Rhizosphere 21 (2022) 100479

Contents lists available at ScienceDirect

Rhizosphere
journal homepage: www.elsevier.com/locate/rhisph

Ralstonia solanacearum, a deadly pathogen: Revisiting the bacterial wilt

biocontrol practices in tobacco and other Solanaceae
Waqar Ahmed a, b, c, Jun Yang b, c, d, Yujiao Tan a, e, Shahzad Munir b, Qi Liu b, c, Jinhao Zhang b, c,
Guanghai Ji b, c, **, Zhengxiong Zhao a, *
a
College of Resources and Environment, Yunnan Agricultural University, Kunming, 650201, China
b
State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University, Kunming, 650201, China
c
Key Laboratory of Agro-Biodiversity and Pest Management of Ministry of Education, Yunnan Agricultural University, Kunming, 650201, China
d
College of Resources, Environment, and Chemistry, Chuxiong Normal University, Chuxiong, 675000, China
e
College of Tobacco Science, Yunnan Agricultural University, Kunming, 650201, Yunnan, China

A R T I C L E I N F O A B S T R A C T

Keywords: Bacterial wilt disease caused by Ralstonia solanacearum species complex poses a great threat to Solanaceae and
Crop pathogen flue-cured tobacco crop production worldwide. R. solanacearum invades plants through roots, colonizes the
Integrated pest management vascular system, and blocks xylem tissues. Typical unilateral wilting symptoms appear on above-ground plant
Nicotiana tabacum
parts that lead to plant death. Integrated disease management strategies in the form of cultural control, chemical
Ralstonia species complex
Rhizosphere
control, and genetic resistance have been employed for years to control the incidence of bacterial wilt disease.
However, none of these strategies has completely controlled the disease due to high genetic diversity, broad host
range, and prolonged survival of pathogen in soil and on plant parts. Owing to co-management strategies,
biological control is the best approach for human health and environmentally safety. Biocontrol agents (endo­
phytes and rhizobacteria) are ubiquitous with all plant parts (leaves, stem, roots, and rhizosphere), play an
important role in disease suppression and growth promotion. The possible biocontrol mechanisms involve
multifaceted interactions between host, pathogen, and antagonists is niche exclusion, nutrient acquisition, direct
antagonistic, induction of resistance, and production of antimicrobial compounds. Studies have shown that
biocontrol agents efficiently reduce the incidence of bacterial wilt disease in greenhouse experiments, but the
field trials have not produced fruitful results. In this review, we made an effort to summarize the information
related to microbe-assisted biocontrol of plant pathogens with main focus on bacterial wilt disease of flue-cured
tobacco and Solanaceous crops.

1. Introduction measures are imperatives. Nowadays, biological control through indig­

Bacterial wilt caused by the soilborne plant pathogenic bacterium
Ralstonia solanacearum is a devastating disease of Solanaceae family
(tomato, potato, pepper, ginger, eggplant) including flue-cured tobacco
crop production worldwide and in China (Mamphogoro et al., 2020; Cai
et al., 2021). Currently R. solanacearum is the most intensively studied
phytopathogenic bacterium due to its lethal nature in flue-cured tobacco
and important Solanaceous crops. Irrespective of the development of
several integrated disease management strategies to control the bacte­
rial wilt disease, an effective and environmentally friendly control
enous disease suppressive biocontrol agents (endophytes and rhizobac­
teria) is considered as an alternative measure to reduce the incidence of
bacterial wilt (Chunyu et al., 2017; El Sayed et al., 2019). These
biocontrol agents confer broad-spectrum benefits to host plants in the
form of nitrogen fixation, antimicrobial compounds, plant growth pro­
moters, and induction of plant immune resistance (Sahu et al., 2017;
Zhang et al., 2020; Wei et al., 2021).
Yield losses caused by bacterial wilt pathogen in many Solanaceous
crops are ranged between 15–55% around the globe (Kim et al., 2016).
In Uganda, the tomato crop was badly affected by R. solanacearum, and

