3 Current trends in management of bacterial pathogens infecting plants

Abstract

Plants are continuously challenged by different pathogenic microbes that reduce the quality and quantity of produce and therefore pose a serious threat to food security. Among them bacterial pathogens are known to cause disease outbreaks with devastating economic losses in temperate, tropical and subtropical regions throughout the world. Bacteria are structurally simple prokaryotic microorganisms and are diverse from a metabolic standpoint. Bacterial infection process mainly involves successful attachment or penetration by using extracellular enzymes, type secretion systems, toxins, growth regulators and by exploiting different molecules that modulate plant defence resulting in successful colonization. Theses bacterial pathogens are extremely difficult to control as they develop resistance to antibiotics. Therefore, attempts are made to search for innovative methods of disease management by the targeting bacterial virulence and manipulating the genes in host plants by exploiting genome editing methods. Here, we review the recent developments in bacterial disease management including the bioactive antimicrobial compounds, bacteriophage therapy, quorum-quenching mediated control, nanoparticles and CRISPR/Cas based genome editing techniques for bacterial disease management. Future research should focus on implementation of smart delivery systems and consumer acceptance of these innovative methods for sustainable disease management.

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https://doi.org/10.1007/s10482-023-01809-0
REVIEW PAPER
Current trends inmanagement ofbacterial pathogens
infecting plants
AditiSharma · A.K.Gupta· BanitaDevi
Received: 8 September 2022 / Accepted: 8 January 2023
© The Author(s), under exclusive licence to Springer Nature Switzerland AG 2023
Abstract Plants are continuously challenged by dif-
ferent pathogenic microbes that reduce the quality
and quantity of produce and therefore pose a serious
threat to food security. Among them bacterial patho-
gens are known to cause disease outbreaks with dev-
astating economic losses in temperate, tropical and
subtropical regions throughout the world. Bacteria are
structurally simple prokaryotic microorganisms and
are diverse from a metabolic standpoint. Bacterial
infection process mainly involves successful attach-
ment or penetration by using extracellular enzymes,
type secretion systems, toxins, growth regulators and
by exploiting different molecules that modulate plant
defence resulting in successful colonization. Theses
bacterial pathogens are extremely difficult to control
as they develop resistance to antibiotics. Therefore,
attempts are made to search for innovative methods
of disease management by the targeting bacterial
virulence and manipulating the genes in host plants
by exploiting genome editing methods. Here, we
review the recent developments in bacterial disease
management including the bioactive antimicrobial
compounds, bacteriophage therapy, quorum-quench-
ingmediated control, nanoparticles and CRISPR/Cas
based genome editing techniques for bacterial disease
management. Future research should focus on imple-
mentation of smart delivery systems and consumer
acceptance of these innovative methods for sustain-
able disease management.
Keywords Phytopathogenic bacteria·
Virulence· Bioactive compounds· Bacteriophage·
Nanoparticles· Quorum-quenching· CRISPR/Cas9
genome editing
Introduction
Plant pathogenic bacteria cause disease outbreaks in
many economically important plants with severe con-
sequences on food production and security. Infected
plants exhibit different types of damaging symptoms
such as blight, canker, galls and overgrowths, wilts,
leaf spots, specks, scab and soft rots etc. Bacteria
vary in shape and sizes, cell wall structure, presence
or absence of flagella, biochemical properties and
genetic basis (Fuchs 1998; Buonaurio 2008). The
taxonomy of plant pathogenic bacteria is in continu-
ous flux and the classification is being revised based
on recent advancements in genomic approaches.
Mainly, most of the phytopathogenic bacteria belong
to family Xanthomonadaceae, Pseudomonadaceae,
A.Sharma(*)
College ofHorticulture andForestry, Thunag- Mandi,
Dr. Y. S. Parmar University ofHorticulture andForestry,
Nauni,Solan, HimachalPradesh173230, India
e-mail: aditi.bhardwaj650@gmail.com
A.K.Gupta· B.Devi
Department ofPlant Pathology, Dr. Y.S. Parmar
University ofHorticulture andForestry, Nauni,Solan,
HimachalPradesh173230, India

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Rhizobiaceae and Enterobacteriaceae. The most vir-
ulent plant pathogenic bacteria in these families are
Pseudomonas, Ralstonia, Xanthomonas, Erwinia,
Pectobacterium, Pantoea, Agrobacterium, Burkholde-
ria, Acidovorax, Clavibacter, Streptomyces, Xylella,
Spiroplasma and Phytoplasma. Some of these bac-
teria such as Xylella fastidiosa, Erwinia amylovora,
Acidovorax citrulli, Ralstonia solanacearum, Curto-
bacterium flaccumfaciens pv. flaccumfaciens, Xan-
thomonas arboricola pv. pruni, Xanthomonas citri,
Clavibacter michiganensis subsp. Sepedonicus, Can-
didatus liberibacter spp., Candidatus Phytoplasma
vitis etc. are now posing a serious threat in many
countries (such as America, Canada, Mexico, South
America, Australia, Korea, Iran) and are therefore
considered as quarantine pest (Schwarczinger et al.
2018; Scortichini and Cesari 2019; Sánchez et al.
2019; Tegli etal. 2020).
Most of the plant pathogenic bacteria are aerobic
and some of them are facultative anaerobes. They
provoke disease by invading and colonizing differ-
ent plant parts including xylem and phloem, inter and
intracellular spaces (Agrios 2005). Epiphytic bacte-
ria often reach population densities of between 106
and 107 cells/cm2 of leaves, roots, apoplast, rhizos-
phere and other plant surfaces (Andrews and Harris
2000). The infection process of bacterial phytopath-
ogens is relatively different from fungi and other
parasites (Salmond 1994; Dong etal. 2000; Dellagi
et al. 2009). Different pathogenicity factors such as
secretion systems (type I, II, III, IV), quorum sens-
ing (QS), plant cell-wall-degrading enzymes, toxins,
hormones, polysaccharides, proteinases, siderophores
etc. contribute to disease development in host plants
(Molina etal. 2005; Zhou etal. 2013; Francis etal.
2017; Siphathele etal. 2018). These factors together
promote the development of disease in plants result-
ing in qualitative and quantitative losses to food
production. Strategic management of these bacterial
diseases require substantial knowledge of the patho-
gen biology in order to identify the appropriate tim-
ing for targeting pathogen populations. Previously
the control measures were generally based on preven-
tive application of copper-containing compounds and
antibiotics (Kumar etal. 2005). The use of antibiotics
against plant pathogenic bacteria has been exponen-
tially increased over past few years and has resulted
in antibiotic resistance in most plant pathosystems.
These antibiotics were considered as silver bullets
that would eradicate infectious bacteria (Levy 2002;
Walsh 2003). There are various mechanisms through
which bacteria has evolved antibiotic resistance such
as by acquisition of a resistance determinant via hori-
zontal gene transfer, by inactivation of the antibiotic
and by synthesizing new target proteins insensitive to
antibiotics (Davies and Davies 2010; D’Costa et al.
2011).
Continuous use and higher dose of these prod-
ucts resulted in bacterial resistance and also gener-
ated adverse impacts on the plants as well environ-
ment (McLeod etal. 2017). Thus, due to increasing
resistance to existing bactericides identification and
implementation of novel management tactics has to
come fore in bacterial disease management. With
the advent of new technologies a number of central
research foci that involve basic research on identifi-
cation of critical stages of pathogen infection, novel
methods of delivery systems for target pathogen
control are now emerging as new paradigm. Natural
antimicrobial bioactive compounds generally syn-
thesized from plant, microbial and animal sources
are known to modulate plant defence responses and
growth. These natural compounds usually belong
three chemical classes i.e. phenolics, terpenoids
and alkaloids (Freeman and Battie 2008). To date,
many bioactive antimicrobial compounds have been
isolated, characterized and have been used as novel
biopesticides for food production. Several studies
have shed light on use of different plant based anti-
microbial compounds with promising antimicro-
bial activity against some phytopathogenic bacteria
(Kulshreshtha and Velusamy 2012; de Oliveira etal.
2016; Jamiołkowska 2020). These studies report
the anti quorum sensing and anti biofilm effect of
these natural compounds on pathogenic bacteria.
Another biocontrol method that has been the sub-
ject of research over past four decades in bacterial
disease management is the use of bacteriophages
(Jones etal. 2007). Phage therapy generally has nar-
row host-range, high specificity and eliminates only
specific bacteria without damaging others. Due to
specific action of bacteriophages they are employed
as detection tools for phytopathogenic bacterial
diagnosis. Several reports advocates the use of these
phages against pathogenic bacteria such as Ral-
stonia solanacearum, Dickeya spp., Pseudomonas
tolaasii, Pectobacterium spp. Xanthomonas oryzae
pv. oryzae (Lim etal. 2013; Czajkowski etal. 2017;

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Stefani etal. 2021). Furthermore, quorum quench-
ing (QQ) mediated control of bacterial pathogens
is an emerging approach in bacteriology. Quorum
quenching methods are effective against wide range
of signalling molecules. This disruption of signal-
ling can be theoretically achieved by inhibiting
the synthesis or the detection of signal molecules
and also by the enzyme-catalyzed modification
and degradation the signal molecules involved in
quorum sensing (Grandclement et al. 2016). Quo-
rum quenching bacteria and enzymes (lactonases,
acylases and oxidoreductase) generally targets the
N-acyl homoserine lactone (AHL), diffusible signal
factor (DSF), autoinducer-2 (AI-2) and 2-heptyl-
3-hydroxy-4-quinolone (Roy et al. 2010; Fetzner
2015; Wang etal. 2020). Interestingly, advances in
the field of nano-bio pesticides as “smart delivery
systems of bio-pesticides” lead to creation of novel
materials with excellent properties has opened up
wide opportunities in their applications in preci-
sion agriculture. Over the past decades a large vol-
ume of research has been focused to create better
performing nano-materials with efficient disease
control potential. Several studies advocates the use
of nanoparticles in bacterial disease control (Chen
et al. 2016; Moradian and Biparva 2018; Shahr-
yari etal. 2020; Parveen and Siddiqui 2021). Sev-
eral creative strategies have been used to achieve
demonstrable plant resistance to pathogens through
gene editing. Editing of plant genes that encode
susceptibility factors or negative defence regulators
can result in resistance to various pathogens. Gene
editing is a way to precise changes to the genomic
DNA by using sequence-specific nucleases that gen-
erally recognize specific DNA sequences and pro-
duce double stranded DNA breaks at targeted sites.
Currently, three major types of sequence-specific
nucleases are employed in genome editing systems
such as zinc finger nucleases (ZFNs), transcrip-
tion activators like effector nuclease (TALENs) and
the clustered regularly interspaced short palindro-
mic repeats (CRISPR/Cas) (Voytas and Gao 2014;
Smargon etal. 2017). CRISPR/Cas based genome
editing techniques has been found effective against
bacterial pathogens and is one of the most exploited
method used in control of bacterial and other plant
pathogens (Zhou etal. 2015; Peng etal. 2017; Suni-
tha and Rock 2020; Tripathi et al. 2021). In this
review, we have addressed important pathogenic
bacteria and the current management approaches
adopted for targeted control of bacterial pathogens.
Bacterial pathogenesis andvirulence
Natural openings are the most obvious entry point for
bacterial pathogenesis (Agrios 2005). Viable inocu-
lum of bacteria successfully gets attached to plant
surface for establishment and this is the first step in
pathogenesis (Fig. 1a). Plant defence mechanisms
pose a serious challenge to invading bacteria and for
successful invasion they need to overcome the plant
resistance. Virulent phytopathogenic bacteria are
able to alter expression of genes for their successful
survival and thereby adapt to harsh environmental
factors and host responses. Such alteration in gene
expression is mediated by the phenomenon known
as quorum sensing (QS) and the bacteria accumulate,
detect and respond to communication signals called
autoinducers (Barber etal. 1997; Antunes etal. 2010).
This mechanism of quorum sensing leads to compat-
ible communication between different cells of bac-
teria and also regulates various activities and behav-
iour of bacterial cells such as conjugation, motility,
pathogenicity, growth inhibition, biofilm formation,
secondary metabolite and toxin production, secretion
systems, CRISPR-Cas, extracellular polysaccharides
and siderophore biosynthesis etc. (Siphathele et al.
2018).
Phytopathogenic bacteria constitute various viru-
lence factors that enable them to infect and colonize
host tissues successfully. In some bacteria (such as
P. Syringae, R. solanacearum, E. amylovora, and X.
campestris) virulence is correlated with their abil-
ity to produce various exopolysaccharide (EPS)
polymers during active growth on and in host plant
(Denny 1995). Xanthomonas campestris produces
yellow EPS known as xanthan gum, pectic enzymes
and cellulases to degrade the cell wall of the host
plants (Ryan etal. 2011). These enzymes results in
maceration of the host tissues resulting in rotting and
death of plants. Quorum sensing (QS) signaling also
controls virulence factors in some soft rot causing
bacteria i.e. E. Chrysanthemi, E. carotovora and Ral-
stonia solanacearum etc. These factors often regulate
the production of extracellular pectolytic enzymes,
exopolysaccharide, and tolerance to free radicals after
attack, and symptom development in the host (Toth

