Saudi Journal of Biological Sciences 28 (2021) 6495–6499

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Saudi Journal of Biological Sciences

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Original article

Spatial changes of arbuscular mycorrhizal fungi in peach and their

correlation with soil properties
Sheng-Min Liang a, Feng-Ling Zheng a, Elsayed Fathi Abd_Allah b, Pandiyan Muthuramalingam c,
Qiang-Sheng Wu a,⇑, Abeer Hashem d,⇑
a
Ministry of Education, Engineering Research Center of Ecology and Agricultural Use of Wetland, Hubei Key Laboratory of Waterlogging Disaster and Agricultural Use of
Wetland, College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei 434025, China
b
Plant Production Department, Faculty of Food and Agricultural Sciences, King Saud University, Riyadh 11451, Saudi Arabia
c
Department of Biotechnology, Sri Shakthi Institute of Engineering and Technology, Coimbatore 641062, Tamil Nadu, India
d
Botany and Microbiology Department, College of Science, King Saud University, P.O. Box. 2460, Riyadh 11451, Saudi Arabia

a r t i c l e i n f o a b s t r a c t

Article history: Arbuscular mycorrhizal (AM) fungi have beneficial effects on host plants, but their growth is influenced
Received 3 June 2021 by various factors. This study was carried out to analyze the variation of AM fungi in soils and roots of
Revised 28 June 2021 peach (Prunus persica L. var. Golden Honey 3, a yellow-flesh variety) trees in different soil layers (0–
Accepted 5 July 2021
40 cm) and their correlation with soil properties. The peach tree could be colonized by indigenous AM
Available online 12 July 2021
fungi (2.2–8.7 spores/g soil and 1.63–3.57 cm hyphal length/g soil), achieving 79.50–93.55% of root
AM fungal colonization degree. The mycorrhizal growth, root sugars, soil three glomalins, NH+4-N, NO
3-
Keywords:
N, available P and K, and soil organic matter (SOM) had spatial heterogeneity. Soil spores, but not soil
Glomalin
Mycorrhiza
hyphae contributed to soil glomalin, and soil glomalin also contributed to SOM. There was a significant
Nitrate nitrogen correlation of soil hyphae with spore density, soil NO
3 -N, and SOM. Root mycorrhiza was positively cor-

Nutrients related with spore density, NH+4-N, NO
3 -N, and easily extractable glomalin-related soil protein. Notably,
Peach spore density positively correlated with NO
3 -N, available K, SOM, and root fructose and glucose, while
Sugar negatively correlated with available P and root sucrose. These findings concluded that mycorrhiza of
peach showed spatial distribution, and soil properties mainly affected/altered based on the soil spore
density.
Ó 2021 The Author(s). Published by Elsevier B.V. on behalf of King Saud University. This is an open access
article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction 2012). In the rhizosphere of Ulmus pumila var. sabulosa in the hun-
sandak sandy land, the spatial distribution of AM fungi was mainly
A kind of beneficial microorganisms in the soil, viz., arbuscular influenced by soil physicochemical properties including soil cata-
mycorrhizal (AM) fungi, establish a mutual beneficial symbiosis in lase, easily extractable glomalin-related soil protein (EEG), avail-
roots of higher plants for the absorption of water and nutrients able K, soil organic matter (SOM), and alkaline phosphatase (Ma
(Bücking and Kafle, 2015). In general, the colonization and distri- et al., 2018). In Amorpha fruticosa grown on the Loess Plateau
bution of AM fungi depend upon environmental conditions rather (China), soil EEG, root AM colonization, soil spore density, and soil
than host plants, and thus root mycorrhizal colonization and soil pH value played major roles in determining soil ecology (Xie and
spore density are primarily governed by soil factors (Gong et al., Tang, 2012).
Peach is a deciduous fruit tree that is widely planted around the
world and has been shown to be an AM-dependent plant. Previous
⇑ Corresponding authors. studies indicated the promoted effects in growth performance and
E-mail addresses: [email protected], [email protected] (Q.-S. P, Zn, and Cu uptake of peach seedlings grown in fumigated nurs-
Wu), [email protected] (A. Hashem). ery soils and Zn-deficient soils after AM fungi inoculation (Gilmore,
Peer review under responsibility of King Saud University. 1971; Lambert et al., 1979). AM fungi-inoculated peach seedlings
recorded higher nutrient acquisition than non-inoculated seedlings
(Wu et al., 2011). An AM fungus Acaulospora scrobiculata dramati-
cally alleviated the obstacle of continuous cropping of peach in the
Production and hosting by Elsevier soil through changing root exudate compositions and up-

