Int. J. Agron. Agri. R.

International Journal of Agronomy and Agricultural Research (IJAAR)

ISSN: 2223-7054 (Print) 2225-3610 (Online)
http://www.innspub.net
Vol. 21, No. 4, p. 18-25, 2022
RESEARCH PAPER OPEN ACCESS

Efficacy of Microbial Biopesticide Formulations in the control

of Xanthomonas citri pv. Mangiferaeindicae in Cashew
(Anacardium occidentale L.) in Cote D'ivoire
Tehua Amoa Armist*1, Kouman Abenan Manou Natacha1, Koffi Yao Fulgence2,
Alloue-Boraud Waze Aimée Mireille3 et Kone Daouda1

Centre d’Excellence Africain Sur Le Changement Climatique, La Biodiversité Et L’Agriculture Durable

1

(CEA-CCBAD), Université Félix Houphouët-Boigny (UFHB), Abidjan, Côte d’Ivoire

2
Département de Biochimie-Génétique, UFR Sciences Biologiques, Université Péléforo Gon
Coulibaly De Korhogo, Korhogo, Côte d’Ivoire
3
Laboratoire de Biotechnologie et Microbiologie des Aliments, Unité de Formation et de Recherche en
Sciences et Technologie des Aliments (UFR-STA), Université Nangui Abrogoua, Abidjan, Côte d’Ivoire

Article published on October 10, 2022

Key words: Cashew tree, Bacterial blight, Biocontrol agents, Formulation, Biological control

Abstract

The cashew tree (Anacardium occidentale L.) occupies an important place in the world because of its cashew nut.
However, its cultivation is confronted with bacteriosis, a bacterial disease caused by Xanthomonas citri pv.
Mangiferaeindicae. This disease is one of the main causes of the low yield per hectare of cashew nuts, which
fluctuates between 350 and 500 kg/ha. In view of this, it is wise to find ways of controlling this disease. It is in
this context the objective of this work was to produce bio-formulations based on bacteria isolated from the
rhizosphere of cashew trees, in order to evaluate their effectiveness on the growth of the agent responsible for
cashew bacteriosis (Xanthomonas citri pv. Mangiferaeindicae). Thus, two liquid formulations were made from
Pseudomonas fluorescens and Bacillus subtilis isolated from the rhizosphere of cashew. Stability, in vitro
antagonism and biocontrol tests against Xanthomonas citri pv. Mangiferaeindicae were performed. The results
obtained showed an inhibition of the Xanthomonas citri pv. Mangiferaeindicae bacterium with inhibition zones
of 8.13 ± 2.1 and 25.20 ± 3.9 mm in diameter respectively for the products formulated with Bacillus subtilis and
Pseudomonas fluorescens. In biocontrol tests, both formulated products showed their ability to protect cashew
plants against bacterial blight with reduction rates of 80.95 ± 2.3 % and 73.80 ± 5.2% for the Pseudomonas
fluorescens and Bacillus subtilis formulations, respectively. These two formulations of bacterial, once tested in
cashew plantations, could be used in the biological control of cashew bacterial blight in Côte d'Ivoire.
* Corresponding Author: Tehua Amoa Armist  [email protected]

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Introduction pesticide residues in foodstuffs (Kouassi, 2012). In

