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Arbuscular mycorrhizal fungi ameliorate the chemical properties and enzyme activities of rhizosphere soil in reclaimed mining subsidence in northwestern China

Journal of Arid Land volume 11, pages 135–147 (2019)Cite this article

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<0.05), 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<0.05) 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.

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References

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Bao S D. 1998. Soil Agricultural and Chemical Analysis. Beijing: China Agriculture Press, 56–83. (in Chinese)

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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)

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Giovannetti M, Mosse B. 1980. An evaluation of technique for measuring vesicular-arbuscular mycorrhizae infection in roots. New Phytologist, 84(3): 489–500.

    Article  Google Scholar 

  • Guan S Y. 1996. Soil Enzymes and Research Methods. Beijing: China Agriculture Press, 274–321. (in Chinese)

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Rillig M C. 2004. Arbuscular mycorrhizae, glomalin, and soil aggregation. Canadian Journal of Soil Science, 84(4): 355–363.

    Article  Google Scholar 

  • Rillig M C, Mummey D L. 2006. Mycorrhizas and soil structure. New Phytologist, 171(1): 41–53.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Sanâa 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Veresoglou S D, Chen B D, Rillig M C. 2012. Arbuscular mycorrhiza and soil nitrogen cycling. Soil Biology & Biochemistry, 46: 53–62.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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)

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

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Acknowledgements

The study was funded by the National Natural Science Foundation of China (51574253), the National High Technology Research and Development Program of China (2013AA102904), and the Open Research Project of the State Key Laboratory of Coal Resources and Safe Mining, China University of Mining and Technology (Beijing) (SKLCRSM16KFA01).

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  1. The first and second authors contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Coal Resources and Safe Mining, China University of Mining and Technology (Beijing), Beijing, 100083, China

    Lang Qiu, Yinli Bi, Bin Jiang, Zhigang Wang & Yanxu Zhang

  2. College of Geoscience and Surveying Engineering, China University of Mining and Technology (Beijing), Beijing, 100083, China

    Lang Qiu, Yinli Bi, Bin Jiang, Zhigang Wang & Yanxu Zhang

  3. Satbayev University, Almaty, 050013, Kazakhstan

    Yryszhan Zhakypbek

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  1. Lang Qiu
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  2. Yinli Bi
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  4. Zhigang Wang
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Correspondence to Yinli Bi.

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Qiu, L., Bi, Y., Jiang, B. et al. Arbuscular mycorrhizal fungi ameliorate the chemical properties and enzyme activities of rhizosphere soil in reclaimed mining subsidence in northwestern China. J. Arid Land 11, 135–147 (2019). https://doi.org/10.1007/s40333-018-0019-9

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Keywords

  • revegetation
  • mycorrhizal colonization
  • glomalin-related soil proteins
  • arbuscular mycorrhizal fungi
  • coal mining
  • Amorpha fruticose