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Journal of Arid Land  2019, Vol. 11 Issue (1): 135-147    DOI: 10.1007/s40333-018-0019-9
Orginal Article     
Arbuscular mycorrhizal fungi ameliorate the chemical properties and enzyme activities of rhizosphere soil in reclaimed mining subsidence in northwestern China
Lang QIU1,2, Yinli BI1,2,*(), Bin JIANG1,2, Zhigang WANG1,2, Yanxu ZHANG1,2, ZHAKYPBEK Yryszhan3
1 State Key Laboratory of Coal Resources and Safe Mining, China University of Mining and Technology (Beijing), Beijing 100083, China
2 College of Geoscience and Surveying Engineering, China University of Mining and Technology (Beijing), Beijing 100083, China
3 Satbayev University, Almaty 050013, Kazakhstan
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Abstract  

In semi-arid region of northwestern China, underground mining subsidence often results in decreased vegetation coverage, impoverishment of soil fertility and water stress. In addition, the physical-chemical and biological properties of soil also change, resulting in more susceptible to degradation. In particular, subsidence causes disturbance of the symbioses of plant and microbe that can play a beneficial role in the establishment of vegetation communities in degraded ecosystems. The objective of this study was to evaluate the effects of revegetation with exotic arbuscular mycorrhizal fungi (AMF) inoculum on the chemical and biological properties of soil over time in mining subsidence areas. Soils were sampled at a depth up to 30 cm in the adjacent rhizosphere of Amorpha fruticose Linn. from five reclaimed vegetation communities in northwestern China. In August 2015, a field trial was set up with five historical revegetation experiments established in 2008 (7-year), 2011 (4-year), 2012 (3-year), 2013 (2-year) and 2014 (1-year), respectively. Each reclamation experiment included two treatments, i.e., revegetation with exotic AMF inoculum (AMF) and non-AMF inoculum (the control). Root mycorrhizal colonization, glomalin-related soil protein (GRSP), soil organic carbon (SOC), soil nutrients, and enzyme activities were also assessed. The results showed that mycorrhizal colonization of inoculated plants increased by 33.3%-163.0% compared to that of non-inoculated plants (P<0.05). Revegetation with exotic AMF inoculum also significantly improved total GRSR (T-GRSP) and easily extracted GRSP (EE-GRSP) concentrations compared to control, besides the T-GRSP in 1-year experiment and the EE-GRSP in 2-year experiment. A significant increase in SOC content was only observed in 7-year AMF reclaimed soils compared to non-AMF reclaimed soils. Soil total N (TN), Olsen phosphorus (P) and available potassium (K) were significantly higher in inoculated soil after 1-7 years of reclamation (except for individual cases), and increased with reclamation time (besides soil Olsen P). The exotic AMF inoculum markedly increased the average soil invertase, catalase, urease and alkaline phosphatase by 23.8%, 21.3%, 18.8% and 8.6%, respectively (P<0.01), compared with the control. Root mycorrhizal colonization was positively correlated with soil parameters (SOC, TN and soil available K) and soil enzyme activities (soil invertase, catalase, urease and alkaline phosphatase) in both AMF and non-AMF reclaimed soils (P<0.05), excluding available K in non-AMF reclaimed soils. T-GRSP (P<0.01) and EE-GRSP (P<0.05) were significantly correlated with the majority of edaphic factors, except for soil Olsen P. The positive correlation between root mycorrhizal colonization and available K was observed in AMF reclaimed soils, indicating that the AMF reclaimed soil with a high root mycorrhizal colonization could potentially accumulate available K in soils. Our findings concluded that revegetation with exotic AMF inoculum influenced soil nutrient availability and enzyme activities in the semi-arid ecosystem, suggesting that inoculating AMF can be an effective method to improve soil fertility and support restoration of vegetation communities under poor conditions like soil nutrient deficiency and drought.



Key wordsrevegetation      mycorrhizal colonization      glomalin-related soil proteins      arbuscular mycorrhizal fungi      coal mining      Amorpha fruticose     
Received: 01 August 2017      Published: 10 February 2019
Corresponding Authors:
Cite this article:

Lang QIU, Yinli BI, Bin JIANG, Zhigang WANG, Yanxu ZHANG, ZHAKYPBEK Yryszhan. Arbuscular mycorrhizal fungi ameliorate the chemical properties and enzyme activities of rhizosphere soil in reclaimed mining subsidence in northwestern China. Journal of Arid Land, 2019, 11(1): 135-147.

