Arch. Biol. Sci., Belgrade, 67(2), 411-426, 2015 DOI:10.

2298/ABS140417007K

MORPHOLOGICAL IDENTIFICATION OF
VESICULAR-ARBUSCULAR MYCORRHIZA
ON BULBOUS PLANTS
(TAURUS MOUNTAIN IN TURKEY)

Emel Karaarslan1,*, Refik Uyanz1 and Sleyman Dou2

1
Selcuk University, Agriculture Faculty, Soil Science and Plant Nutrition Department, Kampus, Konya, Turkey

Necmettin Erbakan University, Ahmet Kelesoglu Faculty of Education, Science Teacher Training Department,
3

Meram, Konya, Turkey

*Corresponding author: ekaraarslan@selcuk.edu.tr

Abstract: This study was conducted to investigate the morphological identification of vesicular-arbuscular
mycorrhiza (VAM) on bulbous plants in the Taurus Mountains in Turkey. Thirteen soil samples and bulbous
roots were taken from the rhizosphere of bulbous plants. The soils were analyzed for the number of VAM spores
and chemical and physical properties. In addition, the roots were examined for infection levels, and morphologi-
cal identification of VAM spores was made. All tested plants are considered mycorrhizal plants. We determined
three spore species (Glomus mosseae, Glomus hoi and Scutellospora calospora) from the surveyed soils. The
spore distribution rates were as follows: G. Mossea 61.54 %, G. Hoi 23.07 % and Scutellospora calospora 15.38 %.
Results suggest that VAM fungal spores and root colonization display variation in rhizosphere under bulbous
plants in different ecological conditions.
Key words: Taurus Mountains; bulbous plants; mycorrhiza; spore; morphological identification.
Received April 17, 2014; Accepted October 20, 2014

INTRODUCTION The presence of arbuscular mycorrhizal fungi

The mutualistic association observed between
vesicular-arbuscular mycorrhiza (VAM) and
host plants is important in various natural and
agricultural ecosystems (Sylvia and Williams,
1992). This association plays an essential role
in enhancing plant growth in semi-arid agro-
ecosystems (McGee, 1989), especially for plants
grown in degraded soils.
411
(AMF) may be essential for ecosystem sustain-
ability, establishment of plants and maintenance
of biological diversity. The participation of AMF
in the biodiversity and ecosystem functioning is
now being recognized, particularly due to their
effect on plant diversity and productivity (van der
Heijden et al., 1998). Several authors have report-
ed positive relationships between plant diversity
and AMF colonization (Grime et al., 1987; van
der Heijden et al., 1998).
412 Karaarslan et al.

Mycorrhizal fungi provide inorganic nutrients,
mainly phosphorus and other complexed com-
pounds, to the plant through the extensive network
of their hyphae that forage for soil nutrients more
effectively than plant roots (Van der Heijden et al.,
1998). For this association to occur, there must be
a host plant (the phytobiont), an ecological habitat
(the soil) and a suitable fungus (the mycobiont).
Interactions among AMF, host plants and en-
vironmental factors (particularly the availability
of nutrients in the soil and other soil organisms)
are complex. Mycorrhizal associations of plant
roots with fungi are ubiquitous in nature and
therefore, this symbiosis is of enormous ecologi-
cal importance (Sykorov, 2007). In other words,
soils, plants and management factors mainly af-
fect the mycorrhizal fungi and their development
in an ecosystem. There are some indications that
the diversity of VAM fungal species declines from
natural ecosystems to high-input agricultural sys-
tems (Sharif and Moawad, 2006).
These fungi apparently have a limited toler-
ance range to environmental conditions (Stahl et
al., 1988) and possess specific adaptations to the

Table 1. Localization of the searched plants.