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et al. 2003; von Bodman et al. 2003; Barnard and
Salmond 2007). Besides these mechanisms bacte-
rial pathogens produce various low-molecular-weight
phytotoxins that contribute to bacterial virulence and
increase thereby increase disease symptoms. These
toxins act on the protoplasm and affect the metabo-
lism of the host for successful infection (Bender etal.
1999). Most studied and characterized phytotoxins
are produced by P. Syringae species and includes
syringomycins, syringopeptins, tabtoxin, coronatine,
phaseolotoxin and syringolin etc. (Bender and Scholz
2004).
In addition to the above mentioned factors bacte-
ria utilize type secretion systems for virulence. Plant
pathogenic bacteria passes effector proteins into the
plant host cells by secretion systems. In gram nega-
tive bacteria these systems are classified into five
groups Type I, Type II, Type III, Type IV and Type V
and in gram-positive bacteria as Type I, Type II Type
V. Reports have revealed that Type IISS is necessary
for the pathogenesis and virulence in Erwinia, Dick-
eya, Pectobacterium, Xanthomonas, and Ralstonia
(Szczesny etal. 2010). Generally, most of phytopath-
ogenic gram-negative bacteria have type III secretion
system that is encoded by hypersensitive response and
pathogenicity (hrp) genes. The name hrp represents
the elicitation of hypersensitive response in resistant
plants and pathogenic response in susceptible plants
(Ryan etal. 2011). Recent findings on genome analy-
sis have revealed the presence of multiple secretion
pathways in P. syringae and Xanthomonas (Francis
et al. 2017; Siphathele etal. 2018). Type IV secre-
tion system utilized by Agrobacterium tumefaciens
for translocation of a T-DNA and vir genes in the
host plant nucleus is the most versatile of the secre-
tion systems (Zechner etal. 2012; Chang etal. 2014).
The T VSS passenger domains are variable and func-
tion in bacterial colonization, biofilm formation and
virulence (Grijpstra et al. 2013). Various types of
virulence factors utilized by pathogenic bacteria are
illustrated in Fig.1b.
Major phytopathogenic bacteria include Pseu-
domonas syringae pathovars, Ralstonia solanacearum,
Agrobacterium tumefaciens, Xanthomonas oryzae pv.
Oryzae, Xanthomonas campestris pathovars, Xan-
thomonas axonopodis pathovars, Erwinia amylovora,
Xylella fastidiosa, Dickeya (dadantii and solani) and
Pectobacterium carotovorum (or Pectobacterium
atrosepticum (Mansfield et al. 2012). Pseudomonas
syringae is a phytopathogenic model bacterium used
Fig. 1 a Bacterial pathogenesis (Bacteria enter into plant
system through natural openings, wounds and insect vec-
tors). b Virulence factors (enzymes, toxins, secretion systems
and virulence genes) and induction of immunity (Hypersensi-
tive response, reactive oxygen species, mitogen activated pro-
tein kinases, pathogenesis related proteins, systemic acquired
resistance) in resistant host plant

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by researchers all over the world to study bacterial viru-
lence mechanisms, plant-bacteria interactions, biofilm
formation, and host adaptation of pathogens, microbial
evolution, ecology and epidemiology. Pathovar syrin-
gae is the most studied pathovar due to its wide host
range. Multiple host plants are affected by this organ-
ism including cereals, annual crops, vegetables and
woody plants. Recent research advocates more than 10
species of Pseudomonas and over 60 pathovars with
different host ranges (Green et al. 2010; Arnold and
Preston 2019). Agrobacterium tumefaciens is the best
known pathogenic bacteria due to inter kingdom gene
transfer ability. It causes crown gall disease in many
economically important host plants (Gupta etal. 2015;
Sharma and Gupta 2017; Sharma etal. 2017; Kawagu-
chi etal. 2019). Bacteria belonging to the genus Xan-
thomonas are responsible for diseases on more than 400
different economically important host plants (Hayward
1993; Nino Liu et al. 2006). Among different patho-
genic species Xanthomonas oryzae pv. oryzae (Xoo),
X. campestris pv. campestris (Xcc), X. campestris pv.
malvacearum, X. axonopodis pv. manihotis, X. axono-
podis pv. allii and X. axonopodis pv. punicae are stud-
ied in detail (Daughtrey etal. 2006; Neves etal. 2014;
Wang etal. 2019a, b). Erwinia amylovora belonging to
family Enterobacteriaceae is amongst the smallest of
the plant pathogenic bacteria that have been sequenced
so far (Sebaihia etal. 2010). It can adopt a biotrophic
or necrotrophic lifestyle and could easily overwinter
in dead apple leaves (Sobiczewski et al. 2017). The
bacteria can manipulate host defense mechanisms to
cause disease and the effector proteins such as AvrRp-
t2EA are transferred into hosts by type IIISS to cause
fire blight in susceptible Malus genotypes (Emeriewen
etal. 2019). Another major bacteria Xylella fastidiosa
has been reported to cause bacterial leaf scorch, olean-
der leaf scorch, coffee leaf scorch, alfalfa dwarf, phony
peach disease, the economically important Pierce’s dis-
ease of grapes, citrus variegated chlorosis, olive quick
decline syndrome (Kyrkou etal. 2018). Different pec-
tinolytic bacteria belongong to genus Dickeya and Pec-
tobacterium are known to infect many economically
important crops (Table1; Toth etal. 2011; Parkinson
etal. 2014; Tian etal. 2016; Dees et al. 2017; Pedron
etal. 2019).
Current approaches inmanagement ofbacterial
pathogens
Bioactive compounds against bacterial pathogens
The prominence on plant protection has shifted from
the prevailing chemical methods to the integrated
disease management strategies and the emphasis is
on biological control techniques and other natural
resources (Raymaekers et al. 2020). Current trends
in advancement and use of natural bioactive com-
pounds are becoming more popular around the globe
due to their environment friendly nature. These bioac-
tive compounds are isolated from plant sources, algal
sources, microbial sources and marine sources. They
act as elicitors for plant defence and thereby activat-
ing resistance in plants against pathogens. Majority of
them are salicylic acid (SA), benzoic acid, chitosan,
benzothiadiazole, alkaloids, flavonoids, terpenes,
proteins, peptides, blasticidin, mildiomycin, polyox-
ins, phenolic compounds, etc., that works as antimi-
crobial agents. Diverse genera belonging to different
plant families such as Apocynaceae, Flacourtiaceae,
Fabaceae, Lamiaceae, and Asteraceae, are reported as
potent sources of biopesticides and bioactive natural
products (Denaro etal. 2020; Shrinet etal. 2021).
Biofilm formation is considered as one of the most
essential factors that cause bacterial resistance toward
different traditional chemical and physical treatments
and antimicrobial agents (Coenye and Nelis 2010;
Ivanova et al. 2018). Family Lamiaceae, Verben-
aceae and Rutaceae are considered as most important
families of medicinal and aromatic plants that con-
stitute important essential oils that have promising
antiquorum sensing properties to combat phytopath-
ogenic bacteria (Mancini etal. 2014; Asfour 2018).
Several reports advocated the antimicrobial activity
of essential oils against Clavibacter michiganensis,
Xanthomonas campestris and Pseudomonas syringae
pv. phaseolicola (Elshafie etal. 2016; Camele etal.
2019). Plant extracts of Caatinga is also known to
inhibit plank tonic growth and biofilm formation in
Ralstonia solanacearum (Malafaia etal. 2018). Anti-
bacterial activities of phenolic and flavonoid com-
pounds extracted from Acacia saligna flower extract

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Table 1 Major bacterial pathogens infecting plants
Bacteria Family Description Species/Pathovars/ Biovars Host References
Pseudomonas syringae Pseudomonadaceae Rod-shaped,Gram-nega-
tivebacteriumwith polarfla-
gella
P. s.pv.pisi, P. s.pv.aceris,
P. s.pv.actinidiae, P.
s.pv.phaseolicola, P.
s.pv.syringae, P. s.pv.gly-
cinea, P. s.pv.aesculi, P.
s.pv.aptata, P. s.pv.atrofa-
ciens, P. s.pv.dysoxylis, P.
s.pv.japonica, P. s.pv.pan-
ici, P. s.pv.papulans
Pea, kiwifruit, beans,
Syringa,Prunus,Phaseolus,soy-
bean,horse chestnut,
beets,wheat, kohekohe, bar-
ley,Panicumgrass, crabapple
Green etal. (2010)
Ralstonia Burkholderiaceae Rod shaped, Aerobicnon-
spore-forming,Gram nega-
tive bacterium motilewith
apolar flagellar tuft
Ralstonia solanacearum spe-
cies complex
Potato, tomato,soybean, eggplant,
banana, geranium, ginger,
tobacco, bell pepper, olive, rose
Wairuri etal. (2012)
Agrobacterium tumefaciens Rhizobiaceae Rod-shaped,Gram-nega-
tivesoilbacterium Agrobacterium tumefaciens,
A. vitis, A. rubi, A. alber-
timagni, A. arsenijevicii,
A. bohemicum, A. cavarae,
Agrobacterium deltaense, A.
fabacearum, A. fabrum, A.
nepotum, A. rosae
Apple, Walnuts,grape vines,stone
fruits,nuttrees,sugar
beets,horse radish, rose andrhu-
barb
Kuzmanovic etal. (2018)
Xanthomonas Xanthomonadaceae Rod-shaped,Gram-nega-
tivebacteria with one polar
flagella
X. oryzae, X.albilineans, X.
alfalfae, X. ampelina, X.
arboricola, X. axonopodis,
X. boreopolis, X. campes-
tris, X. cassavae, X. citri, X.
codiaei, X. cucurbitae, X.
cyanopsidis, X. cynarae, X.
euvesicatoria, X. frageriae,
X. gardneri, X. holcicola, X.
hortorum, X. hyacinthi, X.
maliensis, X. malvacearum,
X. maltophila, X. manihotis,
X. melonis, X. papavericola,
X. perforans, X. phaseoli, X.
pisi, X. populi, X. sacchari,
X. theicola, X. translucens,
X. vasicola, X. vesicatoria
Rice, sugarcane, alfalfa, Pru-
nus,hazelnut, cabbage, cauli-
flower, cucurbits, strawberries,
cotton, bean, citrus, cassava,
pepper, tomato
Neves etal. (2014)
Erwinia amylovora Enterobacteriaceae Gram negative; rod shaped,
facultative anaerobic bac-
teria
Erwinia amylovora, Erwinia
papayae, Erwinia psidii,
Erwinia pyrifoliae, Erwinia
tracheiphila
Apple, pear, papaya, guava,
cucumber, muskmelon
Sobiczewski etal. (2017)

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have shown activity against different bacterial patho-
gens (Al-Huqail etal. 2019). Shaheen and Issa (2020)
reported invitro and in vivo activity of Peganum har-
mala L. alkaloids against Ralstonia solanacearum
Phylotype II, Erwinia amylovora, Pectobacterium
carotovorum subsp. Carotovorum, and Burkholderia
gladioli, the causal agents of potato brown rot, pear
fire blight, potato soft rot, and onion slippery skin
diseases, respectively. Toxicity effects of essential oil
from Eriocephalus africanus L. leaves was evaluated
against the growth of some phytopathogenic bacteria
including Agrobacerium tumifaciens, Dickeya solani,
Erwinia amylovora, Pseudomonas cichorii and Serra-
tia pulmithica (Behiry etal. 2020). Secondary metab-
olites from filamentous fungi isolated from soil and
marine sediments of Antarctic ecosystems have also
shown antibacterial activity against phytopathogenic
bacteria (Purić et al. 2018). Bioactive secondary
metabolites from different Trichoderma spp. have also
shown antibacterial potential against Ralstonia sola-
nacearum and Xanthomonas compestris (Khan etal.
2020). Bactericidal activity of hydroalcoholic extract
from Larrea tridentate has been recently reported
against Clavibacter michiganensissbsp.michiganen-
sis,Pseudomonas syringae, andXanthomonas camp-
estris (Morales etal. 2021). Some recently published
articles addressing the use of bioactive compounds
is listed in Table2. Thus, use of different plants as
‘biofactories’ for the synthesis of antimicrobial com-
pounds represents an efficient environment friendly
method facilitating use of these compounds in man-
agement of pathogenic microbes.
Bacteriophage therapy forinactivation
ofphytopathogenic bacteria
Bacteriophages are viruses that infect and replicate
within host bacteria and are the most abundant bio-
logical entity in the biosphere with an estimated
no. of 1031 on the planet with a total weight of 109
tons (Wommack and Colwell 2000; Frampton et al.
2012; Dou etal. 2018). The method of utilizing bac-
teriophages to treat pathogenic bacterial infections
was developed and widely used between the 1920s
and 1940s (Cisek etal. 2017). After the emergence
of antibiotic resistance in bacteria, phage therapy
was adopted for sustainable management of bacte-
rial diseases (Burch et al. 2017). Phages are more
Table 1 (continued)
Bacteria Family Description Species/Pathovars/ Biovars Host References
Xylella fastidiosa Xanthomonadaceae Aerobic,Gram-negativebac-
terium Xylella fastidiosa Grapevine, oleander, coffee alfalfa,
olive, peach, citrus
Kyrkou etal. (2018)
Dickeya spp Pectobacteriaceae Straight rod-shaped, gram-
negative with peritrichous
flagella
Dickeya dadantii, Dickeya
dieffenbachiae, Dickeya
chrysanthemi, Dickeya para-
disiaca, Dickeya zeae, Dick-
eya dianthicola, D. Dadantii
subsp. Dieffenbachiae, D.
Solani, Dickeya aquatica,
Dickeya fangzhongdai
peppers, potato, eggplant, tomato,
tobacco, broccoli, radishes,
sugar cane, sorghum, rice, onion,
orchids, tulips, chickory, chry-
santhemums, begonia
Parkinson etal. (2014)
Pectobacterium spp Pectobacteriaceae Gramnegative, rod-shaped,
non-sporulating, faculta-
tively anaerobic bacterium
with peritrichous flagella
P. carotovorum, P. atrosep-
ticum, P. cacticidum, P.
aroidearum, P. aquaticum,
P. betavasculorum, P.
wasabiae,, P. parmentieri,
P. peruviense, P. polaris, P.
punjabense, and P. zantede-
schiae
Potato, ornamentals and vegeta-
bles
Pedron etal. (2019)

