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In vitro evaluation of compost extracts efficiency as biocontrol agent of date

palm Fusarium wilt

Article in African Journal of Microbiology Research · August 2017

DOI: 10.5897/AJMR2017.8567

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 Vol. 11(29), pp. 1155-1161, 7 August, 2017
DOI: 10.5897/AJMR2017.8567
Article Number: F6DB6AD65426
ISSN 1996-0808 African Journal of Microbiology Research
Copyright © 2017
Author(s) retain the copyright of this article
http://www.academicjournals.org/AJMR

Full Length Research Paper

In vitro evaluation of compost extracts efficiency as

biocontrol agent of date palm Fusarium wilt
El kinany Said1,2,3*, Achbani El hassan2, Haggoud Abdellatif3, Ibijbijen Jamal4, Belmalha
Saadia1, Rachidi Fouad1, Echchgadda Ghizlane1 and Bouamri Rachid1*
1
Department of Plant and Environment Protection, National School of Agriculture, Meknes, Morocco.
2
Laboratory of Plant Protection URPP, National Institute for Agricultural Research, Meknes, Morocco.
3
Laboratory of Microbial Biotechnology, Faculty of Sciences and Technology, Sidi Mohamed Ben Abdellah University,
Fez, Morocco.
4
Department of Biology, Faculty of Sciences, Moulay Ismail University, Meknes, Morocco.
Received 20 April, 2017; Accepted 14 June, 2017

Bayoud, vascular wilt of date palm caused by Fusarium oxysporum f. sp. albedinis (Foa), is widely
distributed in all date palm growing regions of Morocco. It is the most serious disease of the date palm.
Compost is recognized for their ability to improve soil characteristics and to protect the crops against
biotic and abiotic stress. In this experiment, in vitro effects of different concentrations of sterilized and
unsterilized compost extract on the growth of F. oxysporum f. sp. albedinis were evaluated. All
concentration of unsterilized compost extract decreased radial growth of Foa. In fact, fungal radial
growth inhibition ranged from 20 to 97%. Higher antifungal activity was noted in 30 and 40%
concentration (more than 93%). Nevertheless, sterile compost extract inhibited mycelia growth only for
the 40% concentration with 18% fungal growth inhibition, while lower concentrations were not effective.

Key words: Date palm, Fusarium oxysporum f. sp. albedinis, compost extract, mycelium growth, inhibition rate.

INTRODUCTION

The date palm, Phoenix dactylifera L. is one of the most oasis agriculture where abiotic factors are extreme.
important species in the palm family (Palmaceae) which Otherwise it creates favorable conditions for improving
includes 200 genera and more than 2500 species (El growth of secondary crops like olive tree, wheat and
Hadrami and Al-Khayri, 2012; Hadrami and Hadrami, others leguminous plants. In the world, 100 million trees
2009). The genus Phoenix consists of fourteen species were estimated with an average of production of 7.62
distributed in the tropical and sub-tropical regions (Al- million tons (FAO, 2010). Moroccan palm groves alone
balqa, 2016). P. dactylifera L. is claimed to encompass cover 50 000 ha corresponding to 5 million tree and
over 5000 cultivars, some of which have been more or 100.000 tons/year (Sedra, 2012). In Morocco, 223
less characterized in detail (El-Hadrami and Al-Khayri, cultivars have been absolutely characterized since 1992
2012). Date palm is of great economic importance to (Saaidi, 1992; http://www.agriculture.gov.ma).

*Corresponding author: E-mail: [email protected] or [email protected].

Author(s) agree that this article remains permanently open access under the terms of the Creative Commons Attribution
License 4.0 International License
1156 Afr. J. Microbiol. Res.

A B C

Figure 1. Bayoud symptoms: A, unilateral wilting of rachis; B, Fusarium wilt

within rachis; C, late stage of infection (plant death).

