Vericillium wilt of olive tree (Olea europaea L.) is one of the most important diseases of olive plantations worldwide. Four distinguishable native AMF species (Paraglomus occultum (C. Walker), Glomus etunicatum W.N. Becker & Gerd. Glomus fasciculatum (Thaxt.) Gerd. & Trappe and Glomus clarum T.H. Nicolson & N.C. Schenck) were morphologically identified. The effectiveness of these native AMF fungi as inoculants for two target varieties of olive (Roghani and Zard), currently used in Iran was assessed. The current study in interaction of AMF fungi with Verticillium dahliae kleb. of olive inoculated with four different AMF fungi were used to suppress Verticillium wilt under greenhouse conditions. The fresh and dry weight of shoots and roots and the rate of increase in plant height and leaf number were significantly greater for olive seedlings inoculated with both AMF and Verticillium. No significant differences were observed between growth of olive seedlings inoculated with V. dahliae and control. This study supports the need to explore and exploit the natural diversity of AMF fungi as a starting point to formulate inoculants to be applied during the commercial nursery production of olive varieties.

1. Interaction between Arbuscular Mycorrhiza Fungi (AMF) with Verticillium dahliae Kleb. on Olive Tree under Greenhouse Conditions
Interaction between Arbuscular Mycorrhiza Fungi (AMF) with
Verticillium dahliae Kleb. on Olive Tree under Greenhouse
Conditions
*Mohammad Imad Khrieba1, Bahram Sharifnabi2, Sima Zangeneh3
1National Center for Biotechnology (NCBT), Damascus, Syria
2Deptartment of Plant Protection, College of Agriculture, Isfahan University of Technology, Isfahan. Iran,
3 Iranian Research Institute of Plant Protection, Tehran, Iran.
Vericillium wilt of olive tree (Olea europaea L.) is one of the most important diseases of olive
plantations worldwide. Four distinguishable native AMF species (Paraglomus occultum (C.
Walker), Glomus etunicatum W.N. Becker & Gerd. Glomus fasciculatum (Thaxt.) Gerd. & Trappe
and Glomus clarum T.H. Nicolson & N.C. Schenck) were morphologically identified. The
effectiveness of these native AMF fungi as inoculants for two target varieties of olive (Roghani
and Zard), currently used in Iran was assessed. The current study in interaction of AMF fungi with
Verticillium dahliae kleb. of olive inoculated with four different AMF fungi were used to suppress
Verticillium wilt under greenhouse conditions. The fresh and dry weight of shoots and roots and
the rate of increase in plant height and leaf number were significantly greater for olive seedlings
inoculated with both AMF and Verticillium. No significant differences were observed between
growth of olive seedlings inoculated with V. dahliae and control. This study supports the need to
explore and exploit the natural diversity of AMF fungi as a starting point to formulate inoculants
to be applied during the commercial nursery production of olive varieties.
Key words: Glomus, Olea europaea, Paraglomus, Mycorrhiza, Veticillium wilt.
INTRODUCTION
Olive (Olea europaea L.) is the most important oil crop of
Guilan province (Northern Iran), where olive trees occupy
about 110,000 ha. In recent years, the Iranian olive–
growing sector has experienced a phase of expansion in
new land brought under cultivation (Belaj et al., 2011). This
expansion is due to the increasing demand for olive oil by
National and International markets. Verticillium wilt is a
disease of the vascular system of plants caused by the
soil-borne fungi Verticillium dahliae Klebahn and
Verticillium albo-atrum Reink and Berthold (Pegg et al.,
2002; Stapleton and Duncan, 2000; Jimenez Dıaz et al.,
1984; Trapero and Blanco 1999; Soriano et al., 2000). The
disease can occur anywhere in the world (Bilodeau et al.,
2012) and has recently appeared in the olive groves of
Guilan and Isfahan province, Iran. It attacks especially new
plantations, sometimes very severely. In adult plants the
infection generally spreads slowly, but to such an extent
that they can eventually die. Young plants can recover
from mild attacks, but they can die in one season if
infection is heavy (Trapero and Blanco, 1999). The control
of this disease is difficult and expensive (Sinclair and
Hudler, 1998). Conventional fungicides are ineffective:
therefore, treatment usually involves cultivation practices
(Tjamos et al., 2000). The benefit of endophytic, AMF fungi
in the nutrition and development of host plants is well
known (Karajeh and Al-Raddad, 1999). Many papers have
reported that numerous plants depend on mycorrhiza for
achieving a higher growth rate (Berruti et al., 2016).
