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Journal of Integrative Agriculture  2022, Vol. 21 Issue (10): 3051-3066    DOI: 10.1016/j.jia.2022.07.045
Special Issue: 农业生态环境-土壤微生物合辑Agro-ecosystem & Environment—Soil microbe
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Indigenous arbuscular mycorrhizal fungi play a role in phosphorus depletion in organic manure amended high fertility soil

HUO Wei-ge1, CHAI Xiao-fen1, WANG Xi-he2, William David BATCHELOR3, Arjun KAFLE4, FENG Gu1

College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, P.R.China

Research Institute of Soil, Fertilizer and Agricultural Water Conservation, Xinjiang Academy of Agricultural Sciences, Urumqi 830091, P.R.China   

Biosystems Engineering Department, Auburn University, AL 36849, USA

Department of Crop and Soil Sciences, North Carolina State University, NC 27695, USA

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摘要  集约化农业生产的土壤中含有丰富的AM真菌种类和孢子数目。以往的研究表明,在低磷条件下AM真菌能够提高作物的磷吸收,但在高磷土壤中AM真菌是否依然发挥着作用并不清楚。在本文中,我们原位研究了长期高磷肥投入的农田中,土著AM真菌是否对P的利用依然有贡献。我们设计了菌丝室装置,通过在PVC管两端分别密封不同孔径的膜(30 或 0.45 µm),允许或阻止菌丝穿透尼龙膜,进入菌丝室,并阻止棉花根系的进入。我们用土壤速效磷(Olsen-P)的耗竭来表征土著AMF对磷的吸收。结果表明,土著AMF能够介导磷的耗竭和微生物量磷(MBP)的周转,并且在高磷条件下(Olsen-P: 78.29 mg kg-1),速效磷的耗竭和MBP的周转率最大;不同施肥处理的棉花根内定殖着特有的AM真菌群落,且Glomus 和 Paraglomus占主导地位,暗示了长期的施肥能够驯化AM真菌群落。在本研究结果中,我们得出了即使在高磷条件下,土著AM真菌在土壤磷的耗竭和周转中依然发挥着重要作用。


The species richness and propagule number of arbuscular mycorrhizal fungi (AMF) are high in intensively-managed agricultural soils.  Past research has shown that AMF improve crop phosphorus (P) uptake under low soil P conditions, however it is unclear if AMF play a role in high Olsen-P soils.  In this study, we investigated whether native fungal benefits exist under high P input field conditions in-situ and contribute to P utilization.  We installed in-grow tubes which were sealed with different membrane pore sizes (30 or 0.45 µm) to allow or prevent AMF hyphae access to the hyphal compartment and prevent cotton roots from penetrating the chamber.  We used the depletion of soil available P (Olsen-P) in the hyphae accessed compartment to indicate P uptake by the native AMF community.  Our results showed that the native AMF mediated P depletion and microbial biomass P (MBP) turnover and caused the largest Olsen-P depletion ratio and MBP turnover ratio in the high P treatments (Olsen-P: 78.29 mg kg–1).  The cotton roots in each fertilization regime were colonized by a unique AMF community and Glomus and Paraglomus were the dominant genera, implying the long-term fertilization regimes domesticated the AMF community.  We conclude that native AMF caused the P depletion and P turnover even under high soil Olsen-P conditions.

Keywords:  arbuscular mycorrhizal fungi       phosphorus depletion       high P soil       Gossypium spp       indigenous community       mesh cores  
Received: 26 August 2021   Accepted: 25 November 2021
Fund: This study was financially supported by the Beijing Natural Science Foundation, China (6202015), the National Natural Science Foundation of China (U1703232) and the Hatch Project (ALA014-1-16016) funded by the National Institute of Food and Agriculture, US Department of Agriculture.
About author:  HUO Wei-ge, E-mail:; Correspondence FENG Gu, Tel: +86-10-62733885, E-mail:

Cite this article: 

HUO Wei-ge, CHAI Xiao-fen, WANG Xi-he, William David BATCHELOR, Arjun KAFLE, FENG Gu. 2022. Indigenous arbuscular mycorrhizal fungi play a role in phosphorus depletion in organic manure amended high fertility soil. Journal of Integrative Agriculture, 21(10): 3051-3066.