* Corresponding author. College of Resources and Environment, Yunnan Agricultural University, Kunming, 650201, China.
** Corresponding author. State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University, Kunming, 650201,
China.
E-mail addresses: ahmed.waqar1083@yahoo.com (W. Ahmed), jghai001@163.com (G. Ji), zhaozx0801@163.com (Z. Zhao).

https://doi.org/10.1016/j.rhisph.2022.100479
Received 27 October 2021; Received in revised form 20 January 2022; Accepted 20 January 2022
Available online 26 January 2022
2452-2198/© 2022 Published by Elsevier B.V.
W. Ahmed et al. Rhizosphere 21 (2022) 100479

yield losses were recorded at 88%; and in Ethiopia, the incidence of

pepper bacterial wilt disease was recorded about 100% (Mamphogoro
et al., 2020). Potato bacterial wilt disease caused by R. solanacearum is
the 2nd most important disease of potato after late blight caused by
Phytophthora infestans, and yield losses reached up to 50–75% (Felix
et al., 2010; Chamedjeu et al., 2019). It was estimated that 1.7 MH of
potato field in more than 80 countries is affected by R. solanacearum,
with $950 million loss annually (Charkowski et al., 2020).
In China, yield losses and bacterial wilt disease incidence vary from
host-host, soil type, climatic condition, pathogen strain, and region-
region (Jiang et al., 2017). For example, along with the Yangtze River
regions, tomato bacterial wilt disease incidence is recorded about
10–80%, depending on the crop season (Wei et al., 2017). Bacterial wilt
disease of potato occurs in more than ten provinces of China with esti­
mated yield losses of 10–15% and reached up to 80–100% in case of a
severe outbreak (Li-yuan and Jin, 2005). Incidence of tobacco bacterial
wilt was recorded in 14 out of 22 tobacco-growing regions of China. The
average disease incidence of tobacco bacterial wilt was recorded
approximately 15–35% and extended up to 75% when it prevails with
other root rot diseases (Black shank) caused by Phytophtora nicotianae. In
mono-cropping and high humidity regions, yield losses are ranged be­
tween 50–60% and reached up to 100% (Jiang et al., 2017).
In this review, we made an effort to summarize the effective envi­
ronmentally friendly disease management strategies to suppress inci­
dence of plant pathogens through biocontrol agents (endophytes and
rhizobacteria) with main focus on bacterial wilt disease of Solanaceous
crops and flue-cured tobacco. This study will provide the basic knowl­
edge on biocontrol agents (endophytes and rhizobacteria) mediated
management of bacterial wilt disease and some suggestions for further Fig. 1. Symptoms produced by bacterial wilt Pathogen Ralstonia sol­
studies, to mitigates such destructive disease. anacearum on tobacco (Nicotiana tabacum L.) plant. (A–B): Healthy plant;
A: Leaves remain green and healthy; B: Parenchyma cells remain white-colored;
2. Symptoms, epidemiology, and survival (C–D): Diseased plant; C: Yellowing and unilateral wilting of leaves with
marginal necrosis; D: Light yellow to dark brown color of parenchyma cells and
dark water-soaked lesions on the stem.
Symptoms, epidemiology, and survival of bacterial wilt pathogen of
flue-cured tobacco and other Solanaceous crops is almost same, so here
we selected flue-cured tobacco (Nicotiana tabacum L.) as a model plant. 3. Biology of bacterial wilt pathogen
Unilateral wilting and yellowing of younger leaves followed by a total
collapse of the plant are the characteristics symptoms produced by Ralstonia solanacearum was reported first time on potato, groundnut,
R. solanacearum in susceptible host. When performing a cross section and tomato plants at the end of the 19th century in South America and
along the central axis, a reddish to brown discoloration of the vascular Asia (Smith, 1896). In 1896, Erwin F. Smith first described this pathogen
system is observed. Dark black water-soaked lesions develop on the stem as Bacillus solanacearum, and later in 1914, he changed its name to
surface as a results of pith rotting, whereas healthy plants remain green Pseudomonas solanacearum (Smith, 1896, 1914; García et al., 2019).
(Healthy plant: Fig. 1A and B; Disease plant: Fig. 1C and D) (Karim and R. solanacearum was first described by Smith in 1908 in the tobacco field
