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iForest - Biogeosciences and Forestry

iForest - Biogeosciences and Forestry
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Arbuscular mycorrhizal fungal symbiosis with Sorbus torminalis does not vary with soil nutrients and enzyme activities across different sites

iForest - Biogeosciences and Forestry, Volume 8, Issue 3, Pages 308-313 (2015)
doi: https://doi.org/10.3832/ifor1236-008
Published: Sep 03, 2014 - Copyright © 2015 SISEF

Research Articles

Effects of soil chemical properties on arbuscular mycorrhizal fungal (AMF) symbiosis with wild service tree (Sorbus torminalis L. Crantz) were examined for study the rates of root colonization at three forest sites: Kheiroud, Lalis, and Takrin in northern Iran. Soil characteristics including pH, available phosphorus (P), potassium (K), organic matter, total nitrogen, acid and alkaline phosphatase activities, CaCO3, spore density (SD) and AMF colonization of soil and root samples were analyzed. The study sites were investigated in spring and autumn to highlight the effects of soil chemical properties on AMF statues for better nurseries and reforestation management of this rare tree species in forests. Changes in soil pH, P, K, organic matter, total nitrogen, acid and alkaline phosphatase, CaCO3, SD, and AMF colonization of soil and root samples were analyzed at the study sites. K, pH, root colonization, SD and acid phosphatase activity showed no significant differences among sites in spring and autumn, while total nitrogen, P, organic matter and alkaline phosphatase activities showed significant differences among sites and seasons. AMF colonization rates were more than 51% and 32% of roots in spring and autumn, respectively. No correlation between root colonization and soil chemical parameters in spring and autumn were detected. There was no correlation between percentage of AM root colonization and SD nor other soil parameters in spring and autumn. SD and CaCO3 were significantly negatively correlated in spring and autumn. Despite differences in soil characteristics, the results showed that SD and root colonization were not significantly different among the sites. They also showed that wild service trees had strong symbiosis with AMF, while soil properties might not have a significant effect on this symbiosis. Therefore, colonized seedlings can be considered as an appropriated method for reforestation and conservation of this rare tree species.

Arbuscular Mycorrhizae, Soil Nutrients, Colonization, Soil Enzyme, Sorbus torminalis

  Introduction 

Arbuscular mycorrhizal fungi (AMF) play a critical role in the early establishment of land plants ([44]). They can improve the host plants growth ([56]), improve plant nutrient and water uptake, enhance plant tolerance to environmental stresses, including metal tolerance, and are abundant in the plant rhizosphere interface ([49], [57], [2]). AMF are important micro-organisms which contribute to plant diversity and ecosystem functions ([53]). About 80% of higher plants have associations with arbuscular mycorrhizae ([49]). These associations lead to better phosphorous (P) absorption ([46]) and the fungi can supply up to 80% of P and 25% of nitrogen (N) to the host plants ([27]). In turn, the fungi are highly dependent on their host plants for carbon nutrition ([48]). P is an important element which is actively supplied to host plants by AMF. The amount of P influx into colonized roots can be three to five times higher than non-mycorrhizal roots ([50]).

Some soil characteristics have significant influences on the development of mycorrhizal fungi in roots, such as potassium (K), nitrogen ([52]), pH ([20]), and compaction ([55]), as well as climatic conditions and host plant effects ([23]). Increasing soil acidity or alkalinity was also a detrimental factor to AMF sporulation in field soils ([20]). AMF also affect soil enzymes ([19], [56]) by increasing activities such as dehydrogenase, phosphatase and urease ([19]).

Wild service tree (Sorbus torminalis L. Crantz) is widely distributed across Europe, north-western African forests, and south-western Asia ([35]). It is also a rare, protected tree species found in the northern forests of Iran at elevations between 170 to 2700 m a.s.l., where it can reach up to 34 m in height ([41]). Different species of the genus Sorbus are found in association with both arbuscular mycorrhizal and ecto-mycorrhizal fungi ([43]).

In this study, we hypothesized that AMF colonization of specific plants can vary significantly between sites with different soil characteristics. A comprehensive study was conducted to determine how AMF colonization of a wild service tree (Sorbus torminalis) was influenced by soil nutrients and enzyme activities at three different sites. A better understanding of AMF relationships with the wild service tree and its role in nutrient absorption and soil enzymes will enable better management of the tree stands in terms of nutrient uptake and more vigorous tree growth.

  Materials and methods 

Study sites and sampling

The study was conducted in a natural mixed forest of northern Iran consisting of Fagus orientalis Lipsky, Carpinus betulus L., and Acer cappadoeicum Gled along with a minor population of Sorbus torminalis. According to differences in aspect, slope, elevation, precipitation and some soil edaphic features, three sites were selected for this study: Kheiroud, Lalis, and Takrin (Tab. 1).

