solani is being more frequently identified. Both also cause restricted used of antibiotics for agriculture in certain regions of
disease in other regions of the world (Toth et al., 2011). The the world such as EU countries (Ordax et al., 2006; Russo et al.,
economic impact of these potato infections can be severe. In the 2008; Mayerhofer et al., 2009; de León Door et al., 2013). As
Netherlands, they cause annual losses in the seed potato sector of mentioned, biological controls using antagonistic bacteria have
as much €30 million per year and in Israel, potato yield losses due shown a capacity for controlling the disease (Mikiciński et al.,
to Dickeya have been as much as 20–25% (Prins and Breukers, 2016)
2008; Tsror (Lahkim) et al., 2008).
With regard to the potato, there are no effective bactericides Ralstonia solanacearum
to protect against SRE and the most effective approach has Ralstonia solanacearum is a Gram negative soil-borne bacterium.
been through careful culturing practices, involving avoidance It is considered to be one of most destructive phytopathogens
of contamination and the removal of diseased plants and/or with a host range of up to 200 plant species from over 50
diseased tissue. Certification systems are also employed. These families (Denny, 2007). The bacterium is highly heterogeneous,
involve the propagation of seed plants using healthy tissue historically being divided into five races (based on plant host
culture plantlets followed by propagation in greenhouses, and range) and five biovars (based on carbon utilization) (Denny,
then open field grow-out production. It is accompanied by 2007). It causes diseases of economically important crops, such
careful monitoring and removal of diseased plants before release as bacterial wilt of tobacco, banana and tomato as well as brown
for general production. The generation number of these crops rot of the potato (Sanchez Perez et al., 2008). The bacterium has
is also kept low to limit bacterial build up. However, the global distribution (Sanchez Perez et al., 2008), and with regard
success of these certification schemes has been variable and to tomato and potato production, has quarantine status in the
heavily weather dependant (De Boer, 2004; Czajkowski et al., EU (Anonymous, 2000). The species has considerable economic
2011). impact: for example, brown rot of the potato has been estimated
to exceed more than €950 million in losses per year worldwide
Erwinia amylovora (Scherf et al., 2010). Infection begins by the bacterium entering
Erwinia amylovora, a member of the family of Enterobacteriacea, the host plant though its roots where it will then colonize the
is the causative agent of fire blight which is a destructive xylem. Infection typically leads to the development of yellowing
disease that occurs to species of the plant family Rosaceae. of the plant, stunted growth, wilting and death, although the
The disease has been reported in 40 countries across North bacterium is also capable of asymptomatic infections (Sanchez
America, Europe, the Pacific Rim, and the Middle East (Bonn Perez et al., 2008). Typical methods of control include the use of
and van der Zwet, 2000). It heavily affects apple and pear cultural practices such as selection of planting time, crop rotation,
production in several regions, with costs estimated as much using clean seedlings and the use of resistant cultivars (Mariano
as $100 million per year in the USA due to production losses et al., 1998). However, the use of such cultivars has shown a
and control measures (Norelli et al., 2003). It is considered negative correlation between resistance and yields (Yuliar et al.,
to be a quarantine concern in countries belonging to plant 2015). Also, resistance possessed by these cultivars tends to be
protection agencies of APPPC (Asia and Pacific Plant Protection strain specific (Wang et al., 2000).
Commission), COSAVE (Comite Regional de Sanidad Vegetal
para el Cono Sur), EPPO (Europe and Mediterranean Plant Pseudomonas syringe
Protection Organisation) and IAPC (Inter-African Phytosanitary The bacterial phytopathogen P. syringea belongs to the class of
Council) (CABI, 2016). Gammaproteobacteria (Hirano and Upper, 2000). The species is