Hossain, 2018). During the pathogen life cycle, the bacterium becomes (Smith, 1908). In China, in the 1930s, R. solanacearum was first reported
motile and it can be isolated from all the plant parts (Denny, 2000; Nion on peanut plants (Ma and Gao, 1956), and around 90 plant species from
and Toyota, 2015). It survives on diseased plant debris, vegetative 39 botanical families were reported as a host of bacterial wilt pathogen
propagative materials, wild host, in the absence of the host plant, and in (She et al., 2017). Later in 1946, the pathogen was reported in sweet
fresh water for a longer time (up to 40 years), but loses its viability in potato and in the 1950s, from potato, ginger, tobacco, tomato, and
extreme conditions (high pH, salt, and temperature) (Álvarez et al., sesame (Hwang et al., 1956; Wang, 1959; He et al., 1983). In China,
2010). tobacco bacterial wilt disease is mostly caused by biovar 3 (a biological
Infected soil acts as a primary source of inoculum (Fig. 2) (Álvarez group of bacterial strain, different from other strains of same species
et al., 2010). Compared with other plant pathogenic bacteria such as based on physiological characteristics) and phylotype 1 of
Pseudomonas sp., Streptomyces sp., etc., R. solanacearum needs only one R. solanacearum, which belong to race 1 (Li et al., 2016).
entry site to set up a systemic infection (Denny, 2007). It invades the R. solanacearum is classified into four phylotypes, five races, and six
plant through wounds produced as a result of mechanical operation and biovars based on broad host range and uneven geographical distribution
spots at primary and secondary roots development (He et al., 2014; (Buddenhagen, 1962; Fegan and Prior, 2005; Genin and Denny, 2012).
Singh et al., 2018). After entering into a susceptible host, it multiplies In recent studies, R. solanacearum was classified into three species;
systemically in the xylem tissue that blocks water transportation and R. pseudosolanacearum (phylotype 3), R. syzygii (phylotype 4), and
produces typical wilting symptoms (Wang and Lin, 2005; She et al., R. solanacearum (phylotype 1 and 2) (Safni et al., 2014; Prior et al.,
2017). During the disease cycle, pathogen becomes motile and spreads 2016). Based on geographical distribution, R. solanacearum was classi­
along with transpiration flow in the vascular system. When pathogen fied into four phylotypes: phylotype 1 (Asia), phylotype 2 (America),
completes its life cycle in a plant, a number of bacteria ooze out in the phylotype 3 (Africa), and phylotype 4 (Indonesia) (Prior and Fegan,
rhizosphere from the roots of symptomatic plants and spread from 2004). Due to the high genetic diversity of R. solanacearum, a total of
diseased to healthy plants through rain and irrigation water (Char­ 291 genomes are submitted in the NCBI database to date, and a few
kowski et al., 2020; Qi et al., 2020). genomes (≥14) are completed (https://www.ncbi.nlm.nih.gov/genome
/?term=Ralstoniasolanacearum).

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W. Ahmed et al. Rhizosphere 21 (2022) 100479

Fig. 2. General life cycle of Ralstonia solanacearum causing bacterial wilt of tobacco (Nicotiana tabacum L.). A: Infected field and soil act as a primary source
of inoculum, and cells of R. solanacearum survive in the soil for a long period in the absence of a suitable host; B: During cropping season, resting spores converts into
primary motile cells with polar flagella; C: These motile bacterial cells enter in the host plant through wounds and spots at primary and secondary root development;
D: After entering in the host plant it multiply systemically in the xylem tissues and produces typical wilting symptoms, and the huge number of bacteria ooze out in
the rhizosphere from the roots; E: Secondary motile cells of R. solanacearum and spread from disease to healthy plants through rain and irrigation water; F: In case of
severe pathogen attack disease spread in the whole field initially lower leaves turn yellow, clogging of xylem tissue, and dark water-soaked lesion produce on the
stem and in result whole plant collapse.