Colonized plants produce higher yields, are more tolerant
to the stress of transplanting, show greater affinity for soil
nutrients, and are more resistant to certain diseases
(Chliyeh et al., 2014; Requena et al., 1997). Many reports
indicated an interaction between AMF fungi and plant
pathogenic organisms (Davis et al., 1992; Bodker et al.,
*Corresponding Author: Mohammad Imad Khrieba,
National Center for Biotechnology (NCBT), Damascus,
Syria. Email: imadkhrieba@gmail.com
Co-Authors 2
Email: sharifna@cc.iut.ac.ir
Research Article
Vol. 6(3), pp. 185-191, December, 2019. © www.premierpublishers.org. ISSN: 2326-3997
Research Journal of Agricultural SciencesWorld

2. Interaction between Arbuscular Mycorrhiza Fungi (AMF) with Verticillium dahliae Kleb. on Olive Tree under Greenhouse Conditions
Khrieba et al. 186
2002; Jiménez‐Fernández et al., 2016). Diseases caused
by soil borne fungi can be influenced by the formation of
AMF in the root system (Artursson et al., 2006). In general,
mycorrhizal plants suffer less damage and the incidence
of deceased or the pathogen development is inhibited
(Dehne, 1982). Garmendia et al. (2006) suggested that the
arbuscular mycorrhizal fungus (AMF) Glomus deserticola
could reduce the deleterious effect of V. dahliae on pepper
growth and yield. In olive trees, Glomus intraradices and
G. claroideum have been shown to be the most influential
AM fungi (Caravaca et al., 2003). G. mosseae has been
successfully used in the mycorrhization of other woody
species such as Pinus halepensis and P. nigra (Pirazzi et
al., 1999; Monticelli et al., 2000). Olive trees are known to
form arbuscular mycorrhiza and get benefit of this
interaction (Roldan-Fajardo and Baerea, 1985). The most
common mycorrhizal type involved in normal cropping
systems, being considered as key component in
environmentally agro-biotechnologies (Jeffries and Bera,
2001). AMF fungi are known to play a critical role in plant
nutrition and enhancing mineral acquisition by the plant
(Smith and Read, 1997). One critical step for applying AMF
fungi is the appropriate selection. For this purpose, it is
recommended to test native ecotype that is considered
highly effective from established culture collections (Dodd
and Thomson, 1994). Considering the novel aspects in
studying rhizosphere ecology, a series of experiment was
carried out aimed at analyzing the natural diversity of AMF
in the rhizosphere of mature olive tree growing under
normal cultivation, at determining the efficiency of AMF
fungi isolated from target olive plantation as inoculants for
the target olive cultivars. The aim of the present study was
to examine the influence of AMF fungi on the growth and
resistance to V. dahliae.
MATERIALS AND METHODS
Sampling of olive soils
Soil samples from mature field-grown olive trees were
collected in a major olive plantation area in the Guilan
province (Rudbar, loshan and Manjil), in northern Iran.
Gilan has a humid subtropical climate with, by a large
margin, the heaviest rainfall in Iran: reaching as high as
1,900 millimetres (75 in) in the southwestern coast and
generally around 1,400 millimetres (55 in). Rasht, the
capital of the province, is known internationally as the "City
of Silver Rains" and in Iran as the "City of Rain". For the
mycorrhizal survey, 20 individual trees were randomly
chosen at four plantation sites in the studied area. Five
root-associated soil samples from each individual plant
were collected, each sample consisting of five bulked sub-
samples (250 cm3 soil cores) randomly collected at 10 to
25 cm in depth. The samples were taken in the summer of
2009.
