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Agricultural Science Digest, volume 42 issue 4 (august 2022) : 385-392

Biocontrol Capacity of the Soil Fungus Trichoderma harzianum against Fusarim oxysporum f. sp. albedinis, a Causal Agent of Fusarium Wilt (Bayoud) Disease of Date Palm (Phoenix dactylifera L.)

H. Belaidi1,*, F. Toumi-Benali1, I.E. Benzohra2, M. Megateli2, B. Boumaaza3, A. Megherbi1, M.A. Bouzidi1
1Laboratory of Ecodevelopment of Spaces, Department of Environmental Sciences, Djillali Liabes University of Sidi Bel Abbes, Algeria.
2Department of Phoeniciculture, Experimental Station for Biophysical Environment-centre for Scientific and Technical Research on Arid Regions (CRSTRA), Campus Universitaire B.P. 1682 RP, Biskra, Algeria.
3Department of Agronomy, Ibn Khaldoun University, Tiaret, Algeria.
Cite article:- Belaidi H., Toumi-Benali F., Benzohra I.E., Megateli M., Boumaaza B., Megherbi A., Bouzidi M.A. (2022). Biocontrol Capacity of the Soil Fungus Trichoderma harzianum against Fusarim oxysporum f. sp. albedinis, a Causal Agent of Fusarium Wilt (Bayoud) Disease of Date Palm (Phoenix dactylifera L.) . Agricultural Science Digest. 42(4): 385-392. doi: 10.18805/ag.D-372.
Backgraound: This study has the objective to study antifungal effect of the antagonistic fungus of soil named Trichoderma harzianum on mycelial growth of twenty isolates of Fusarium oxysporum f. sp. albedinis (Foa), agent of the bayoud disease on the date palm, originated from south western region of Algeria.

Methods: Twenty Foa isolates obtained from isolation of the spines carrying the typical symptoms of Bayoud disease were used. The strain of T. harzianum was isolated from rhizosphere soils of the date palm trees. The in vitro test affected by two tests of confrontation, direct which is dual confrontation and indirect confrontation by volatiles substances, on mycelial growth.

Result: A statistical analysis showed a significant difference (P<0.05), of Foa isolates reaction against the antagonistic fungus T. harzianumin the test realized.The results of in vitro test showed a significant effect (P<0.05), on mycelial growth in both tests used. The inhibition rate (IR) of mycelial growth of Foa by T. harzianum varies between 28.42 and 59.12%, with 12 Foa isolates showed IR, more than 50% in the direct test and between 3.3 and 56% with just three (3) isolates have IR more than 50% in the indirect test by volatile substances. Based on these encorageous results, we can apply of this antagonistic fungus to protect our groves contaminated by Bayoud disease and also contain this susceptible commercial variety.
In the oasis system of southern Algeria, the date palm represents the key to the agroecological equilibrium of the desert and ensures the socio-economic stability of the local Saharan populations (Dubost, 1992). The phoeniciculture is an essential element in the agro-economic development of oases (Bouguedoura et al., 2015). The proposal of new management method using biotechnological procedures like plant breeding, phylogenic selection, micropropagation etc.), has become more than necessary for the future of this field (Sedra, 2003). But all these methods have limits against bayoud disease on date palm culture (Djerbi, 2003). Bayoud disease, is a vascular wilt caused by Fusarium oxysporum f. sp. albedinis (Foa), is considered as the most destructive fungal disease in Moroccan and Algerian palm groves cultivated with important economical varieties like Bouskri, Majhoul, Boufeggous,but all are susceptibles to this plant pathogen (Sedra 2005a, b; Djerbi, 2003). Since its first appearance, which goes back more than a century, in the Moroccan palm groves where it has been recorded the disappearance of more than 12 million palm trees (Djerbi, 2003). Its progression continues to advance from the west to the palm groves of central and eastern of Algeria (Djerbi, 2003).
In the absence of an updated estimate of the last years, the losses reported since 2003 (Djerbi, 2003), estimated at more than 3 million palms are in a clear evolution, especially since several unaffected regions in the past are reconsidered as contaminated by Bayoud (Essarioui and Sedra, 2017). Bayoud represents not only the risk to elimine the best commercial varieties, but also to the phenomenon of desertification and the immigration of oasis habitants to large urban cities (Bouguedoura et al., 2015).
Due to the biological and pathogenic characteristics of Fusarium oxysporum f. sp. albedinis and its host date palm, any attempt at chemical control remains ineffective for old palm groves where their rooting is deeper and harmful to the environment and human health (Saaidi, 1990). On the other hand, the proposed prophylactic measures don’t seem able to stop its progression, especially since the epidemiological data are favoured by a progressive spread of this disease, but these measures are important to protect the Southern Algerian of healthy date palms (Benzohra et al., 2017).
Genetic control by resistant varieties is therefore another promising way of reducing the damage caused by this constraint, but unfortunately all resistant cultivars haven’t high quality in date fruits (Benzohra et al., 2021a; Sedra, 2005b).
In this latest decade, a bayoud has eliminated thousands of individuals “Khalts” (natural hybrids) and important populations of better quality date, were widely cultivated as Mejhoul, Boufeggous and Jihel in Morocco, have disappeared (Sedra, 2005b). The selection of productive date palms, with good quality date palms and resistance to Bayoud requires a rigorous methodology and a broad time to select these cultivars (Benzohra et al., 2021b; Sedra, 1993; Sedra, 1994a, b; Sedra and Besri, 1994).
To control and limit this constraint, the biological control through the use of antagonistic (El-Hassni et al., 2007; Negi et al., 2019; Kuchlan et al., 2017) and mycorrhizal microorganisms remains the best way to combat this threat in palm groves contaminated by Bayoud (Jaiti et al., 2006; 2008; Dihazi et al., 2012).
The objective of this work is to study the in vitro antagonistic effect of Trichoderma harzianum on the mycelial growth of twenty isolates of Fusarium oxysporum f. sp. albedinis (Foa).
Isolates of Fusarium oxysporum f. sp. albedinis
Twenty (20) isolates of Fusariumoxysporum f. sp. albedinis (Foa) used in this study of different originsprovided by CRSTRA (Center for Scientific and Technical Research on Arid Regions, Biskra). The citation of isolates and its origins was presented in Table 1. All isolates were conserved in PDA medium (For 1000 ml : 200 g potato juice; 15 g glucose; 20 g agar-agar; pH =5.5), with temperature of conservation at 04°C and incubation at 23°C (Sedra, 2005a).