Number Name Localization Height References

1 Crocus biflorus Mill, sub sp. isauricus Karaman; Sarveliler, Asar Hill, 1750 m 25.04.2009, S. Dou
(Sieche ex Bowles) Mathew rocky slopes 1992 ve Bac
2 Eranthis hyemalis (L.) Salisb Karaman; Sarveliler, Turanah 1750 m 25.04.2009, S. Dou
Mountain, Kllin Locality, 1995 ve Bac.
rocky localities
3 Tulipa armena Boiss. var. lycica (Baker) Karaman; Sarveliler, Kabalakta 1750 m 25.04.2009, S. Dou
Marais Hill, rocky sites 2004 ve Bac.
4 Galanthus elwesii Hook. f. Karaman; Sarveliler, Boyal Y, 1600 m 25.04.2009, S. Dou
rocky slopes 2005 ve Bac.
5 Ornithogalum lanceolatum Labill. Karaman; Sarveliler, Kabalakta 1750 m 25.04.2009, S. Dou
Hill, rocky localities, 2006 ve Bac.
6 Gagea villosa (Bieb.) Duby var. villosa Karaman; Sarveliler, Turanah 1750 m 25.04.2009, S. Dou
Da, Kllin Mevkii, rocky 2014 ve Bac.
localities,
7 Gagea granatellii (Parl.) Parl. Karaman; Ermenek, Elmay- 1550 m 25.04.2007, S. Dou
urdu Ky, Dulavrat T., rocky 1995 ve Bac.
localities,
8 Hyacinthella lazulina K.M. Press.&Jim. Karaman; Ermenek, Elmayurdu 1760 m 25.04.2009, S. Dou
Press. Village, Dulavrat T., Degraded 2009 ve Bac.
Pinus opening
9 Muscari muscarimi Medikus Karaman; Sarveliler, Esentepe 1250 m 25.04.2009, S. Dou
Village, skele Locality, rocky 2012 ve Bac.
localities,
10 Muscari bourgaei Baker. Karaman; Sarveliler, At 1200 m 25.04.2009, S. Dou
Meydan Site, rocky localities, 2011 ve Bac.
11 Muscari armeniacum Leichtlin ex Baker Karaman; Sarveliler, orak 1520 m 25.04.2009, S. Dou
Mountain, rocky localities, 2015 ve Bac.
12 Gagea peduncularis (J.&C.Presl) Pascher Karaman; Sarveliler, Turanah 1750 m 25.04.2009, S. Dou
Mountain, Kllin Site, rocky 2010.
localities,
13 Muscari neglectum GUSS. Karaman; Sarveliler, orak 1600 m 25.04.2009, S. Dou
Mountain, rocky localities, 2016 ve Bac.
 VAM identification on bulbous plants
soil in which they occur (Lambert et al., 1980).
These adaptations apparently can influence the
outcome of competition between VAM fungi
(Gerschefske Kitt et al., 1987). For example, high
or low soil P levels (Boerner, 1990; Davis et al.,
1984; Henkel et al., 1989; Haas and Krikun, 1985;
Johnson, 1976; Krikun, 1983; Thomson et al.,
1986), soil micronutrient levels (Killham, 1985),
aridity (Bethlenfalvay et al., 1989; Sieverding and
Toro, 1988; Simpson and Daft, 1990a; Stahl and
Smith, 1984), salinity (Pond et al., (1984), low soil
pH (Adelman and Morton, 1986; Hayman and
Tavares, 1985; Howeler et al., 1987; Koomen et
al., 1987; Porter et al., 1987b), toxic levels of met-
als (Dueck et al., 1986; Gildon and Tinker, 1983;
Koslowsky and Boerner, 1989), low or high tem-
peratures (Dodd and Jeffries, 1986; Raju et al.,
1990; Schenck and Smith 1982; Sieverding, 1988).
Fig. 1. Glomus mosseae
413
Indeed, mycorrhizas, not roots, are the main
organs of nutrient uptake by most terrestrial
plants. Mycorrhiza can exist in many forms; its
morphology is determined by the characteris-
tics of each partner involved and by the specific
plant-fungus combination. This research was
conducted to investigate morphological proper-
ties of VAM in some bulbous plants grown in the
Taurus Mountains.
MATERIALS AND METHODS
Description of the study sites
The vegetation of Anti-Taurus Mountains
(Aladaglar), which are part of the middle Tau-
rus Mountain system, includes vegetation types
414 Karaarslan et al.
of Mediterranean, Iranian-Turan and European-
Siberian floristic regions such as forests, shrubs
and grassland formations. Several environmen-
tal conditions such as climate, relief (topogra-
phy), soil, hydrographic and biotic factors have
a significant impact on vegetation development.
These factors have led to rich and strong vegeta-
tion formations. However, climate is the main
factor that determines the rich biodiversity in
the study area. Topography makes a difference
by helping climate conditions; on the other hand,
soil and hydrography have a local impact on veg-
etation growth. Biotic factors have a negative im-
pact on vegetation. In particular, human beings
have been destroying the vegetation formations
for several hundred years. Because of degrada-
tion caused by humans, erosion has become one
of the main problems in the study area (Torolu
and nald, 2008).
Thirteen species of bulbous plants were
sampled in the Taurus Mountains during the
spring of 2013. The study was conducted in two
localities. One of them is Karaman/Sarveliler
and the other is Karaman/Ermenek. These two
areas are located in the central part of the Tau-
rus Mountains. Two soil and plant materials
were collected from the Ermenek location and
ten samples were sampled from Sarveliler. The
sample areas height ranges from 1 200 to 1 760
m (Table 1.).
Soil and plant samples
Soil samples were taken from soil layers at 0 to
20 cm below the surface using a spade to collect
about 1 kg of soil. The number of soil samples
was based on the number of dominant native
plant. Plant names, localities and heights are pre-
sented in Table 1. The samples were placed in a
plastic bag and stored in a refrigerator on the day
of collection; they were immediately refrigerated
at 4C when they arrived in the laboratory. Root
fragments in these samples were examined for
VAM colonization (Phillips and Hayman, 1970).
The soil samples were then air-dried in the shade
at laboratory temperature for spore counting
and identification. The total vegetation cover is
quite different in terms of density and endemic
species. (The plants were identified by Biologist
Dr. Yavuz Baci according to the procedures de-
scribed by Davis, 1965-1985).
Physical and chemical properties
of the studied site soils
The soil samples taken from 0 to 20 cm depth
were air dried and passed through a 2-mm sieve
before laboratory analysis. The analysis was con-
ducted to determine soil characteristics such as
electrical conductivity (EC), pH, available P, K,
total nitrogen, CaCO3, organic matter, texture,
Fe, Zn, Cu, Mn and soil moisture. The electri-
cal conductivity (EC) and pH were determined
by using an electric and pH meter, respectively
(Richards, 1954). The soluble potassium was de-
termined with a flame photometer according to
Knudsen et al. (1982). The available P was de-
termined using a spectrophotometer according
to Olsen et al. (1954). Total nitrogen was deter-
mined according to Bremner (1965) using the
Kjeldahl method while the CaCO3 percentage
was determined according to Hzalan and nal
(1965); organic matter was determined accord-
ing to Jackson (1973) and texture according to
Bouyoucos (1995) using the hydrometer meth-
od. In addition, Zn, Fe, Mn and Cu contents of
the soil samples were analyzed using ICP-AES
(Soltanpour and Workman, 1981). All the soil
analyses and measurements were triplicated
and average values were used in the statistical
analysis.
 VAM identification on bulbous plants 415