Tab. 1 - Basic information of the study sites.

Site Aspect Elevation
(m a.s.l.)
Latitude
N
Longitude
E
Slope
(%)
Rainfall
(mm)
Soil
Texture
Temperature (°C)
Min Max Mean
Kheiroud S 1000 36° 40′ 51° 43′ 30-70 1457 clay 7 25 16
Lalis N-NW 1700 36° 32′ 51° 23′ 0-60 731 clay -10 29 10
Tarkin N 1500 36° 28′ 51° 51′ 30-80 1085 clay-silt -13 32 10

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Five S. torminais trees were randomly selected from each of the three sites. Five root and soils samples were collected at the crown projection area at the bottom of each tree in spring and autumn. Fine roots and soil samples were collected to a depth of 15 cm after removal of forest litter and organic horizon. Samples were bulked, air-dried, sieved (< 2 mm), sealed in plastic bags, and stored at 4 °C until further analyses.

Soil chemical parameters

Soil pH was measured in a soil:deionized water suspension of 1:2.5. Due to their alkaline nature, P content in the soil samples was determined using the method developed by Olsen et al. ([37]).

Soil K was extracted using the neutral ammonium acetate method ([32]) and was quantified using a flame photometer. Soil organic carbon (%) was determined according to the Walkley & Black ([54]) method. In addition, soil organic carbon was converted to soil organic matter (OM, %) using a factor of 1.724. Total nitrogen (TN, %) was determined using the conventional standard Kjeldhal procedure ([5]).

The method of Ohlinger ([36]) was used to measure acid and alkaline phosphatase activities using p-nitrophenyl as substrate. Analyses were conducted in duplicate with one non-substrate control. Results were expressed as μg p-nitrophenol g-1 h-1 at 37 °C.

AMF root colonization and spore density

The five root samples from each site were carefully washed to remove soil and organic particles. Root samples were then cut into pieces of one cm and preserved in FAA buffer (5 ml formalin: 5 ml acetic acid in 90 ml of 70% alcohol). Roots were stained using 0.05% trypan blue in lactophenol ([40]) and mounted on a petri dish with grid-line intersects. Root length colonization was measured under a dissecting microscope (Olympus CH2) using the method proposed by Giovannetti & Mosse ([13]) and intraradical status of hyphae, arbuscules and vesicles was used to determined root length colonization.

AMF spores were extracted by wet sieving (sieves of size 500 and 38 µm), and decanting ([12]), followed by centrifugation in water. For estimation of the AMF spore density (SD) in soil surrounding each host tree, 15 g sub-samples of soils in two replications were analyzed, and all spores were counted. Average of the two sub-samples was taken and expressed as number of AMF spores per gram soil sample (g-1).

Data analysis

Statistical analysis was conducted using the package SPSS® v. 16 for Windows. Data was subjected to one-way analysis of variance followed by Tukey’s test (α = 0.05) to detect differences in variable means among the three sites. Student t test was used to determine acid and alkaline phosphatase activity differences between seasons. The relationship between soil chemical characteristics and AMF colonization were determined by Pearson’s correlation coefficients. Magnitude of correlations were interpreted according to Guilford’s rule-of-thumb ([15]) as follows: (i) r < 0.20: negligible correlation; (ii) 0.20 < r < 0.40: weak correlation; (iii) 0.40 < r < 0.70: moderate correlation; (iv) 0.70 < r < 0.90: strong correlation; (v): r > 0.90: very strong correlation.

  Results 

N, P, K, pH and OM

Average values of the soil nutrients at the three sites are presented in Tab. 2. Pearson’s correlation coefficients (r) for each feature in spring and autumn are presented in Tab. 3 and Tab. 4.

Tab. 2 - Mean soil parameters in different seasons at the three study sites. (TN): total nitrogen; (P): phosphorous; (K): potassium; (OM): organic matter; (RC): root colonization; (SD): spore density; (A.P): acid phosphatase; (Al.P): alkaline phosphatase. (*): μg p-nitrophenol g-1 h-1. Means within columns (in separate sites) followed by the same letters were not significantly different (p>0.05) after Tukey’s test.

Site Season TN (%) P
(ppm)
K
(ppm)
pH OM
(%)
RC
(%)
SD
(N/g)
A.P* ALP*
Kheiroud Spring 0.25a 7.16a 312.23a 7.99a 8.29ab 59.0a 69a 499.51a 627.76ab
Autumn 0.22a 8.64a 311.70a 7.93a 8.13a 38.5a 81a 554.96a 608.24a
Tarkin Spring 0.44b 10.02ab 315.60a 7.69a 12.72a 60.0a 56a 825.06a 837.77b
Autumn 0.43b 9.46a 342.10a 7.62a 14.15b 42.0a 79a 891.62a 843.00a
Lalis Spring 0.18a 12.22b 566.40a 7.32a 6.64b 61.0a 50a 597.95a 408.94a
Autumn 0.28a 14.66b 532.10a 7.05a 9.52ab 44.5a 77a 872.85a 563.00a

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Tab. 3 - Correlation coefficients between soil parameters in autumn. (TN): total nitrogen; (P): phosphorous; (K): potassium; (OM): organic matter; (SD): spore density; (A.P): acid phosphatase; (Al.P): alkaline phosphatase; (Elev): elevation; (*): p<0.05. (**): p<0.01.