Economically, the date palm fruit and by-product are the last years. Several researchers showed that the
precious for their nutritional and dietetic properties and compost extract can control several pathogenic fungi like
income generating for oasis’ populations (Al-shahib and Botrytis cinerea, Alternaria alternata, Pyrenochaeta
Marshall, 2003; Chao and Krueger, 2007; Saafi et al., lycopersici (Palou et al., 2013; Pane et al., 2012),
2008). “Bayoud” disease (Figure 1) is the most Pythium debaryanum, Sclerotium bataticola and
destructive fungal disease of date palm. Its causal agent Fusarium oxysporum f. sp. lycopersici (El-Masry et al.,
is Fusarium oxysporum f. sp. albedinis (Foa). The impact 2002). Nine compost extracts based on animal manures
of the disease is very serious in North Africa, particularly (cattle manure, sheep manure, chicken manure and
in Morocco where 2/3 of palm tree were destroyed so far horse manure) were used in vitro against numerous
(Chakroune et al., 2008; Pereau-Leroy, 1958). In addition, pathogenic fungi causing different plant diseases
Fusarium wilt has killed more than 10 million palm trees (Fusarium oxysporum f. sp. radici-lycopercisi, Fusarium
during the last 100 years (Dihazi et al., 2012; Saaidi, solani, Fusarium graminerum, Fusicoccum amugdalis,
1992). The control of the disease using chemicals Alternaria sp., Colletotrichum coccodes, Botrytis cinerea,
products is not effective and implies negative effects on Sclerotinia sclerotiorumn Aspergilus niger, Rhizoctonia
environmental and human health (Bernal-Vicente et al., solani, Rhizoctonia bataticola, Phytium sp. and
2008; Boulter et al., 2000; Brimner and Boland, 2003). Verticilium dahliae) and revealed important results
Prophylactic methods are not of interest due to the (Kerkeni and Khedher, 2007). The suppressiveness of
contamination of several date palm groves and to their compost extract is mostly due to its microbial community
non-durable impact (Jaiti et al., 2007; Saaidi, 1992). (Koné et al., 2010; Lin et al., 2014; Pane et al., 2012;
Planting resistant cultivars constitutes the only efficient Powell and Barry, 2017; Suárez-Estrella et al., 2013;
and economic method to control Fusarium wilt despite Ventorino et al., 2016). These microbes exert their
the fact the available cultivars have produced poor date antagonism by microbiostasis, antibiosis and
(Saaidi, 1992). In Morocco, cultivars that are sensitive are hyperparasitism and/or stimulate systemic resistance in
economically important (Mejhoul and Boufegous). host plants (Le Page and Bousquet, 2007). However,
Another alternative method to control phytopathogenic other researchers reported that compost actions are due
fungi consists of applications of compost and/or its to physical, chemical, biochemical and microbiological
extract (Alberto et al., 2016; El-Masry et al., 2002; dynamic interactions with plant-pathogen system (Le
Markakis et al., 2016; Pane et al., 2013, 2012; Sghir et Page and Bousquet, 2007). Indeed, several organic
al., 2015). The compost extract is an organic product chemicals present in compost or released by compost-
obtained after fermentation of compost in liquid phase for inhabiting microorganisms have been identified as
a few days to up two weeks or just for few hours of providing disease suppressive effects, including phenolic
mixing with or without aeration (short preparation) compounds, volatile fatty acids and salicylic acid (Le
(Ingham, 2003; Lanthier, 2007). A number of factors Page and Bousquet, 2007). It is also demonstrated that
which are involved in the compost extraction process, compost or its extract induce systemic resistance against
such as temperature, aeration, organic matter and pathogenic fungi in numerous plants (Kavroulakis et al.,
microbiological properties, are responsible for their 2005; Sang et al., 2010).
efficiency in plant disease suppression (Pane et al., Therefore, the main objective of this study was to
2012). The use of compost extract as a biological control investigate the suppressive capacity of unsterilized (UCE)
agent (BCA) against soil borne diseases has increased in and sterilized (SCE) compost extract against Foa growth,
 Said et al. 1157

Table 1. Rates of raw materials used in composting process.

Raw matter CM (%) OMWW (%) DOMW (%) OMW (%) VS (%)
Rate (%) 47 5 12 17 19
CM: Chicken manure, OMWW: olive mill waste water, DOMW: dry olive mill waste, OMW: two phases
olive mill waste, VS: vine shoot.

Table 2. Physical and chemical properties of different composting raw materials.

Parameter CM OMWW DOMW OMW VS

Moisture (%) 63.5 77.7 19.8 54.2 39.2

pH 7.9 4.9 8.5 6.3 8.7
-1
CE (mS. Cm ) 12.0 29.9 6.6 2.4 3.3
C/N 7.4 27.0 44.8 29 41
Organic carbon (%) 13.2 6.7 76.1 20.3 29.2
Total nitrogen (%) 1.8 0.3 1.7 0.7 0.7
P2O5 (%) 1.3 0.3 0.3 1.0 0.2
K2O (%) 1.1 3.0 1.0 0.4 0.5
CM: Chicken manure, OMWW: olive mill waste water, DOMW: dry olive mill waste, OMW:
two phases olive mill waste, VS: vine shoot.