URL:

http://jal.xjegi.com/10.1007/s40333-018-0019-9     OR     http://jal.xjegi.com/Y2019/V11/I1/135

[1] Aroca R, Porcel R, Ruiz-Lozano J M.2007. How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytologist, 173(4): 808-816.
[2] Azcón R, Barea J.1998. Mycorrhizal dependency of a representative plant species in Mediterranean shrublands (Lavandula spica L.) as a key factor to its use for revegetation strategies in desertification-threatened areas. Applied Soil Ecology, 7(1): 83-92.
[3] Bai C M, He X L, Tang H L, et al.2009. Spatial distribution of arbuscular mycorrhizal fungi, glomalin and soil enzymes under the canopy of Astragalus adsurgens Pall. in the Mu Us sandland, China. Soil Biology & Biochemistry, 41(5): 941-947.
[4] Bao S D.1998. Soil Agricultural and Chemical Analysis. Beijing: China Agriculture Press, 56-83. (in Chinese)
[5] Barea J M, Palenzuela J, Cornejo P, et al.2012. Ecological and functional roles of mycorrhizas in semi-arid ecosystems of Southeast Spain. Journal of Arid Environments, 75(12): 1292-1301.
[6] Bárzana G, Aroca R, Bienert G P, et al.2014. New insights into the regulation of aquaporins by the arbuscular mycorrhizal symbiosis in maize plants under drought stress and possible implications for plant performance. Molecular Plant-microbe Interactions, 27(4): 349-363.
[7] Bell F G, Stacey T R, Genske D D.2000. Mining subsidence and its effect on the environment some differing examples. Environmental Geology, 40(1-2): 135-152.
[8] Bheemareddy V S, Lakshman H C.2011. Effect of AM fungus Glomus fasciculatum on metabolite accumulation in four varieties of Triticum aestivum L. under short-term water stress. Vegetos, 24(1): 41-49.
[9] Bi Y L, Li X L, Christie P, et al.2003. Growth and nutrient uptake of arbuscular mycorrhizal maize in different depths of soil overlying coal fly ash. Chemosphere, 50(6): 863-869.
[10] Bi Y L, Wang J, Feng Y B, et al.2014. Effect of arbuscular mycorrhiza on root self-repairing action of Amorpha fruticose L. in coal mining subsidence land in arid areas. Journal of China Coal Society, 39(8): 1758-1764. (in Chinese)
[11] Bird S B, Herrick J E, Wander M M, et al.2002. Spatial heterogeneity of aggregate stability and soil carbon in semi-arid rangeland. Environmental Pollution, 116(3): 445-455.
[12] Bonanomi G, Chirico G B, Palladino M, et al.2017. Combined application of photo-selective mulching films and beneficial microbes affects crop yield and irrigation water productivity in intensive farming systems. Agricultural Water Management, 184: 104-113.
[13] Caravaca F, Alguacil M M, Figueroa D, et al.2003. Re-establishment of Retama sphaerocarpa as a target species for reclamation of soil physical and biological properties in a semi-arid Mediterranean area. Forest Ecology and Management, 182: 49-58.
[14] Chen Y F, Yu F H, Dong M.2002. Scale-dependent spatial heterogeneity of vegetation in Mu Us sandy land, a semi-arid area of China. Plant Ecology, 162(1): 135-142.
[15] Cheng, X, An S, Chen J, et al.2007. Spatial relationships among species, above-ground biomass, N, and P in degraded grasslands in Ordos Plateau, northwestern China. Journal of Arid Environments, 68: 652-667.
[16] Conesa H M, García G, Faz á, et al.2007. Dynamics of metal tolerant plant communities' development in mine tailings from the Cartagena-La Unión Mining District (SE Spain) and their interest for further revegetation purposes. Chemosphere, 68(6): 1180-1185.
[17] Cumming J R, Ning J C.2003. Arbuscular mycorrhizal fungi enhance aluminium resistance of broomsedge (Andropogon virginicus L.). Journal of Experimental Botany, 54(386): 1447-1459.
[18] Franzluebbers A J, Wright S F, Stuedemann J A.2000. Soil aggregation and glomalin under pastures in the Southern Piedmont USA. Soil Science Society of America Journal, 64(3): 1018-1026.
[19] Giovannetti M, Mosse B.1980. An evaluation of technique for measuring vesicular-arbuscular mycorrhizae infection in roots. New Phytologist, 84(3): 489-500.