4. Integrated disease management approaches for bacterial wilt
disease
Due to the broad host range, high species complex, and prolonged
survival in the soil and persistence on vegetation as a latent infection,
more challenges emerge to control bacterial wilt disease. Especially once
it is established in the soil, it’s difficult to control bacterial wilt disease
(Kurabachew and Ayana, 2017). However, many integrated disease
management approaches like crop rotation, cultural practices, biochar
amendments, use of bioorganic fertilizers (BOFs), and breeding of
resistant cultivars were adopted to control this wilt disease (Balota et al.,
2014; Chen et al., 2020; Wu et al., 2020). So far, pesticides in the form of
bismerthiazol, saisentong, and zinc thiazole are used to manage this
bacterial disease, however, they pose serious environmental threats,
lead to pathogen resistance as well as negatively affect the native po­
tential microbes (Nicolopoulou-Stamati et al., 2016; Meftaul et al.,
2020).
The development of resistant cultivars through crop breeding is
considered a fundamental approach, and significant progress has been
achieved to develop the resistant varieties for some important cash crops
(Liu et al., 2012; Deng et al., 2014). Genetic analysis has been conducted
on tomatoes, potatoes, eggplant, and tobacco; multiple genes have been
reported to be involved in resistance (Salgon et al., 2017; Habe et al.,
2019; Qiu et al., 2019). Therefore, resistance is difficult to inherit, and
more time is needed for breeding. Because crop lose its resistance
against pathogen, and resistant cultivars cannot produce desired yields
(Qian et al., 2013; Nelson et al., 2018). On the other hand, molecular
markers linked to major resistance genes have been developed in
tomatoes (Abebe et al., 2020), and further breeding of resistant cultivars
is expected.
Crop rotation is considered a practical approach to control many
soilborne diseases because most soilborne pathogens can persist for a
long time in soil on infected plant residues (Niu et al., 2017; Fan et al.,
2020). The use of winter cover crops and soil amendments with organic
matter is a valuable approach to control soilborne disease. Cover crops
can improve soil nutrients and suppress soilborne diseases by destroying
the pathogen life cycle (Balota et al., 2014; Yang et al., 2019). The
addition of biochar in soil alters the soil microbial diversity, activity, and
community composition. Most importantly, biochar reduces plant dis­
ease severity and induces plant resistance to disease, increases nutrient
retention, alleviates soil acidity, alters microbial community, and pro­
motes better soil structure (Graber et al., 2014; Jaiswal et al., 2017; Li
et al., 2022). Developing novel antibacterial agents in tobacco against
bacterial wilt pathogen will provide remarkable practical approach.
Antibacterial agent Lansiumamide B, isolated from Clausena lansium
seeds, can control bacterial wilt disease (Li et al., 2014).
5. Biocontrol of plant pathogens
Microorganisms mediated biocontrol provides a desirable solution
for sustainable agriculture to meet ever increasing agricultural de­
mands. A mutualistic relationship is found between plants and biocon­
trol agents through colonization in plant parts without causing any
apparent disease and they also compete with the pathogen (Fig. 3)
(Brader et al., 2017; Dong et al., 2019). Biological control agents protect
plants from biotic and abiotic stress through well-recognized direct and

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W. Ahmed et al. Rhizosphere 21 (2022) 100479

Fig. 3. Mechanism of biocontrol agents

(endophytes and rhizobacteria) mediated
resistance in plant against pathogen and
insect pest. Beneficial biocontrol agents
(brown) increase the plant resistance against
biotic and abiotic stress through a direct and
indirect mechanism. Biocontrol agents colo­
nize in the internal plant tissues; compete
with the pathogen (red) and other microor­
ganisms present in their surroundings, and
improve plant health. Some examples of
different mechanisms SAR, hyperparasitism,
niche exclusion, ISR, and antibiosis are
shown (blue and gray), respectively.