Table 2. Some properties in soil of the research area in April 2013.

EC
Soil pH
25C Organic
samples CaCO3 % (insatu- Texture (Bouyoucos) Texture class
(insaturated) matter %
no rated)
dS/cm
%Clay %Sand %Silty
1 1.580.03 7.230.03 86.60.19 2.610.03 420.94 261.49 320.94 Clay
2 1.260.02 7.360.04 194.30.55 6.770.06 320.94 300.94 380.94 Clay loam
3 9.500.07 7.860.02 83.30.78 1.590.01 460.94 240.94 300.94 Clay
4 23.70.27 7.780.02 1050.34 1.460.03 480.94 260.94 260.94 Clay
5 1.580.02 7.810.02 99.80.57 7.930.03 100.94 560.94 340.94 Sandy loam
6 6.330.04 7.650.03 1660.58 6.570.03 36.60.89 260.94 37.40.85 Clay loam
7 50.60.33 8.130.03 132.50.79 1.530.02 300.94 360.94 340.94 Clay loam
8 40.30.03 7.930.04 128.70.95 5.480.03 360.94 260.94 380.94 Clay loam
9 16.60.04 7.680.04 2890.94 8.130.03 340.94 260.94 380.94 Clay loam
10 29.30.16 8.130.02 177.81.18 7.420.05 240.94 440.94 320.94 Loam
11 12.60.01 7.450.04 3061.46 14.330.05 220.94 57.40.83 20.60.85 Sandy clay loam
12 5.540.03 7.770.03 250.11.37 7.160.04 400.94 260.94 340.94 Clay
13 7.120.04 7.890.02 153.92.07 6.940.03 360.94 300.94 340.94 Clay loam
LSD 0.6336 0.1479 4.423 0.1743 4.521 4.498 4.469

Table 3. Macro and micro element analysis of studied soils (mg kg-1).

Soil Total Nitrogen

P2O5 K2O Cu Fe Mn Zn
sample no (%)
1 0.130.01 4.180.03 122.350.77 1.600.01 16.340.02 38.310.16 1.360.02
2 0.340.02 12.30.03 84.550.77 1.180.01 9.020.02 9.380.04 1.020.01
3 0.080.01 1.040.02 61.780.82 1.030.02 13.740.03 8.350.04 0.180.01
4 0.070.01 1.900.01 112.240.79 1.200.01 10.840.02 10.630.04 0.320.01
5 0.400.01 5.900.04 64.090.73 0.840.02 17.910.03 12.330.01 3.100.03
6 0.330.01 19.700.03 78.820.97 1.430.01 8.830.02 7.850.02 2.120.01
7 0.080.01 19.790.04 198.490.87 1.610.01 12.330.03 7.390.01 0.440.01
8 0.270.01 3.990.06 86.290.81 1.250.02 12.140.01 7.840.05 0.710.01
9 0.410.01 5.520.02 174.280.94 0.860.01 22.780.02 31.810.07 1.680.01
10 0.370.01 5.520.02 140.321.24 1.100.04 12.860.02 10.060.01 0.840.01
11 0.720.01 10.560.03 139.630.95 1.060.02 33.810.48 19.470.02 4.050.02
12 0.360.01 11.230.05 85.360.88 0.930.03 18.140.05 25.630.31 1.10.03
13 0.350.01 9.130.07 91.480.82 2.600.11 48.960.91 16.960.04 1.070.02
LSD 0.05412 0.1757 4.257 0.1729 1.378 0.4971 0.07627
416 Karaarslan et al.