Parameter P OM% pH TN% K CaCO3 A.P Al.P SD Elev Slope%
P 1 - - - - - - - - - -
OM% .161 1 - - - - - - - - -
pH -.080 -.032 1 - - - - - - - -
TN% .179 .844** .090 1 - - - - - - -
K .670** .089 -.050 .168 1 - - - - - -
CaCO3 -.362 -.422 .470 -.424 -.367 1 - - - - -
A.P .457 .739** -.514* .603* .384 -.553* 1 - - - -
Al.P .104 .730** .549* .741** -.035 .077 .233 1 - - -
SD -.030 .091 -.434 .030 .048 -.577* .181 -.368 1 - -
Elev .594* .312 -.416 .280 .487 -.537* .574* .055 .420 1 -
Slope% -.340 .376 -.113 .447 -.249 -.501 .162 .068 .752** -.018 1

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Tab. 4 - Acid and alkaline phosphatase differences between seasons. Values are means ± SE. Means were not significantly different between spring and autumn (p > 0.05) after Student’s t test.

Season Acid phosphatase
(A.P)
Alkaline phosphatase
(Al.P)
Spring 640.83 ± 56.90 624.82 ± 61.45
Autumn 773.14 ± 68.01 671.41 ± 54.37

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The value of total nitrogen in the soil was significantly higher for Tarkin than for the other areas in both seasons (p < 0.01 - Tab. 2). The mean values of total nitrogen as a critical soil component in Kheiroud and Lalis were in the same range with no significant differences between them. The values of total nitrogen between the spring and autumn seasons in all sites were not significantly different.

The P showed no significant differences among Kheiroud and Takrin during spring and autumn seasons. On the other hand, significant differences among these two sites and Lalis were observed (p < 0.05). In general, the highest amount of P was observed in the autumn samples from Lalis.

The mean values of exchangeable K for the sites ranged between 312.23 (Kheiroud) and 566.41 (Lalis) in spring, and between 311.73 (Kheiroud) and 532.05 (Lalis) in autumn. This represents 81.4% and 70.7% differences between minimum and maximum values of K in spring and autumn, respectively. No significant differences were found between K values observed in the Kheiroud and Takrin sites compared to Lalis. In addition, no significant differences were evident between spring and autumn for all sites.

Soil pH was a significant factor in the three sites during spring and autumn. The lowest pH in this study was 6.15 at Lalis and the highest was 8.75 at Kheiroud.

Concerning OM, Tarkin had the highest values during spring and autumn. There was a significant difference among values for Tarkin and Lalis in the spring. In autumn however, significant differences (p < 0.05) were observed among Tarkin and Kheiroud (Tab. 3).

Root length colonization and SD

The average colonization rates for all sites during the spring and autumn seasons are presented in Tab. 2. Over all the sites, AMF colonization rates in spring and autumn showed an average of about 60 and 41.6%, respectively. Root colonization in spring and autumn ranged between 51.0-68.5% and 32.4-55.3%, respectively. No significant differences among the three sites were detected (p > 0.05), but root colonization was significantly different between the two seasons in each site (p < 0.01).

Concerning AMF spore numbers, results showed that there was no significant difference in SD among sites during the spring and autumn seasons (Tab. 2).

Soil acid and alkaline phosphatase

As shown in Tab. 2, acid phosphatase activity showed no significant difference among the sites during spring and autumn, but alkaline phosphatase activity showed a significant difference among Lalis and Tarkin in the spring (p<0.05). In autumn, there were no significant differences among the sites (Tab. 2). Moreover, no significant differences were observed between acid and alkaline phosphatase activities in spring and autumn (Tab. 4).

The degree of variation observed indicates that the studied parameters were not equally variable among the sites (Tab. 2).

Correlation of soil chemical properties, SD and root length colonization

The Pearson’s correlation coefficients between soil chemical properties, SD and root length colonization are presented in Tab. 5.

Tab. 5 - Correlation coefficients between root colonization and soil parameters in spring and autumn. (TN): total nitrogen; (P): phosphorous; (K): potassium; (OM): organic matter; (SD): spore density; (A.P): acid phosphatase; (Al.P): alkaline phosphatase; (Elev): elevation.