currently subdivided into more than 50 pathovars, with different Xylella fastidiosa
pathovars representing different strains with differing plant host Xylella fastidiosa belongs to the of class of Gammaproteobacteria.
ranges (Hirano and Upper, 1990; Parkinson et al., 2011). Stains It is a xylem-limited phytopathogen that requires insect vectors
of most pathovars typically exhibit narrow host ranges, with (such as sharpshooters) for its distribution and infection of
pathovar P. syringea pv. syringea being an exception, having been its host plants (Chatterjee et al., 2008). It causes disease
reported to infect more than 80 plant species (Hirano and Upper, on a number of crops such as the grape, citrus, almond,
2000). peach and coffee (Hopkins and Purcell, 2002). While it has
Pseudomonas syringea pv. tomato causes necrotic lesions primarily been contained in the Americas, it has been indentified
surrounded by a yellow chlorotic halos on tomato, a disease in Europe in recent years causing disease on olive trees
known as bacterial speck (Cruz et al., 2010). The pathovar can (Hopkins and Purcell, 2002; Loconsole et al., 2014). Disease
also infect members of genera of Arabidopsis and Brassica in caused by the bacterium is believed to be induced by the
laboratory setting (Elizabeth and Bender, 2007). The disease formation of biofilm aggregates in the vascular system, which
reduces yields while also affecting fruit quality (Fatmi, 2003). restricts the movement of nutrients and water throughout
Pathogenesis by the bacterium involves the invasion of plant the plant (Chatterjee et al., 2008). It causes Pierce disease
tissue from natural openings, such as stomata, where a type III of the grapevine, a highly destructive infection, which heavily
secretion system plays a major role in its virulence with the affects grape production in the USA, and has been estimated
release of effectors to overcome the plant immune system (Xin to cost as much as $104.4 million annually to the state of
and He, 2013). It is spread by contaminated tomato seeds but California (Tumber et al., 2014). Existing control methods have
can also survive as an epiphyte for extended periods on tomato been limited in their management of the disease and include
plant surfaces and is dispersed in windblown rain (Smitley and removal of infected plants and control of the infected insect
McCarter, 1982; McCarter, 1983; Preston, 2000). Control of the vector populations with neonicotinoid-based insecticides (Janse
organism typically involves the use of uncontaminated seeds and and Obradovic, 2010). However, the use of these insecticides
the used of bactericides (copper and streptomycin) to limit its has seen restrictions in recent years due to their possible
spread (Preston, 2000; Fatmi, 2003). However, copper tolerant effects on honey bee populations (Anonymous, 2013; Lu et al.,
strains of the bacterium have been reported (Alexander et al., 2014).
1999).
Xanthomonas species CRITICAL SUMMARY OF RECENT

Xathomonas is a large genus, which belongs to the class of PHAGE BIOCONTROL STUDIES ON
Gammaproteobacteria, containing at least 27 official species, CROPS
many of which also possess several pathovars. Collectively, the
genus host range is broad: infecting around 400 plant hosts, There is growing evidence showing that phage have promising
a number of which are important crops such rice, banana, biocontrol applications for number of plant diseases in different
tomato, and citrus fruits. Species and pathovars of this genus crops. The following section describes recent studies that have
typically exhibit a high degree of host- as well as tissue-specificity, been conducted since the year 2000 and the findings from these
invading either the xylem or intercellular spaces of the mesophyll is summarized in Table 1.
parenchyma tissue (Ryan et al., 2011). The most common crops that appear to benefit from the
Xathomonas campestris pv. vesicatoria is the causitive agent application of phages for biocontrol in recent scientific literature
of bacterial spot disease of tomato and pepper, with the disease are the potato and the tomato, as both have been the focus
having been identified in many countries worldwide (Jones of numerous recent studies. The bacterial pathogens in the
et al., 2005). This tomato disease can be very severe with yield case of the potato are predominantly the SRE. As mentioned
losses of up to 50% reported for tomatoes grown both in above, one of the most important SREs in Europe is D. solani;
greenhouses and fields in the USA and Caribbean (Camesano, and the potential of phage to control this phytopathogen have
2015). Disease is caused by the bacterium entering the plant been assessed indicating strong potential for disease control. For
though stomata or wounds. The bacteria then colonize the example, Adriaenssens et al. (2012) conducted a bioassay and
intercellular space of the plant, inducing water-soaked lesions a field trial using phage (LIMEstone1). The bioassay involved
that later become necrotic, which can result in defoliation the incubation of seed tubers (cultivar Bintje), which had either
and severely spotted fruit (Thieme et al., 2005). Control of been inoculated with the bacteria or co-inoculated with the
the disease has involved preventative cultural practices such as bacteria and the phage (MOI of 100). They showed that tubers
avoiding unnecessary crop damage and using uncontaminated inoculated with the bacteria alone would experience to 40%
seed, but also includes use of resistant cultivars as well as maceration of tuber tissue, while those co-inoculated with the
chemical controls with copper or streptomycin (Goode and phage and bacteria exhibited no more than 10% maceration
Sasser, 1980). However, the use of resistant cultivars has not of tuber tissue. Similar results were observed with the seed
always been successful and there have been reports of bacteria tuber cultivar Kondor. The field trial using the same phage
developing resistance to the above two agents (Goode and Sasser, against the same pathogen also suggested it was capable of
1980; Ritchie and Dittapongpitch, 1991; McDonald and Linde, exerting this biocontrol effect in-planta, as phage treated infected
2002). seed potatoes resulted in higher crop yields than those without