Assessment of arbuscular mycorrhizal pus SX 60 trinocular microscope) at 40 X magni-

fungi colonization and spores fication. Turgid spores (suggesting viability) were
grouped under the dissecting microscope accord-
The root samples were washed carefully with ing to morphological characteristics. Diagnostic
deionized water and the roots were cleared. The permanent slides were prepared for each different
staining procedure was performed according spore morphotype using either polyvinyl alcohol
to the method described by Koske and Gemma alone or mixed with Melzers solution (1:1).
(1989). Roots were treated with KOH (10%) for
15-20 min at 121C in an autoclave. Clear pieces
of roots were rinsed with tap water to remove
KOH. Dark roots were further bleached with
10% H2O2 for 3 min at room temperature. Then
the roots were acidified with 2% HCl (v/v) for
1 h at room temperature and stained with Try-
pan blue (0.05%) (Phillips and Hayman, 1970),
with the lactophenol being changed to lacto-
glycerol (Lactic acid:glycerol:deionized water,
in a 5:1:1 ratio). Excess stain was removed using
50% glycerol for 1-2 h. Samples were then stored
for microscopic analysis. Three slides, each with
10 randomly selected stained roots (1 cm long)
were prepared from every individual plant sam-
ple. A total of 30 roots per species were examined
to determine structures characteristic of VAM.
Fig. 2. Sporocarps in the soil-water suspension
The percentages of root colonization were
examined under a microscope (Novew b-series
biological trinocular microscope) at 10X-20 X
and 40 X magnification and were calculated by
the gridline intersect method (Giovanetti and
Mosse, 1980).

Each soil sample (10 g fresh mass) was sieved

according to the sieving and decanting procedure
of Gerdeman and Nicolson (1963) and INVAM
(2004). The sieved samples were centrifuged at 3500
rpm (10 g) for 10 min. The pellet was resuspended
in 50% sucrose and centrifuged again at 3500 rpm
(10 g) for 1 min. After centrifuging, the superna-
tants were poured on to 38-50, 50-100, 100-250 and
>250m sieve team, washed thoroughly with de-
ionized water and then placed in 9-cm Petri dishes Fig. 3. Mycorrhizal infected in sampled plant roots (Crocus biflorus
for examination under a stereomicroscope (Olym- Mill, subsp. isauricus (Siehe ex Bowles) Mathew
 VAM identification on bulbous plants
Spore identification was based mainly on
spore size, color, wall structure and hyphal at-
tachment (Walker, 1983; Morton and Benny,
1990; Schenk and Perez, 1990). For spore ob-
servation and identification, the spores were
mounted on glass slides and identified to genus
level whenever possible, using a compound mi-
croscope of 100-400 X magnification, based on
descriptions in Brundrett et al. (1996) and infor-
mation from the INVAM website (http://www.
invam.caf.wvu.edu).
Data analysis
The obtained data was analyzed using one-
way analysis of variance and the means were
separated by the Duncans multiple range test
(P<0.01 and 0.05) using Minitab software.
Fig. 4. Glomus hoi
417
RESULTS
Variation of physical and chemical properties
of the site soil
The results of the soil physicochemical analyses
are shown in Tables 2 and 3. Soil characteristics
of the survey area varied as follows: pH: 7.23-
8.13; organic matter content: 1.46-14.33 %; elec-
trical conductivity: 83.3-250.1 dS/cm; percentage
of CaCO3: 1.26-50.6; texture class: L, SL, SCL and
CL (Table 2). Other properties of the soil varied
as follows: available P2O5: 1.04-19.79 mg kg-1;
K2O: 61.78-198.49 mg kg-1: total nitrogen: 0.07-
0.72% (Table 3). The Cu, Fe, Mn and Zn contents
of the soil were found to be between 0.84-2.60,
8.83-48.96, 7.39-38.31 and 0.18-4.05 mg kg-1, re-
spectively.
418 Karaarslan et al.
Occurrence of arbuscular mycorrhizal fungi
Mycorrhizal colonization in different
bulbous plants
The VAM statuses of the thirteen dominant na-
tive (bulbous) plants are shown in Table 4. All
of the plant species in the surveyed area were
colonized by VAM. The root colonization rate
showed variation depending on both soil prop-
erties and on each plant species. The coloniza-
tion percentage ranged from 20 to 93%. There
were significant differences in mycorrhizal col-
onization between plants and the differences
were found to be statistically significant (P<0.01
and P<0.05). Of the thirteen plant species, Or-
nithogalum lanceolatum Labill. had the highest
colonization (93%) whereas Tulipa armena Boiss.
var. lycica (Baker) Marais. had the lowest (20%)
colonization. On the other hand, Table 4 shows
Fig. 5. Scutellospora calospora
that most of the researched plants had the same
infection rate. There was a positive correlation
between the rate of mycorrhizal infection (% in-
fection) and EC (0.404*), rate of sand (0.405*),
organic matter (0.473**), P2O 5 (0.419**), Zn
(0.333*); on the other hand, there was a negative
correlation between the rate of mycorrhizal in-
fection (% infection) and rate of clay (-0.610**),
belonging to 50-100 , spore number (-0.504**),
>250 , spore number (-0.560**) (not shown in
the Table).
AMF spore density in rhizosphere soils
The total amounts of AMF spores were obtained
from the rhizosphere region of the sampled
plants. Large spore populations were observed
in most soil samples, but variance was high. The
spore density in the rhizosphere zone under
 VAM identification on bulbous plants 419