Isolation and multiplication of AMF fungal spores
The AMF fungal spores were extracted from the
rhizosphere soil by wet sieving and decanting followed by
sucrose centrifugation (Sieverding 1991). After
centrifugation, the supernatant solution was poured
through a 50µm mesh sieve and quickly rinsed with tap
water. Intact and crushed spores were mounted in
polyvinyl alcohol-lactic acid-glycerol (PVLG) and a mixture
of PVLG and Meltzer's reagent (1:1 v/v), to make
diagnostic slides. Spores were grouped, according to their
morphological characteristics and used to initiate cultures
of the different native AMF fungal isolates. For this spore
multiplication process, a sterile mixture of soil/sand (v/v)
was used as substrate for the host plant sorghum
(Sorghum bicolor (L.) Moench). Sorghum seeds were
surface-sterilized (10 min in a 10% diluted commercial
Sodium hypochlorite solution followed by several washes
with sterile water), pre-germinated and transplanted after
emergence into 28 pots and inoculated with about 70
spores of mixture of AMF fungi. Sorghum plants were
grown under greenhouse conditions and maintained for
three months. All plants were provided monthly with 100
ml of Hewitt’s (1952) modified nutrient solution (20 ml
MgSo4 .7H2O/l [18.4 g/l], 10 ml EDTA-Fe/l [2.45 g/l], 1 ml
MnSo4 .7H2O/l [2.23 g/l], 0.1 ml CuSo4 .5H2O/l [2.4 g/l], 0.1
ml ZnSo4 .2H2O/l [2.9 g/l], 0.1 ml H3Bo3/l [18.6 g/l], 0.1 ml
Na2MnO4 .2H2O/l [0.35 g/l], 10 ml KNo3/l [30.3 g/l], 20 ml
Ca [NO3]2/l [70.8 g/l] and 1 ml Na H2Po4 .2H2O/l [20.8 g/l]).
Eight replicates per treatment were prepared. Soil samples
were taken periodically to confirm the AMF colonization.
Morphological identification of AMF fungi
The mixture of AMF fungi spores were identified to species
level. Criteria used were mainly based on spore size and
color, wall structure and hyphal attachment (Walker, 1983;
Morton and Benny, 1990; Schenk and Perez, 1990; Dodd
and Rosendahl, 1996; INAMF, 1997). Permanent slides
were prepared for each isolate using both polyvinyl-alcohol
and polyvinyl-alcohol plus Melzer’s solution (1:1), as
described by Walker (1983).
Molecular identification of Verticillium isolates
Morphological and Molecular identification of Verticillium
isolates The Verticillium isolates were identified according
to conidia and phialides size, microsclerotia characters
and colony characteristics (zare et al., 2002). Verticillium
isolates They were also analyzed by using molecular
approach. Total DNA was extracted according to Raeder
and Broada, 1985 procedure, and used as template for
PCR. ITS sequences were amplified using:
D-1: '5-CATgTTgCTCTgTTgACTgg-3'
D-2:'5-gACACggTATCTTTgCTgAA-3'

3. Interaction between Arbuscular Mycorrhiza Fungi (AMF) with Verticillium dahliae Kleb. on Olive Tree under Greenhouse Conditions
World Res. J. Agric. Sci. 187
The V. dahliae specific primers. The expected specific
band of 548bp were purified using a gel extraction Kit
(Qiagen, Hilden, Germany) and sequenced in both strands
at Macrogen company, Korea. Data sequences were
compared to Gen BANK with BLAST programs.
Evaluation of AMF fungi association with Verticillium
The AMF isolates were assayed for their interaction with
Verticillium isolate. The mixture of four species of AMF
fungi cultures was established and two olives commercial
varieties currently used to produce olive oil in Iran (Zard
and Roghani) were chosen. Rooted micro- propagated
olive plantlets of these varieties were transplanted in
(35×25cm) pots containing a mixture (1:1) was made from
the mycorrhizal inoculums and autoclaved sandy soil.
Thirty-two olive seedling, sixteen were transplanted into
pots containing the previous mixture and other sixteen into
similar pots, containing a 1:1 mixture of autoclaved clay
and sandy soil. From each group, eight seedlings
remained as control, eight were inoculated with V. dahliae,
eight were inoculated with V. dahliae + mycorrhiza and
other eight were inoculated with mycorrhiza alone.
Inoculated and non-inoculated control plantlets were
grown in greenhouse. The effect of mycorrhizal fungi on
olive Verticillium wilt disease traits (leaf number, branch
number, plant height, fresh and dry weight of olive shoots
and roots) were studied in the factorial design with eight
replications.
Data analysis
Data were processed by the analysis of variance (ANOVA)
using the SAS/STAT Version 6 (1990). Appropriate
statistical differences were determined by using the least
significant difference (LSD) test at p<0.05.