[20] Guan S Y.1996. Soil Enzymes and Research Methods. Beijing: China Agriculture Press, 274-321. (in Chinese)
[21] Habibzadeh Y, Pirzad A, Zardashti M R, et al.2013. Effects of arbuscular mycorrhizal fungi on seed and protein yield under water-deficit stress in mung bean. Agronomy Journal, 105(1): 79-84.
[22] Haddad M J, Sarkar D.2003. Glomalin, a newly discovered component of soil organic matter: Part II Relationship with soil properties. Environmental Geosciences, 10(3): 99-106.
[23] He X L, Li Y P, Zhao L L.2010. Dynamics of arbuscular mycorrhizal fungi and glomalin in the rhizosphere of Artemisia ordosica Krasch. in Mu Us sandland, China. Soil Biology & Biochemistry, 42(8): 1313-1319.
[24] Lazcano C, Barrios-Masias F H, Jackson L E.2014. Arbuscular mycorrhizal effects on plant water relations and soil greenhouse gas emissions under changing moisture regimes. Soil Biology & Biochemistry, 74: 184-192.
[25] Lei S G, Bian Z F, Daniels J L, et al.2010. Spatio-temporal variation of vegetation in an arid and vulnerable coal mining region. Mining Science and Technology, 20(3): 485-490.
[26] Levy M A, Cumming J R.2014. Development of soils and communities of plants and arbuscular mycorrhizal fungi on West Virginia surface mines. Environmental Management, 54(5): 1153-1162.
[27] Li S P, Bi Y L, Kong W P, et al.2015. Effects of arbuscular mycorrhizal fungi on ecological restoration in coal mining areas. Russian Journal of Ecology, 46(5): 431-437.
[28] Li Y Y, Chen LQ, Wen H Y, et al.454 pyrosequencing analysis of bacterial diversity revealed by a comparative study of soils from mining subsidence and reclamation areas. Journal of Microbiology and Biotechnology, 24(3): 313-323.
[29] Liu H L, Tan Y, Nell M, et al.2014. Arbuscular mycorrhizal fungal colonization of Glycyrrhiza glabra roots enhances plant biomass, phosphorus uptake and concentration of root secondary metabolites. Journal of Arid Land, 6(2): 186-194.
[30] Marcin C, Maria N.2010. The effect of different tree species on the chemical and microbial properties of reclaimed mine soils. Biology and Fertility of Soils, 46(6): 555-566.
[31] Marschner P, Baumann K.2003. Changes in bacterial community structure induced by mycorrhizal colonisation in split-root maize. Plant and Soil, 251(2): 279-289.
[32] Marulanda A, Azcón R, Ruiz-Lozano J M.2003. Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa plants under drought stress. Physiologia Plantarum, 119(4): 526-533.
[33] Orwin K H, Kirschbaum M U, St John M G, et al.2011. Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: a model-based assessment. Ecology Letters, 14(5): 493-502.
[34] Pereira R, Marques S M, Antunes S C, et al.2008. Comparison of portuguese soils from different geographical regions using physicochemical, biological and biochemical parameters. Journal of Soils and Sediments, 8(2): 106-115.
[35] Phillips J M, Hayman D S.1970. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society, 55(1): 158-161.
[36] Qi Y B, Yang F Q, Shukla M K, et al.2015. Desert soil properties after thirty years of vegetation restoration in Northern Shaanxi Province of China. Arid Land Research and Management, 29(4): 454-472.
[37] Read D J, Leake J R, Perez-Moreno J.2004. Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes. Canadian Journal of Botany, 82(8): 1243-1263.
[38] Requena N, Perez-Solis E, Azcón-Aguilar C, et al.2001. Management of indigenous plant-microbe symbioses aids restoration of desertified ecosystems. Applied and Environmental Microbiology, 67(2): 495-498.
[39] Rillig M C.2004. Arbuscular mycorrhizae, glomalin, and soil aggregation. Canadian Journal of Soil Science, 84(4): 355-363.
[40] Rillig M C, Mummey D L.2006. Mycorrhizas and soil structure. New Phytologist, 171(1): 41-53.
[41] Rillig M C, Steinberg P D.2002. Glomalin production by an arbuscular mycorrhizal fungus: a mechanism of habitat modification? Soil Biology & Biochemistry, 34(9): 1371-1374.
[42] Sanaa W, Tasnime M, Mohamed H, et al.2016. Enhanced transfer of biologically fixed N from faba bean to intercropped wheat through mycorrhizal symbiosis. Applied Soil Ecology, 107: 91-98.