Table 1: Foa isolates with its origin.

Strain of antagonist Trichoderma harzianum
The strain of the antagonist Trichoderma harzianum (Th-Lpv-Most-2018), was provided by the Laboratory of Plant Protection (LPV) of the University of Mostaganem (Table 2). The strain was used in the confrontation tests.

Table 2: Informations of antgonistic fungi strains’ species used in ‘in vivo’ biocontrol test against bayoud disease.

Dual confrontation
We performed the method of Howell (2003) to evaluate the inhibitory action of T. harzianum on mycelial growth of Foa. We have in Petri dishes containing 15 ml of diametrically opposed PDA medium; two explants (5 mm in diameter) from the Foa and the antagonist (Fig 1), with four repetitions were performed. The control consisted by colonies of Foa in petri dishes without the antagonist. The mycelial growth of Foa isolates was assessed by measuring the radial diameter of mycelial growth of Foa for 6 days of incubation.

Fig 1: Colonies of twenty Foa isolates in dual confrontation with T. harzianm. Z: Zone of inhibition.

Indirect confrontation 
This technique consists in depositing at the center of each Petri dish containing the PDA culture medium, an explant of 5 mm in diameter one from colony of the antagonist and another from Foa (Aydi et al., 2013; Belaidi et al., 2021). The lower part containing the antagonist Trichoderma harzianum is sealed with another containing the pathogen, by a band of parafilm so as to avoid any contamination and any loss of volatile substance (Aydi et al., 2018). Four repetitions are made with an untreated control (Aydi et al., 2014).
Evaluation of mycelial growth
For the estimation of mycelial growth, the technique used is that indicated by Hibar et al., (2007b). This method consists in measuring the daily linear mycelial growth of the colonies until the seventh day, according to the following formula:
L = (D-d) / 2        