Root
colonization
pH P OM% TN% CaCO3 K A.P Al.P SD Elev Slope%
Spring -.425 .201 -.114 -.126 -.207 .155 -.025 -.240 -.090 .158 -.015
Autumn -.146 .216 .091 .025 -.326 -.145 .011 -.006 .043 .402 .090

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There was a significant and positive relationship between K and P in autumn (r =0.670; p<0.01) with moderate magnitude (Tab. 3), while there was no correlation between them in spring (p>0.05 - Tab. 6).

Tab. 6 - Correlation coefficients between soil parameters in spring. (TN): total nitrogen; (P): phosphorous; (K): potassium; (OM): organic matter; (SD): spore density; (A.P): acid phosphatase; (Al.P): alkaline phosphatase; (Elev): elevation; (*): p<0.05; (**): p<0.01.

Parameter pH P OM% TN% K CaCO3 A.P Al.P SD Elev Slope%
pH 1 - - - - - - - - - -
P -.571* 1 - - - - - - - - -
OM% .320 .008 1 - - - - - - - -
TN% .254 -.009 .977** 1 - - - - - - -
K -.345 .506 .036 -.284 1 - - - - - -
CaCO3 .484 -.462 -.298 -.297 -.352 1 - - - - -
A.P -.103 .165 .776** .747** .523 -.496 1 - - - -
Al.P .563* -.220 .884** .882** -.240 .091 .612* 1 - - -
SD -.152 -.060 .210 .235 .130 -.515* .172 -.040 1 - -
Elv -.498 .628* -.016 -.032 .481 -.511 .314 -.220 .230 1 -
Slope% -.052 -.113 .450 .560* -.253 -.513 .291 .272 .814** -.018 1

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There was a non-significant decrease in pH values from Kheiroud to Lalis (Tab. 2, p>0.05).

A negative correlation with moderate magnitude was observed between pH and soil P in spring (r=0.571, Tab. 1). However, this correlation was not significant in autumn (p>0.05).

There was a significant negative correlation between SD and CaCO3 in spring and autumn (Tab. 6 and Tab. 3). However, root colonization was not significantly correlated with soil chemical and physiological parameters (Tab. 5).

No significant correlations between SD and other soil parameters between spring and autumn seasons were detected except for CaCO3. As shown in Tab. 6 and Tab. 3, there was significant positive correlation between AMF spore density and slope in both spring and autumn seasons. No significant differences were observed between SD and elevation (Tab. 6 and Tab. 3).

The correlation coefficient between soil alkaline phosphatase and pH was positive and significant in the spring with r = 0.563 (p < 0.05 - Tab. 3). In addition, the soil acid and alkaline phosphatase in relation to OM and TN were significantly correlated (p < 0.01). The magnitude of correlations between these factors was very high (Tab. 6 and Tab. 3).

  Discussion 

The significant effect of AMF on plant growth and leaf mineral concentrations has been previously documented ([33]). Our result showed that despite differences in soil properties in the studied sites, no significant differences in SD and root length colonization were observed. In a similar study on Araucaria angustifolia, Moreira et al. ([31]) showed similar rates of root colonization in spring. A reasonable colonization rate is usually about 40% ([51]). In the present study, based on observation of vesicle, arbuscule and mycelia in roots, AMF colonization rates were more than 51% and 32% of roots in spring and autumn, respectively. These results confirm a high level of symbiosis between wild service trees and AMF in spring. As mentioned earlier, the highest colonization rate was observed in spring. This response was similar to several earlier reports ([45], [6]).

Forest plantation management could greatly benefit from the use of wild service tree with high levels of root colonization by AMF, in particular in arid environments ([26]). Indeed, previous reports have demonstrated the tolerance of wild service tree to arid environmental conditions ([38]). Additionally, no significant correlations between root colonization and soil chemical parameters in spring and autumn were observed, consistently with several previous findings ([28], [10], [6], [45]).

Usually, spore density of AMF can be related to root colonization ([34]), nutrient status ([29]), elevation ([10]), pH and soil P ([25], [30]). However, in the present study no relationship between the percentage of AM colonization and spore density was found, according to previous literature reports ([4]). Similar results were observed for other soil parameters with negative correlations between spore density and CaCO3 in spring and autumn. Due to the same root colonization rates in the studied sites, no significant correlation between root colonization and spore density was expected. Trees in Kheiroud were located in areas with high pH and CaCO3 which negatively influences AMF and spore density. Similar results were reported by Labidi et al. ([24]). As stated by Mendoza et al. ([29]), the SD level is related to nutrient status, especially nitrogen content. While a direct correlation between N and SD was not observed in this study, both N and SD were positively correlated with slope across all sites.