indirect mechanisms (Degrassi and Carpentieri-Pipolo, 2020). Direct
mechanisms of biocontrol agents occur through the acquisition of
essential macronutrients (nitrogen and phosphorus), micronutrients
(iron), and by the production of certain hormones (gibberellins, auxin,
and cytokinin) (Glick, 2015; Santoyo et al., 2016). While in indirect
mechanisms, biocontrol agents (endophytes and rhizobacteria) pro­
duced substances that inhibit the growth of phytopathogens (bacteria,
fungi, nematodes, protists, and viruses) by direct antagonistic effect and
compete with the pathogen for iron (Chaturvedi et al., 2016; Ek-Ramos
et al., 2019). Niche exclusion is considered a possible mechanism for

Table 1
Bacterial endophytes and rhizobacteria used as a biocontrol agent against different plant pathogens and their biocontrol mechanism.
Biocontrol agents Mechanism Target pathogen Effective against Host plant/isolated References
disease

Ochrobactrum pseudintermedium, Niche Exclusion P. syringae pv. lachrymans Angular leaf spot Cucumber Akbaba and Ozaktan,
Pantoea agglomerans (2018)
B. subtilis Antibiosis Xanthomonas oryzae pv. Bacterial leaf blight Rice Kumar et al., (2020)
oryzae
B. subtilis HJ5 Niche exclusion and Biofilm Verticillium dahliae Verticillium wilt of Cotton Li et al., (2013)
formation cotton
B. amyloliquefaciens, B. pumilus, and Antibiosis Fusarium graminearum Fusarium head blight of Wheat Comby et al., (2017)
B. subtilis wheat
B. velezensis Antibiosis Xylella fastidiosa Olive Quick Decline Olive trees Zicca et al., (2020)
Syndrome
B. subtilis L1-21 ISR Candidatus Liberibacter Citrus Greening Citrus Munir et al., (2020)
asiaticus Disease
B. licheniformis ESR 26, B. subtilis-ESR VOCs Colletotrichum falcatum Red rot of sugarcane Sugarcane Jayakumar et al.,
24 (2020)
L. antibioticus 13–6, L. capsici ZST1-2, Niche exclusion, Antibiosis, and Plasmodiophora brassicae Clubroot of Chinese Konjac, Purple Wei et al., (2021)
and B. cereus BT-23 production of metabolites cabbage potato
B. velezensis PCSE10 and Rhizobium Antibiosis Phytophthora capsici Foot rot Black pepper Kollakkodan et al.,
radiobacter PCRE10 (2020)
Enterobacter cloacae Antibiosis Pythium aphanidermatum Pythium damping-off Cucumber Kazerooni et al.,
(2020)
Brevibacterium halotolerans JZ7 Antibiosis and ISR Fusarium oxysporum Root rot disease of Chinese Jujube Wang et al., (2020)
Chinese Jujube
B. velezensis 8-4 Antibiosis Streptomyces galilaeus, Potato scab, Black scurf Potato Cui et al., (2020)
Rhizoctonia solani of potato
B. halotolerans Niche exclusion and SAR Fusarium oxysporum f. sp. Bayoud disease of date Limoniastrum Slama et al., (2019)
albedinis palm monopetalum
B. subtilis, P. flourscence Antibiosis and ISR Fusarium oxosporium Fusarium wilt disease Tomato Mohammed and
Toama, (2019)
B. amyloliquefaciens (PsL) Antibiosis and ISR Phytophthora capsici Phytophthora blight Papaya Bhusal and Mmbaga,
(2020)

Here; B. = Bacillus, L. = Lysobacter, ISR = Induced systemic resistance, SAR = Syetemic acquired resistance