Abuduwaili J, Tang Y, Abulimiti M, Liu D, Ma L. 2012. Spatial distribution of soil moisture, salinity and organic matter in Manas River watershed, Xinjiang, China. Journal of Arid Land, 4, 441–449.
Aghili F, Jansa J, Khoshgoftarmanesh A H, Afyuni M, Schulin R, Frossard E, Gamper H A. 2014. Wheat plants invest more in mycorrhizae and receive more benefits from them under adverse than favorable soil conditions. Applied Soil Ecology, 84, 93–111.
Agnolucci M, Battini F, Cristani C, Giovannetti M. 2015. Diverse bacterial communities are recruited on spores of different arbuscular mycorrhizal fungal isolates. Biology and Fertility of Soils, 51, 379–389.
Altschul S F, Gish W, Miller W, Myers E W, Lipman D J. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.
Battini F, Gronlund M, Agnolucci M, Giovannetti M, Jakobsen I. 2017. Facilitation of phosphorus uptake in maize plants by mycorrhizosphere bacteria. Scientific Reports, 7, 4686.
Bowles T M, Barrios-Masias F H, Carlisle E A, Cavagnaro T R, Jackson L E. 2016. Effects of arbuscular mycorrhizae on tomato yield, nutrient uptake, water relations, and soil carbon dynamics under deficit irrigation in field conditions. Science of the Total Environment, 566, 1223–1234.
Brito I, Carvalho M, Goss M J. 2013. Soil and weed management for enhancing arbuscular mycorrhiza colonization of wheat. Soil Use and Management, 29, 540–546.
Brígido C, van Tuinen D, Brito I, Alho L, Goss M J, Carvalho M. 2017. Management of the biological diversity of AM fungi by combination of host plant succession and integrity of extraradical mycelium. Soil Biology & Biochemistry, 112, 237–247.
Brookes P C, Powlson D S, Jenkinson D S. 1982. Measurement of microbial biomass phosphorus in soil. Soil Biology & Biochemistry, 14, 319–329.
Buysens C, De Boulois H D, Declerck S. 2015. Do fungicides used to control Rhizoctonia solani impact the non-target arbuscular mycorrhizal fungus Rhizophagus irregularis? Mycorrhiza, 25, 277–288.
Bücher M. 2007. Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytologist, 173, 11–26.
Bünemann E K, Marschner P, McNeill A M, McLaughlin M J, Biochemistry. 2007. Measuring rates of gross and net mineralisation of organic phosphorus in soils. Soil Biology and Biochemistry, 39, 900–913.
Caporaso J G, Kuczynski J, Stombaugh J, Bittinger K, Bushman F D, Costello E K, Fierer N, Pena A G, Goodrich J K, Gordon J I, Huttley G A, Kelley S T, Knights D, Koenig J E, Ley R E, Lozupone C A, McDonald D, Muegge B D, Pirrung M, Reeder J, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7, 335–336.
Cely M V, De Oliveira A G, De Freitas V F, de Luca M B, Barazetti A R, Dos Santos I M, Gionco B, Garcia G V, Prete C E, Andrade G. 2016. Inoculant of arbuscular mycorrhizal fungi (Rhizophagus clarus) increase yield of soybean and cotton under field conditions. Frontiers in Microbiology, 7, 720.
Cheng Y, Ishimoto K, Kuriyama Y, Osaki M, Ezawa T. 2013. Ninety-year-, but not single, application of phosphorus fertilizer has a major impact on arbuscular mycorrhizal fungal communities. Plant and Soil, 365, 397–407.
Chu Q, Wang X X, Yang Y, Chen F J, Zhang F S, Feng G. 2013. Mycorrhizal responsiveness of maize (Zea mays L.) genotypes as related to releasing date and available P content in soil. Mycorrhiza, 23, 497–505.
Chu Q, Zhang L, Zhou J W, Yuan L X, Chen F J, Zhang F S, Feng G, Rengel Z. 2020. Soil plant-available phosphorus levels and maize genotypes determine the phosphorus acquisition efficiency and contribution of mycorrhizal pathway. Plant and Soil, 449, 357–371.
Clark N M, Rillig M C, Nowak R S. 2009. Arbuscular mycorrhizal fungal abundance in the Mojave Desert: Seasonal dynamics and impacts of elevated CO2. Journal of Arid Environments, 73, 834–843.