https://doi.org/10.1016/j.sjbs.2021.07.024
1319-562X/Ó 2021 The Author(s). Published by Elsevier B.V. on behalf of King Saud University.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Sheng-Min Liang, Feng-Ling Zheng, E. Fathi Abd_Allah et al. Saudi Journal of Biological Sciences 28 (2021) 6495–6499

regulating the expression level of disease-resistant genes (Lǚ et al., dichromate oxidation method (Lao, 1988). Soil’s NH+4-N, NO
3 -N,
2019; Gao et al., 2020). In addition, AM fungi-inoculated peach available K, and available P contents were analyzed with a HM-
plants showed stronger flooding tolerance than non-AM plants TYD Soil Fertilizer Nutrient Tester (Shandong Hengmei Electronic
through accelerating the accumulation of proline and improving Technology Co., Ltd, Weifang, China) according to the users’
the root growth (Zheng et al., 2020). Field inoculation with AM fun- guidelines.
gal biofertilizer of a commercial product in a nectarine (Prunus per- GRSP fractions including EEG and DEG (difficultly extractable
sica laevis) orchard increased root survivorship and leaf P levels, GRSP) were extracted from soils with 20 mM citrate buffer (1 : 8,
indicating the positive impact on field peach (Baldi et al., 2016). g/v) for half an hour and 50 mM citrate buffer for an hour at
Such results provide the evidence regarding the positive roles of 121 °C, respectively (Wu et al., 2015a), and the concentration of
AM symbiosis in peach trees. However, it is important to under- these GRSPs was analysed according to Bradford’s assay (1976).
stand which soil factors affect the mycorrhizal development in
the rhizosphere and endosphere of peach trees.
In peach, the yellow-fleshed peach is characterized by round 2.4. Data analyses
and yellow fruits, along with a red blush. In yellow-fleshed peach
cultivars, the ’Golden Honey 30 cultivar is almost round with most The data obtained from the experiment were statistically ana-
of the fruit surface being dark red and the flesh being orange- lyzed using SAS. Significant (P = 0.05) differences between four soil
yellow with numerous red pigments near the core (Niu et al., layers were performed by the Duncan’s new multiple range test.
2018). As a result, the ’Golden Honey 30 variety is widely cultivated Correlation coefficients between selected variables were achieved
and increasingly popularized in China. However, there is no rele- using Pearson’s Product Moment (r).
vant information in the mycorrhizal status of this variety and the
soil factors influencing it. The objectives of the present study were
to assess the symbiosis of the ’Golden Honey 30 variety with AM 3. Results
fungi and also to analyze the relationship between various soil
characteristics and AM status. 3.1. Spatial distribution of AM fungi in the rhizosphere and endosphere

2. Materials and methods In the rhizosphere of’ yellow-fleshed peach variety ’Golden
Honey 30 , soil mycorrhizal hyphae (Fig. 1a) and mycorrhizal fungal
2.1. Experimental materials spores (Fig. 1b) were observed, ranging in 1.63–3.57 cm/g soil and
2.2–8.7 spores/g soil, respectively (Table 1). Roots could be colo-
The tested plant material was the five-year-old ’Golden Honey nized by indigenous AM fungi (Fig. 1c), varying in 79.50%-93.55%
30 (Prunus persica L. var. Golden Honey 3) grafted on P. persica L. (Table 1). A good symbiotic relationship could be formed between
Batseh at an inter-planting spacing of 3  4 m. The orchard was peach roots and indigenous AM fungi. The root mycorrhizal colo-
located in the Special Fruit Garden of Yangtze University nization degree and soil spore density decreased gradually with
(30°210 2700 N, 112°30 500 E) along with a total annual solar radiation increasing soil depths (0–40 cm). The length of soil hyphae gradu-
of 104–110 kcal/cm2, an annual sunshine hours of 1800–2000 h, ally decreased with the increase of 0–30 cm soil layer and then
and an annual rainfall between 1100 and 1300 mm. The orchard increased in the 30–40 cm depth soil.
soil was the Xanthi-Udic-Ferralsols according to FAO system.