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environmentally friendly, can be easily tailored
against specific phytopathogenic bacteria, and their
reformulation is also easily if resistance develops.
Infection of bacteria by virulent bacteriophage results
in viral replication, lysis of the bacterial cells and
release of abundant progeny phages. The resulting
progeny phages then infect the bacteria in the vicin-
ity. In this way the numbers of phage will exponen-
tially expand when target bacteria are encountered
and the phage therapy will essentially be amplified
in response to the bacterial infection (Keen 2015).
These biocontrol phages have certainly proved the
proverb—‘The enemy of my enemy is my friend’. In
any successful example of biocontrol with bacterio-
phage the main deciding factor is whether a phage is
lytic (virulent) or temperate in nature (Łobocka etal.
2004).
In the recent years, several studies with promising
results have been published worldwide on application
of different bacteriophages on major bacterial patho-
gens under invitro and field conditions. Goyer (2005)
isolated phages Stsc1 and Stsc3 infecting Streptomy-
ces scabiei. Phage therapy using skim milk formula-
tion reduced disease severity of citrus canker and cit-
rus bacterial spot by 59% (Balogh etal. 2008). Brown
blotch in mushroom caused by Pseudomonas tolaasii
was managed by co-incubating the pathogen with
bacteriophages (Kim etal. 2011). Wilt caused by Ral-
stonia solanacearum is most devastating disease in
many economically important crops and appropriate
use of lytic phage PE204 with surfactant to plant root
system effectively controls the pathogen (Bae et al.
2012). Similarly, several bacteriophages have been
isolated and characterized against Pectobacterium
spp. and Dickeya spp. (Czajkowski 2016). Bacterio-
phage PP1 belonging to Podoviridae family exhibit-
ing icosahedral heads and short non-contractile tails
showed high specificity for P. carotovorum subsp.
carotovorum (Lim etal. 2013). Under simulated stor-
age conditions novel six-phage cocktail reduced the
population of Pectobacterium atrosepticum caus-
ing soft rot infection in potato tubers (Carstens etal.
2019). There are various reports in literature that
cite the successful use of bacteriophage technology
against bacterial pathogens (Table3).
Lytic bacteriophages can generally affect the struc-
ture of bacterial cell and may influence spread, sur-
vival and virulence of the pathogen. Lytic bacterio-
phage ΦD5 inhibiting Dickeya solani in potato was
isolated and phage population was found to be stable
for up to 28days on potato tuber surface and in pot-
ting compost. Potato plants grown in tissue culture
and compost inoculated with phage ΦD5 reduced
infection of D. solani by more than 50% compared
to untreated plants (Czajkowski etal. 2017). Ideally,
phages in a cocktail should cover the widest pos-
sible range of target pathogens and should have bet-
ter viability. Many researchers advocated the use of
phages for biocontrol of bacteria belonging to genus
Xanthomonas (da Silva et al. 2019; Stefani et al.
2021). Lytic bacteriophage XCC9SH3 infecting Xan-
thomonas campestris pv. campestris was character-
ized by Bhoyar etal. (2017). A novel phage Xoo-
sp2 infecting Xanthomonas oryzae pv. oryzae was
isolated and characterized for the control of bacte-
rial blight in rice (Dong etal. 2018). Later sequence
analysis of a Jumbo bacteriophage Xoo-sp14 infect-
ing Xanthomonas oryzae pv. oryzae was performed
(Nazir et al. 2020, 2021). Different phage mixtures
have also been used to control a variety of bacte-
rial plant pathogens such as R. solanacearum, Xan-
thomonas sp. and P. carotovorum sp. carotovorum
(Ramírez etal. 2020; Vu and Oh 2020). These stud-
ies further shows significant potential of bacterio-
phage usage to reduce agrochemicals based tools for
the control of bacterial diseases in plants. Research
should be focused on characterization and host speci-
ficity of bacteriophages, and more field trials are nec-
essary for further validation.
Quorum quenching mediated management
ofphytopathogenic bacteria
Prokaryotes have developed very sophisticated
mechanism for sensing and communicating with
the local environment known as Quorum sensing.
Advancements in new molecular biology techniques
have given the insight in understanding the cell to
cell communication and the synchronization of their
microbial activities among their family members to
attack their respective host. The understanding of
these mechanisms has also given a new perspective
to manage the pathogenic bacteria by disrupting QS
mechanisms known as quorum quenching (QQ).
Dong et al. (2001) identified first quorum sup-
pressing molecule from Bacillus. The process of QQ
can occur by four major mechanisms as described

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in Fig.2. It involves the inhibition of synthesis of
quorum sensing signals such as Acyl homoserine
lactones (AHL) by L-S-adenosyl homocysteine,
sinefungin and triclosan. QQ can be inhibited by
halogenated furanones, plant extracts exhibiting QQ
activity, patulin, phenyl-AHL and chlorophenyl-
AHL that generally inhibits quorum sensing signals.
Degradation of quorum sensing molecules (such as
AHL, 3-Hydroxy palmitic acid methyl ester hydro-
lase and diffusible signal factor) produced by several
bacteria are reported to occur by the action of AHL
acylase, AHL lactonase, esterase enzymes (Faure
and Dessaux 2007; Helman and Chernin 2015;
Achari and Ramesh 2015; Caicedo et al. 2016).
Pseudomonas spp. has emerged as a frequent quo-
rum quenching bacterium with biocontrol capability
Table 2 Recent examples of bioactive compounds used against phytopathogenic bacteria
Bioactive compound Source Target Bacteria Disease References
Alkaloids, tannins, gly-
cosides, flavonoids and
saponins
Peganum harmala,
Allium sativum, Witha-
nia somnifera, Melia
azedarach, Calotro-
pis procera, Mentha
piperitaandNerium
oleander
Clavibacter michigan-
ensissubsp.michigan-
ensis
Canker Siddique etal. (2020)
Essential oils andTram-
etes versicolorextract
Essential oils (EOs)
of oregano (Origa-
num vulgare), garlic
(Allium sativum), basil
(Ocimum basilicum),
cinnamon (Cinnamo-
mum zeylanicum),
clove buds (Syzygium
aromaticum), thyme
(Thymus vulgaris),
andTrametes versi-
colorextract (Tve)
Clavibacter michiganen-
sissubsp.michiganen-
sisandRalstoniasola-
nacearum
Wilt Orzali etal. (2020)
Phenolic and flavonoid
compounds Acacia saligna Agrobacterium tume-
faciens, Enterobacter
cloacae, Erwinia
amylovora,andPecto-
bacterium carotovorum
subsp. carotovorum
Rot and crown gall Al-Huqail etal. (2019)
Alkaloids Peganum harmalaseeds Ralstonia solanacearum
Phylotype II, Erwinia
amylovora, Pectobac-
terium carotovorum
subsp. Carotovorum,
and Burkholderia
gladioli
Potato brown rot, pear
fire blight, potato soft
rot, and onion slippery
skin
Shaheen and Issa (2020)
Metabolites Trichoderma pseudohar-
zianum andT. viridae Ralstonia solanacearum
and Xanthomonas
compestris
Wilts and bacterial spots Khan etal. (2020)
Hydroalcoholic extract Larrea tridentata Clavibacter michigan-
ensissbsp.michigan-
ensis,Pseudomonas
syringae, andXan-
thomonas campestris
Canker, speck, and spot Morales etal. (2021)
Bioactive extracts Bacillus sp. H8-1 and
Bacillus sp. Clavibacter michigan-
ensis subsp. michigan-
ensis
Wilt Jang etal. (2022)

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against many phytopathogens (Alymanesh et al.
2016). Sekeli et al. (2019) reported enhanced
resistance to papaya die back disease by quorum
quenching mechanism. The results suggested that
transforming AHL lactonase gene into Eksotika
papaya was indeed a promising approach to acquire
resistance against Erwinia mallotivora. Diffusible
signal factor (DSF) represents a family of widely
conserved QS signals that plays a key role in bio-
film formation, antibiotic resistance, and interspe-
cies and interkingdom communication in a variety
of gram-negative bacteria including Xanthomonas
campestris (He and Zhang 2008; Zhou etal. 2017a,
b). Diffusible signal factor degrading Acinetobacter
lactucae strain QL-1 was also reported as a novel
quorum quenching candidate against Xanthomonas
campestris pv. campestris (Ye etal. 2019). Quo-
rum‐quenching endophytic bacteria i.e. Bacillus
cereus Si-Ps1 and Pseudomonas azotoformans La-
Pot3-3, isolated from Citrus sinensis and C. sinensis
var. Thomson’s leaves inhibited N-acyl homoserine-
based quorum sensing mechanism of Pseudomonas
syringae pv. syringae in Citrus cultivars (Akbari
et al. 2020). Quorum-quenching bacteria associ-
ated with rhizosphere were also exploited against
soft rot causing Pectobacterium carotovorum subsp.
carotovorum (Alinejad etal. 2020). Recently, Rho-
dococcus erythropolis was used for controlling the
biofilm formation in Rhizobium rhizogenes causing
hairy root disease (Bourigault etal. 2021). Quorum-
Quenching N-acyl homoserine lactonase was identi-
fied and characterized in Erwinia amylovora (Yaar
etal. 2021). The literature (Table4) suggests that,
QQ strategies are now emerging as new approach to
switch off the cell to cell communication in bacteria
that poses serious threat to food production.
Nanobiopesticides targeting bacterial infection
The emerging science of nanotechnology has tre-
mendous potential to detect and monitor pathogens,
improve crop productivity and food production and
managing pathogens thereby increasing sustainable
food production (Frewer et al. 2011; Prasad et al.
2014). Due to ultra small size of nanoparticles (NPs)
they possess high surface-to-volume ratio. There-
fore, they are highly reactive in nature and have great
potential to be used for diagnosis and management
of different pathogenic microbes (Dubchak et al.
2010; Sofi et al. 2012). The nanoparticles can also
be integrated with other biological materials for the
detection of bacterial infections. Yao and co-workers
(2009) used silica NPs and probes along with anti-
bodies to detect Xanthomonas axonopodis pv. vesi-
catoria. Three major antimicrobial activities of NPs
Table 3 Recent examples of bacteriophage therapy used against phytopathogenic bacteria
Bacteriophage Phage family Disease Bacteria References
Phage φRSM Inoviridae Wilt Ralstonia solanacearum Addy etal. (2012)
Lytic Bac-
teriophage
phiEaP-8
Podoviridae Fire blight and black shoot
blight Erwinia amylovoraandE.
pyrifoliae Park etal. (2018)
Phage Xoo-sp2 Siphoviridae Bacterial leaf blight Xanthomonas oryzaepv.ory-
zae Dong etal. (2018)
Phage cocktail PodoviridaeandMyoviridae Soft rot Pectobacterium atrosepti-
cumandPectobacterium
carotovorumsubsp.caro-
tovorum
Zaczek etal. (2020)
Phage RpY1 Podoviridae Wilt Ralstonia solanacearum Lee etal. (2021)
Phage FBB1 Myoviridae Wilt Erwinia tracheiphila Fu etal. (2021)
Phage Xoo-sp13 Myoviridae Bacterial leaf blight Xanthomonas oryzaepv.ory-
zae Nazir etal. (2021)
Phage PN09 Myoviridae Canker Pseudomonas syrin-
gaepv.actinidiae Ni etal. (2021)
Phage cocktail Podoviridae andSiphoviridae Leaf scorch, die-back and
leaf scald Xylella fastidiosaandXan-
thomonas albilineans Clavijo etal. (2021)

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such as photocatalysis, physical damage to bacterial
cell envelope and release of toxic metal ions have
been reported so far. In addition to these NPs can
exert antimicrobial activity through the release of
ions, such as Ag+, Zn2+ and Cu2, which are toxic to
bacteria (Lok et al. 2007). Ralstonia solanacearum
causing bacterial wilt in tomato and potato can be
controlled by using silver and copper oxide nano-
particles (Chen etal. 2016, 2019). Nanoparticles can
be synthesized from beneficial microbes and plant
extracts. Abdel (2013) reprted the efficacy of nano-
particles synthesized from Streptomyces bikinien-
sis against Pseudomonas syringae. Graphene oxide
loaded with copper oxide nanoparticles were also
assessed as an antibacterial agent against Pseu-
domonas syringae pv. tomato (Li etal. 2017).Antimi-
crobial activity of silver nanoparticles (AgNPs) was
tested against Erwinia carotovora subsp. atroseptica
(Abbas etal. 2019). For the management of bacterial
leaf blight of rice silver nanoparticles were synthe-
sized by using Bacillus cereus (Ahmed etal. 2020).
Similarly, biogenic synthesis of iron oxide nanopar-
ticles via Skimmia laureola extracts showed antibac-
terial efficacy against Ralstonia solanacearum (Alam
etal. 2019). Green synthesis of chromium nanopar-
ticles by using aqueous extract of plant extracts such
as Melia azedarach, Artemisia herba-alba has shown
activity against Erwinia amylovora (Kotb etal. 2020).
Similarly, biogenic synthesis of Ag nanoparticles
using Pimpinella anisum L seed extract significantly
inhibited some phytopathogenic bacteria (Moham-
med etal. 2020).Antibacterial effects of Fe and Cu
nanoparticles on Xanthomonas campestris and the
effect of these NPs on pathogenic gene hrpE has been
assessed by Moradian and co-workers (2018). Cop-
per nanoparticles synthesized with sumac extract
and copper-chitosan nanocomposite showed activity
against some plant pathogenic bacteria in laboratory
(Shahryari etal. 2020). Johnson etal. (2020) reported
non-hydrolytic synthesis of caprylate capped cobalt
ferrite nanoparticles and their application against soft
rot causing Erwinia carotovora. Recently, Parveen
and Siddiqui (2021) reported the impact of silicon
dioxide NPs on growth, photosynthetic pigments,
proline, activities of defense related enzymes and
inhibitory activity against some bacterial and fungal
pathogens infecting tomato.Table5 depicts the recent
Fig. 2 Mechanism of quorum quenching (QQ) in bacteria

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reports addressing the use of nanoparticles against
bacterial pathogens.
The nanomaterials possess desirable traits to be
used in diagnosis and management of bacterial dis-
eases in future. Nanomaterials, nanocapsules and
nanotubes efficiently possees higher concentration of
active ingredients of pesticides and direct application
of nanoparticles may suppress plant pathogenic bac-
teria. Besides being efficient antimicrobials targeting
pathogens, there are certain limitations that still need
to be resolved. Moreover, the environmental fate of
NPs needs to be determined before commercializa-
tion and toxicity effects also need to be addressed.
Role ofresistance genes inbacterial disease
management
Over past 100years breeding for disease resistance
has been a desirable method for the control of bacte-
rial pathogens. This method of deploying gene-con-
ferred plant resistance furnish an economical, effec-
tive and environment friendly technique to reduce
the losses caused by plant diseases (Kou and Wang
2010). Researchers throughout the globe have made
significant efforts to gain much understanding of the
key determinants of pathogenic bacteria and host
interactions. Effective implementation of specific R
genes into agronomically important plants has also
generated positive impulse for disease management
Table 4 Recent examples of quorum-quenchingmechanism used against phytopathogenic bacteria
Quorum-quenching organ-
ism
Mode of action Target Bacteria Disease References
PseudomonasandBacillus Alteration in bacterial attach-
ment and biofilm formation,
factors that are known to
contribute to Xcc virulence
Xanthomonas citrisubsp.
citri Citrus canker Caicedo etal. (2016)
Bacillus spp Inactivation of AHL signalling Pectobacterium carotovo-
rum subsp. carotovorum Soft rot Garge and Nerurkar (2017)
Acinetobacter lactucae Inactivation of AHL signalling Xanthomonas campestris
pv. campestris
Black Rot Ye etal. (2019)
Pseudomonas segetis Enzymatic degradation of
signal molecules Dickeya solani,Pecto-
bacterium atrosepti-
cumandP. carotovorum
Soft rot Rodríguez etal. (2020)
Bacillus cereusSi-Ps1
andPseudomonas azoto-
formansLa-Pot3-3
ReducedN-acyl homoserine-
based quorum sensing
signals, biofilm production
and swarming motility
Pseudomonas syringaepv.
syringae
Citrus blast Akbari etal. (2020)
Bacillus pumi-
lus,Pseudomonas
fluorescensandPseu-
domonassp.
Degradation acyl-homoserine
lactone signalling molecules Pectobacterium carotovo-
rumsubsp.carotovorum Soft rot Alinejad etal. (2020)
Burkholderia anthina Diffusible signal factor degra-
dation Xanthomonas campes-
trispv.campestris Black Rot Ye etal. (2020)
Pseudomonas nitroredu-
cens Degradation of AHLs includ-
ingN-(3-oxohexanoyl)-
L-homoserine lactone
(OHHL),N-(3-oxooctanoyl)-
L-homoserine lactone
(OOHL), andN-hexanoyl-L-
homoserine lactone (HHL)
Dickeya zeae Plant rot Zhang etal. (2021)
Oak bark Degradation of AHLs Pectobacterium caroto-
vorum Soft rot Vasilchenko etal. (2022)
Rhodococcus pyridini-
vorans Degradation of QS signals or
interference of signal genera-
tion or perception
Pectobacterium caroto-
vorum Soft rot Zhou etal. (2022)