L: Mycelial growth (mm).
D: Colony diameter (mm).
d: Explant diameter (5 mm).
The mycelial growth averages are calculated by the following formula:
V(mm/j) = Σ(Ln - Ln-1) / n
V: Mycelial growth per day (mm/j).
Ln, Ln-1: Mycelial growth during the day n.
The inhibition rate (%), is calculated as follows:
 IR (%) = (Lt - L) × 100 / Lt
IR: Pourcentage of inhibition rate (%).
Lt: Daily mycelial growth of control.
L: Daily mycelial growth by T. harzianum effect.
Multiplication of foa
The multiplication of the inoculum was carried out in petri dishes containing PDA medium (Potato Dextrose Agar), autoclaved for 25 min at a pressure of 1 bar and a temperature of 121°C, to which we have added 10 ml of a liquid culture of F. oxysporum f. sp. albedinis. These dishes are then incubated at 22±3°C for two weeks (Hibar et al., 2007).
Multiplication of the antagonist
The multiplication of T. harzianum was carried out in the same way as for F. oxysporum f. sp. albedinis, but with an incubation period of one week.This is explained by the fact that T. harzianum has a faster of mycelialgrowth than F. oxysporum f. sp. albedinis (Hibar et al., 2005).
Statistical analysis
The device used is a univariate total randomization and nonparametric comparison of K samples. The significance study is performed with the 5% Kruskal-Wallis test (P<0.05). The analysis was done using the XLStat 2009.1.02 software, (AddinSoft, USA). The studied factor is the inhibition of mycelial growth; the observation is the Foa strains and the experimental unitsarethe linear or radial of mycelial growth.
Dual confrontation
Statistical analysis revealed a highly significant effect (P<0.05), a remarkable difference in mycelial growth of Foa isolates with Trichoderma harzianum (TH), compared to the control (Table 2), with formation of zone inhibition (Z), (Fig 1). We found that the mycelial growth in the control is always greater that obtained with the direct (dual) confrontations (Foa + TH), (Table 3).

Table 3: Averages of mycelial growth of foa by direct effect of T. harianum in dual confrontation.

The averages of mycelial growth of Foaisolates were consistently lower (between 2.04 and 2.53 mm / day), than the control (between 3.15 and 5.42 mm / day), (Table 3). This reduction is followed by a complete stop of the growth.
The inhibition rate (%) of mycelial growth (RI), of Foa under the direct effect of T. harzianum varies between 28.42 and 59.12% (Fig 2), according to the isolate. 12  isolates (S1, S3, S9, S10, S11, S12, S15, S16, S17, S18, S19, S20), showed a very high inhibition rate that exceeded 50%. Also, we observed that all four isolates of Ghardaia region showed IR more than 50% (S17, S18, S19 and S20), (Table 3; Fig 2).

Fig 2: Inhibition rates (IR) of mycelial growth of Foa isolates by direct and indirect effects of T. harzianum.

Indirect confrontation
Also, a significant effect (P<0.05) was observed by appearance of a difference on mycelial growth of Foa isolates in the effect of volatile substances indirectly confronted against Trichoderma harzianum compared to the control (Table 4).

Table 4: Averages of mycelial growth of foa isolates by indirec effect of T. harianum in indirect confrontation.