According to Yong et al. ([58]), we found that root AMF colonization was affected by environmental conditions and host plants. Our results showed that available soil P in spring was significantly different among Lalis and Kheiroud, while in autumn Lalis was significantly different from the other two sites. Since there was no significant difference in root colonization among sites, soil available P differences can be attributed to the soil pH, that was the lowest in both seasons in Lalis compared to Tarkin and Kheiroud. Furthermore, pH had a significant negative correlation with available P. Zhao et al. ([59]) stressed that available P increases with decreasing pH. It should be noted that in calcareous soil, P is retained by Ca ions and in acid soils it is retained by Fe and Al ions ([17]).

There was a significant difference in total nitrogen among Tarkin and the other two sites for both seasons. In addition, the results indicated that the organic matter, the most important nitrogen source ([11]), was higher in Tarkin than in the other sites. Moreover, we observed a significant correlation between total nitrogen and the organic matter, according to Gairola et al. ([11]).

Factors such as temperature, moisture content ([22], [21]), elevation ([7]), precipitation and geographical aspects ([14]) significantly affect soil OM content. For example, it is known that OM soil levels in north-facing slopes (as in Tarkin) are higher as a consequence of its lower decomposition rate ([42]). Since Kheiroud, Tarkin and Lalis are located in south, north, and northwest slopes, respectively, we hypothesize that the aforementioned differences in total nitrogen between Tarkin and the other two sites may be attributed to the higher amount of organic matter in Tarkin (as a consequence of its aspect) rather than other factors.

Several authors have reported that soil K content is influenced by elevation, total nitrogen, and organic matter ([3], [11]). In the present study, no significant differences among sites and no significant correlations between K and soil chemical properties were detected, according to previous findings by Paudel & Sah ([39]).

It is reported that AMF colonization could result in higher acid and alkaline phosphatase activities, leading to higher P, N and K content in plant leaves ([1]). However, in the present study we did not found significant differences among sites in autumn as for such enzyme activities. On the other hand, alkaline phosphatase activity in Lalis was significantly different from that in Tarkin in spring. Such difference could be attributed to the effect of soil pH. Indeed, it has been documented that acid phosphatase activity is higher in acidic soils, while alkaline phosphatase activity was higher in calcareous or neutral soils ([9]). The importance of soil availability of N, pH, moisture content and total soil carbon in acid and alkaline activities has also been suggested ([8], [47], [16], [18]). In our study, there were significant correlations between the above enzyme activities and OM, TN, pH and CaCO3. Highest acid and alkaline phosphatase activity from Tarkin in both seasons was likely due to the higher amount of OM and TN in this site.

  Conclusion 

Wild service tree is a rare species in the northern forest of Iran. This species is important due to its economic and ecological value. Our results revealed that different soil chemical properties did not have significant effect on root colonization and spore density in the studied sites. Despite the strong differences in site conditions, our results revealed that up to 68% of roots of wild service trees could be colonized by AMF. Since this species is tolerant to direct sunlight and short-time water deficits, the use of wild service trees colonized by AMF could help in afforestation plans, particularly in arid areas.

  Acknowledgements 

We would like to thank the staff of Iranian forest, range and watershed organization. This study was partly supported by University of Tehran.