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in bacterial disease pathosystems (Sundin etal. 2016;
Li etal. 2020a, b). A large pool of Rgenes that rep-
resents key components of the plant immune system,
have been identified and intensively studied in past
two decades (Van Schie and Takken 2014). Accord-
ing to gene-for-gene concept, a plant carrying a resist-
ance gene struggle against pathogen races that carry
corresponding effector proteins (Flor 1971). These
effectors present in bacteria elicit resistance response
in the host cells. Therefore, a large number of resist-
ance genes conferring resistance have been studied
so far against Xanthomonas oryzae, Xanthomonas
campestris, P. syringae etc. (Minsavage etal. 1990;
Chern et al. 2001). Rice is grown as a staple crop
worldwide and the plant is affected by major bacterial
pathogens that reduce overall production of rice every
year. Rice bacterial blight (BB) and bacterial leaf
streak (BLS) are two major bacterial diseases caused
by Xanthomonas oryzae pv. oryzae(Xoo) and Xan-
thomonas oryzae pv. oryzicola(Xoc), respectively
(Liu et al. 2014). Untill now, more than 40 resist-
ance (R) genes that confer resistance to various races
ofXanthomonas oryzaepv.oryzaehave been identi-
fied and more then twelve of these genes have been
Table 5 Recent nanomaterials used against phytopathogenic bacteria
Nanoparticles (NPs) Diseases Bacteria References
AgNPs Bacterial wilt Ralstonia solanacearum Chen etal. (2016)
Graphene oxide loaded with
copper oxide NPs
Bacterial speck Pseudomonas syringaepv.
tomato
Li etal. (2017)
Fe and CuNPs Black rot Xanthomonas campestris Moradian and Biparva (2018)
Copper oxide nanoparticles
(CuONPs)
Bacterial wilt Ralstonia solanacearum Chen etal. (2019)
Iron oxidenanoparticles
(Fe2O3−NPs)
Bacterial wilt Ralstonia solanacearum Alam etal. (2019)
AgNPs Soft rot Erwinia carotovora subsp.
atroseptica Abbas etal. (2019)
Zinc oxide and titanium dioxide
NPs
Soft rot Dickeya dadantii Hossain etal. (2019)
AgNPs Bacterial leaf blight Xanthomonas oryzae pv. oryzae Ahmed etal. (2020)
CuNPs and copper-chitosan
(Cu-Cs) nanocomposite
Leaf spot, wilt, blight Xanthomonas perforans,
Clavibacter michiganensis
subsp. michiganensis, Erwinia
amylovora and Pseudomonas
syringae pv. syringae
Shahryari etal. (2020)
Caprylate capped cobalt ferrite
NPs
Soft rot Erwinia carotovora Johnson etal. (2020)
Chromium NPs Fire blight Erwinia amylovora Kotb etal. (2020)
AgNPs Crown gall, fire blight, soft rot,
spot, wilt Agrobacterium tumefa-
ciens, Erwinia amylovora,
Pectobacterium caroto-
vormsubsp.carotovo-
rum,Pseudomonas lachry-
mans, Ralstonia solanacearum
Mohammed etal. (2020)
Silicon dioxide nanoparticles
(SiO2NPs)
Bacterial leaf spot and speck,
rot, wilt Pseudomonas syringaepv.
tomato, Xanthomonas
campestrispv.vesica-
toria,Pectobacterium
carotovorumsubsp.caroto-
vorumandRalstonia solan-
acearum
Parveen and Siddiqui (2021)
Carboxymethylcellulose copper-
montmorillonite nanocom-
posite
Soft rot Erwinia carotovora Rienzie etal. (2021)

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cloned i.e., Xa1,Xa3/Xa26,Xa4,xa5,Xa10,xa13,X
a21, Xa23, xa25, Xa27, xa41 and Xa 43 (Kim and
Reinke 2019; Jiang etal. 2020; Luo etal. 2021). In
pepper, a cluster of five predictedRgenes and three
defense-related genes were quantified as important
candidate genes that may confer resistance to bacte-
rial wilt caused by Ralstonia solanacearum(Du etal.
2019). Several workers have also emphasized on
quantitative trait locus (QTL) and marker based anal-
ysis approaches for identification of resistance sources
against Ralstonia solanacearum (Habe et al. 2019;
Pandiyaraj etal. 2019). Immune receptors encoded by
nucleotide binding leucine rich repeat (NLR) genes
are known to confer resistance to many pathogens
producing cognate elicitor. One such immune recep-
tor Roq 1 has been provedeffective against Ralstonia,
Xanthomonas and Pseudomonas syringae in tomato
(Thomas etal. 2020). In kiwifruit, multiple QTL have
been identified that provide resistance against bacte-
rial canker caused byPseudomonas syringaepv.acti-
nidiae(Tahir etal. 2019). Mazo etal. (2019) discov-
ered a locus in Solanum lycopersicoides that confers
resistance to race 1 of Pseudomonas syringae pv
tomato. This Ptr1gene has the potential to become
an important component for the control of Ralstonia
pseudosolanacearum and bacterial speck disease in
tomato. In addition to these bacterial pathogens Xan-
thomonas campestrispv.campestris (Xcc) is one of
the major bacteria that cause systemic infection of
black rot in susceptible Brassica plants. Against this
bacteria durable resistance can be achieved by accu-
mulating strong race specific genes through advanced
breeding methods (Collard et al. 2005). Different
group of researchers have reported R genes/QTL and
co-segregating DNA markers for resistance against
Xcc (Soengas etal. 2007; Kifuji etal. 2013; Sharma
etal. 2016; Singh etal. 2018). Genus Xanthomonas is
also known to cause bacterial spot of pepper and the
development of resistant cultivars through molecular
breeding has been deployed for many years. Accord-
ing to recent data, five non-allelic dominant hypersen-
sitive resistance genes (Bs1–Bs4, Bs7) and two reces-
sive non-hypersensitive resistance genes (bs5 and
bs6) have been used in pepper for molecular breed-
ing (Jones etal. 2002; Stall etal. 2009; Potnis etal.
2012; Gao etal. 2021). Recently, Transcription acti-
vator-like effectors (TALEs)assisted engineering for
disease resistance is emerging as a promising strategy
for development of broad-spectrum durable resistance
against Xanthomonas spp. (Luo et al. 2021). These
TALE proteins are produced by plant pathogenicXan-
thomonasspp and exhibit conserved structure that has
the ability to directly bind with promoter region of
host target genes. TALEs in Xoo plays important role
in inducing resistance (ETI) and susceptibility (ETS)
for rice immunity against pathogen (Xu etal. 2022).
In addition to these genes, SWEET genes that encode
sugar transporter proteins are also being deployed for
developing disease-resistant cultivars by using dif-
ferent conventional breeding methods and genome
editing techniques (Eom et al. 2019). The practical
approach to elevate resistance by using SWEET genes
is to use the system in that reduces sugar supply.
This mechanism is known as “starvation-mediated
resistance” or “resistance by loss of susceptibility”
(Oliva and Quibod 2017). Therefore, to design strate-
gies for disease-resistant crops, knowledge about the
molecular basis of pathogenesis involving TALE and
SWEET genes has to be used for effective manage-
ment under field conditions. In near future, a large
number of bioinformatics tools and diagnostic kits
can be helpful for researchers in designing new meth-
ods for developing disease-resistant plants.
Genome‑editing forbacterial disease management
For sustainable food production, the concept of new
genome modification techniques is essential as trans-
genic crops have been lesser accepted due to certain
limitations. Phytopathogenic bacteria are very diffi-
cult to control due to their diversity, rapid multiplica-
tion and easy spread to healthy plants. The new alter-
native methods enhancing food production such as
cisgenesis, intragenesis and the most recent genome
editing, aims to eliminate public concerns associated
with the transgenic crops. Genome editing gener-
ally involve point specific mutations in genome such
as site-directed nucleases (SDN) and oligo-directed
mutagenesis (ODM). The SDN technology includes
zinc-finger nucleases (ZFN), transcription activator-
like effector nuclease (TALEN), and clustered regu-
larly interspaced short palindromic repeat-associated
endonucleases (CRISPR/Cas) (Doudna and Charpen-
tier 2014; Songstad etal. 2017).
To improve crop productivity and to induce resi-
sance response in plants two important biotechnology
techniques i.e. cisgenesis and intragenesis are being

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employed in different parts of the globe. Cisgen-
esis involves the isolation of integral Cis-genes and
related promoter/terminator from the same spe-
cies which are integrated with identical or a closely
related genome. Whereas, intragenesis involves dif-
ferent coding and controlling sequences are accumu-
lated (Chibage et al. 2022). Cisgenic tomato plants
obtained by Agrobacterium-mediated gene transfor-
mationresulted in production of tomato lines resist-
ant to bacterial wilt disease caused byRalstonia sola-
nacearum (Morais et al. 2019). First cisgenic apple
was developed by using the cisgene FB_MR5 from
wild apple Malus × robusta 5 (Mr5) and Agrobacte-
rium mediated gene transformation technique. This
combination resulted in development of cisgenic
apple with resistance to fire blight pathogenic bacte-
ria (Kost etal. 2015). Recently, intragenesis approach
has been used in apple against Erwinia amylovora
by utilizing pathogen inducible promoter (Gaucher
et al. 2022). Cisgenic rice was also produced by
these techniques that imparts resistance against Xan-
thomonasoryzae pv. oryzicola (Schmidt etal. 2021).
Further, these approaches are also being deployed for
resistance against Xanthomonasoryzae pv. oryzae
and Ralstoniasolanacearum (Sharma et al. 2022;
Mangal etal. 2022).
To create multiple changes in a single gene or at
multiple sites in the genome at same time, CRISPR/
Cas9 is most commonly used (Georges and Ray 2017;
Scheben and Edwards 2018). Jiang etal. (2013) suc-
cessfully completed the first genome-based editing in
Arabidopsis using CRISPR/Cas9 system. Recently,
the CRISPR/Cas9 genome editing technique has
been successfully employed in several economically
important plants (Shan etal. 2014; Baltes etal. 2015;
Borrelli etal. 2018; Kumar etal. 2020). Xanthomonas
citri subsp. citri (Xcc) causes canker in citrus via
secretion of transcription activator like (TAL) effec-
tor i. e. PthA4, which activates the expression of the
cognate susceptibility (S) gene via binding of effec-
tor binding elements (EBE) in the promoter region
(Li et al. 2014). Consequently, with the advent of
CRISPR technology many researchers have gener-
ated canker-resistant citrus varieties by mutation
of the EBE or coding region of the LOB1 gene (Jia
et al. 2016; Peng et al. 2017). CRISPR/Cas9-tar-
geted modification of the CsLOB1 promoter gene
has improved resistance to citrus canker (Zhou etal.
2017a, b). Similarly CRISPR/Cas9-mediated edit-
ing of CsWRKY22 genes reduces susceptibility to
Xanthomonas citri subsp. citri in Citrus sinensis and
site-specific genome editing is a powerful method for
Table 6 Recent examples of CRISPR/Cas9 based genome editing against phytopathogenic bacteria
Disease Host Bacteria Target gene Nuclease References
Bacterial blight Rice Xanthomonas oryzae
pv. oryzae OsSWEET13/exon CRISPR/Cas9 Zhou etal. (2015)
Bacterial speck,
Bacterial spot
Tomato Pseudomonas syringae
pv. tomato,
Xanthomonas spp.
SlDMR6-1/exon CRISPR/Cas9 de Toledo etal. (2016)
Canker Citrus Xanthomonas citri CsLOB1/exon CRISPR/Cas9 Jia etal. (2017)
Canker Citrus Xanthomonas citri CsLOB1/promoter CRISPR/Cas9 Peng etal. (2017)
Bacterial blight Rice Xanthomonas oryzae
pv. oryzae SWEET11, SWEET13
and SWEET14
promoter
CRISPR/Cas9 Oliva etal. (2019)
Bacterial blight Rice Xanthomonas oryzae
pv. oryzae Os8N3 CRISPR/Cas9 Kim etal. (2019)
Fire blight Apple Erwinia amylovora MdDIPM4 CRISPR/Cas9-FLP/
FRT
Pompili etal. (2020)
Bacterial blight Rice Xanthomonas oryzae
pv. oryzae Xa13 promoter CRISPR/Cas9 Li etal. (2020a, b)
Canker Citrus Xanthomonas citri LOB1 promoter CRISPR-SpCas9p Jia and Wang (2020)
Pierce’s disease Grapevine Xylella fastidiosa TAS4andMYBA7 CRISPR/Cas9 Sunitha and Rock (2020)
Wilt Banana Xanthomonas campes-
trispv.musacearum DMR6 orthologue CRISPR/Cas9 Tripathi etal. (2021)