the plants on the Taurus Mountains ranged from
62-1771 per 10 g dry soil with an average of 419
(Table 4). Differences were observed between
rhizospheres of different plant species and the
differences were found to be statistically sig-
nificant (P<0.01 and P<0.05). Spore densities
of AMF in the rhizospheres of Galanthus elwesii
Hook. f. were lower (62 in 10 g soil-1) than in the
rhizosphere of other bulbous plant. The highest
number of spores was found in the rhizosphere
of Eranthis hyemalis (L.) Salisb and Tulipa ar-
mena Boiss. var. lycica (Baker) Marais (1771 and
1193) 10 g soil-1. Soil properties had a significant
effect on spore density. On the other hand, the
distribution of spore numbers changed accord-
ing to sieve size and plant variety. The highest
spore numbers were taken from the smallest
sieve size (between 38-50m), whereas the low-
est spore densities were taken from the highest
sieve size (>250 m, Table 4). In addition, posi-
tive and negative correlations were found among
the numbers of mycorrhizal spores and some
soil properties. There was a positive correlation
between the number of spores (including sporo-
carps) and spore diameters (38, 50 (0.961**),
50 and100 (0.916**), 100-250 (0.904**)
and >250 (0.379*); there was a negative cor-
relation between the number of spores and pH
(-0.518**), CaCO3 (-0.481**) and K2O (-0.350*)
(not shown in the Table).

Table 4. VAM fungi infection status of plants and spore densities of VAM fungi around Taurus Mountain (in Turkey).

Spore distribution according to sieve diameter

Root length Mycorrhizal (10 g soil)
Plant Species
(m/g) infection (%) Total spore
38-50 50-100 100-250 >250
numbers
Crocus biflorus Mill, sub sp. 1239.291.68d 270.94 3052.36c 4671.70c 672.42cd 90.27a 8487.39c
isauricus (Sieche ex Bowles)
Mathew
Eranthis hyemalis (L.) Salisb 8452.12e 870.94bc 7601.96a 530 3.31b 4804.00a 10.00e 177122.88a
Tulipa armena Boiss. var. 28331.41c 20 1.18 j 3451.90b 6762.59a 1680.72b 40.00b 11938.11b
lycica (Baker) Marais
Galanthus elwesii Hook. f. 235.381.46 l 600.98g 452.12h 110.47h 60.00h 00.00e 621.88g
Ornithogalum lanceolatum 325.971.69k 930.94a 900.94g 760.98d 610.27d 00.00e 2270.98d
Labill.
Gagea villosa (Bieb.) Duby 85002.76b 801.44d 1231.65f 300.54ef 470.98ef 00.00e 2006.40e
var. villosa
Gagea granatellii (Parl.) Parl. 164002.62a 670.92f 200.94 220.27g 341.88g 00.00e 767.85fg
Hyacinthella lazulina K.M. 662.51.00h 400.54h 210.94 130.47h 510.27e 00.00e 851.24fg
Press.&Jim. Press.
Muscari muscarimi Medikus 176.391.26m 801.08cd 2131.41d 110.27h 490.98ef 30.00c 2762.62d
Muscari bourgaei Baker. 723.331.90g 870.98b 210.54 290.72ef 720.94c 20.00d 1240.98ef
Muscari armeniacum 437.52.09j 601.69g 451.18h 230.47fg 100.27h 00.00e 780.98fg
Leichtlin ex Baker
Gagea peduncularis (J.&C. 528.131.24 670.98f 1661.41e 300.98e 610.72d 20.00d 2591.65d
Presl) Pascher
Muscari neglectum GUSS. 756.522.18f 731.18e 1321.44f 691.18d 420.27f 20.00d 2452.23d
LSD 9.075 5.292 7.525 6.806 7.281 0.9599 57.53
Table 5. Morphological character of spores of VAM fungi in studied plants. 420
(http://www.zor.zut.edu.pl/Glomeromycota/Species%20descriptions%20of%20AMF.html and (http://invam.wvu.edu/thefungi/classification/glomaceae/glomus)