4
W. Ahmed et al.
biological control, in which the biocontrol agents compete with the
pathogen for shelter, minerals, and nutrients (Pohjanen et al., 2014).
Similarly, some bacterial endophytes antagonize disease-causing agents
through hyperparasitism (Law et al., 2017). The mechanism of hyper­
parasitism has been mostly observed in fungi and less reported in bac­
teria. In hyperparasitism, microorganisms compete with each other for
nutrient acquisition, secretions of some extracellular enzymes (chitinase
and glucanase), and biofilm formation (Köhl et al., 2019).
Indirect mechanism involves induction of resistance and direct an­
tagonists by production of antimicrobial substances or volatile organic
compounds (VOCs) (Morita et al., 2019; Ek-Ramos et al., 2019). Plant
growth promoting rhizobacteria mainly trigger induced systemic resis­
tance in host plants against pathogens through the signaling pathway of
ethylene and jasmonic acid (Latha et al., 2019). While systemic acquired
resistance is triggered upon activation of a pathogen-associated molec­
ular pattern -triggered immunity, effector-triggered immunity (Mishina
and Zeier, 2007), and by the accumulation of salicylic acid and
pathogenesis-related (PR) genes, many of which encode PR proteins
with antimicrobial activity (van Loon et al., 2006; Vlot et al., 2009).
Finally, antibiosis is a well-recognized mechanism of biocontrol by
which biocontrol agents antagonize phytopathogens by producing
antimicrobial compounds, enzymes, and VOCs (Torres et al., 2017;
Morita et al., 2019). Some biocontrol agents (endophytes and rhizo­
bacteria) showing these diverse mechanisms of biological control
against plant pathogens have been enlisted in Table 1.
6. Biocontrol mechanism in Solanaceae and flue-cured tobacco
Endophytic bacteria Enterobacter cloacae PS14 was isolated from the
healthy potato plant parts and used as a biocontrol against potato bac­
terial wilt disease. E. cloacae PS14 suppressed potato bacterial wilt dis­
ease up to 26.5% and increased the yield up to 40.96% through
operating the mechanisms of antibiosis and induction of plant systemic
resistance (Mohamed et al., 2020). Rhizobacteria Paenibacillus polymyxa
was isolated from the soil of potato field, significantly the suppressed
incidence of potato bacterial wilt up to 80% (Soliman, 2020). Biocontrol
potential of native Bacillus subtilis (KJ-2) isolated from the seed endo­
sphere of a bacterial wilt tolerant chilli cv. Firingi Jolokiawas was
assessed against chilli bacteial wilt disease in vitro.Results showed that
B. subtilis (KJ-2) significantly suppress the incidece of chilli bacterial wilt
having control effect of 86.6% (Dowarah et al., 2021).
Effect of rhizobacteria Pseudomonas syringae and P. aeruginosa were
studied in tomato crops infected with bacterial wilt disease. The results
revealed that the application of P. syringae and P. aeruginosa effectively
control bacterial wilt disease through antibiosis and induction of host
resistance (Mohammed et al., 2020). Around 40 endophytes were iso­
lated from Gnetum gnemon plant, and their antagonistic activity was
checked against tomato bacterial wilt pathogen Ralstonia solanacearum.
Only two endophytic bacteria Bacillus velezensis GL3 and Staphylococcus
warneri GL1 antagonized the pathogen through antibiosis and assisted in
plant growth promotion (Agarwal et al., 2020). A total of 19/420 iso­
lated strains showed antagonistic activity against ginger bacterial wilt
pathogen R. solanacearum with a biocontrol effect between
26.09–69.17% (Yang et al., 2012). A rhizospheric bacterial strain Ba­
cillus cereus AR156 was isolated from forest soil exhibiting a
broad-spectrum biocontrol ability against many crop diseases. The