  References

(1)
Amaya-Carpio L, Davies FTJr, Fox T, He C (2009). Arbuscular mycorrhizal fungi and organic fertilizer influence photosynthesis, root phosphatase activity, nutrition, and growth of Ipomoea carnea ssp. fistulosa. Photosynthetica 47 (1): 1-10.
CrossRef | Gscholar
(2)
Barea JM, Palenzuela J, Cornejo P, Sánchez-Castro I, Navarro- Fernández C, Lopéz-arcía A, Estrada B, Azcón R, Ferrol N, Azcón-Aguilar C (2011). Ecological and functional roles of mycorrhizas in semi-arid ecosystems of Southeast Spain. Journal of Arid Environments 75 (12): 1292-1301.
CrossRef | Gscholar
(3)
Basumatary A, Bordoloi PK (1992). Forms of potassium in some soils of Assam in relation to soil properties. Journal of the Indian Society of Soil Science 40 (3): 443-446.
Gscholar
(4)
Becerra GA, Cabello M, Zak RM, Bartoloni N (2009). Arbuscular mycorrhizae of dominant plant species in Yungas forests, Argentina. Mycologia 101 (5): 612-621.
CrossRef | Gscholar
(5)
Bremner JM, Mulvaney CS (1982). Nitrogen total. In: “Method of soil analysis - part 2: chemical and microbiological methods (2nd edn)” (Miller RH, Kieney DR eds). Agronomy series no. 9, American Society for Agronomy and Soil Sciences, Madison, WI, USA, pp. 595-624.
Gscholar
(6)
Closa I, Goicoechea N (2011). Infectivity of arbuscular mycorrhizal fungi in naturally regenerating, unmanaged and clear-cut beech forests. Pedosphere 21 (1): 65-74.
CrossRef | Gscholar
(7)
Dai W, Huang Y (2006). Relation of soil organic matter concentration to climate and altitude in zonal soils of China. Catena 65: 87-94.
CrossRef | Gscholar
(8)
Dick WA, Cheng L, Wang P (2000). Soil acid and alkaline phosphatase activity as pH adjustment indicators. Soil Biology and Biochemistry 32 (13): 1915-1919.
CrossRef | Gscholar
(9)
Dick WA, Tabatabai MA (1984). Kinetic parameters of phosphatases in soils and organic waste materials. Soil Science 137 (1): 7-15.
CrossRef | Gscholar
(10)
Gai JP, Tian H, Yang FY, Christie P, Li XL, Klironomos JN (2012). Arbuscular mycorrhizal fungal diversity along a Tibetan elevation gradient. Pedobiologia 55: 145- 151.
Gscholar
(11)
Gairola S, Sharma CM, Ghildiyal SK, Suyal S (2012). Chemical properties of soils in relation to forest composition in moist temperate valley slopes of Garhwal Himalaya, India. The Environmentalist 32 (4): 512-523.
CrossRef | Gscholar
(12)
Gerdemann J, Nicolson T (1963). Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Transactions of the British Mycological Society 46 (2): 235-244.
CrossRef | Gscholar
(13)
Giovannetti M, Mosse B (1980). An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytologist 84 (3): 489-500.
CrossRef | Gscholar
(14)
Griffiths RP, Madritch MD, Swanson AK (2009). The effects of topography on forest soil characteristics in the Oregon Cascade Mountains (USA): implications for the effects of climate change on soil properties. Forest Ecology and Management 257 (1): 1-7.
CrossRef | Gscholar
(15)
Guilford JP (1973). Fundamental statistics in psychology and education. McGraw-Hill, New York, USA, pp. 546.
Gscholar
(16)
Hamman ST, Burke IC, Knapp EE (2008). Soil nutrients and microbial activity after early and late season prescribed burns in a Sierra Nevada mixed conifer forest. Forest Ecology and Management 256 (3): 367-374.
CrossRef | Gscholar
(17)
Hisinger P (2001). Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant and Soil 237 (2): 173-195.
CrossRef | Gscholar
(18)
Hrynkiewicz K, Baum C, Leinweber P (2009). Mycorrhizal community structure, microbial biomass P and phosphatase activities under Salix polaris as influenced by nutrient availability. European Journal of Soil Biology 45 (2): 168-175.
CrossRef | Gscholar
(19)
Huang H, Zhang S, Wu N, Luo L, Christie P (2009). Influence of Glomus etunicatum / Zea mays mycorrhiza on atrazine degradation, soil phosphatase and dehydrogenase activities, and soil microbial community structure. Soil Biology and Biochemistry 41 (4): 726-734.
CrossRef | Gscholar
(20)
Isobe K, Aizawa E, Iguchi Y, Ishii R (2007). Distribution of arbuscular mycorrhizal fungi in upland field soils of Japan. 1. Relationship between spore density and the soil environmental factor. Plant Production Science 10 (1): 122-128.
CrossRef | Gscholar
(21)
Kane ES, Valentine DW, Schuur EA, Dutta K (2005). Soil carbon stabilization along climate and stand productivity gradients in black spruce forests of interior Alaska. Canadian Journal of Forest Research 35 (9): 2118-2129.
CrossRef | Gscholar
(22)
Kirschbaum MUF (1995). The temperature dependence of soil organic matter decomposition, and the effect of global warming on soil organic storage. Soil Biology and Biochemistry 27 (6): 753-760.
CrossRef | Gscholar
(23)
Kivlin SN, Hawkes CV, Treseder KK (2011). Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biology and Biochemistry 43 (11): 2294-2303.
CrossRef | Gscholar
(24)
Labidi S, Calonne M, Ben JF, Debiane D, Rezgui S, Laruelle F, Tisserant B, Ferjani GA, Lounès HSA (2011). Calcareous impact on arbuscular mycorrhizal fungus development and on lipid peroxidation in monoxenic roots. Phytochemistry 72: 2335-2341.
CrossRef | Gscholar
(25)
Li LF, Yang AN, Zhao ZW (2005). Seasonality of arbuscular mycorrhizal symbiosis and dark septate endophytes in a grassland site in southwest China. FEMS Microbiology Ecology 54: 367-373.
CrossRef | Gscholar
(26)
Liu J, Wu L, Wei S, Xiao X, Su C, Jiang P, Song Z, Wang T, Yu Z (2007). Effects of arbuscular mycorrhizal fungi on the growth, nutrient uptake and glycyrrhizin production of licorice (Glycyrrhiza uralensis Fisch). Plant Growth Regulation 52 (1): 29-39.
CrossRef | Gscholar
(27)
Marschner H, Dell B (1994). Nutrient uptake in mycorrhizal symbiosis. Plant and Soil 59: 89-102.
Online | Gscholar
(28)
Matevz L, Katarina H, Tomislav R, Marjana R (2013). Distribution and diversity of arbuscular mycorrhizal fungi in grapevines from production vineyards along the eastern Adriatic coast. Mycorrhiza 23 (3): 209-219.
CrossRef | Gscholar
(29)
Mendoza RE, Goldmann V, Rivas J, Escudero V, Pagani E, Collantes MB, Marbán L (2002). Arbuscular mycorrhizal fungi populations in relationship with soil properties and host plant in grasslands of Tierra del Fuego. Ecologia Austral 12: 105-116.
Gscholar
(30)