Food security is defined as access to safe and order to mitigate the adverse effects of chemical
sufficient food for all. Meeting the food demand of a pesticides, biological control agents are emerging as
rapidly growing world population is becoming a promising alternatives for the management of crop
major challenge for humanity. To meet the food needs pathogens. Among these biological agents, microbial
of the population, agricultural productivity will have biopesticides (bacteria, fungi, viruses) are the most
to be increased in a sustainable manner worldwide appropriate. Indeed, they offer advantages of higher
(Kumar et al., 2012). However, insect pests and plant selectivity and lower toxicity compared to
pathogens (fungi, bacteria or viruses) contribute to conventional chemical pesticides (MacGregor et al.,
the decline in agricultural productivity, which can be 2006). Recent studies have shown their importance
as high as 70%. Indeed, plants as well as harvested in disease biocontrol (Pérez-Garcia et al., 2011).
and stored products are subjected to attacks by many However, the formulation of microbial biopesticides
pathogens (Popp et al., 2013). This is the case for is a key element in the design of control strategies for
cashew (Anacardium occidentale L.) in Côte plant and crop diseases caused by plant pathogens
d'Ivoire.Cashew, a crop that plays an important role (Nam et al., 2018).
in the Ivorian economy because of its cashew nut, is a
During this decade, numerous works in greenhouse
particular strategic and income-generating resource
and field trials have shown the potential value of
for farmers in the North, South, Centre and East of
rhizosphere bacteria, including Pseudomonas
the country (Soro, 2012). However, despite the
fluorescens and Bacillus subtilis as biological control
economic and nutritional importance of cashew, its
agents for plant pathogens (Akram, 2008). A work of
cultivation is subjected to several phytopathological
Koua (2020) showed that B. subtilis strains isolated
problems that compromise the quality and quantity of
from the rhizosphere of cocoa trees in Côte d'Ivoire
cashew yield (Silué et al., 2017). Bacterial blight is a
would be effective bioinoculants in the control of
bacterial disease of cashew caused by Xanthomonas
cocoa diseases in greenhouses such as swollen shoot.
citri pv. Mangiferaeindicae. This disease manifests
It would therefore be interesting to find a stable
itself by oily angular spots on the leaves surrounded
bacterial biopesticide formulation suitable for the
or not by a halo-chlorotic. It attacks all the vital
control of bacterial diseases of cashew trees and thus
organs of the plant with high severity (Zombre et al., find a sustainable solution to the problem posed by
2017). In Benin, a work of Afouda et al. (2013) synthetic products in Côte d'Ivoire. The general
revealed average severities of 32.96%. This high objective of this work is to evaluate the efficacy of a
severity of bacterial blight could lead to a decrease in formulation of bacterial biocontrol agents based on
cashew nut yield. Also, Soro et al. (2017) found bacteria (P. fluorescens and Bacillus subtilis) isolated
evidence of bacterial blight in cashew orchards in from the rhizosphere of cashew trees against
Côte d'Ivoire with relative incidences of 15%. To Xanthomonas citri pv. Mangiferaeindicae.
control this disease, producers resort to the use of
chemical pesticides (Camara et al., 2015). Materials and methods
Material
This strategy can be effective, but the repeated use of The material used in this study consisted of two
these chemicals generates harmful consequences for bacterial strains isolated from the rhizosphere of
the environment and the health of the user. Indeed, cashew (Pseudomonas fluorescens and Bacillus
these products favour the resistance mechanism in subtilis) used for the formulation. On the other hand,
pathogens and the ecological imbalance due to the pathogenic isolates of Xanthomonas citri pv.
broad spectrum of action of most synthetic Mangiferaeindicae isolated from cashew in Côte
compounds. This would lead to the destruction of d'Ivoire were used to evaluate the effectiveness of the
pests, but also of other populations in the ecosystem formulations. Greenhouse cashew plants were also
and can also cause serious health problems due to used for the biocontrol test.

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Methods Stability testing of formulations