We observed that the average of the mycelial growth of Foa isolates by the effect of T. harzianum (Table 3), is always lower (between 2.04 and 2.53 mm/day), than the control (between 2.13 and 4.88 mm/day).
The inhibition rate (IR%) of the mycelial growth of Foa under the effect of T. harzianumvaries between 3.3 and 52.9% (Fig 2).
In comparison between the two tests of confrontation effects, we observed that the dual confrontation presented IR values very important with global average very close to 50% (49.80%), than IR values of indirect confrontation with global average under 50% (35.9%).
The potential of microoganisms as biological control agents against plant diseases has been identified for several years (Howell, 2003). The antagonism action of microorganisms has been studied for many plant diseases (Wells et al., 1972; Schirmbock et al., 1994; Elad and Kapat,1999; Yedidia et al., 1999; Yedidia et al., 2001; Harman, 2000; Sharon et al., 2001; Ozbay and Newman, 2004; Hibar et al., 2007; El-Hassni et al., 2007; Kuçuk et al., 2007; Dawidziuk et al., 2016; Benzohra et al., 2020).
The direct and indirect confrontation between the fungal antagonist Trichoderma harzianum and the pathogen Fusarium oxysporum f. sp. albedinis (Foa) showed significant reductions in mycelial growth compared with the controlin all the isolates used. This reduction was represented by the inhibition rate (IR%) of mycelial growth. In dual confrontation, this rate varies between 28.42 and 59.12% and the indirect confrontation showed an inhibition rate varies between 3.3 and 56%, by the effect of T. harzianum
Hibar et al., (2007) reported that T. harzianum was able to show a growth inhibition rate of 70 to 76% of Fusarium oxysporum f. sp. radici-lycopersici, tomato vascular wilt agent (Lycopersicum esculentum L.). While Boughedid and Filali (2015) reported aninhibition rate of mycelial growth by T. harzianum varies between 50 and 57% on Fusarium graminearum, Fusarium wilt agent of barley (Hordum vulgare L.). Concerning a bayoud disease, Sidaoui et al., (2018) reported that Trichoderma longibrachiatum had a 63% inhibition rate on mycelial growth. These last two results are very closer to those obtained in our tests.
This inhibition of mycelial growth is known in the bibliography as “antibiosis”. Antibiosis is one of antagonism mode actions carried out by antagonistic fungi by the secretion of secondairyvolatile substances such as glio-viridines and glio-toxins, substances that act as antibiotics, can inhibit the development of several phytopathogenic fungi (Howell, 2003).
In direct confrontation, there is another mode of antagonism called “mycoparasitism”. An example of this mode of action is on the T. atroviride strains, which showed a mycoparasitism action against Fusarium oxysporum f. sp. ciceris (Foc), a vascular wilt agent in chickpea (Cicer arietinum L.), by its ability to invade Foc colonies and sporulate above (Mach et al.,1999). A significantly positive correlation exists between the efficacy of Trichoderma strains in reducing disease index and growth inhibition in indirect confrontation under the effect of volatile antifungal substances (Howell, 2003; Kala et al., 2016; Fitrianingsih et al., 2019). This finding suggests that the antagonistic activation of our Foo isolates may be due in part to these volatile antifungal substances (Mach et al., 1999). Many researches showed the biological control activity of T. atroviride, that was due in part to the production of endochitinases (Kullnig et al., 2000), to the production of antibiotics (antifungals), including aromatic antibiotics such as pyrones (Keszeler et al., 2000), peptides (Oh et al., 2000) and induction of resistance mechanisms in plants (Brunner et al., 2005).
T. atroviride has shown a good efficacy in the biological control of Rhizoctonia solani on potato in the field (Kullnig et al., 2000) and also good protection against Fusarium graminearum, when applied by treatment wheat seed (Roberti et al., 2000). Recently, the biological control capabilities of this species have been shown against Cryphonectria parasitica (Murril) Barr., the agent of chestnut cankerin USA (Dodd et al., 2003).
According to Hervas et al., (1997), the contribution of T. harzianum (marketed biofungicide) to soil significantly reduces the incidence of Fusarium wilt of chickpea, caused by Fusarium oxysporum f. sp. ciceris. Dubey et al., (2007) reported a significant reduction in glasshouses by seed application of T. harzianum isolates against Pythium root rot.
Wang et al., (2003) reported that the other species of the antagonistic fungus, Trichoderma viride, influences the development and survival of A. rabiei, agent of ascochyta blight on chickpea. Some authors have noted that the absence of Bayoud disease in the palm groves of some Moroccan regions such as Marrakesh, seems linked to the phenomenon of the presence of antagonistic microorganisms in the soil (Sedra, 1993; Sedra and Rouxel, 1989). This remark was observed also in Algeria in the oases of Mizab region (Benzohra et al., 2017).
All these results confirmed the importance of application of this fungal species as a means of biological control and are promising for the future in the program of integrated control of the Bayoud date palm.
This study investigated the antagonistic capacity of Trichoderma harzianum on mycelial growthof twenty isolates of Fusarium oxysporum f. sp. albedinis (Foa), agent responsible for Bayoud disease on date palm. This in vitro test, affected by two antagonism methods was carried out by direct (or dual) and indirect confrontation using 20 Foa isolates.
The results of in vitro test indicate that there is an antagonistic effect made by T. harzianum on the development of Fusarium oxysporum f. sp. albedinis. Significant differences (P<0.05) were observed in both tests performed, direct and indirect confrontation.
These results in the two tests carried out, showed appreciable results of antagonistic capacities in Trichoderma harzianum on isolates of Fusarium oxysporum f. sp. albedinis, which can inhibit the development of Bayoud in the soil when these antagonists enter Foa, compete in space and nutrients, in antibiosis by the secretion of antibiotics and in mycoparasitism by invasion of filamentous mycelia of Foa by the secretion of lytic enzymes.
In perspectives, this biological control approach study showed the important effect of the antagonistic fungi on Foa. These results obtained in vitro, must be confirmed by in situ soil tests, in palm groves contaminated with Bayoud with currently no resistant cultivars exist yet (Djerbi, 2003; Sedra, 2003; Sedra, 2005b).
We would like to thanks the DGRSDT (Direction Générale de la Recherche Scientifique et du Développement Technologique, Algiers, Algeria), affiliated with the Ministryof High Education and Scientific Research of Algeria, for itsfunding support which facilitated us to realize this work in the Social-Economical project (DGRSDT-003-UDL-SBA-2019).

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