Morpho-
logical Plants and Soils of Number
characters
for identi-
fication 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13.
Shape: Globose to Globose, Globose to Globose to Globose, Globose to Globose to Globose to Globose to Globose to globose, Globose to Globose to
ovoid subglobose, ovoid ovoid subglobose, ovoid ovoid subglobose ovoid ovoid subglobose, subglobose ovoid
ellipsoidal or ellipsoidal or ellipsoidal or
irregular irregular irregular
Size: 105-310x (50-) 80-120 105-310x 105-310x (50-) 80-120 105-310x 105-310x (160-)214 105-310x 105-310x (50-) 80-120 (160-)214 105-310x
110-305 (-155) x (45-) 110-305 110-305 (-155) x (45-) 110-305 110-305 (-260) or 110-305 110-305 (-155) x (45-) (-260) or 110-305
75-120 (-140) 75-120 (-140) 150-190x 75-120 (-140) 150-190x
20-30(-50) m diam 20-30(-50) 20-30(-50) m diam 20-30(-50) 20-30(-50) 210-260 20-30(-50) 20-30(-50) m diam 210-260 20-30(-50)
diam diam diam diam diam diam diam diam diam diam
Color: Pale light yellow to Pale Pale light yellow to Pale yellow Pale yellow Pastel Pale Pale light yellow to Pastel Pale
yellow orange-yellow yellow yellow orange-yellow (2A2) to (2A2) to yellow yellow yellow orange-yellow yellow yellow
(2A2) (2A2) (2A2) golden golden (2A4) (2A2) (2A2) (2A4) to (2A2)
to golden to golden to golden yellow yellow to dark to golden to golden dark to golden
yellow yellow yellow (5B8) (5B8) orange yellow yellow orange yellow
(5B8) (5B8) (5B8) (5A8) (5B8) (5B8) (5A8) (5B8)
Hyphal Septate Subtending Septate Septate Subtending Septate Septate Bulbous Septate Septate Subtending Bulbous Septate
attachment: hyphae hypha single hyphae hyphae hypha single hyphae hyphae suspensor hyphae hyphae hypha single suspensor hyphae
Karaarslan et al.

(2-12) (2-12) (2-12) (2-12) (2-12) (2-12) (2-12) (2-12)

Auxiliary none none none none none none none none none none none none none
cell:
Sporocarp: presence presence presence presence presence presence presence presence none presence presence none presence

Germination none none none none none none none presence none none none presence none
shield:

Surface No, but No, but Outer No, but No, but No, but Outer No, but No, but with or No, but No, but No, but Outer with or No, but
ornamenta- Outer layers layers of the Outer layers Outer layers layers of the Outer Outer without Outer Outer layers of the without Outer
tion: of the spore spore wall of- of the spore of the spore spore wall of- layers of layers of ornamen- layers of layers of spore wall of- ornamen- layers of
wall often ten slough as wall often wall often ten slough as the spore the spore tations, the spore the spore ten slough as tations the spore
slough as the spore ages slough as slough as the spore ages wall often wall often outer orna- wall often wall often the spore ages wall often
the spore (in soil or in the spore the spore (in soil or in slough as slough as mentations slough as slough as (in soil or in outer orna- slough as
ages (in soil pot culture ages (in soil ages (in soil pot culture the spore the spore develop the spore the spore pot culture mentations the spore
or in pot storage). or in pot or in pot storage). ages (in ages (in (if present ages (in ages (in storage). develop ages (in
culture culture culture soil or in soil or in in the soil or in soil or in (if present soil or in
storage). storage). storage). pot culture pot culture species) pot culture pot culture in the pot culture
storage). storage). storage). storage). species) storage).