RESULTS AND DISCUSSION
Veriticillium wilt of olive trees constitutes a relevant
economic problem because of its world distribution and
host range (Trapero et al., 2011). Arbuscular mycorrhizal
(AM) fungi are the most common types of all mycorrhiza
and their occurrence as root symbionts has been reported
from exceptionally wide range of plants (Porras-Soriano et
al., 2006). In the current research of interaction of AMF
fungi with Verticillium wilt of olive trees in Iran, based on
the morphological characters of spores and mycological
keys, four AMF species were indentified e.g. Paraglomus
occultum, Glomus etunicatum, G. fasciculatum and G.
clarum, among them, P. occultum and G. fasciculatum are
new to olive rhizosphere in Iran (Figure 1). In the present
study, P. occultum (80%) showed the highest frequency
of occurrence followed by G. etunicatum (26%), G. clarum
(20%), and G. fasciculatum (13%). Symptoms of olive wilt
were observed in Isfahan province during summer of 2009.
The incidence of wilt was occurred on several branches
that gradually dried up and the other branches were
destroyed. On the infected branches, petioles were bent
and finally leaves dried and fall down on earth. Browning
and discoloring of the vessels were observed on the
infected branches. From branches of infected trees
Verticillium was isolated. Fungus was grown on PDA, and
the colony was dark and, in the center, microsclerotia were
formed. Colorless conidiophores were simple or branched
verticillate in branched two to four phialides were observed
(Figure 3). Phialides were thicker at the junction and slim
at the end. The average dimensions of phialides were
29.8×2.1 µm, of spores 2.4×1.9 µm and microsclerotia
79 ×34 µm. Koch's postulate was performed on olive
seedlings and symptoms of wilt and browning vessels was
observed after two months. Based on morphological and
molecular characterization, the fungus was identified, as
V. dahliae and this is the first report of V. dahliae from olive
trees in Isfahan province, Iran (Figure 2). The effect of
mycorrhizal fungi on olive Verticillium wilt disease traits
(leaf number, branch number, plant height, fresh and dry
weight of olive shoots and roots) revealed that fresh and
dry weights of roots inoculated with AMF alone and/or both
the symbiotant and pathogenic fungus were significantly
greater than those inoculated with Verticillium alone and/or
none inoculated ones (Table 1 and Figure 4). These
results are in concordance with the studies performed on
the other fruit trees (Vidal et al., 1992). The olive plantlets
were highly susceptible to infection by the defoliating V.
dahliae pathotypes used, as reported by Trapero and
Blanco (1999). The V. dahliae significantly reduced the
number of leaf and shoot, plant height, dry and fresh
weight of the plants compared to the control seedlings
(Tables 1, 2). In comparison to control with inoculated
olive seedling, results revealed that eight months after
inoculation, number of shoots and leaves and plant height
were significantly increased. The results also showed that
plant growth, root fresh and dry weight, shoot dry and fresh
weight were significantly greater with AMF in presence of
Verticillium inoculation over Verticillium alone, or control
when compared (Table 2). The growth rate of mycorrhizal
olive seedlings was greater than that of non-mycorrhizal
seedlings. Higher fresh and dry weights of shoots and
roots in mycorrhizal and non-mycorrhizal olive seedling
might improve the resistance of these seedlings to
Verticillium wilt. Several pathogenic fungi like species of
Fusarium, Rhizoctonia, Pythium, and Verticillium were
found to have higher frequency of occurrence on the
rhizosphere and rhizoplane of non-mycorrhizal plants as
compared to root-zone of mycorrhizal plants (Chliyeh et
al., 2014; Jiménez‐Fernández et al., 2016). Several
phosphorus solubilizing fungi like Aspergillus spp. and
other saprophytes were found to be higher in number on
mycorrhizal roots as compared to non-mycorrhizal roots
(Mamta and Mukerji, 1990). Olive seedlings inoculated
with mycorrhizal fungi G. mosseae and planting them in
soil contaminated with V. dahliae, reduced disease
severity and increased the growth of seedlings as reported
by Karajeh and Al-Raddad, 1999. Tolerance in citrus to
Phytophthora root rot inoculated by G. fasciculatus
appeared to be due to the ability of mycorrhizal roots to

4. Interaction between Arbuscular Mycorrhiza Fungi (AMF) with Verticillium dahliae Kleb. on Olive Tree under Greenhouse Conditions
Khrieba et al. 188
absorb more phosphorus and other minerals (Davis and
Menge, 1980) than non-mycorrhizal roots in P-deficient
soils. Mycorrhizal fungi alone on plant showed a positive
effect on traits as compared with control. It seems that
mycorrhizal fungi can be used as an appropriate solution
to reduce the degree of olive tree Verticillium wilt disease
(Porras-Soriano et al., 2006) if the mycorrhiza could be
produced commercially in each native land. Liu (1995)
investigated the effect of mycorrhizal fungi on verticillium
wilt of cotton and the role of disease resistance. In another
study, G. fasciculatum decreased the number of sclerotia
and infection rate of root rot of peanut caused by
Sclerotium rolfsii, effectively, under the pot conditions
(Krishna and Bagyaraj, 1983). Although many researchers
have noticed that plant diseases are reduced by AMF, few
have conducted further research on the relationship
between the development of the arbuscules or vesicles
and plant disease tolerance/resistance (O'Bannon et al.,
1979) and according to our findings, it seems that AMF
fungi could help the tolerance of olive seedlings to
Verticillium wilt disease.