Clark R B, Zeto S K. 2000. Mineral acquisition by arbuscular mycorrhizal plants. Journal of Plant Nutrition, 23, 867–902.
Collos Y, Mornet F. 1993. Automated procedure for determination of dissolved organic nitrogen and phosphorus in aquatic environments. Marine Biology, 116, 685–688.
Corkidi L, Allen E B, Merhaut D, Allen M F, Downer J, Bohn J, Evans M. 2004. Assessing the infectivity of commercial mycorrhizal inoculants in plant nursery conditions. Journal of Environmental Horticulture, 22, 149–154.
Deng Y, Feng G, Chen X P, Zou C Q. 2017. Arbuscular mycorrhizal fungal colonization is considerable at optimal Olsen-P levels for maximized yields in an intensive wheat–maize cropping system. Field Crops Research, 209, 1–9.
Douds D D, Millner P D. 1999. Biodiversity of arbuscular mycorrhizal fungi in agroecosystems. Agriculture Ecosystems Environment, 74, 77–93.
Dueñas J F, Camenzind T, Roy J, Hempel S, Homeier J, Suárez J P, Rillig M C. 2020. Moderate phosphorus additions consistently affect community composition of arbuscular mycorrhizal fungi in tropical montane forests in southern Ecuador. New Phytologist, 227, 1505–1518.
Edgar R C. 2013. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10, 996–998.
Egerton-Warburton L M, Johnson N C, Allen E B. 2007. Mycorrhizal community dynamics following nitrogen fertilization: a cross-site test in five grasslands. Ecological Monographs, 77, 527–544.
FAO (Food and Agriculture Organization). 2006. World reference base for soil resources. In: World Soil Resources Report. Rome, Italy.
Feng G, Song Y C, Li X L, Christie P. 2003. Contribution of arbuscular mycorrhizal fungi to utilization of organic sources of phosphorus by red clover in a calcareous soil. Applied Soil Ecology, 22, 139–148.
Feng G, Su Y B, Li X L, Wang H, Zhang F S, Tang C X, Rengel Z. 2002. Histochemical visualization of phosphatase released by arbuscular mycorrhizal fungi in soil. Journal of Plant Nutrition, 25, 969–980.
Ferrol N, Azcón-Aguilar C, Pérez-Tienda J. 2019. Arbuscular mycorrhizas as key players in sustainable plant phosphorus acquisition: An overview on the mechanisms involved. Plant Science, 280, 441–447.
Gaur A, Adholeya A. 2004. Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Current Science, 86, 528–534.
Gianinazzi S G. 2014. Domestication of beneficial soil microorganisms: An innovative technology for agriculture. In: Proceedings of International Congress on Mycorrhizae.Marrakesh. p. 26.
Grant C, Bittman S, Montreal M, Plenchette C, Morel C. 2005. Soil and fertilizer phosphorus: Effects on plant P supply and mycorrhizal development. Canadian Journal of Plant Science, 85, 3–14.
Grigera M S, Drijber R A, Wienhold B J. 2007. Increased abundance of arbuscular mycorrhizal fungi in soil coincides with the reproductive stages of maize. Soil Biology & Biochemistry, 39, 1401–1409.
Gryndler M, Hrselova H, Cajthaml T, Havrankova M, Rezacova V, Gryndlerova H, Larsen J. 2009. Influence of soil organic matter decomposition on arbuscular mycorrhizal fungi in terms of asymbiotic hyphal growth and root colonization. Mycorrhiza, 19, 255–266.
Gryndler M, Sudová R, Püschel D, Rydlová J, Janoušková M, Vosátka M. 2008. Cultivation of high-biomass crops on coal mine spoil banks: Can microbial inoculation compensate for high doses of organic matter? Bioresource Technology, 99, 6391–6399.
Habte M, Zhang Y C, Schmitt D P. 1999. Effectiveness of Glomus species in protecting white clover against nematode damage. Canadian Journal of Botany, 77, 135–139. 
Van Der Heijden M G A, Klironomos J N, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders I R. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature, 396, 69–72.
Helgason T, Fitter A H. 2009. Natural selection and the evolutionary ecology of the arbuscular mycorrhizal fungi (Phylum Glomeromycota). Journal of Experimental Botany, 60, 2465–2480.