phage treatment. Similar findings were reported by Czajkowski also received an OMRI listing making it suitable for use by
et al. (2014) who also isolated phages specific for D. solani. commercial organic growers (OmniLytics, 2006). A Hungarian
These workers conducted bioassays with tuber slices incubated company Enviroinvest was the second company to receive
with the bacterial pathogen with or without phages (MOI of registration for their biopesticide named Erwiphage for the
0.01) and showed that the application of phages could prevent control of fire blight of apple trees (specific for Erwinia
potato tuber tissue maceration by up to 70%. SREs other than amylovora) (Enviroinvest, n.d.). There is also a Scottish company,
D. solani were also studied for their susceptibility to phages APS biocontrol, which has developed a bacteriophage-based
by the same group. They found that the application of phages wash solution (Biolyse) for potatoes tubers, which is to be
(MOI of 0.01) to control P. carotovorum ssp carotovorum and used for prevention of soft rot disease (specific against soft rot
P. wasabie destruction could prevent damage of up to 80% Enterobacteriacea) during storage (APS Biocontrol Ltd, n.d.).
on tuber slices and up to 95% on whole tubers against tissue Interestingly this product has been reported to be used by the
maceration from a mixed bacterial infection (Czajkowski et al., Tesco supermarket chain (Branston, 2012).
2015). Such data is highly encouraging as many SRE infections However, in some regions of the world there are delays
tend to result for a mixture of genera/species. Aside from potato, that have to be overcome with regard to legislation allowing
SRE infections have also been controlled by phage in lettuce, phage biocontrol approaches for the of control of bacterial
with high levels of disease prevention being reported (Lim plant diseases. A problem with phage-mediated biocontrol is
et al., 2013). Aside from the SRE problem, potato infections that phage mixtures/cocktails need to be updated constantly
from the Gram-positive bacterium Streptomyces scabies results in order to lyse as many newly emerging strains of the target
in the formation of a corky lesion (known as common scab) bacterium as possible. This approach is used by Omnilytics
on the tuber and indeed other root vegetables also, as well as (OmniLytics, 2004). This allows a phage cocktail to be adapted
causing the reduced growth of seedlings (Lerat et al., 2009). to the relevant disease-causing bacterial strains in a given
This pathogen has also been successfully treated in potato by situation, also facilitating counteraction of any phage resistance
phage biocontrol and thus has implications for other crops also development during the phage application. However, EU
as demonstrated by Goyer (2005). In conclusion, the above regulations (1107/2009 EC) require that any change to one of
studies indicate strong potential for phage based control of these the components of a phage cocktail would require reregistering
diseases. which requires time and expense, making the US approach
Another crop which has been the focus of several studies in currently unfeasible in the EU (Doffkay et al., 2015). Legislation
the context of phage therapy is the tomato, which is commonly governing phage biocontrol may need to become more malleable
infected by R. solanacearum (also causes brown rot in the potato) in the EU for the best application and performance of phage
and X. campestris pathovars. Again, phage biocontrol approaches products as biopesticides.
have been demonstrated to give a significant reduction in
bacterial wilt (Ralstonia) and leaf spot caused by Xanthomonas.
Indeed, the successful trials against R. solanacearum reported by OTHER PHAGE APPLICATIONS OF THE
Mansfield et al. (2012) are significant considering the wide host PAST AND POSSIBLE FUTURE WITH
range of the bacterium. Similarly, in the case of Xanthomonas, REGARDS TO PHYTOPATHOGENS
the observed beneficial effect of the application of phages can also
be extrapolated to other plants affected by pathogens belonging to Phage typing schemes have been employed for several
the same genus. Indeed, studies on elimination of Xanthomonas phytopathogens for epidemiology studies (Toth et al., 1999;
using phage have been conducted with successful outcomes on Ahmad et al., 2014). These systems allow the identification of
both grapefruit and orange (Balogh et al., 2008) as well as onion a particular strain of a species based on their susceptibility to
(Lang et al., 2007). A variety of other crop infections have also series of phage. The downfall of this method, however, is that
been reduced in severity in other phage biocontrol studies. These it depends on the isolation of pure cultures for identification
include Pseudomonas infections of mushrooms (brown blotch) as well as the maintenance of stocks of typing phage as well as
and leeks (bacterial blight) and infection of the grapevine by host strains for which to propagate them. Nowadays, studies
Xylella (Das et al., 2015). of phytopathogens has moved away from phage typing due
to its tendency to generate false positives and false negatives
results as well as its low resolution and the development
COMMERCIALIZATION OF PHAGE FOR of new and improved molecular techniques (Czajkowski,
BIOCONTROL IN CROP DISEASE 2016)
Several phage-based detection systems have been developed
In recent years, several phage biocontrol products have reached for human and animal pathogens (van der Merwe et al.,
the market. A USA based company Omnilytics was the first 2014). Recently however, work has been published on the
company to receive registration (from the US Environmental promising application of these methods for the detection of
protection agency) for their phage based biopesticide product plant pathogens. Such a detection system has been developed for
Agriphage. The product is designed for the control of bacterial R. solanacearum, which is based on detection of the bacterium
spot or speck of tomatoes and peppers (specific for X. campestris by phage propagation followed with quantitative PCR (qPCR).
pv. vesicatoria, or P. syringae pv. tomato). This product has Samples that contain the bacterium will cause added phage