Figure 1. Spores mycorrhizal fungi of olive tree A. Glomus clarum. Broken mature spores with wall layers sw1, sw2 and
sw3. B. Glomus etunicatum. Spore base with short subtending hypha (sh) spores with wall layers sw1 and sw2. C. Glomus
fasciculatum. Spore base with short subtending hypha (sh) spores with wall layers sw1 and sw2 D. Paraglomus occultum
Spore base with short subtending hypha (sh) with wall layers sw1 and sw2
Figure 2. Agarose gel electrophoresis of PCR Figure 3. A: Phialides and conidiophores of Verticillium dahliae
Products With D1/D2 primers for the detection B: microsclerotia of Verticillium dahliae.
of Verticillium dahliae M: 100bp ladder marker
Sw3
Sw2A B C
D
Sw2
Sw1
Sw1
Sw2
Sw2
Sw1
sh
Sw1
sh
sh

5. Interaction between Arbuscular Mycorrhiza Fungi (AMF) with Verticillium dahliae Kleb. on Olive Tree under Greenhouse Conditions
World Res. J. Agric. Sci. 189
Figure 4. The effect of mycorrhizal fungi on olive root volume and the growth seedling. A (Left to right): Four treatments
in a greenhouse (sterilized soil only (control), mycorrhiza, mycorrhiza + Verticillium and Verticillium + sterilized soil) on
olive B (Left to right): sterilized soil only (control), mycorrhiza, mycorrhizal + Verticillium and Verticillium + sterilized soil)
on olive tree.
Table 1. Interaction of AMF fungi and Verticillium dahliae
on shoot, root fresh and dry weight of olive seedlings.
Treatment
Shoot
fresh
weight
(g/plant)
Shoot
dry
weight
(g/plant)
Root
fresh
weight
(g/plant)
Root
dry
weight
(g/plant)
Control 15.03b
8.39b
2.18c
1.16c
AMF 30.22a
17.6a
11.46a
5.91a
Verticillium +
AMF
19.8 b
10 b
5.04 b
2.44 b
Verticillium
alone
6.42c
3.15c
1.05c
0.33d
LSD (5%) 4.90 2.47 1.50 0.717
Means within columns by the same letter are not
significantly differently at p ≥ 0.05 using LSD test
Table 2. Interaction of AMF fungi and Verticillium dahliae
on number of shoots leaves and plant height of olive
seedlings.
Treatment Number of
shoots
Number of
leaves
Plant
height(cm)
Control 3.37ab
50.1ab
34.6b
AMF 3.50a
74.5a
48.1a
Verticillium + AMF 3.75a
74.1a
44.5ab
Verticillium alone 2b
24.7b
21.2c
LSD (5%) 1.44 31.1 12.2
Means within columns by the same letter are not
significantly differently at p ≥ 0.05 using LSD test.
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7. Interaction between Arbuscular Mycorrhiza Fungi (AMF) with Verticillium dahliae Kleb. on Olive Tree under Greenhouse Conditions
World Res. J. Agric. Sci. 191
Accepted 5 December 2019
Citation: Khrieba MI, Sharifnabi B, Zangeneh S (2019).
Interaction between Arbuscular Mycorrhiza Fungi (AMF)
with Verticillium dahliae Kleb. on Olive Tree under
Greenhouse Conditions. World Research Journal of
Agricultural Sciences, 6(3): 185-191.
Copyright: © 2019 Khrieba et al. This is an open-access
article distributed under the terms of the Creative
Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium,
provided the original author and source are cited.