focusing on the abiotic and biotic factors involved in this al. (2002). The mature compost was suspended in phosphate buffer
suppressive mechanism. containing K2HPO4 (8 g/l) and NaH2PO4 (0.34 g/l) at a ratio of 1:2
(w/v). Then, it was well shacked (150 rpm) for 72 h under room
temperature in natural photoperiod (24/11°C day/night). The
MATERIALS AND METHODS mixture was splitted in sterile centrifuge tubes (50 ml) and
centrifuged at 500 g (gravity) for 10 min, to remove large particles,
Fungal isolate then, at 1000 g for 10 min to obtain the active supernatant (compost
extract). A portion of compost extract was autoclaved (120°C for 20
In the Tafilalet date palm grove, the leaf samples were collected min) to obtain a sterile compost extract (SCE).
from symptomatic and non-symptomatic Mejhoul cultivar trees and
used for Fusarium species isolation and identification. Twenty
fragments of date palm leaf of each sample were surface-sterilized
In vitro suppressive effect of compost extract
for 5 min with a 4% sodium hypochlorite solution, rinsed twice in
sterile distilled water and dried in a laminar flow cabinet. The growth
The suppressive effect of the compost extract against F. oxysporum
medium potato dextrose agar (PDA) was used for fungal isolation.
f. sp. albedinis (Foa) was examined using well-cut diffusion
The plates were incubated at 28°C in the dark for 7 days. All
technique (Pane et al., 2013). Both sterilized and unsterilized
Fusarium isolates were subcultured on PDA medium and incubated
composts extracts were used in five different concentrations: 10,
for purification and spores production for 7 days in the dark and two
15, 20, 30 and 40% (v/v). PDA medium (before cooling step) was
weeks of light. After that, cultural characters were assessed by
used for preparation of compost extract concentrations, and
microscopic examination. The morphology of macroconidia,
mixtures were cooled into Petri dishes (90 mm of diameter). For
microconidia and the chlamydospores was assessed and the
control plates, the PDA medium was supplemented with phosphate
identification was made using the criteria of Sedra (2012).
buffer PBS sterile. An active mycelia disk (5 mm in diameter) of
pathogen was placed at the center of the Petri plates. All Petri
Compost source plates were then incubated at 28°C and evaluated for
pathogen growth monitoring during 8 days of incubation. Five
The compost used in this experiment was produced in a private replicate were used per elementary concentration and experiment
composting unit in Meknes, Morocco using a mixture of agricultural was repeated twice.
waste (chicken manure and vine shoot) and agro-industrial waste To determine the inhibition rate (IR) of the pathogen by applying
(olive mill waste and olive mill waste water) (Table 1). The windrow each of the tested compost extract, the radial fungal growth of Foa
composting system was used in which mixtures were subjected to was monitored by measuring the colony diameters for the control
interval turning over every two weeks. Different raw material and and treated plates at 0, 2, 4, 6 and 8 days. The inhibition rate was
compost were analyzed in a private laboratory to determine their calculated according to the formula used by Hibar et al. (2006):
physical and chemical characteristics (Table 2).
IR (%) = (1–(Average diameter of the treated / Average diameter of
the control)) x 100
Compost extract preparation
Five repetitions were carried out for each UCE or SCE
Compost extract were prepared following the method of El Masry et concentrations and controls. All plates were incubated at 26°C until
1158 Afr. J. Microbiol. Res.