Formulation of bacterial biopesticide The stability of the different formulations was
Performing pre-cultures evaluated through a natural ageing test (phase
The preculture was carried out by preparing 100mL of separation observation). For this purpose, the
YPG (Yeast extract-peptone-glucose) medium formulations were poured into transparent glasses
distributed in sterile Erlenmeyer flasks at a volume of and left at room temperature (25°C) for observation
50mL per flask. These different media were then each for up to 30 days. These observations were related to
inoculated with a colony of the two bacterial the change in colouring of the solutions over time
biocontrol agents (Pseudomonas fluorescens and under the effect of oxidation and water activity
Bacillus subtilis) previously isolated on solid medium. without heat treatment of the formulations (Mensah
The pre-culture was then incubated at 30ºC for 8 h et al., 2017).
under agitation at 155 rpm. This preculture was used
to inoculate 200mL of bacterial culture. In vitro antibacterial test
The bactericidal activity of the bacterial formulations
Bacterial culture preparation was evaluated in vitro against the cashew pathogen
The bacterial culture was carried out in 300mL sterile Xanthomonas citri pv. Mangiferaeindicae in Côte
bottles containing 200mL of YPG (Yeast extract- d'Ivoire, using the agar diffusion method described by
peptone-glucose). These media were respectively Toty et al. (2013). Thus, two media were prepared
inoculated with 50mL of pre-culture of each bacterial namely YPGA 100% and YPGA 75% agar media. The
biocontrol agent. These media were then shaken at 155 YPGA 75% agar medium was obtained by the
rpm at 30°C for 72 h. Dissolved oxygen was set at 30% calculation ratio based on the composition of the
and air flow was adjusted to between 2 and 2.5 L. After 100% YPGA medium. Then, different concentrations
72 h, the resulting bacterial culture was centrifuged at (0.1 ; 0.25 ; 0.5 and 1%) of the formulations were
6000 rpm for 10 min using a refrigerated centrifuge prepared in 20mL sterile screw tubes.
(ACM-CFG-54251, India). The supernatant was
collected in 300mL sterile containers and stored at These concentrations were obtained by mixing the
4ºC. To this supernatant was added formulation biocontrol agent formulation with sterile distilled
adjuvants for obtaining bacterial biological product in water. Also, a 5mL bacterial suspension at 108
liquid form (Cabrefiga et al., 2014). CFU/mL was previously prepared from a pure culture
of Xanthomonas citri pv. Mangiferaeindicae aged 24
Formulation h. The resulting bacterial suspension was then mixed
The formulation was carried out according to the with YPGA medium (75%) and distributed evenly over
modified Mensah et al. (2017) method. Thus, the the surface of YPGA agar (100%) in Petri dishes. After
different formulations were prepared by mixing solidification of the mixture, wells were made using a
bacterial supernatant with formulation adjuvants. The sterile Pasteur pipette. Subsequently, 50 µL of each
adjuvants consisted of 5% glucose protectant concentration of each of the bacterial formulations
(Dextrose, alpha-D(+)-glucose, France), 5% glycerol was placed in each well.
(Bright, China), 0,8% dispersing agent (Vegetable oil,
Extra virgin olive oil, Algeria) and 5% emulsifying The negative control was inoculated with 50 µL of
agent (Tween® 20 (Polysorbate), Panreac). sterile distilled water. The inoculations were carried
Subsequently, the mixture of adjuvant and bacterial out in triplicate. After diffusion of the inoculates into
supernatant obtained was homogenised using a vortex the agar, the cultures were incubated at 30°C for 72 h.
(Velp France brand) for 20 min and then stored in At the end of the incubation, the diameters of the
sterile jars, wrapped with aluminium foil and kept at Xanthomonas citri pv. Mangiferaeindicae inhibition
4°C for the determination of stability and verification zones, which were indicated by a clear zone around
of in vitro control and biocontrol in the greenhouse. the well, were measured with a graduated ruler.

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Biocontrol in greenhouses Statistical analysis

A suspension of Xanthomonas citri pv. The collected data were recorded with Excel 2016
Mangiferaeindicae (causal agent of cashew bacterial spreadsheet and analysed with Statistica version 7.1
blight) was previously prepared from pure culture aged software. Analyses of variance (ANOVA) were performed
24-48 h in 5mL of YPG broth for 24 h. This suspension on the mean susceptibility score of Xanthomonas citri
was used to perform infiltrations between the pv. Mangiferaeindicae in the presence of bacterial
secondary veins of young cashew nursery leaves using a biopesticide formulations. The normality of the residuals
needleless syringe. This suspension was used to and the homogeneity of the variances were checked.
perform infiltrations between the secondary veins of Comparisons between means were made using the
young leaves of cashew tree nurseries using a needle- Newman-Keuls test at the 5% level.
less syringe. Twenty-four (24) hours after infiltration of
the plants with the bacterial suspension, the infected Results
plants were treated with the two formulations based on
Duration of stability of formulated biocontrol agents
Pseudomonas fluorescens and Bacillus subtilis. Five
The natural ageing analysis of the different liquid
(5) days after application of the different formulations,
formulations of bacterial biopesticide showed
their capacity to reduce infections due to the
products with a stability of at least 3 months. Indeed,
pathogenic bacteria was evaluated. This was done by
during the three months of exposure of the
determining the incidence and the disease severity
formulated products, no phase separation was
index according to formulae 1 and 2 below. The severity
observed, which indicates the homogeneity of the
of the disease was assessed using a visual rating scale
formulated products. Also, no biological degradation
ranging from 0 to 9. The scale as follows (Groth et al.,
was observed due to the high water activity in these
1999; Cardoso et al., 2004): 0 = No symptoms; 1 = 1-
formulated products (Fig. 1).
5%; 3 = 6-10%; 5 = 11-25%; 7 = 26-50%; 9 > 50% of
leaf area infected.