[43] Sheoran V, Sheoran A S, Poonia P.2010. Soil reclamation of abandoned mine land by revegetation: a review. International Journal of Soil, Sediment and Water, 3(2): 1-20.
[44] Shrestha R K, Lal R.2011. Changes in physical and chemical properties of soil after surface mining and reclamation. Geoderma, 161(3-4): 168-176.
[45] Sidle R C, Kamil I, Sharma A, et al.2000. Stream response to subsidence from underground coal mining in central Utah. Environmental Geology, 39(3-4): 279-291.
[46] Singh B K, Nunan N, Ridgway K P, et al.2008. Relationship between assemblages of mycorrhizal fungi and bacteria on grass roots. Environmental Microbiology, 10(2): 534-541.
[47] Smith F A, Jakobsen I, Smith S E.2000. Spatial differences in acquisition of soil phosphate between two arbuscular mycorrhizal fungi in symbiosis with Medicago truncatula. New Phytologist, 147(2): 357-366.
[48] Taheri W I, Bever J D.2010. Adaptation of plants and arbuscular mycorrhizal fungi to coal tailings in Indiana. Applied Soil Ecology, 45(3): 138-143.
[49] Taheri W I, Bever J D.2011. Adaptation of Liquidambar styraciflua to coal tailings is mediated by arbuscular mycorrhizal fungi. Applied Soil Ecology, 48(2): 251-255.
[50] Vázquez M M, César S, Azcón R, et al.2000. Interactions between arbuscular mycorrhizal fungi and other microbial inoculants (Azospirillum, Pseudomonas, Trichoderma) and their effects on microbial population and enzyme activities in the rhizosphere of maize plants. Applied Soil Ecology, 15(3): 261-272.
[51] Veresoglou S D, Chen B D, Rillig M C.2012. Arbuscular mycorrhiza and soil nitrogen cycling. Soil Biology & Biochemistry, 46: 53-62.
[52] Wang Z G, Bi Y L, Jiang B, et al.2016. Arbuscular mycorrhizal fungi enhance soil carbon sequestration in the coalfields, northwest China. Scientific Reports, 6: 34336.
[53] White J A, Tallaksen J, Charvat I.2008. The effects of arbuscular mycorrhizal fungal inoculation at a roadside prairie restoration site. Mycologia, 2008: 100(1): 6-11.
[54] Wright S F, Upadhyaya A.1996. Extraction of an abundant and usual protein from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi. Soil Science, 161(9): 575-586.
[55] Xu Q F, Jiang P K, Wang H L.2009. Improvement of biochemical and biological properties of eroded red soil by artificial revegetation. Journal of Soils and Sediments, 10(2): 255-262.
[56] Yang D J, Bian Z F, Lei S G.2016. Impact on soil physical qualities by the subsidence of coal mining: a case study in Western China. Environmental Earth Sciences, 75: 652.
[57] Yu M, Bi Y L, Zhang C Q.2013. Lasting improvement effects of arbuscular mycorrhizal fungi and Bradyrhizobium japonicum on rhizosphere soil environment in mining subsidence. Transactions of the Chinese Society of Agricultural Engineering, 29(8): 242-248. (in Chinese)
[58] Zhang F W, Song Y X, Zhao H M, et al.2012. Changes of precipitation infiltration recharge in the circumstances of coal mining subsidence in the Shen-Dong Coal Field, China. Acta Geologica Sinica (English Edition), 86(4): 993-1003.
[59] Zhang T, Tian C Y, Sun Y, et al.2012. Dynamics of arbuscular mycorrhizal fungi associated with desert ephemeral plants in Gurbantunggut Desert. Journal of Arid Land, 4(1): 43-51.
[60] Zhang X K, Wu X, Zhang S X, et al.2014. Organic amendment effects on aggregate-associated organic C, microbial biomass C and glomalin in agricultural soils. Catena, 123: 188-194.
[61] Zhao R X, Guo W, Bi N, et al.2015. Arbuscular mycorrhizal fungi affect the growth, nutrient uptake and water status of maize (Zea mays L.) grown in two types of coal mine spoils under drought stress. Applied Soil Ecology, 88: 41-49.
[62] Zhao Z Q, Shahrour I, Bai Z K, et al.2013. Soils development in opencast coal mine spoils reclaimed for 1-13 years in the West-Northern Loess Plateau of China. European Journal of Soil Biology, 55: 40-46.
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