antagonistic effect of B. cereus AR156 was investigated against tomato
bacterial wilt disease, and showed biocontrol efficacy up to 51.02%
compared with control (Wang et al., 2019).
Wu et al. (2016a) assessed the antagonistic effect of Bacillus amylo­
liquefaciens ZM9 isolated from healthy tobacco plant’s rhizosphere to
control bacterial wilt disease of tobacco. B. amyloliquefaciens ZM9 effi­
ciently controls tobacco bacterial wilt through the mechanism of niche
exclusion and has a biocontrol efficacy of about 38.2%. In our previous
study (unpublished data) B. amyloliquefaciens WS-10 (Accession No.
MW730713) isolated from the rhizospheric soil of healthy tobacco
5
Rhizosphere 21 (2022) 100479
plants and it’s biocontrol activity was assessed against tobacco bacterial
wilt disease in a pot experiment. Results showed that
B. amyloliquefaciens WS-10 significantly suppresses the incidence of to­
bacco bacterial wilt disease, through mechanism of direct antagonism
(production of antibacterial compounds), niche exclusion (successfully
colonized in the rhizosphere of tobacco plants), and also reduces gene
copy number of R. solanacearum in the rhizosphere soil (Fig. 4). It is
reported that filed application of B. amyloliquefaciens Y4 and Pseudo­
monas sp. Y8 reduce the incidence of tobacco bacterial wilt disease up to
3–4 fold compared with control (Li et al., 2021).
As per Tahir et al. (2017) findings, B. artrophaeus LSSC22 and
B. amyloliquefaciens FZB42 were found to inhibit R. solanacearum
through VOCs and also acted as plant growth promoters. Many studies
revealed that due to the broad host range and high species complexity,
the use of only biocontrol agents could not give efficient results. How­
ever, biocontrol efficacy was fortified up to >95% when these antagonist
strains were applied in combination with organic fertilizer (OF), BOFs,
and biochar (Ma et al., 2018; Wu et al., 2020). Similarly Yang et al.
(2017) described that more complex soil ecology network may help to
suppress incidence of tobacco wilt disease. Yuan et al. (2014) reported
that application of Bacillus-fortified organic fertilizer significantly
delayed tobacco bacterial wilt development and effectively controlled
the disease incidence under both greenhouse and field conditions.
Combined application of B. amyloliquefaciens ZM9 and marigold powder
suppressed the incidence of tobacco bacterial wilt disease by improving
soil physicochemical properties, soil metabolites, and microbial struc­
ture (Hu et al., 2021b). Some examples of rhizobacteria and endophytic
bacteria used as single or in combination with OF, BOFs, and biochar to
control bacterial wilt disease have been summarized in Table 2.
7. Conclusions and future perspectives
In this review, we made an effort to summarize the currently avail­
able rhizospheric and endophytic bacteria used as biocontrol agents
against different plant pathogens with more focus on bacterial wilt
disease. Here, we propose some suggestions that should be kept in mind
and adapt to control this devastating disease. (i) Isolation and identifi­
cation of bacterial endophytes and rhizobacteria associated with Sol­
anaceae crops and use of these biocontrol agents against R. solanacearum
because these biocontrol agents have good adaptation and colonization
Fig. 4. Bacillus amyloliquefaciensWS-10 successfully control the incidence
of bacterial wilt disease of flue-cured tobacco in pot experiment. Appli­
cation of Ralstonia solanacearum (A), Combined application of R. solanacearum
and B. amyloliquefaciens WS-10 (B). Flue-cured tobacco plant showing the
typical bacterial wilt symptoms (A) and healthy flue-cured tobacco plants (B).
W. Ahmed et al. Rhizosphere 21 (2022) 100479