Table 3. Physical and chemical properties of The most effective concentrations were 30 and 40%
mature compost. where the pathogen development was completely
inhibited (more than 97%). For the remaining con-
Parameter Value centrations (10, 15 and 20%), mycelium growth decrease
Moisture (%) 44.83 ranged from 20 to 44% as compared to the control
pH 6.69 (Figures 1, 2 and Table 6). After the period of incubation,
Organic matter (%) 32.48 some compost-inhabiting microorganisms (bacteria and
Total Kjeldhal nitrogen (NTK) (%) 1.29 fungi species) were observed to develop in the Petri
Phosphorus (P2O5) (%) 1.74 dishes and had antagonistic effect against Foa (Figure 2).
Potassium (K2O) (%) 1.22 On the other hand, no suppressive effect towards Foa
Organic carbon (%) 16.24 was observed in the sterilized compost extract except for
C/N 12.59 high concentration (40%) which showed an inhibitory
-1
24.69
effect of about 18% (Figure 3). This reduction of
Electric conductivity (ms.cm )
mycelium growth in the 40% concentration of sterilized
compost extract may be due to some chemical
compounds elaborated during composting process and
control plates were fully covered by mycelium (8 days). After remained after the sterilization step or some thermo-
incubation, linear reduction of the radius-growth of Foa was stable extracellular metabolites. These results confirm the
measured. findings of Kerkeni and Khedher (2007) and El-Massry et
al. (2002) who showed that compost extract prepared
Experimental design and statistical analysis
from various animal manures had high inhibitory effects
of F. oxysporum f. sp. radices-lycopersici which can be
Petri plates were distributed in a completely randomized design attributed to active microorganisms inhabiting the
with five Petri plates per elementary treatment and the whole unsterilized compost extract. Indeed, as confirmed by
experiment was repeated two times. Data were analyzed using other research, compost extract might have contained
SPSS statistical program version 12.0 and subjected to the analysis antagonistic mycoparasites, such as Trichoderma sp.,
of regression relation between unsterilized extract concentration
and rate inhibition of Foa.
Penicillium sp. and Petriella sp. (Danon et al., 2007;
Zmora-Nahum et al., 2008) or plant growth promoting
bacteria (PGPB) like genera of Azotobacter,
RESULTS AND DISCUSSION Pseudomonas, Stenotrophomonas, Bacillus,
Flavobacterium, Streptomyces or Actinomyces group
Organic matter, C/N ratio, total nitrogen, phosphorus, found in the chestnut compost which has colonized
potassium and pH of raw material and final compost are mycelia and inhibited sclerotia germination of Sclerotium
presented in Table 3. The compost produced and used rolfsii (Danon et al., 2007; Ventorino et al., 2016; Zmora-
showed pH with suitable value of 6.69 and the electrical nahum et al., 2008). In addition, it could be other
-1
conductivity of about 24 ms.cm . Compost had more antagonistic microorganisms inhabiting compost such as
than 32% organic matter content. The total nitrogen, the Nocardiopsis sp., Streptomyces violaceorubidus and
phosphorus and the potassium were greater than 1%. Streptomyces sp. which were identified and screened for
The C/N ration is suitable for sustainable agriculture, their antifungal activities by bio-active substance
because ratio of 27 in OMSW (Table 1) in raw materials production (peptides) (Su et al., 2014). These peptides
was previously confirmed for increasing pore space and were characterized for their antibiosis mechanism
allowing bulk oxygenation (Barje et al., 2016). In addition, (surfactins) and tested for growth inhibition of tomato
the same compost composition was used to promote pathogens such as Alternaria solani and Botrytis cinerea
date palm (cv. Mejhoul) at 1:3 ratio (v/v). It has increased (On et al., 2015). It was also reported that the sterilization
significantly all growth parameters as well as nutrient and of compost destroyed its active microorganisms and
chlorophyll content without any toxicity (data not shown). consequently nullified their antagonistic effect (El Khaldi
After 8 days of incubation at 28°C, results shown in et al., 2016; Hoitink et al., 1997; Raviv, 2014; Zhang et
Figures 2, 3 and 4 revealed that unsterilized compost al., 1998) and the growth inhibition was related to pH
+
extract caused an inhibiting effect on mycelium value and ammonium (NH4 ) concentration in the culture
development of Foa when compared with untreated medium (Danon et al., 2007; Zmora-Nahum et al., 2008).
control (Foa alone). However, the mycelia growth of Foa Fungal colonies grown in plates containing weak
measured in the different Petri plates during incubation concentration of UCE showed that fungal species
varied with the compost extract concentration (Figure 4). inhabiting compost were inhibited by high compost
The results of the regression analysis showed a extract (Figure 2). Hence, microbial activities have
significant relationship, at 5% levels, between suppressive particularly reduced growth radius of Foa pathogen. For
effect and concentration of unsterilized compost extract sterilized compost extract, no limited growth was
(Table 4). The regression coefficient was 0.966 (Table 5). detected in weak percentage because only chemical
 Said et al. 1159

Figure 2. Mycelium growth of F. oxysporum f.sp albedinis in response to different unsterilized

compost extract concentrations after 8 days of incubation in PDA medium. Control plate contains
Foa pathogen alone.

Figure 3. Mycelium growth of F. oxysporum f.sp albedinis in response to different sterilized compost
extract concentrations after 8 days of incubation in PDA. Control plate contains Foa pathogen alone.

a b
Radial growth of mycelium (mm)
Radial growth of mycelium (mm)

100 100
90 90
80 80
70 70
60 60
50 50
40 40
30
30
20
20
10
10
0
0 0 2 4 6 8
0 2 4 6 8 Time (days)
Time (days)
Control 10% 15%
Control 10% 15% 20% 30% 40%
20% 30% 40%

Figure 4. Evolution of mycelia growth of F. oxysporum f.sp albedinis with unsterilized compost extract (a) and
sterilized compost extract (b).

Table 4. Significant regressions of compost extract and rate inhibition of radius growth of Foa

Model Sum of squares ddl Average of squares D Sig.

Regression 4532.931 1 4532.931 41.623 0.008
1 Residue 326.717 3 108.906
Total 4859.648 4
1160 Afr. J. Microbiol. Res.

Table 5. Model of linear regression.

2 2
Model R R R ajusted standard error of the estimation
1 0.966 0.933 0.910 10.43578

Table 6. Rate inhibition of F. oxysporum f.sp albedinis at different concentration of sterilized and unsterilized compost
extracts.

Concentration 10% 15% 20% 30% 40%

Unsterilized compost extract 20.1 37.3 97.9
Sterilized compost extract 4.8 0.5 6.6 0.7 5.6 0.1 5.9 0.53 18.4 2.6

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seedlings. Plant Physiol. Biochem. 55:7-15.
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