Vesicle: presence presence presence presence presence presence presence none presence presence presence none presence
 VAM identification on bulbous plants
Morphological identification of VAM spore
Spores were isolated from the soil of the research
areas soil and then examined for some proper-
ties determined by INVAM (Table 5.) .The spore
colors were also determined according to INVAM
colors chart. G. mosseae was the most common
species among the samples, being found in 85% of
the soil samples collected (Table 6.). These species
are typical of arid and semi-arid environments.
It has been reported that G. mosseae has a vari-
able response to different environmental condi-
tions due to the variable phenotypic plasticity of
this species (Heslop-Harrison, 1964). The Glomus
genus was reported to be dominant in arid and
semi-arid climates due to its resistance to high
soil temperature (Al-Raddad, 1993; Mohammad
et al., 2003). Spores of Glomus mosseae (Fig. 1)
were found in abundance in almost every soil
sample, and spores of Glomus hoi (Fig. 4) were
also identified in the soil samples. Another species
determined was Scutellospora calospora (Fig. 5).
Indigenous VAM fungal communities gener-
ally contain several fungal species. Normally 5-15
species may be found in agro-ecosystems. The
spatial distribution of VAM fungal species can
vary and even when the number is the same at
two different soil sites, the species composition of
the fungal population can be completely different
(Sieverding, 1989). The spores of VAM fungi are
very distinctive. Generally, spore density in the soil
samples seemed to be dominated by the species
of Glomus mosseae, Glomus hoi and S. calospora.
The properties of the identified spore species
are as follows:
Glomus mosseae (Nicol. & Gerd.) Gerd. &
Trappe. Sporocarps have 1-10 spores, are more or
less spherical, their shapes vary from globose to
ellipsoid, and up to 1 mm in diameter. Peridium
421
is variable, consisting of irregularly-branched
septate hyphae frequently anastomosing to form
a thin network, enclosing the chlamydospores
entirely, or incomplete with spores extruding;
sporocarps containing chlamydospores, some-
times only one, usually 2-6, but up to 32 in num-
ber; chlamydospores yellow, spherical to oval,
occasionally irregularly-shaped, variable in size
60-320 , generally with only one but occasional-
ly two distinct funnel-shaped attachments. Walls
of spores have two layers, a thin outer layer and a
thick inner layer. The inner wall is 2-7 ; ectocar-
pic spores are similar to endocarpic spores, abun-
dant in some collections, rare in others, formed
in soil or sometimes in root tissue.
This species is named in honor of Dr Bar-
bara Mosse, who was the first to demonstrate ex-
perimentally that a sporocarpic Endogone could
produce endotrophic mycorrhizae (Mosse, 1953,
1956). Spores are single in the soil, in loose ag-
gregates or compact sporocarps; pale yellow
(2A2) to golden yellow (5B8) (Nicolson and Ger-
deman 1968) (Fig. 1) (http://www.zor.zut.edu.pl/
Glomeromycota/Glomus%20mossea.html).
Glomus hoi. This description is a combina-
tion of information obtained from the protologue
(Berch and Trappe, 1985), type specimens, and
universal patterns of morphological organization
and structure in Glomaceae. A living culture of
this species has never been obtained by INVAM.
Spores are borne singly in the soil, globose,
subglobose, ellipsoidal or irregular in shape, (50-)
80-120 (-155) x (45-) 75-120 (-140) m in diam-
eter and light brown in color. The spore wall is
composed of two distinct, separable layers (L1
and L2). The outer layer (L1) is light yellow to
orange-yellow in color under transmitted light;
(2-) 4-6 (-8) m thick, with an outer surface
that fractures and sloughs. The inner layer (L2)
422 Karaarslan et al.
is hyaline to light yellow, very thin, 1 um thick.
The subtending hypha is single, cylindrical or
slightly flared toward the point of attachment,
(5-) 8-11(-13) m wide at the spore base. The
hyphal wall consists of a single layer, 2.5-5 m
thick, sometimes bearing fine, thin-walled, sep-
tate, lateral branches. The occlusion appears to
be a thin, curved septum in the hypha lumen at
or somewhat below its point of attachment to the
spore (Berch and Trappe, 1985) (Fig. 4).
Scutellospora calospora (Nicol. & Gerd.)
Walker & Sanders. Spores formed singly in the
soil are terminally on a bulbous suspensor-like
cell, translucent, hyaline to pale greenish-yellow;
globose, ellipsoidal or cylindrical, occasionally
broader than long; 114-285(-511) x 110-412(-
511) m. There are four walls in the spore struc-
ture and they are divided into two groups (groups
A and B). Group A: i.e. the inner wall, is brittle,
hyaline to pale yellow, very finely laminated wall
(wall 2) 3-5 m thick that may be surrounded by
a thin, very closely appressed hyaline unit wall
(wall 1), 0.5-1 m thick. Group B has two hyaline
membranous walls (walls 3 and 4). Wall 3 is 0.5-1
m thick, often wrinkling in crushed spores. Wall
4 is 1-1.5 m thick, staining red in Melzers re-
agent. Germination shield is oval, 35-70 x 50-90
m, often with invaginations along the margin.
Suspensor-like cell is borne terminally on a sep-
tate subtending hypha, 33-48 m wide; walls of
the spore are concolorous with each other; walls
are 1 m thick distally, thickening somewhat near
the spore base (Koske and Walker, 198
DISCUSSION
This is the first study reporting the morphologi-
cal identification of VAM associated with bul-
bous plants of the Taurus Mountains in Turkey.
We have determined rates of VAM colonization
in plant roots and mycorrhizal spore number in
rhizosphere soils belonging to bulbous plants. The
results showed that soils in two locations of the
Taurus Mountains contained the highest num-
ber of mycorrhiza spores and the highest mycor-
rhizal infection rate in plant roots. The number
of spores examined (62-1771 spores/10g soil)
is much higher than the number isolated from
agricultural soils (0.1 to 5 spores/g soil, Mosse
1979). However, there was much variability in
the number of spores from rhizosphere to rhi-
zosphere. We found that the numbers of VAM
spores vary with soil texture. The clay-loamy and