     
I (%) = ×100 (1)
       

IS = (∑ (Xi ×ni) / N Z) × 100 (2)

- I : Incidence of the disease

- Is : Severity index
Fig. 1. Stability of different formulations of bacterial
- Xi : Note i of the disease ;
biocontrol agents. A- Day 0 after formulation et B- 3
- ni : Number of plants with grade i ;
months after formulation.
- N : Total number of plants assessed ;
- Z : Highest score.
In vitro antibacterial activities
The biological efficacy of the different bacterial
Determination of the reduction rate of both diseases
after treatment biopesticide formulations was verified by in vitro
antibacterial tests against Xanthomonas citri pv.
The rate of reduction of bacterial disease by
Mangiferaeindicae, the causal agent of the cashew
formulations of bacterial biocontrol agents is
bacterial disease in Côte d'Ivoire. The results obtained
determined by the following formula :
showed an inhibition of the bacterium which is
R = (IsT - IsE) / IsT) × 100 (3) reflected by the appearance of clear and smooth
R : Disease reduction rate inhibition zones in the wells after the addition of the
IsT : Severity index of pathogen-infected plants not different formulations (Fig. 2). The diameters of these
treated with bacterial biocontrol formulation inhibition zones were 8.13 ± 2.1 and 25,20 ± 3,9 mm
IsE : Severity index of pathogen-infected plants respectively for the Bacillus subtilis and
treated with biocontrol formulation Pseudomonas fluorescens formulations (Fig. 3).

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Fig. 2. Inhibition of Xanthomonas citri pv.

Mangiferaeindicae by the formulations : A - Control
without formulation B- Xanthomonas citri pv.
Mangiferaeindicae Vs 1% of B. Subtilis formulation Fig. 4. Development of bacterial blight in treated and
and C- Xanthomonas citri pv. Mangiferaeindicae Vs untreated plants after one month : A- Plants not
1% P. fluorescens formulation. inoculated with the pathogen and not treated; B-
Plants inoculated with Xanthomonas citri pv.
Mangiferaeindicae sp; C: Plants inoculated with the
pathogen and treated with biocontrol agents.

Bacterial blight infection rate after treatment of

plants
The results of development of disease occurrence on
treated and untreated plants are presented in Fig. 5.
These results show that all treated and untreated
plants showed symptoms of bacterial blight.

Fig. 3. Effect of different formulations of bacterial

biocontrol agents on the growth of Xanthomonas citri
pv. Mangiferaeindicae.
Biobact 1 : P. fluorescens formulation and Biobact 2 :
B. Subtilis formulation
Bands topped by the same alphabetical letter are not
statistically different (p ≤ 0.05) (Newman and Keuls)