Minggui G, Ming T, Qiaoming Z, Xinxin F (2012). Effects of climatic and edaphic factors on arbuscular mycorrhizal fungi in the rhizosphere of Hippophae rhamnoides in the Loess Plateau, China. Acta Ecologica Sinica 32 (2): 62-67.
CrossRef | Gscholar
(31)
Moreira M, Baretta D, Mui TS, Cardoso EJBN (2006). Spore density and root colonization by arbuscular mycorrhizal fungi in preserved or disturbed Araucaria angustifolia (Bert.) O. Ktze. ecosystems. Scientia Agricola 63 (4): 380-385.
CrossRef | Gscholar
(32)
Morwin HD, Peach PM (1951). Exchangeability of soil potassium in and, silt and clay fractions as influenced by the nature of complementary exchangeable cations. Soil Science Society of America Journal 15: 125-128.
CrossRef | Gscholar
(33)
Motosugi H, Yamamoto Y, Naruo T, Kitabyashi H, Ishi T (2002). Comparison of the growth and leaf mineral concentrations between three grapevine rootstocks and their corresponding tetraploids inoculated with an arbuscular mycorrhizal fungus Gigaspora margarita. Vitis 41:21-25.
Online | Gscholar
(34)
Muthukumar T, Sha LQ, Yang XD, Cao M, Tang JW, Zheng Z (2003). Distribution of roots and arbuscular mycorrhizal associations in tropical forest types of Xishuangbanna, southwest China. Applied Soil Ecology 22 (3): 241-253.
CrossRef | Gscholar
(35)
Nicolescu VN, Hochbichler E, Coello Gomez J, Ravagni S, Giulietti V (2009). Ecology and silviculture of wild service tree (Sorbus torminalis (L.) Crantz): a literature review. Die Bodenkultur 60 (3): 35-44.
Online | Gscholar
(36)
Ohlinger R (1996). Acid and alkaline phosphomonoesterase activity with the substrate p-nitrophenyl phosphate. In: “Methods in Soil Biology” (Schinner F, Kandeler E, Ohlinger R, Margesin RE eds). Springer-Verlag, Berlin, Germany, pp. 210-214.
Gscholar
(37)
Olsen SR, Cole CV, Watanabe FS, Dean LA (1954). Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circular 939: 1-19.
Gscholar
(38)
Paganová V (2008). Ecological requirements of wild service tree (Sorbus torminalis [L.] Crantz.) and service tree (Sorbus domestica L.) in relation with their utilization in forestry and landscape. Journal of Forest Science 54 (5): 216-226.
Gscholar
(39)
Paudel S, Sah JP (2003). Physiochemical characteristics of soil in tropical Sal (S. robusta Gaertn) forest in eastern Nepal. Himalayan Journal of Sciences 1 (2): 107-110.
Online | Gscholar
(40)
Phillips JM, Hayman DS (1970). Improved procedures for clearing and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55 (1): 158-161.
CrossRef | Gscholar
(41)
Pourmajidian M (2000). A study on the silvicultural characteristics and reproduction methods of Sorbus torminalis (L.) Crantz in western Mzandaran (Iran). PhD thesis, University of Tarbiyat Modares, Tehran, Iran, pp. 257.
Gscholar
(42)
Quideau SA (2002). Organic matter accumulation. In: “Encyclopedia of Soil Science”. Marcel Dekker Inc., New York, USA, pp. 891-894.
Gscholar
(43)
Raspe O, Findlay C, Jacquemart AL (2000). Sorbus aucuparia L. Journal of Ecology 88 (5): 910-930.
CrossRef | Gscholar
(44)
Redecker D, Kodner R, Graham LE (2000). Glomalean fungi from the Ordovician. Science 289: 1920-1921.
CrossRef | Gscholar
(45)
Rodriguez-Echeverria S, Gera Hol WH, Freitas H, Eason WR, Cook R (2008). Arbuscular mycorrhizal fungi of Ammophila arenaria (L.) Link: Spore abundance and root colonization in six locations of the European coast. European Journal of Soil Biology 44 (1): 30-36.
CrossRef | Gscholar
(46)
Rooney DC, Prosser JI, Bending GD, Baggs EM, Killham K, Hodge A (2011). Effect of arbuscular mycorrhizal colonisation on the growth and phosphorus nutrition of Populus euramericana c.v. Ghoy. Biomass and Bioenergy 35 (11): 4605-4612.
CrossRef | Gscholar
(47)
Sardans J, Penuelas J, Ogaya R (2008). Experimental drought reduced acid and alkaline phosphatase activity and increased organic extractable P in soil in a Quercus ilex Mediterranean forest. European Journal of Soil Biology 44 (5-6): 509-520.
CrossRef | Gscholar
(48)
Smith SE, Read DJ (1997). Mycorrhizal symbiosis (2nd ed). Academic Press, San Diego, USA, pp. 605.
Gscholar
(49)
Smith SE, Read DJ (2008). Mycorrhizal symbiosis. Academic Press Inc., London, UK, pp. 800.
Gscholar
(50)
Smith SE, Smith, FA, Jakobsen I (2003). Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiology 133 (1): 16-20.
CrossRef | Gscholar
(51)
Thonar C, Schnepf A, Frossard E, Roose T, Jansa J (2011). Traits related to differences in function among three arbuscular mycorrhizal fungi. Plant and Soil 339 (1-2): 231-245.
CrossRef | Gscholar
(52)
Treseder KK (2004). A meta-analysis of mycorrhizal responses to nitrogen, phosphorus and atmospheric CO2 in field studies. New Phytologist 164 (2): 347-355.
CrossRef | Gscholar
(53)
Van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998). Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396 (6706): 69-72.
CrossRef | Gscholar
(54)
Walkley A, Black IA (1934). An examination of the Degtjareff method for determining organic carbon in soils: effect of variations in digestion conditions and of inorganic soil constituents. Soil Science 63 (4): 251-264.
CrossRef | Gscholar
(55)
Waltert B, Wiemken V, Rusterholz H., Boller T, Baur B (2002). Disturbance of forest by trampling: effects on mycorrhizal roots of seedlings and mature trees of Fagus sylvatica. Plant and Soil 243 (2): 143-154.
CrossRef | Gscholar
(56)
Wu Q, Zou YN, He XH (2011). Differences of hyphal and soil phosphatase activities in drought-stressed mycorrhizal trifoliate orange (Poncirus trifoliata) seedlings. Scientia Horticulturae 129: 294-298.
CrossRef | Gscholar
(57)
Xu P, Christie P, Liu Y, Zhang J, Li X (2008). The arbuscular mycorrhizal fungus Glomus mosseae can enhance arsenic tolerance in Medicago truncatula by increasing plant phosphorus status and restricting arsenate uptake. Environmental Pollution 156 (1): 215-220.
CrossRef | Gscholar
(58)
Yong SZ, Chao ZC, Yun LZ, Gu F, Peter C, Yan CT, Lin XL (2007). Diversity and zonal distribution of arbuscular mycorrhizal fungi on the northern slopes of the Tianshan Mountains. Sci China Ser D-Earth Sci 50: 135-141.
Gscholar
(59)
Zhao J, Dong Y, Xie X, Li X, Zhang X, Shen X (2011). Effect of annual variation in soil pH on available soil nutrients in pear orchards. Acta Ecologica Sinica 31 (4): 212-216.
CrossRef | Gscholar