titres to increase, these titre increases can then be detected using However, approaches have been found to overcome some of these
qPCR. This method was found to be faster than conventional limitations with the use of UV protectant formulas and timing
methods with greater sensitivity allowing detection of 102 CFU/g of the application of phage to crops to avoid interaction with
of soil, 103 CFU/ml from drainage water from potted plants and chemical pesticides and exposure to UV light. In addition to
102 CFU/g in 0.1 g of leaf tissue. The method also does not biocontrol applications, there is also good potential for phage-
require the destruction of a plant for the detection of bacterium based diagnostics for plant pathogenic bacteria with a high
unlike those currently used to detect R. solanacearum (Kutin sensitivity aimed specifically at viable bacteria.
et al., 2009). It is possible to engineer phage of phytobacteria into Many pesticide companies are moving away from investment
reporter systems that can emit a detectable bioluminescent signal in chemical pesticides and increasingly directing their attention
during infection. A “luxAB-tagged” reporter phage was developed to biopesticides. The pesticide market is worth $56 billion with
for Pseudomonas cannabina pv. alisalensis (agent of bacterial the biopesticides forming only $2–3 billion of this. However,
blight of crucifers) which was shown capable of detecting the growth of the biopesticide sector is expected to outpace chemical
bacteria within minutes. This phage was also capable of emitting pesticides in the future (Marrone, 2014). This change is believed
a detectable signal during infection of both cultures and diseased to be due to an increasing customer demand for chemical residue
plant samples (Schofield et al., 2013). Both the mentioned systems free foods and increasing legalization on the use of synthetic
have advantages over other molecular detection methods, in pesticides in certain regions in the word. In addition, many
that phage propagation requires active metabolism, conveniently biopesticide products are potentially cheaper to develop and
limiting it to viable bacterial cells. quicker to bring to the market (Marrone, 2014). With this
economic environment, one can expect to see increased activity
in the development of phage biocontrol as a viable approach for
CONCLUSION crop disease control in the future.
Effective control of plant disease typically calls for a disease
management strategy that involves several integrated approaches.
Currently, the use of phage biocontrol is an emerging, but as AUTHOR CONTRIBUTIONS
yet uncommon practice. However, phages do possess several
properties which can add to the arsenal of controls for crop CB wrote this article. OM, RR, CH, JO, and AC critiqued
diseases. They are natural, making them suitable for organic and provided direction towards the article. AC is financing the
farming. They can be used to create phage cocktails with publication.
tailored host ranges. Also, phages naturally have the potential
to evolve to adapt to overcome phage-resistance or overcome
new strains of bacteria. They can be combined with other FUNDING
chemical or biocontrol agents. A possible limitation to their use
is their sensitivity to UV light and to certain soil conditions. CIT Rísam Ph.D. Scholarship.
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published: 20 January 2017

Bacteriophages and Bacterial Plant

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BACTERIOPHAGES, THEIR LIFE

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Pathogen Host Disease Information Reference

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Pathogen Host Disease Information Reference

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Dickeya and Pectobacterium Pathogenesis typically involves the bacterium entering a

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Xanthomonas species CRITICAL SUMMARY OF RECENT

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REFERENCES Ahmad, M. H., and Morgan, V. (1994). Characterization of a cowpea (Vigna

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