3.2. Spatial distribution of root sugars

2.2. Experimental sampling
The sucrose content in the root of 0–10 cm depth soil was sig-
The root and soil sampling was carried out in December 2020. nificantly lower than that in the root of other three soil layers,
Fifteen peach trees with consistent cultivation and management while no significant differences in root sucrose content were found
were selected. Fine roots were collected within the canopy, and among the root isolated from 10 to 40 cm soil layers (Table 1). The
the soil attached to the roots was gently shaken off as the rhizo- root fructose content was the highest in the root grown in the sur-
spheric soil. Samples of the three trees were mixed into one repli- face soil (0–10 cm) and the lowest in the 30–40 cm depth soil. The
cate, with a total of five replicates. Meanwhile, root samples and root glucose content showed significant differences among all
rhizospheric soils were collected at four soil layers, including 0– treatments and decreased after the soil deep was increased.
10 cm, 10–20 cm, 20–30 cm, and 30–40 cm. Soils from the same
layer of the three trees were uniformly mixed, naturally dried
and sieved by a mesh with a diameter of 2 mm. 3.3. Spatial distribution of soil nutrients

2.3. Variable determinations Soil nutrients in rhizosphere of yellow-fleshed peach showed

certain spatial distribution (Table 2). As the depth of the soil
Mycorrhizal hyphal length in the soil was analyzed immedi- increased, SOM and NO
3 -N content gradually decreased, while soil
ately after soil samples were collected from the field using the available P content increased. NH+4-N and available K in the soil
method described by Bethlenfalvay and Ames (1987). Root AM showed diversified variations in soil layers, along with the highest
fungi colonization was carried out by Phillips and Hayman value in the 0–10 depth soil.
(1970) after staining 0.05% trypan solution. Root AM structures
were examined microscopically, and the colonization degree of
AM fungi in roots was estimated using the formula described by 3.4. Spatial distribution of soil glomalin
Cheng et al. (2021). Root glucose, fructose, and sucrose contents
were measured by Wu et al. (2015b). Soil EEG, DEG and TG contents decreased with the increase of
Spore density in the soil was measured using the sucrose soil depth, whilst the significantly increasing trend of EEG and
centrifugation-wet sieve decantation method outlined by Ianson TG concentrations was shown as the soil of 1–10 cm > 10–20 cm
and Allen (1986). SOM content was assayed using the potassium  20–30 cm > 30–40 cm layer (Fig. 2).
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Sheng-Min Liang, Feng-Ling Zheng, E. Fathi Abd_Allah et al. Saudi Journal of Biological Sciences 28 (2021) 6495–6499

Fig. 1. Soil mycorrhizal hyphae (a), indigenous spores (b), and root mycorrhizal fungal colonization (c) of the yellow-fleshed peach variety ‘Golden Honey 30 .

Table 1
Changes in mycorrhizal status and root sugar contents in the yellow-fleshed peach variety ‘Golden Honey 30 .

Soil depth Mycorrhizal status Root sugar (mg/g DW)

(cm)
Root mycorrhizal colonization Soil hyphal length (cm/g Soil spore density (spores/g Sucrose Fructose Glucose
(%) soil) soil)
0–10 93.55 ± 8.75a 3.57 ± 0.31a 8.7 ± 2.0a 19.97 ± 3.97b 60.43 ± 4.35a 18.45 ± 0.48a
10–20 88.04 ± 13.36ab 2.93 ± 0.43ab 6.0 ± 0.8b 44.71 ± 13.79a 51.60 ± 3.61b 17.47 ± 0.57b
20–30 83.56 ± 16.41ab 1.63 ± 0.41c 2.5 ± 1.3c 43.70 ± 7.48a 53.09 ± 3.13b 16.17 ± 0.57c
30–40 79.50 ± 17.42b 2.77 ± 0.54b 2.2 ± 0.8c 46.32 ± 19.69a 41.46 ± 5.61c 14.82 ± 0.75d

The data followed by different letters mean significant differences at the 0.05 level.

Table 2
Spatial distribution of soil physical–chemical properties in the yellow-fleshed peach variety ‘Golden Honey 30 .

Soil depth (cm) NH+4-N (mg/kg) NO—

3 N (mg/kg) Available P (mg/kg) Available K (mg/kg) SOM (g/kg)
0–10 72.18 ± 3.13a 73.83 ± 7.49a 39.99 ± 8.11c 311.70 ± 12.46a 11.67 ± 2.38a
10–20 68.02 ± 4.24a 61.84 ± 1.35b 40.94 ± 8.31bc 230.53 ± 6.78c 8.08 ± 0.50b
20–30 71.98 ± 2.32a 55.74 ± 2.81bc 50.77 ± 4.23ab 274.95 ± 5.58b 5.49 ± 0.68c
30–40 53.26 ± 6.65b 50.67 ± 3.08c 52.81 ± 3.59a 225.03 ± 7.32c 3.89 ± 0.88c

The data followed by different letters mean significant differences at the 0.05 level.

was also positively correlated with NO
3 -N, available K, SOM,

EEG, DEG, and TG, whereas it negatively correlated with available
P. There was a positive correlation of soil hyphal length with
NO
3 -N and SOM.