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citrus improvement (Wang etal. 2019a, b). Recently,
CRISPR‐SpCas9p was used for development of
homozygous canker‐resistant citrus in the T0 genera-
tion (Jia and Wang 2020). For the efficient control of
bacterial blight of rice natural variations in the pro-
moter of OsSWEET13 and OsSWEET14 was done by
genome editing to expand the resistance response in
plants (Zaka etal. 2018). CRISPR/Cas9 system was
used for editing the Xa13 gene to get transgene‐free
bacterial blight‐resistant rice plants (Li et al. 2020a,
b). Table6 depicts the recent examples of CRISPR/
Cas9 based system targeting different genes against
phytopathogenic bacteria. Together, these results sug-
gest that knocking out different genes by CRISPR/
Cas based editing system may be a promising strategy
to confer broad-spectrum disease resistance to bacte-
rial pathogens in crops.
Conclusion
Global environmental changes have greatly influ-
enced the plant diseases as pathogenic microbes
respond differently to the changing environment.
The virulence mechanisms such as the production
of toxins and virulence proteins, pathogen coloniza-
tion, reproduction, survival and spread are greatly
influenced by climate. Emergence of antibiotic resist-
ant bacterial strains and new pathovars has driven
research efforts to discover alternative strategies in
bacterial disease management. Besides, plant resist-
ance mechanisms, RNA interference, defence hor-
mone networks etc. are affected by environmental
factors. The discovery of different virulence factors
associated with disease development has led to esca-
lated research towards discovering the possible bio-
logical control measures to target the specific genes
responsible for extracellular polysaccharide secretion,
effector proteins, quorum sensing regulation, toxin
and hormonal production. Understanding the patho-
genicty and virulence mechanisms in bacterial infec-
tion could provide useful management strategies to
combat potential threat to global agriculture. Moreo-
ver, this is the need of the hour to amalgamate all the
traditional and recent molecular knowledge to under-
stand the multi dimensional plant–pathogen interac-
tions and to focus on production of disease-resistant
crop plants that are resilient to changing environ-
ment. During the past few decades innovations in
bioactive natural compounds is getting growing atten-
tion worldwide for plant disease management. These
molecules have been deployed in bacterial disease
management in several crops. Similarly, nanobiopes-
ticides are also efficiently used against bacteria. Bac-
teriophage mediated and quorum quenching mediated
control also represents a new frontier in bacterial dis-
ease management. Continuously increasing amount
of research data has opened up greater understanding
of quorum sensing mechanisms, biofilm formation
and function of type III effector proteins. This area of
research has now broadened the new possibilities for
the management of disease. Further, the role of resist-
ance genes in plant diseases has also strengthened
the management practices against bacterial diseases.
With the advent in novel genome editing technologies
such as ZFN, TALEN and CRISPR/Cas9 systems
plant breeders could effectively generate new sources
of resistance within a time framework without intro-
ducing foreign DNA into the host genome. Besides
the potential properties of these novel techniques,
there are certain limitations that need to be addressed
such as methods of delivery of these new molecules
under field conditions, consumer acceptance and pub-
lic acceptance of genome edited crops.
Acknowledgements The authors are grateful to the Depart-
ment of Plant Pathology, Dr. Y. S. Parmar University of Horti-
culture and Forestry Solan, for continuous support.
Author contributions All authors contributed equally for
compilation of manuscript.
Funding There is no financial support for this manuscript.
Declarations
Conflict of interest The authors declare that they have no
conflict of interest.
Ethical approval and consent to participate This article
does not contain any studies with human participants or animals
performed by any of the authors.
Consent for publication All authors approved the manu-
script for publication.
References
Abbas A, Naz SS, Syed SA (2019) Antimicrobial activity of
silver nanoparticles (AgNPs) against Erwinia carotovora

Antonie van Leeuwenhoek
1 3
Vol.: (0123456789)
subsp. atroseptica and Alternaria alternata. Pak J Agric
Sci 56(1):113–117
Abdel MA (2013) Controlling of Pseudomonas syringae by
nanoparticles produced by Streptomyces bikiniensis. J
Pure Appl Microbiol 7:1121–1129
Achari GA, Ramesh R (2015) Characterization of bacteria
degrading 3-hydroxy palmitic acid methyl ester (3OH-
PAME), a quorum sensing molecule of Ralstonia sola-
nacearum. Lett Appl Microbiol 60(5):447–455. https://
doi. org/ 10. 1111/ lam. 12389
Addy HS, Askora A, Kawasaki T, Fujie M, Yamada T (2012)
Loss of virulence of the phytopathogen Ralstonia sola-
nacearum through infection by ϕRSM filamentous
phages. Phytopathology 102(5):469–477
Agrios GN (2005) Plant pathology. Academic Press, London
Ahmed T, Shahid M, Noman M, Niazi MBK, Mahmood F,
Manzoor I etal (2020) Silver nanoparticles synthesized
by using Bacillus cereus SZT1 ameliorated the dam-
age of bacterial leaf blight pathogen in rice. Pathogens
9(3):160
Akbari Kiarood SL, Rahnama K, Golmohammadi M, Nas-
rollanejad S (2020) Quorum-quenching endophytic
bacteria inhibit disease caused by Pseudomonas syrin-
gae pv. syringae in Citrus cultivars. J Basic Microbiol
60(9):746–757
Alam T, Khan RAA, Ali A, Sher H, Ullah Z, Ali M (2019)
Biogenic synthesis of iron oxide nanoparticles via
Skimmia laureola and their antibacterial efficacy
against bacterial wilt pathogen Ralstonia solan-
acearum. Mater Biol Appl 98:101–108
Al-Huqail AA, Behiry SI, Salem MZ, Ali HM, Siddiqui MH,
Salem AZ (2019) Antifungal, antibacterial, and antiox-
idant activities of Acacia saligna (Labill.) HL Wendl.
flower extract: HPLC analysis of phenolic and flavo-
noid compounds. Molecules 24(4):700
Alinejad F, Shahryari F, Eini O, Sarafraz-Niko F, Shekari A,
Setareh M (2020) Screening of quorum-quenching bac-
teria associated with rhizosphere as biocontrol agents
of Pectobacterium carotovorum subsp. carotovorum.
Arch Phytopathol Plant Prot 53(11–12):509–523
Alymanesh MR, Parissa T, Saeed T (2016) Pseudomonas as
a frequent and important quorum quenching bacterium
with biocontrol capability against many phytopatho-
gens. Biocontrol Sci Technol 26(12):1719–1735
Andrews JH, Harris RF (2000) The ecology and biogeog-
raphy of microorganisms of plant surfaces. Annu Rev
Phytopathol 38:145–180
Antunes LCM, Ferreira RB, Buckner MM, Finlay BB (2010)
Quorum sensing in bacterial virulence. Microbiology
156:2271–2282
Arnold DL, Preston GM (2019) Pseudomonas syringae:
enterprising epiphyte and stealthy parasite. Microbiol-
ogy 165:251–253
Asfour HZ (2018) Anti-quorum sensing natural compounds.
J Microsc Ultrastruct 6:1–10. https:// doi. org/ 10. 4103/
JMAU. JMAU- 10- 18
Bae JY, Wu J, Lee HJ, Jo EJ, Murugaiyan S, Chung E, Lee
SW (2012) Biocontrol potential of a lytic bacterio-
phage PE204 against bacterial wilt of tomato. J Micro-
biol Biotechnol 22(12):1613–1620
Balogh B, Canteros BI, Stall RE, Jones JB (2008) Control
of citrus canker and citrus bacterial spot with bacte-
riophages. Plant Dis 92:1048–1052. https:// doi. org/ 10.
1094/ PDIS- 92-7- 1048
Baltes NJ, Hummel AW, Konecna E, Cegan R, Bruns AN,
Bisaro DM, Voytas DF (2015) Conferring resistance
to geminiviruses with the CRISPR–Cas prokaryotic
immune system. Nat Plants 1:15145
Barber C, Tang J, Feng J, Pan M, Wilson T, Slater H, Dow J,
Williams P, Daniels M (1997) A novel regulatory system
required for pathogenicity of Xanthomonas campestris is
mediated a small diffusible signal molecule. Mol Micro-
biol 24(3):555–566
Barnard AML, Salmond GPC (2007) Quorum sensing in
Erwinia species. Anal Biolanal Chem 387:415–423
Behiry SI, El-Hefny M, Salem MZ (2020) Toxicity effects of
Eriocephalus africanus L. leaf essential oil against some
molecularly identified phytopathogenic bacterial strains.
Nat Prod Res 34(23):3394–3398
Bender CL, Alarcon-Chaidez F, Gross DC (1999) Pseu-
domonas syringae phytotoxins: mode of action, regula-
tion and biosynthesis by peptide and polyketide syn-
thetases. Microbiol Mol Biol Rev 63:266–292
Bender CL, Scholz-Schroeder BK (2004) New insights into the
biosynthesis, mode of action, and regulation of syringo-
mycin, syringopeptin, and coronatine. In: Ramos JL (ed)
The pseudomonads. Kluwer, Dordrecht, pp 125–158
Bhoyar MS, Singh UB, Sahu U, Nagrale DT, Sahu PK (2017)
Characterization of lytic bacteriophage XCC9SH3 infect-
ing Xanthomonas campestris pv. campestris. J Plant
Pathol 99:233–238
Borrelli VMG, Brambilla V, Rogowsky P, Marocco A, Lanu-
bile A (2018) The enhancement of plant disease resist-
ance using CRISPR/Cas9 technology. Front Plant Sci
9:1245–1245
Bourigault Y, Rodrigues S, Crépin A, Chane A, Taupin L,
Bouteiller M, Dupont C, Merieau A, Konto-Ghiorghi Y,
Boukerb AM etal (2021) Biocontrol of biofilm forma-
tion: jamming of sessile-associated rhizobial communi-
cation by rhodococcal quorum-quenching. Int J Mol Sci
22:8241
Buonaurio R (2008) Infection and plant defense responses during
plant bacterial interaction. In: Barka EA, Clément C (eds)
Plant-microbe interactions, Research Signpost, Kerala,
India, pp 169–197
Burch TR, Sadowsky MJ, LaPara TM (2017) Effect of different
treatment technologies on the fate of antibiotic resistance
genes and class 1 integrons when residual municipal
waste water solids are applied to soil. Environ Sci Tech-
nol 51:14225–14232
Caicedo JC, Villamizar S, Ferro MIT, Kupper KC, Ferro JA
(2016) Bacteria from the citrus phylloplane can disrupt
cell–cell signalling in Xanthomonas citri and reduce cit-
rus canker disease severity. Plant Pathol 65(5):782–791
Camele I, Elshafie HS, Caputo L, De Feo V (2019) Anti-quo-
rum sensing and antimicrobial effect of mediterranean
plant essential oils against phytopathogenic bacteria.
Front Microbiol 10:2619. https:// doi. org/ 10. 3389/ fmicb.
2019. 02619
Carstens AB, Djurhuus AM, Kot W, Hansen LH (2019)
A novel six-phage cocktail reduces Pectobacterium

Antonie van Leeuwenhoek
1 3
Vol:. (1234567890)
atrosepticum soft rot infection in potato tubers under
simulated storage conditions. FEMS Microbiol Lett
366(9):fnz101. https:// doi. org/ 10. 1093/ femsle/ fnz101
Chang JH, Desveaux D, Creason AL (2014) The ABCs and
123s of bacterial secretion systems in plant pathogenesis.
Annu Rev Phytopathol 52:317–345
Chen J, Li S, Luo J, Wang R, Ding W (2016) Enhancement
of the antibacterial activity of silver nanoparticles
against phytopathogenic bacterium Ralstonia solan-
acearum by stabilization. J Nanomater. https:// doi. org/
10. 1155/ 2016/ 71358 52
Chen J, Mao S, Xu Z, Ding W (2019) Various antibacterial
mechanisms of biosynthesized copper oxide nanopar-
ticles against soil borne Ralstonia solanacearum. RSC
Adv 9(7):3788–3799
Chern MS, Fitzgerald HA, Yadav RC, Canlas PE, Dong X,
Ronald PC (2001) Evidence for a disease-resistance
pathway in rice similar to the NPR1-mediated signaling
pathway in Arabidopsis. Plant J 27:101e13
Chibage FC, Nyoni M, Murashiki TC, Samukange VC,
Muzerengwa R, Mahuni C, Savadye DT (2022)
Cisgenesis and intragenesis: innovative tools for crop
improvement. In: Cisgenic crops: potential and pros-
pects. Springer, Cham, pp 43–65
Cisek AA, Dąbrowska I, Gregorczyk KP, Wyżewski Z (2017)
Phage therapy in bacterial infections treatment: one
hundred years after the discovery of bacteriophages.
Curr Microbiol 74:277–283
Clavijo-Coppens F, Ginet N, Cesbron S, Briand M, Jacques
MA, Ansaldi M (2021) Novel virulent bacterio-
phages infecting mediterranean isolates of the plant
pest Xylella fastidiosa and Xanthomonas albilineans.
Viruses 13(5):725
Coenye T, Nelis HJ (2010) Review, in vitro and in vivo
model systems to study microbial biofilm formation.
J Microbiol Methods 83:89–105. https:// doi. org/ 10.
1016/j. mimet. 2010. 08. 018
Collard BCY, Jahufer MZZ, Brouwer JB, Pang ECK (2005)
An introduction to markers, quantitative trait loci
(QTL) mapping and marker-assisted selection for
crop improvement: the basic concepts. Euphytica
142:169–196
Czajkowski R (2016) Bacteriophages of soft rot Entero-
bacteriaceae—a mini-review. FEMS Microbiol Lett
363:fnv230. https:// doi. org/ 10. 1093/ femsle/ fnv230
Czajkowski R, Smolarska A, Ozymko Z (2017) The viability
of lytic bacteriophage ΦD5 in potato-associated environ-
ments and its effect on Dickeya solani in potato (Sola-
num tuberosum L.) plants. PLoS ONE 12(8):e0183200
D’Costa VM, King CE, Kalan L, Morar M, Sung WWL
et al (2011) Antibiotic resistance is ancient. Nature
477:457–461
da Silva FP, Xavier ADS, Bruckner FP, de Rezende RR,
Vidigal PMP, Alfenas-Zerbini P (2019) Biological and
molecular characterization of a bacteriophage infecting
Xanthomonas campestris pv. campestris, isolated from
brassica fields. Arch Virol 164:1857–1862
Daughtrey ML, Wick RL, Peterson JL (2006) Compendium of
flowering potted plants. The American Phytopathological
Society, St. Paul, pp 55–56
Davies J, Davies D (2010) Origins and evolution of antibiotic
resistance. Microbiol Mol Biol Rev 74:417–433
de Oliveira AG, Spago FR, Simionato AS, Navarro MOP, da
Silva CS, Barazetti AR, Cely MVT etal (2016) Bioactive
organocopper compound from Pseudomonas aeruginosa
inhibits the growth of Xanthomonas citri subsp. citri.
Front Microbiol 7:113
De Toledo Thomazella DP, Brail Q, Dahlbeck D, Staska-
wicz BJ (2016) CRISPR-Cas9 mediated mutagenesis
of a DMR6 ortholog in tomato confers broad-spectrum
disease resistance. bioRxiv, 064824. https:// doi. org/ 10.
1101/ 064824
Dees MW, Lysøe E, Rossmann S, Perminow J, Brurberg MB
(2017) Pectobacterium polaris sp. nov., isolated from
potato (Solanum tuberosum). Int J Syst Evol Microbiol
67:5222–5229
Dellagi A, Segond D, Rigault M, Fagard M, Simon C, Sain-
drenan P, Expert D (2009) Microbial siderophores
exert a subtle role in arabidopsis during infection by
manipulating the immune response and the iron status.
Plant Physiol 150:1687–1696
Denaro M, Smeriglio A, Barreca D, De Francesco C,
Occhiuto C, Milano G, Trombetta D (2020) Antiviral
activity of plants and their isolated bioactive com-
pounds: an update. Phytother Res 34(4):742–768
Denny TP (1995) Involvement of bacterial polysaccharides in
plant pathogenesis. Annu Rev Phytopathol 33:173–197
Dong YH, Xu JL, Li XZ, Zhang LH (2000) Aii A, an enzyme
that inactivates the acyl-homoserine lactone quorum-
sensing signal and attenuates the virulence of Erwinia
carotovora. Proc Natl Acad Sci USA 97:3526–3531
Dong YH, Wang LH, Xu JL, Zhang HB, Zhang XF, Zhang
LH (2001) Quenching quorum-sensing-dependent bac-
terial infection by an N-acyl homoserine lactonase.
Nature 411:813–817
Dong Z, Xing S, Liu J, Tang X, Ruan L, Sun M, Peng D
(2018) Isolation and characterization of a novel phage
Xoo-sp2 that infects Xanthomonas oryzae pv. oryzae. J
Gen Virol 99(10):1453–1462
Dou C, Xiong J, Gu Y, Yin K, Wang J, Hu Y, Zhou D, Fu
X, Qi S, Zhu X, Yao S, Xu H, Nie C, Liang Z, Yang
S, Wei Y, Cheng W (2018) Structural and functional
insights into the regulation of the lysis-lysogeny deci-
sion in viral communities. Nat Microbiol 3:1285–1294
Doudna JA, Charpentier E (2014) The new frontier of
genome engineering with CRISPR–Cas9. Science
346:1258096. https:// doi. org/ 10. 1126/ scien ce. 12580 96
Du H, Wen C, Zhang X, Xu X, Yang J, Chen B, Geng S
(2019) Identification of a major QTL (qRRs-10.1) that
confers resistance to Ralstonia solanacearum in pepper
(Capsicum annuum) using SLAF-BSA and QTL map-
ping. Int J Mol Sci 20(23):5887
Dubchak S, Ogar A, Mietelski AW, Turnau K (2010) Influ-
ence of silver and titanium nanoparticles on arbus-
cularmycorrhiza colonization and accumulation of
radiocaesium in Helianthus annuus. Span J Agric Res
8:103–108
Elshafie HS, Ghanney N, Mang SM, Ferchichi A, Camele
I (2016) An in vitro attempt for controlling severe
phyto and human pathogens using essential oils from