In vivo antibacterial activity

Fig. 4 shows the images of the effect of the different
formulations against Xanthomonas citri pv.
Mangiferaeindicae on cashew plants. These results Fig. 5. Development of the of bacterial blight in
show that the different formulations have the ability treated and untreated plants.
to confer effective protection to cashew plants. Biobact 1 : P. fluorescens formulation and Biobact 2:
Control plants not inoculated with the pathogen B. Subtilis formulation
Xanthomonas citri pv. Mangiferaeindicae and not
treated with the bacterial products did not show any Average severity of bacterial blight after treatment
symptoms of bacterial blight (Fig. 4 A). Plants of plants
inoculated with the bacterial pathogen and not Untreated control plants showed an average severity of
treated with the formulated biological products 28% higher than plants treated with both formulations.
showed yellowing of the leaves with premature fall of Plants treated with the Pseudomonas fluorescens
the younger ones (Fig. 4 B). However, plants treated formulation had a severity of 5.33% while those treated
with the formulated bacterial biocontrol agents with Bacillus subtilis had a severity of 7.33%. However,
showed normal growth resulting in normal leaf statistical analysis showed no significant difference
colouration (Fig. 4 C). between these two values (Fig. 6).

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 Int. J. Agron. Agri. R.

responsible for 20-40% of pre-harvest crop yield

losses (Wojcieh and Lise, 2002). In cashew crops in
Côte d'Ivoire, bacterial blight is a bacterial disease
that causes huge post-harvest losses. In most cases,
this disease is controlled through the use of chemical
pesticides. However, these chemical pesticides have
harmful effects on the environment and on the health
of the user. In view of these disadvantages, it is
important to find alternative solutions that will allow
Fig. 6. Average severity of bacterial blight on plants continued control of plant pathogens while reducing
after inoculation with Xanthomonas citri pv. the use of chemicals. These may involve the
Mangiferaeindicae and treatment with formulated development of bacterial biopesticides that would
biocontrol agents. better protect the environment and the user's health
Biobact 1: P. fluorescens formulation and Biobact 2 : (Thakore, 2006). Thus, the general objective of this
B. Subtilis formulation study was to develop a formulation of bacterial
Bands topped by the same alphabetical letter are not biocontrol agents based on bacteria isolated from the
statistically different (p ≤ 0.05) (Newman and Keuls) rhizosphere of cashew. The biocontrol agent
formulations produced in this study showed good
Bacterial blight reduction rates by biopesticide stability over time, lasting up to 3 months. This
formulations stability is believed to be due to the presence of
In general, the average reduction rates are above formulation adjuvants such as surfactants (Aridity et
50% for both formulation types. The values of the al. 2004; Alvarez-Solano et al., 2006). These results
reduction rates are 80.95 and 73.80 % for differ from those of Mensah et al. (2017) who after
Pseudomonas fluorescens and Bacillus subtilis formulating biopesticides based on nettle plant (Urtica
respectively. These two values are not statistically dioica L.) extract found stability lasting seven days.
different at the 5% threshold (Fig. 7).
In vitro antagonism and greenhouse biocontrol tests
were carried out against the cashew bacterial blight
pathogen Xanthomonas citri pv. Mangiferaeindicae..
Inhibition of the cashew pathogen by the
formulations resulted in zones of inhibition ranging
from 8.13 ± 2.1 to 25.20 ± 3.9 mm in diameter. The
Pseudomonas fluorescens formulation showed the
highest antibacterial activity with a diameter of 25.20
± 3.9 mm. These results are believed to be due to the
production of antibacterial substances by these two
Fig. 7. Reduction rate of bacterial blight on cashew bacteria involved in the formulation of biological
plants by the two formulated biocontrol agents. products that would inhibit the growth of
Biobact 1 : P. fluorescens formulation and Biobact 2 : Xanthomonas citri pv. Mangiferaeindicae in vitro
B. Subtilis formulation (Showkat et al., 2012). This work is in line with that of
Bands topped by the same alphabetical letter are not Nguefack et al. (2005) who showed the efficacy of
statistically different (p ≤ 0.05) (Newman and Keuls) Ocimum gratissimum and Thymus vulgaris
formulations on the bacterial growth of Xanthomonas
Discussion oryzae pv. oryzicola, the causal agent of leaf streak
Pathogenic microorganisms (bacteria, fungi, bacterial disease in rice. In the same vein, the work of
mycoplasma, viruses) and insect pests are generally Zombré et al (2017) on "Antibacterial activity of

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