4. Discussion

The present study showed that the yellow-fleshed peach variety

’Golden Honey 30 could be colonized by indigenous AM fungi (2.2–
8.7 spores/g soil and 1.63–3.57 cm hyphal length/g soil), reaching
79.50%–93.55% of root AM fungi colonization. Correlation studies
also showed the positive correlation between soil hyphal length,
soil spore number, and mycorrhizal colonization, implying that
the three indicators of mycorrhizal development were interrelated
with each other. Similar results were observed in Citrus unshiu
grafted on Poncirus trifoliata conducted by Wu et al. (2006). More-
over, root colonization and spore number decreased as soil depth
Fig. 2. Spatial distribution of soil glomalin-related soil protein concentrations in a
yellow-fleshed peach variety ‘Golden Honey 30 . Data with different letter at the bar
increased, possibly because surface soils accumulated more dead
indicated significant differences at the 0.05 level. leaves and humus, better soil nutrients and gas phase conditions
than sub-surface soils, which is suitable for the growth of aerophi-
lic AM fungi (He and Hou, 2008; Xu et al., 2013). However, other
3.5. Correlation studies studies showed spatial changes in mycorrhizal colonization and
spore density (Wang et al., 2021). As a result, soil conditions, plant
There was not any significant correlation between root glucose, species, and indigenous AM fungal species all affect the mycor-
fructose and sucrose contents and root colonization and soil rhizal formation of host plants. Meanwhile, the SOM content
hyphae (Table 3). Root sucrose was negatively correlated with required for AM fungal growth is relatively high in the 0–20 cm
EEG, DEG, TG, and spore density, while root glucose and fructose deep soil, hence AM fungi grow best in that soil layer. The peach
showed positive correlations with EEG, DEG, TG, and spore density rhizosphere had 2.2–8.7 spores/g soil, which was consistent with
significantly. In addition, root colonization was positively corre- that observed by Guo and He (2013) in the rhizosphere (wind-
lated with NH+4-N, NO
3 -N, TG, and spore density. Spore density sand soil) of Caragana korshinskii in a farming-pastoral zone, Inner
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Table 3
Correlation coefficient between mycorrhizal growth and soil properties.

Root colonization Soil hyphal length Spore density EEG DEG TG

Spore density 0.57* 0.68** 1.00 0.73** 0.57* 0.65**
NH+4-N 0.57* 0.07 0.46 0.75** 0.65** 0.71**
NO
3 -N 0.51* 0.61* 0.83** 0.74** 0.58* 0.65**
Available P
0.21
0.39
0.63**
0.48
0.61*
0.59*
Available K 0.44 0.19 0.53* 0.88** 0.63** 0.73**
SOM 0.50 0.57* 0.87** 0.75** 0.61* 0.68**
Root sucrose
0.18
0.22
0.53*
0.68**
0.60*
0.65**
Root fructose 0.48 0.24 0.65** 0.81** 0.65** 0.72**
Root glucose 0.48 0.44 0.88** 0.76** 0.76** 0.79**
EEG 0.57* 0.24 0.73** 1.00 0.81** 0.90**
DEG 0.33 0.12 0.58* 0.81** 1.00 0.98**
TG 0.41 0.16 0.65** 0.90** 0.98** 1.00

*, P < 0.05; **, P < 0.01.

Mongolia, but, significantly lower than agricultural soils. Such low Declaration of Competing Interest
spore density in the peach rhizosphere may be explained by the
time of sampling, where December is the period of dormancy of The authors declare that they have no known competing finan-
AM fungal spores and their own low spore production (He et al., cial interests or personal relationships that could have appeared
2002; He and Hou, 2008). to influence the work reported in this paper.
Glomalin is a metal ion-containing glycoprotein isolated from
spores and hyphae of AM fungi, which considerably improved Acknowledgements
the soil aggregate stability and increased the SOM pool (He et al.,
2020; Agnihotri et al., 2021). The present study revealed the posi- This study was supported by the Open Fund of Engineering
tive correlation of fungal spore density, but not soil hyphae, with Research Center of Ecology and Agricultural Use of Wetland, Min-
soil EEG, DEG, and TG significantly, indicating that spores could istry of Education (KFT202005). The authors would like to extend
be the essential source of soil GRSPs in mycorrhizosphere. This is their sincere appreciation to the Researchers Supporting Project
in agreement with the results of Li et al. (2020) in extremely dry Number (RSP-2021/356), King Saud University, Riyadh, Saudi
desert shrubs. In addition, soil EEG, but not DEG and TG, positively Arabia.
correlated with root mycorrhizal colonization, because the EEG is
the active and functional component in soil GRSP fractions (Meng
et al., 2020). On the other, all soil GRSPs were significantly corre-
lated with SOM, NH+4-N, and NO
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