Antonie van Leeuwenhoek
1 3
Vol.: (0123456789)
Mediterranean plants of genus Schinus. J Med Food
19:266–273. https:// doi. org/ 10. 1089/ jmf. 2015. 0093
Emeriewen OF, Wöhner T, Flachowsky H, Peil A (2019) Malus
hosts–Erwinia amylovora interactions: strain pathogenic-
ity and resistance mechanisms. Front Plant Sci 10:551
Eom JS, Luo D, Atienza-Grande G, Yang J, Ji C, Van Luu T,
Huguet-Tapia JC, Char SN, Liu B, Nguyen H, Schmidt
SM (2019) Diagnostic kit for rice blight resistance. Nat
Biotechnol 37(11):1372–1379
Faure D, Dessaux Y (2007) Quorum sensing as a target for
developing control strategies for the plant pathogen Pec-
tobacterium. Eur J Plant Pathol 119:353e65. https:// doi.
org/ 10. 1007/ s10658- 007- 9149-1
Fetzner S (2015) Quorum quenching enzymes. J Biotechnol
201:2–14. https:// doi. org/ 10. 1016/j. jbiot ec. 2014. 09. 001
Flor HH (1971) Current status of the gene-for-gene concept.
Annu Rev Phytopathol 9:275e98
Frampton RA, Pitman AR, Fineran PC (2012) Advances in
bacteriophage-mediated control of plant pathogens. Int J
Microbiol. https:// doi. org/ 10. 1155/ 2012/ 326452
Francis VI, Stevenson EC, Porter SL (2017) Two-component
systems required for virulence in Pseudomonas aerugi-
nosa. FEMS Microbiol Lett 364:1–22. https:// doi. org/ 10.
1093/ femsle/ fnx104
Freeman BC, Battie GA (2008) An overview of plant defenses
against pathogens and herbivores. In: The plant health
instructor. Iowa State University, Ames, IA, USA, vol 94,
pp 1–12
Frewer LJ, Norde W, Fischer ARH, Kampers FWH (2011)
Nanotechnology in the agri-food sector: implications for
the future. Wiley, Weinheim. https:// doi. org/ 10. 1002/
97835 27634 798
Fu B, Zhai Y, Gleason M, Beattie GA (2021) Characterization
of Erwinia tracheiphila bacteriophage FBB1 isolated
from spotted cucumber beetles that vector E. tracheiph-
ila. Phytopathology 111(12):2185–2194
Fuchs TM (1998) Molecular mechanisms of bacterial patho-
genicity. Naturwissenschaften 85:99–108
Gao S, Wang F, Niran J, Li N, Yin Y, Yu C etal (2021) Tran-
scriptome analysis reveals defense-related genes and
pathways against Xanthomonas campestris pv. vesi-
catoria in pepper (Capsicum annuum L.). PLoS ONE
16(3):e0240279
Garge SS, Nerurkar AS (2017) Evaluation of quorum quench-
ing Bacillus spp. for their biocontrol traits against Pecto-
bacterium carotovorum subsp. carotovorum causing soft
rot. Biocatal Agric Biotechnol 9:48–57
Gaucher M, Righetti L, Aubourg S, de Bernonville TD, Brisset
MN, Chevreau E, Vergne E (2022) An Erwinia amylo-
vora inducible promoter for improvement of apple fire
blight resistance. Plant Cell Rep 41(7):1499
Georges F, Ray H (2017) Genome editing of crops: a renewed
opportunity for food security. GM Crops Food 8(1):1–12
Goyer C (2005) Isolation and characterization of phages Stsc1
and Stsc3 infecting Streptomyces scabiei and their poten-
tial as biocontrol agents. Can J Plant Pathol 27:210–216.
https:// doi. org/ 10. 1080/ 07060 66050 95072 18
Grandclement C, Tannieres M, Morera S, Dessaux Y, Faure
D (2016) Quorum quenching: role in nature and applied
developments. FEMS Microbiol Rev 40:86–116. https://
doi. org/ 10. 1093/ femsre/ fuv038
Green S, Studholme DJ, Laue BJ, Dorati F, Lovell H, Arnold D,
Cottrell JE, Bridgett S, Blaxter M, Huitema E, Thwaites
R, Sharp PM, Jackson RW, Kamoun S (2010) Compara-
tive genome analysis provides insights into the evolution
and adaptation of Pseudomonas syringae pv. aesculi on
Aesculus hippocastanum. PLoS ONE 5:e10224
Grijpstra J, Arenas J, Rutten L, Tommassen J (2013) Autotrans-
porter secretion: varying on a theme. Res Microbiol
164:562–582
Gupta AK, Sharma A, Singh D, Chandel S, Sharma RC,
Mahajan R, Gupta A (2015) Occurrence of crown gall
caused by Agrobacterium tumefaciens on rose. Indian
Phytopathol 68:229–230
Habe I, Miyatake K, Nunome T, Yamasaki M, Hayashi T
(2019) QTL analysis of resistance to bacterial wilt
caused by Ralstonia solanacearum in potato. Breed Sci
69(4):592–600
Hayward AC (1993) The hosts of Xanthomonas. In: Swings
JC, Civerolo EL (eds) Xanthomonas. Chapman and Hall,
London, pp 1–119
He YW, Zhang LH (2008) Quorum sensing and virulence
regulation in Xanthomonas campestris. FEMS Microbiol
Rev 32:842–857. https:// doi. org/ 10. 1111/j. 1574- 6976.
2008. 00120.x
Helman Y, Chernin L (2015) Silencing the mob: disrupting
quorum sensing as a means to fight plant disease. Mol
Plant Pathol 16(3):316–329. https:// doi. org/ 10. 1111/
mpp. 12180
Hossain A, Abdallah Y, Ali M, Masum M, Islam M, Li B etal
(2019) Lemon-fruit-based green synthesis of zinc oxide
nanoparticles and titanium dioxide nanoparticles against
soft rot bacterial pathogen Dickeya dadantii. Biomolecu-
lens 9(12):863
Ivanova A, Ivanova K, Tzanov T (2018) Inhibition of quo-
rum-sensing: a new paradigm, in controlling bacterial
virulence and biofilm formation. In: Kalia VC (ed) bio-
technological applications of quorum sensing inhibitors.
Springer, Berlin
Jamiołkowska A (2020) Natural compounds as elicitors of
plant resistance against diseases and new biocontrol
strategies. Agron 10(2):173
Jang H, Kim ST, Sang MK (2022) Suppressive effect of bioac-
tive extracts of Bacillus sp. H8–1 and Bacillus sp. K203
on tomato wilt caused by Clavibacter michiganensis
subsp. michiganensis. Microorganisms 10(2):403
Jia H, Wang N (2020) Generation of homozygous canker-
resistant citrus in the T0 generation using CRISPR-
SpCas9p. Plant Biotechnol J 18(10):1990
Jia H, Orbovic V, Jones JB, Wang N (2016) Modification of the
PthA4 effector binding elements in Type I CsLOB1 pro-
moter using Cas9/sgRNA to produce transgenic Duncan
grapefruit alleviating XccDpthA4:dCsLOB1.3 infection.
Plant Biotechnol J 14:1291–1301
Jia H, Zhang Y, Orbović V, Xu J, White FF, Jones JB, Wang N
(2017) Genome editing of the disease susceptibility gene
CsLOB1 in citrus confers resistance to citrus canker.
Plant Biotechnol J 15:817–823. https:// doi. org/ 10. 1111/
pbi. 12677
Jiang W, Zhou H, Bi H, Fromm M, Yang B, Weeks DP (2013)
Demonstration of CRISPR/Cas9/sgRNA-mediated
targeted gene modification in Arabidopsis, tobacco,