Table 2
Mechanism of biocontrol agents used as a biocontrol against bacterial wilt disease.
Bacterial strains Mechanism Source Solanacearum crops References

P. syringae and P. aeruginosa Antibiosis and ISR Tomato Tomato Mohammed et al., (2020)
Enterobacter cloacae PS14 Antibiosis and SAR Potato Potato Mohamed et al., (2020)
Paenibacillus kribbensis PS04 SAR – Tobacco Zhao et al., (2020)
B. cereus QJ-1 Antibiosis and BOF Tobacco Tobacco Wu et al., (2020)
Streptomyces rochei L-9, Brevibacillus brevis L- Antibiosis and OF Tobacco Tobacco Liu et al., (2013)
25
Paenibacillus polymyxa (IMA5) Antibiosis and PGP Egg Plant Egg Plant Alamer et al., (2020)
Agrobacterium tumefaciens XB1R,B. cereus Niche Exclusion Egg Plant Egg Plant Achari and Ramesh,
XB177R (2019)
B. amyloliquefaciens SQY 162 Antibiosis and BOF Tobacco Tomato Wu et al., (2016b)
Acinetobacter sp. Xa6 Niche Exclusion and Antibiosis Tomato Tomato Xue et al., (2013)
P. mallei (RBG4, ET17), B. sp. RCh6 Antibiosis and PGPR Egg Plant Egg Plant Ramesh and Phadke,
(2012)
B. amyloliquefaciens DSBA -12 Antibiosis and ISR Tomato Tomato Singh et al., (2016)
B. amyloliquefaciens S20 Antibiosis Egg Plant Egg Plant Chen et al., (2014)
P. fluorescens (P142), B. velezensis (B63) SAR Potato Tomato El Sayed et al., (2019)
Staphylococcus sp., Agrobacterium sp., B. sp Antibiosis Solanaceae crops, chili, Solanaceae crops, chili, Achari and Ramesh,
eggplant eggplant (2014)
P. aeruginosa NXHG29 Antibiosis and BOF Banana Tobacco Ma et al., (2018)
B. amyloliquefaciens SQRT3 ISR Tomato Tomato Chunyu et al., (2017)
B. pumilus, Paenibacillus acerans, P. putida, Niche Exclusion, Antibiosis, and Sweet peppers and Solanaceae Sweet peppers and Solanaceae Mamphogoro et al.,
B. cereus ISR crops crops (2020)
Mitsuaria sp. TWR114 Antibiosis Welsh onion Tomato Marian et al., (2018)
B. amyloliquefaciens ZM9 Niche exclusion, Antibiosis, rice Tobacco Tobacco Hu et al., (2021a)
bran
B. amyloliquefaciens SQR-9 Antibiosis (VOCs) and OF Cucumber Tomato Raza et al., (2016)

Here; P. = Pseudomonas, B. = Bacillus, ISR = Induced systemic resistance, SAR = Systemic acquired resistance, OF = Organic fertilizer, BOF = Bioorganic fertilizer,
VOCs = Volatile organic compounds.

ability in the rhizosphere and plant parts. (ii) The use of microbial
consortia may help us to develop a complex soil microbial network and
restructure the rhizospheric microbiome to manage bacterial wilt dis­
ease. (iii) The use of biotechnological tools for genetic modification of
biocontrol agents to enhance their biocontrol efficacy. Although the
isolation of biocontrol agents is a laborious and time-consuming task,
but we must show patience and never give up. However, this field holds
many mysteries that need to unveil; by adopting the strategies
mentioned above with other control practices, we can achieve the du­
rable biological control of R. solanacearum in near future.
Author’s contribution
ZZ and GJ designed the study. WA, YT, QL, and JZ collected data. WA
and SM wrote the manuscript. WA, JY, and SM made figures. All authors
contributed to the final draft of the manuscript.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgments
This study was financially supported by the Yunnan Agricultural
University Scientific Research Foundation (KX900187) , the Science &
Technology Platform Plan of Yunnan Province (2019IC005), Key
Research and Development Program of Yunnan Province (2018BB019),
Key Science and Technology Program of Yunnan Tobacco Company of
China ( 2018530000241017), the National Key R&D Program of China
(2019YFD1002000), and the Yunnan Ten Thousand Talents Plan Lead­
ing Talents of Industrial Technology Project of China (YNWR-CYJS-
2019-046).
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