Authors’ Affiliation

(1)
Mostafa Moradi
Anoshirvan Shirvany
Vahid Etemad
Samira Sayah
Department of Forestry, Faculty of Natural Resources, University of Tehran, Karaj (Iran)
(2)
Mohammad Matinizadeh
Research Institute of Forests and Rangelands, Tehran (Iran)
(3)
Hamid Reza Naji
Hazandy Abdul-Hamid
Institute of Tropical Forestry and Forest Products (INTROP), Universiti Putra Malaysia (UPM), Serdang, Selangor (Malaysia)

Corresponding author

 
Mostafa Moradi
moradi4@gmail.com

Citation

Moradi M, Shirvany A, Matinizadeh M, Etemad V, Naji HR, Abdul-Hamid H, Sayah S (2015). Arbuscular mycorrhizal fungal symbiosis with Sorbus torminalis does not vary with soil nutrients and enzyme activities across different sites. iForest 8: 308-313. - doi: 10.3832/ifor1236-008

Academic Editor

Gianfranco Minotta

Paper history

Received: Jan 06, 2014
Accepted: May 24, 2014

First online: Sep 03, 2014
Publication Date: Jun 01, 2015
Publication Time: 3.40 months

© SISEF - The Italian Society of Silviculture and Forest Ecology 2015

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