Antonie van Leeuwenhoek
1 3
Vol:. (1234567890)
sorghum and rice. Nucleic Acids Res 41(20):188. https://
doi. org/ 10. 1093/ nar/ gkt780
Jiang N, Yan J, Liang Y etal (2020) Resistance genes and their
interactions with bacterial blight/leaf streak pathogens
(Xanthomonas oryzae) in rice (Oryza sativa L.)—an
updated review. Rice 13:3
Johnson M, Gaffney C, White V, Bechelli J, Balaraman R, Trad
T (2020) Non-hydrolytic synthesis of caprylate capped
cobalt ferrite nanoparticles and their application against
Erwinia carotovora and Stenotrophomonas maltophilia. J
Mater Chem B 8(47):10845–10853
Jones JB, Jackson LE, Balogh B, Obradovic A, Iriarte FB,
Momol MT (2007) Bacteriophages for plant disease con-
trol. Annu Rev Phytopathol 45:245–262
Jones JB, Minsavage GV, Roberts PD, Johnson RR, Kousik
CS, Subramanian S et al (2002) A non-hypersensitive
resistance in pepper to the bacterial spot pathogen is
associated with two recessive genes. Phytopathology
92(3):273–277
Kawaguchi A, Nita M, Ishii T, Watanabe M, Noutoshi Y
(2019) Biological control agent Rhizobium (=Agrobac-
terium) vitis strain ARK-1 suppresses expression of the
essential and non-essential vir genes of tumorigenic R.
vitis. BMC Res Notes 12:1–6
Keen EC (2015) A century of phage research: bacteriophages
and the shaping of modern biology. BioEssays 37:6–9
Khan RAA, Najeeb S, Mao Z, Ling J, Yang Y, Li Y, Xie B
(2020) Bioactive secondary metabolites from Tricho-
derma spp. against phytopathogenic bacteria and Root-
knot nematode. Microorganisms 8(3):401
Kifuji Y, Hanzaea H, Terasawa Y, Nishio T (2013) QTL analy-
sis of black rot resistance in cabbage using newly devel-
oped EST-SNP markers. Euphytica 190:289–295
Kim SM, Reinke RF (2019) A novel resistance gene for bac-
terial blight in rice, Xa43 (t) identified by GWAS, con-
firmed by QTL mapping using a bi-parental population.
PLoS ONE 14(2):e0211775
Kim MH, Park SW, Kim YK (2011) Bacteriophages of Pseu-
domonas tolaasii for the biological control of brown
blotch disease. J Appl Biol Chem 54:99–104. https:// doi.
org/ 10. 3839/ jksabc. 2011. 014
Kim YA, Moon H, Park CJ (2019) CRISPR/Cas9-targeted
mutagenesis of Os8N3 in rice to confer resistance to
Xanthomonas oryzae pv. oryzae. Rice 12(1):1–13
Kost TD, Gessler C, Jänsch M, Flachowsky H, Patocchi A,
Broggini GA (2015) Development of the first cisgenic
apple with increased resistance to fire blight. PLoS ONE
10(12):e0143980
Kotb OM, Abd El-Latif FM, Atawia AR, Saleh SS, El-Gioushy
SF (2020) Green synthesis of chromium nanoparticles
by aqueous extract of Melia azedarach, Artemisia herba-
alba and bacteria fragments against Erwinia amylovora.
Asian J Biotechnol Bioresour 6(2):22–30
Kou Y, Wang S (2010) Broad-spectrum and durability: under-
standing of quantitative disease resistance. Curr Opin
Plant Biol 13:181–185
Kulshreshtha G, Velusamy P (2012) Antibacterial potential of
bioactive compounds from fermented culture of Pseu-
domonas aeruginosa SRM1 against Xanthomonas oryzae
pv. Oryzae Minerva Biotecnologica 24(2):29
Kumar K, Gupta CS, Chander Y, Singh AK (2005) Antibiotic
use in agriculture and its impact on the terrestrial envi-
ronment. Adv Agric 87:1–54
Kumar P, Alok A, Kumar J (2020) Expanding the potential of
CRISPR-Cas9 technology for crops improvement. In:
Advances in synthetic biology. Springer
Kuzmanovic N, Smalla K, Gronow S, Puławska J (2018)
Rhizobium tumorigenes sp. nov., a novel plant tumori-
genic bacterium isolated from cane gall tumors on thorn-
less blackberry. Sci Rep 8:9051
Kyrkou I, Pusa T, Ellegaard JL, Sagot M-F, Hansen LH (2018)
Pierce’s disease of grapevines: a review of control strate-
gies and an outline of an epidemiological model. Front
Microbiol 9:2141
Lee SY, Thapa Magar R, Kim HJ et al (2021) Complete
genome sequence of a novel bacteriophage RpY1 infect-
ing Ralstonia solanacearum strains. Curr Microbiol
78:2044–2050
Levy SB (2002) The antibiotic paradox: how misuse of antibi-
otics destroys their curative powers. Perseus, Cambridge
Li C, Li W, Zhou Z, Chen H, Xie C, Lin Y (2020a) A new
rice breeding method: CRISPR/Cas9 system editing of
the Xa13 promoter to cultivate transgene-free bacterial
blight-resistant rice. Plant Biotechnol J 18(2):313
Li W, Deng Y, Ning Y, He Z, Wang G-L (2020b) Exploit-
ing broad-spectrum disease resistance in crops: from
molecular dissection to breeding. Annu Rev Plant Biol
71:575–603
Li Y, Yang D, Cui J (2017) Graphene oxide loaded with
copper oxide nanoparticles as an antibacterial agent
against Pseudomonas syringae pv. tomato. RSC Adv
7(62):38853–38860
Li Z, Zou L, Ye G, Xiong L, Ji Z, Zakria M, Hong N etal
(2014) A potential disease susceptibility gene CsLOB of
citrus is targeted by a major virulence effector PthA of
Xanthomonas citri subsp. citri. Mol Plant 7:912–915
Lim JA, Lee JS, Roh DH, Jung E, Oh K, Heu S (2013) Bio-
control of Pectobacterium carotovorum subsp. caroto-
vorum using bacteriophage PP1. J Microbiol Biotechnol
23(8):1147–1153
Liu W, Liu J, Triplett L, Leach JE, Wang GL (2014) Novel
insights into rice innate immunity against bacterial and
fungal pathogens. Annu Rev Phytopathol 52:213–241
Łobocka MB, Rose DJ, Plunkett G, Rusin M, Samojedny A,
Lehnherr H et al (2004) Genome of bacteriophage P1.
J Bacteriol 186:7032–7068. https:// doi. org/ 10. 1128/ JB.
186. 21. 7032- 7068. 2004
Lok CN, Ho CM, Chen R, He QY, Yu WY, Sun H, Tam PK,
Chiu JF, Che CM (2007) Silver nanoparticles: partial
oxidation and antibacterial activities. J Biol Inorg Chem
12:527–534
Luo D, Huguet-Tapia JC, Raborn RT, White FF, Brendel VP,
Yang B (2021) The Xa7 resistance gene guards the rice
susceptibility gene SWEET14 against exploitation by the
bacterial blight pathogen. Plant Commun 2(3):100164
Malafaia CB, Jardelino ACS, Silva AG, de Souza EB, Macedo
AJ, dos Santos Correia MT, Silva MV (2018) Effects of
Caatinga plant extracts in planktonic growth and bio-
film formation in Ralstonia solanacearum. Microb Ecol
75(3):555–561

Antonie van Leeuwenhoek
1 3
Vol.: (0123456789)
Mancini E, Camele I, Elshafie HS, De Martino L, Pellegrino C,
Grulova D etal (2014) Chemical composition and bio-
logical activity of the essential oil of Origanum vulgare
ssp. hirtum from different areas in the southern apen-
nines (Italy). Chem Biodiver 11:639–651. https:// doi. org/
10. 1002/ cbdv. 20130 0326
Mangal V, Sood S, Kumar V, Bhardwaj V (2022) Role of
genetic resources in management of potato pests and
diseases. In: Chakrabarti SK, Sharma S, Shah MA (eds)
Sustainable management of potato pests and diseases.
Springer, Singapore, pp 185–211
Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum
M, Ronald P, Dow M, Verdier V, Beer S, Machado M,
Toth I, Salmond G, Foster GD (2012) Top 10 plant
pathogenic bacteria in molecular plant pathology. Mol
Plant Pathol 13:614–629
Mazo-Molina C, Mainiero S, Hind SR, Kraus CM, Vachev
M, Maviane-Macia F, Lindeberg M, Saha S, Strickler
SR, Feder A, Giovannoni JJ (2019) The Ptr1 locus of
Solanum lycopersicoides confers resistance to race
1 strains of Pseudomonas syringae pv. tomato and to
Ralstonia pseudosolanacearum by recognizing the type
III effectors AvrRpt2 and RipBN. Mol Plant Microbe
Interact 32(8):949–960
McLeod A, Masimba T, Jensen T, Serfontein K, Coertze S
(2017) Evaluating spray programs for managing cop-
per resistant Pseudomonas syringae pv. Tomato popu-
lations on tomato in the Limpopo region of South
Africa. Crop Protection 102: 32–42
Minsavage GV, Dahlbeck D, Whalen MC, Kearney B, Bonas
U, Staskawicz BJ etal (1990) Gene-for-gene relation-
ships specifying disease resistance in Xanthomonas
campestris pv. vesicatoria–pepper interactions. Mol
Plant Microbe Int 3:41e7
Mohammed TG, Gomah AA, Abd El-Rahman AF (2020)
Biogenic synthesis of silver nanoparticles using Pimpi-
nella anisum L seed aqueous extract and its inhibitory
action against some phytopathogens. J Mater Sci Res
Rev 6(2):30–39
Molina L, Rezzonico F, De Fago G, Duffy B (2005) Auto-
induction in Erwinia amylovora: evidence of an acyl-
homoserine lactone signal in the fire blight pathogen. J
Bacteriol 187:3206–3213
Moradian F, Ghorbani R, Biparva P (2018) Assessment of
different antibacterial effects of Fe and Cu nanoparti-
cles on Xanthomonas campestris growth and expres-
sion of its pathogenic gene hrpE. J Agric Sci Technol
20(5):1059–1070
Morais TP, Zaini PA, Chakraborty S, Gouran H, Carvalho
CP, Almeida-Souza HO, Souza JB, Santos PS, Goulart
LR, Luz JM, Nascimento R (2019) The plant-based
chimeric antimicrobial protein SlP14a-PPC20 protects
tomato against bacterial wilt disease caused by Ralsto-
nia solanacearum. Plant Sci 280:197–205
Morales-Ubaldo AL, Rivero-Perez N, Avila-Ramos
F, Aquino-Torres E, Prieto-Méndez J, Hetta HF,
Zaragoza-Bastida A (2021) Bactericidal activity of
Larrea tridentata hydroalcoholic extract against phy-
topathogenic bacteria. Agronomy 11(5):957
Nazir A, Dong Z, Liu J, Zhang X, Tahir RA, Ashraf N,
Qing H, Peng D, Tong Y (2020) Sequence analysis
of a jumbo bacteriophage, Xoo-sp14, that infects
Xanthomonas oryzae pv. oryzae. Microbiol Resour
Announc 9(48):e01072-20. https:// doi. org/ 10. 1128/
MRA. 01072- 20
Nazir A, Dong Z, Liu J, Tahir RA, Rasheed M, Qing H, Tong
Y (2021) Genomic analysis of bacteriophage Xoo-sp13
infecting Xanthomonas oryzae pv. oryzae. Arch Virol
166(4):1263–1265
Neves DA, Guimarães LMS, Ferraz HGM, Alfenas AC
(2014) Favorable conditions for Xanthomonas axono-
podis infection in Eucalyptus spp. Trop Plant Pathol
39:428–433
Ni P, Wang L, Deng B, Jiu S, Ma C, Zhang C, Wang S (2021)
Characterization of a lytic bacteriophage against Pseu-
domonas syringae pv. actinidiae and its endolysin.
Viruses 13(4):631
Nino Liu D, Ronald P, Bogdanove A (2006) Xanthomonas
oryzae pathovars: model pathogens of a model crop.
Mol Plant Pathol 7:303–324
Oliva R, Quibod IL (2017) Immunity and starvation: new
opportunities to elevate disease resistance in crops.
Curr Opin Plant Biol 38:84–91
Oliva R, Ji C, Atienza Grande G, Huguet Tapia JC, Perez
Quintero A, Li T, Yang B (2019) Broad-spectrum
resistance to bacterial blight in rice using genome edit-
ing. Nature Biotechnol 37(11):1344–1350
Orzali L, Valente MT, Scala V, Loreti S, Pucci N (2020)
Antibacterial activity of essential oils and Trametes
versicolor extract against Clavibacter michiganen-
sis subsp. michiganensis and Ralstonia solanacearum
for seed treatment and development of a rapid invivo
assay. Antibiotics 9(9):628
Pandiyaraj P, Singh TH, Reddy KM, Sadashiva AT,
Gopalakrishnan C, Reddy AC, Pattanaik A, Reddy DL
(2019) Molecular markers linked to bacterial wilt (Ral-
stonia solanacearum) resistance gene loci in eggplant
(Solanum melongena L.). Crop Prot 124:104822
Park J, Lee GM, Kim D, Park DH, Oh CS (2018) Charac-
terization of the lytic bacteriophage phiEaP-8 effective
against both Erwinia amylovora and Erwinia pyrifoliae
causing severe diseases in apple and pear. Plant Pathol
J 34(5):445
Parkinson N, DeVos P, Pirhonen M, Elphinstone J (2014)
Dickeya aquatica sp. nov., isolated from water-ways.
Int J Syst Evol Microbiol 64:2264–2266
Parveen A, Siddiqui ZA (2021) Impact of silicon dioxide
nanoparticles on growth, photosynthetic pigments, pro-
line, activities of defense enzymes and some bacterial
and fungal pathogens of tomato. Vegetos 35(1): 83–93
Pedron J, Bertrand C, Taghouti G, Portier P, Barny MA
(2019) 511 Pectobacterium aquaticum sp. nov., isolated
from waterways. Int J Syst Evol Microbiol 69:745–775
Peng A, Chen S, Lei T, Xu L, He Y, Wu L, Yao L, Zou X
(2017) Engineering canker-resistant plants through
CRISPR/Cas9-targeted editing of the susceptibility
gene CsLOB1 promoter in citrus. Plant Biotechnol J
15:1509–1519
Pompili V, Dalla Costa L, Piazza S, Pindo M, Malnoy M
(2020) Reduced fire blight susceptibility in apple cul-
tivars using a high-efficiency CRISPR/Cas9-FLP/