clay soils were generally richer in VAM spores
(with high variation in frequency), while sandy
soil contained lower numbers of endogonaceous
spores, the range being from 78-124 spores/l0 g
soil. The present survey indicated strong depen-
dence of VAM spores on the pH and CaCO3, K2O
content of the soil, but this dependence was found
as negative. Unlike findings by other researchers,
we found a very high percentage of organic matter
present in the topsoil since the topsoil was cov-
ered with plant residue. Sheikh et al. (1975) did
not find high numbers of spores with respect to
organic matter levels (Table 2). However, the re-
sults of some other studies show that organic mat-
ter content of the soil was positively related to the
endogonaceous spore population. Our findings
about the number of spores have shown fluctua-
tion depending on organic matter content. The
results obtained from this survey further showed
that the rate of mycorrhizal colonization showed
variation among bulbous plants and the root colo-
nization rate varied depending on both soil prop-
erties and plant species. The variation could be
due to environmental factors and physicochemi-
cal characteristics of the soil, which can have an
effect on colonization. Also, we found significant
and positive effects on plant root colonization of
organic matter, total nitrogen, phosphorus, EC,
 VAM identification on bulbous plants
Zn and soil texture (r=0.473, 0.473, 0.419, 0.404,
0.333, 0.405, respectively). We can say that the
mentioned parameters increased root infection
rate in such a way that P2O5 is one of the impor-
tant factors that affects both mycorrhizal infec-
tion rate and root length. It affected both mycor-
rhizal infection rate and root length positively.
Generally, a high density of P2O5 had a negative
effect on mycorrhizal colonization but the level
of P2O5 in the studied soil was not very high for
the colonization rate. Furthermore, the impor-
tance of soil parameters for the diversity of the
VAM fungus species is not well known, but over-
all VAM fungus production in the form of spore
propagules may increase with soil pH and organic
carbon, and decrease with increasing amounts of
soil phosphorous. The level of phosphorus in the
plant has also been shown to influence the es-
tablishment of VAM with high levels inhibiting
colonization by mycorrhizae (Menge et al., 1978).
Table 6. Occurrence of genera and species of VAM fungi and
their hosts Taurus Mountains of two locations (Karaman/
Sarveliler, Karaman/Ermenek). Percent occurrence is based on
the number of plant species associated with a specific genus and
species of VAM fungi divided by the total (13) major plant spe-
cies present.
Genus Species % Hosts
Occurrence
Glomus mosseae 61.54 1, 3, 4, 6, 7, 9, 10, 13
hoi 23.07 2, 5, 11
Scutellospora calospora 15.38 8, 12
In the present study, the population dynamics
of AM fungi were determined by collecting the
resting spores under rhizosphere soils of differ-
ent bulbous plants. As VAM fungi are widespread,
they occurred in almost all soils, but with a varia-
tion in both number and type of spores and sporo-
carps. The surveyed soils gave very high numbers
of VAM propagules and they changed from plant
to plant. This is due to low nutrient status (1.04-
19.79 mg/kg of P2O5 and 61.78-198.49 mg/kg
423
of K), zinc (0.18-4.05 mg/kg). Altogether, three
VAM fungal species were isolated from thirteen
different bulbous plants under rhizosphere soils.
The VAM fungal species belonging to the genera
of Glomus, and Scutellospora were isolated.
In conclusion, there is no direct relation be-
tween the number of spores and the number of
species. It is a well-established fact that these two
factors need not be directly proportional to one
another. In the present study, Glomus dominated
the rhizosphere soils of bulbous plants. This was
similar to earlier reports of VAM association on
other vegetable crops (Bagyaraj et al., 1979; Subha,
2001). Similar reference was observed in the case
of chili (Bagyaraj and Manjunath, 1980; Bagyaraj
and Sreeramulu, 1982; Manoharachary and Su-
lochana, 1989; Janakirani, 1991; Vani, 1993; Hin-
dumathi, 1999; Subha, 2001) in studies of the AM
fungal association in onion, chili, okra, sesame,
safflower, castor, sorghum and sweet potato. Also,
Karaarslan and Uyanz (2010; 2011) reported that
Glomus dominated the rhizosphere soils of natu-
ral plants. We can say that early researchers ob-
tained results similar to the present study (Kara-
arslan and Uyanz, 2008; Uyanz and Karaarslan,
2012). Spores, subtending hyphae, and sporocarp
morphology are used as taxonomical features in
VAM fungal identification. However, fungal anat-
omy in roots is not generally used in taxonomi-
cal descriptions to separate taxa below the generic
level. Morton (1985) and Hall (1977) reached the
conclusion that the morphological characteristics
(spore size, color and structure) and ontogenetic
characteristics (production of arbuscules, vesicles
and number of spores) were not influenced sig-
nificantly by the host.
All major genera (Acaulospora, Entrophospora,
Gigaspora, Scutellospora, Sclerocystis and Glomus)
of VAM fungi have been found in arid, semi-ar-
id, and sand dune soils around the globe (Khan,
424 Karaarslan et al.
1974; El-Giahmi et al., 1976; Redhead, 1977; Diem
et al., 1981; Schwab and Reeves, 1981; Bloss, 1985;
Halvorson and, Koske, 1988; McGee, 1989). Of the
148 species of VAM fungi, 31 species were first re-
ported from sand dunes (Schenck and Prez, 1990).
The 31 species are in three genera: Glomus
(14 species), Scutellospora (12 species), and Acau-
lospora (5 species). VAM inoculum density varies
from site to site and decreases with soil depth
(Sutton and Barron, 1972; Miller, 1979; Reeves
et al., 1979; Buchholz and Motto, 1981; Schwab
and Reeves, 1981; Allen et al., 1984; Zajicek et al.,
1986; Koide and Mooney, 1987). The distribu-
tion of VAM fungal species appears to be more
closely related to host plant, soil structure and
environmental conditions than to the competi-
tion by other VAM fungal species (Koske, 1981).
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