Antonie van Leeuwenhoek
1 3
Vol:. (1234567890)
FRT-based gene editing system. Plant Biotechnol J
18(3):845–858
Potnis N, Minsavage G, Smith JK, Hurlbert JC, Norman D,
Rodrigues R et al (2012) Avirulence proteins AvrBs7
from Xanthomonas gardneri and AvrBs1.1 from Xan-
thomonas euvesicatoria contribute to a novel gene-for-
gene interaction in pepper. Mol Plant Microbe Interact
25(3):307–320
Prasad R, Kumar V, Prasad KS (2014) Nanotechnology in sus-
tainable agriculture: present concerns and future aspects.
Afr J Biotechnol 13(6):705–713
Purić J, Vieira G, Cavalca LB, Sette LD, Ferreira H, Vieira
MLC, Sass DC (2018) Activity of Antarctic fungi
extracts against phytopathogenic bacteria. Lett Appl
Microbiol 66(6):530–536
Ramírez M, Neuman B, Ramírez CA (2020) Bacteriophages
as promising agents for the biological control of moko
disease (Ralstonia solanacearum) of banana. Biol Con-
trol (in Press). https:// doi. org/ 10. 1016/j. bioco ntrol. 2020.
104238
Raymaekers K, Ponet L, Holtappels D, Berckmans B, Cammue
BP (2020) Screening for novel biocontrol agents applica-
ble in plant disease management—a review. Biol Control
144:104240
Rienzie R, Sendanayake L, De Costa D, Hossain A, Brestic
M, Skalicky M, Adassooriya NM (2021) Assessing the
carboxymethylcellulose copper-montmorillonite nano-
composite for controlling the infection of Erwinia caro-
tovora in Potato (Solanum tuberosum L.). Nanomaterials
11(3):802
Rodríguez M, Torres M, Blanco L etal (2020) Plant growth-
promoting activity and quorum quenching-mediated
biocontrol of bacterial phytopathogens by Pseudomonas
segetis strain P6. Sci Rep 10:4121
Roy V, Fernandes R, Tsao CY, Bentley WE (2010) Cross spe-
cies quorum quenching using a native AI-2 processing
enzyme. ACS Chem Biol 5:223–232. https:// doi. org/ 10.
1021/ cb900 2738
Ryan RP, Vorholter FJ, Potnis N, Jones JB, Van Sluys MA,
Bogdanove AJ, Dow JM (2011) Pathogenomics of Xan-
thomonas: understanding bacterium-plant interactions.
Nat Rev Microbiol 9:344–355
Salmond GPC (1994) Secretion of extracellular virulence fac-
tors by plant pathogenic bacteria. Annu Rev Phytopathol
32:181–200
Sánchez B, Barreiro-Hurle J, Soto Embodas I, Rodriguez-
Cerezo E (2019) The Impact Indicator for Priority Pests
(I2P2): a tool for ranking pests according to Regulation
(EU) No 2016/2031. EUR29793 EN, Publications Office
of the European Union, Luxembourg. July
Scheben A, Edwards D (2018) Bottlenecks for genome-
edited crops on the road from lab to farm. Genome Biol
19(1):1–7
Schmidt SM, Luu VT, Buchholzer M, Arra Y, Frommer WB
(2021) Options for tackling pathogen resistance by
genome editing in rice. CABI Reviews
Schwarczinger I, Bozsó Z, Szatmári Á, Süle S, Szabó Z,
Nagy G, Király L (2018) First report of bacterial leaf
spot caused by the quarantine pathogen Xanthomonas
arboricola pv. pruni on peach in Hungary. Plant Dis
102(8):1654
Sebaihia M, Bocsanczy AM, Biehl BS, Quail MA, Perna NT,
Glasner JD, De Clerck GA, Cartinhour S, Schneider
DJ, Bentley SD, Parkhill J, Beer SV (2010) Complete
genome sequence of the plant pathogen Erwinia amylo-
vora strain ATCC 49946. J Bacteriol 192:2020–2021
Sekeli R, Nazaruddin NH, Tamizi AA, Amin NM, Wee CY,
Sarip J, Zulkifli Z (2019) Enhancing Eksotika papaya
resistance to dieback disease through quorum quenching.
J Trop Plant Physiol 11(1):1–9
Shaheen HA, Issa MY (2020) Invitro and invivo activity of
Peganum harmala L. alkaloids against phytopathogenic
bacteria. Sci Hortic 264:1089. https:// doi. org/ 10. 1016/j.
scien ta. 2019. 108940
Shahryari F, Rabiei Z, Sadighian S (2020) Antibacterial
activity of copper nanoparticles synthesized with
sumac extract and copper-chitosan nanocomposite
against some plant pathogenic bacteria in laboratory.
https:// doi. org/ 10. 22084/ ab. 2020. 19130. 1410
Shan Q etal (2014) Genome editing in rice and wheat using
the CRISPR/Cas system. Nat Protoc 9:2395–2410
Sharma BB, Kalia P, Yadava DK, Dingh D, Sharma TR
(2016) Genetics and molecular mapping of black rot
resistance locus Xca1bc on chromosome B-7 in Ethio-
pian mustard (Brassica carinata A. Braun). PLoS ONE
11:e0152290
Sharma A, Gupta AK (2017) New insights in the biologi-
cal control of crown gall through native Agrobacte-
rium radiobacter strain UHFBA-218. Plant Dis Res
32:137–152
Sharma A, Gupta AK, Mahajan R, Bharti MPK (2017) Antag-
onistic potential of native agrocin producing non-patho-
genic Agrobacterium tumefaciens strain UHFBA-218 in
control of crown gall on peach. Phytoprotection 97:1–11
Sharma A, Abrahamian P, Carvalho R, Choudhary M, Paret
ML, Vallad GE, Jones JB (2022) Future of bacterial dis-
ease management in crop production. Annu Rev Phyto-
pathol 60:259–282
Shrinet K, Singh RK, Chaurasia AK, Tripathi A, Kumar A
(2021) Bioactive compounds and their future therapeutic
applications. In: Natural bioactive compounds. Academic
Press, pp 337–362
Siddique M, Din N, Ahmad M etal (2020) Bioefficacy of some
aqueous phytoextracts against ClavibacterMichiganensis
subsp. Michiganensis (Smith), the cause of bacterial can-
ker of tomato. Gesunde Pflanzen 72:207–217
Singh S, Dey SS, Bhatia R, Batley J, Kumar R (2018) Molecu-
lar breeding for resistance to black rot [Xanthomonas
campestris pv. campestris (Pammel) Dowson] in Brassi-
cas: recent advances. Euphytica 214(10):1–7
Siphathele S, Lucy NM, Divine YS, Teresa AC (2018) Quorum
sensing in gram-negative plant pathogenic bacteria. Adv
Plant Pathol. https:// doi. org/ 10. 5772/ intec hopen. 78003
Smargon AA etal (2017) Cas13b is a type VI-B CRISPRas-
sociated RNA-guided RNase differentially regulated by
accessory proteins Csx27 and Csx28. Mol Cell 65:618–
630. https:// doi. org/ 10. 1016/j. molcel. 2016. 12. 023
Sobiczewski P, Lakimova ET, Mikiciński A, Węgrzynowicz
Lesiak E, Dyki B (2017) Necrotrophic behaviour of
Erwinia amylovora in apple and tobacco leaf tissue.
Plant Pathol 66:842–855

Antonie van Leeuwenhoek
1 3
Vol.: (0123456789)
Soengas P, Hand P, Vicente JG, Pole JM, Pink DAC (2007)
Identification of quantitative trait loci for resistance to
Xanthomonas campestris pv. campestris in Brassica
rapa. Theor Appl Genet 114:637–645
Sofi W, Gowri M, Shruthilaya M, Rayala S, Venkatraman G
(2012) Silver nanoparticles as an antibacterial agent for
endodontic infections. BMC Infect Dis 12(1):60
Songstad DD, Petolino JF, Voytas DF, Reichert NA (2017)
Genome editing of plants. Crit Rev Plant Sci 36:1–23
Stall RE, Jones JB, Minsavage GV (2009) Durability of resist-
ance in tomato and pepper to Xanthomonads causing
bacterial spot. Annu Rev Phytopathol 47(1):265–284
Stefani E, Obradovic A, Gasicc K, Altin I, Nagy IK, Kovacs
T (2021) Bacteriophage-mediated control of phy-
topathogenic Xanthomonads: a promising green solu-
tion for the future. Microorganisms 9:1056
Sundin GW, Castiblanco LF, Yuan X, Zeng Q, Yang CH
(2016) Bacterial disease management: challenges,
experience, innovation and future prospects: challenges
in bacterial molecular plant pathology. Mol Plant
Pathol 17(9):1506–1518
Sunitha S, Rock CD (2020) CRISPR/Cas9-mediated targeted
mutagenesis of TAS4 and MYBA7 loci in grapevine
rootstock 101–14. Transgenic Res 29(3):355–367
Szczesny R, Jordan M, Schramm C, Schulz S, Cogez V etal
(2010) Functional characterization of the Xcs and Xps
type II secretion systems from the plant pathogenic
bacterium Xanthomonas campestris pv. vesicatoria.
New Phytol 187:983–1002
Tahir J, Hoyte S, Bassett H, Brendolise C, Chatterjee A,
Templeton K, Deng C, Crowhurst R, Montefiori M,
Morgan E, Wotton A (2019) Multiple quantitative trait
loci contribute to resistance to bacterial canker incited
by Pseudomonas syringae pv. actinidiae in kiwifruit
(Actinidia chinensis). Hortic Res 1:6
Tegli S, Biancalani C, Ignatov AN, Osdaghi E (2020) A pow-
erful LAMP weapon against the threat of the quaran-
tine plant pathogen Curtobacterium flaccumfaciens pv.
flaccumfaciens. Microorganisms 8(11):1705
Thomas NC, Hendrich CG, Gill US, Allen C, Hutton SF,
Schultink A (2020) The immune receptor Roq1 con-
fers resistance to the bacterial pathogens Xanthomonas,
Pseudomonas syringae, and Ralstonia in tomato. Front
Plant Sci 11:463
Tian Y, Zhao Y, Yuan X, Yi J, Fan J, Xu Z etal (2016) Dick-
eya fangzhongdai sp. nov., a plant-pathogenic bac-
terium isolated from pear trees (Pyrus pyrifolia). Int
JSyst Evol Microbiol 66:2831–2835
Toth IK, Bell KS, Holeva MC, Birch PR (2003) Soft rot
erwiniae: from genes to genomes. Mol Plant Pathol
4:17–30
Toth IK, van der Wolf JM, Saddler G, Lojkowska E, Hélias
V, Pirhonen M, Tsror L, Elphinstone JG (2011) Dick-
eya species: an emerging problem for potato produc-
tion in Europe. Plant Pathol 60:385–399
Tripathi JN, Ntui VO, Shah T, Tripathi L (2021) CRISPR/
Cas9-mediated editing of DMR6 orthologue in banana
(Musa spp.) confers enhanced resistance to bacterial
disease. Plant Biotechnol J 19(7):1291–1293
Van Schie CC, Takken FL (2014) Susceptibility genes
101: how to be a good host. Annu Rev Phytopathol
52:551–581
Vasilchenko AS, Poshvina D, Sidorov R, Iashnikov A,
Rogozhin EA, Vasilchenko A (2022) Oak Bark
(Quercus sp. cortex) protects plants through the inhi-
bition of quorum sensing mediated virulence of Pecto-
bacterium carotovorum. https:// doi. org/ 10. 21203/ rs.3.
rs- 13608 81/ v1
Von Bodman SB, Bauer WD, Coplin DL (2003) Quorum sens-
ing in plant pathogenic bacteria. Annu Rev Phytopathol
41:455–482
Voytas DF, Gao C (2014) Precision genome engineering and
agriculture: opportunities and regulatory challenges.
PLoS Biol 12:e1001877. https:// doi. org/ 10. 1371/ journ al.
pbio. 10018 77
Vu NT, Oh CS (2020) Bacteriophage usage for bacterial dis-
ease management and diagnosis in plants. Plant Pathol J
36(3):204
Wairuri CK, van der Waals JE, van Schalkwyk A, Theron J
(2012) Ralstonia solanacearum needs Flp pili for viru-
lence on potato. Mol Plant Microbe Interact 25:546–556
Walsh CT (2003) Antibiotics: actions, origins, resistance. ASM
Press, Washington
Wang L, Yang Li Y, Gan YL, Yang F, Liang XL, Li WL, Le
JB (2019a) Two lytic transglycosylases of Xanthomonas
campestris pv. campestris associated with cell separation
and type III secretion system, respectively. FEMS Micro-
biol Lett 366:1–18
Wang L, Chen S, Peng A, Xie Z, He Y, Zou X (2019b)
CRISPR/Cas9-mediated editing of CsWRKY22 reduces
susceptibility to Xanthomonas citri subsp. citri in Wan-
jincheng orange (Citrus sinensis (L.) Osbeck). Plant Bio-
technol Rep 13(5):501–510
Wang H, Liao L, Chen S, Zhang LH (2020) A quorum quench-
ing bacterial isolate contains multiple substrate-inducible
genes conferring degradation of diffusible signal factor.
Appl Environ Microbiol 86:e02930-e3019. https:// doi.
org/ 10. 1128/ AEM. 02930- 19
Wommack KE, Colwell RR (2000) Virioplankton: viruses in
aquatic ecosystems. Microbiol Mol Biol Rev 64:69–114.
https:// doi. org/ 10. 1128/ MMBR. 64.1. 69- 114. 2000
Xu X, Li Y, Xu Z, Yan J, Wang Y, Wang Y, Cheng G, Zou L,
Chen G (2022) TALE-induced immunity against the bac-
terial blight pathogen Xanthomonas oryzae pv oryzae in
rice. Phytopathol Res 4(1):1
Yaar Bar S, Dor S, Erov M, Afriat-Jurnou L (2021) Iden-
tification and characterization of a new quorum-
quenching N-acyl homoserine lactonase in the plant
pathogen Erwinia amylovora. Agric Food Chem
69(20):5652–5662
Yao KS, Li SJ, Tzeng KC, Cheng TC, Chang CY, Chiu CY,
Liao CY, Hsu JJ, Lin ZP (2009) Fluorescence silica nan-
oprobe as a biomarker for rapid detection of plant patho-
gens. Adv Mater Res 79:513–516
Ye T, Zhou T, Fan X, Bhatt P, Zhang L, Chen S (2019) Aci-
netobacter lactucae strain QL-1, a novel quorum quench-
ing candidate against bacterial pathogen Xanthomonas
campestris pv. campestris. Front Microbiol 10:2867
Ye T, Zhang W, Feng Z, Fan X, Xu X, Mishra S etal (2020)
Characterization of a novel quorum-quenching bacterial

Antonie van Leeuwenhoek
1 3
Vol:. (1234567890)
strain, Burkholderia anthina HN-8, and its biocon-
trol potential against black rot disease caused by Xan-
thomonas campestris pv. campestris. Microorganisms
8(10):1485
Zaczek-Moczydłowska MA, Young GK, Trudgett J, Plahe C,
Fleming CC, Campbell K, O’Hanlon R (2020) Phage
cocktail containing Podoviridae and Myoviridae bac-
teriophages inhibits the growth of Pectobacterium
spp. under in vitro and in vivo conditions. PLoS ONE
15(4):e0230842
Zaka A etal (2018) Natural variations in the promoter of OsS-
WEET13 and OsSWEET14 expand the range of resist-
ance against Xanthomonas oryzae pv. oryzae. PLoS ONE
13:e0203711
Zechner EL, Lang S, Schildbach JF (2012) Assembly and
mechanisms of bacterial type IV secretion machines.
Philos Trans R Soc Lond B 367:1073–1087
Zhang W, Fan X, Li J, Ye T, Mishra S, Zhang L, Chen S
(2021) Exploration of the quorum-quenching mecha-
nism in Pseudomonas nitroreducens W-7 and its poten-
tial to attenuate the virulence of Dickeya zeae EC1. Front
Microbiol 12: 694161. https:// doi. org/ 10. 3389/ fmicb.
2021. 694161
Zhou L, Huang TW, Wang JY, Sun S, Chen G, Poplawsky A,
He YW (2013) The rice bacterial pathogen Xanthomonas
oryzae pv. oryzae produces 3-hydroxybenzoic acid and
4-hydroxybenzoic acid via XanB2 for use in xanthomon-
adin, ubiquinone, and exopolysaccharide biosynthesis.
Mol Plant Microbe Interact 26(10):1239–1248
Zhou J etal (2015) Gene targeting by the TAL effector PthXo2
reveals cryptic resistance gene for bacterial blight of rice.
Plant J 82:632–643. https:// doi. org/ 10. 1111/ tpj. 12838
Zhou L, Zhang LH, Cámara M, He YW (2017a) The DSF fam-
ily of quorum sensing signals: diversity, biosynthesis,
and turnover. Trends Microbiol 11:974. https:// doi. org/
10. 1016/j. tim. 2016. 11. 013
Zhou P, Jia R, Chen SC, Xu LZ, Peng AH, Lei TG, Li Q etal
(2017b) Cloning and expression analysis of four citrus
WRKY genes responding to Xanthomon asaxonopodis
pv. citri. Acta Horticult Sin 44(3):452–462
Zhou Z, Wu X, Li J, Zhang Y, Huang Y, Zhang W etal (2022)
A novel quorum quencher, Rhodococcus pyridinivorans
XN-36, is a powerful agent for the biocontrol of soft rot
disease in various host plants. Biol Control 169:104889
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