Hodge A, Campbell C D, Fitter A H. 2001. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature, 413, 297–299.
Javot H, Penmetsa R V, Terzaghi N, Cook D R, Harrison M J. 2007a. A medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences of the United States of America, 104, 1720–1725.
Javot H, Pumplin N, Harrison M J. 2007b. Phosphate in the arbuscular mycorrhizal symbiosis: Transport properties and regulatory roles. Plant Cell and Environment, 30, 310–322.
Jeffries P, Gianinazzi S, Perotto S, Turnau K, Barea J M. 2003. The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biology and Fertility of Soils, 37, 1–16.
Jiao X G, Gao C S, Lü G H, Sui Y Y. 2011. Effect of long-term fertilization on soil enzyme activities under different hydrothermal conditions in Northeast China. Agricultural Sciences in China, 10, 412–422.
Jin H Y, Germida J J, Walley F L. 2013. Suppressive effects of seed-applied fungicides on arbuscular mycorrhizal fungi (AMF) differ with fungicide mode of action and AMF species. Applied Soil Ecology, 72, 22–30.
Johnson N C. 1993. Can fertilization of soil select less mutualistic mycorrhizae? Ecological Applications, 3, 749–757.
Kahiluoto H, Ketoja E, Vestberg M, Saarela I. 2001. Promotion of AM utilization through reduced P fertilization 2. Field studies. Plant and Soil, 231, 65–79.
Karandashov V, Kuzovkina I, Hawkins H J, George E. 2000. Growth and sporulation of the arbuscular mycorrhizal fungus Glomus caledonium in dual culture with transformed carrot roots. Mycorrhiza, 10, 23–28.
Kiers E T, Duhamel M, Beesetty Y, Mensah J A, Franken O, Verbruggen E, Fellbaum C R, Kowalchuk G A, Hart M, Bago A, Palmer T M, West S A, Vandenkoornhuyse P, Jansa J, Bücking H. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science, 333, 880–882.
Kitson R E, Mellon M G. 1944. Colorimetric determination of phosphorus as molybdivanadophosphoric acid. Industrial & Engineering Chemistry Analytical Edition, 16, 379–383.
Lee J, Lee S, Young J P W. 2008. Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiology Ecology, 65, 339–349.
Lekberg Y, Koide R T, Twomlow S J. 2008. Effect of agricultural management practices on arbuscular mycorrhizal fungal abundance in low-input cropping systems of southern Africa: A case study from Zimbabwe. Biology and Fertility of Soils, 44, 917–923.
Liu S L, Guo X L, Feng G, Maimaitiaili B, Fan J L, He X H. 2016. Indigenous arbuscular mycorrhizal fungi can alleviate salt stress and promote growth of cotton and maize in saline fields. Plant and Soil, 398, 195–206.
Liu W, Zhang Y L, Jiang S S, Deng Y, Christie P, Murray P J, Li X L, Zhang J L. 2016. Arbuscular mycorrhizal fungi in soil and roots respond differently to phosphorus inputs in an intensively managed calcareous agricultural soil. Scientific Reports, 6, 1–11.
Liu Y, He L, An L Z, Helgason T, Feng H Y. 2009. Arbuscular mycorrhizal dynamics in a chronosequence of Caragana korshinskii plantations. FEMS Microbiology Ecology, 67, 81–92.
Martínez-García L B, Armas C, Miranda J D D, Padilla F M, Pugnaire F I. 2011. Shrubs influence arbuscular mycorrhizal fungi communities in a semi-arid environmen. Soil Biology and Biochemistry, 43, 682–689.
McLaughlin M J, McBeath T M, Smernik R, Stacey S P, Ajiboye B, Guppy C. 2011. The chemical nature of P accumulation in agricultural soils-implications for fertiliser management and design: An Australian perspective. Plant and Soil, 349, 69–87.
Murphy J, Riley J P. 1962. A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta, 27, 31–36.
Oehl F, Laczko E, Oberholzer H R, Jansa J, Egli S. 2017. Diversity and biogeography of arbuscular mycorrhizal fungi in agricultural soils. Biology and Fertility of Soils, 53, 777–797.
Oehl F, Sieverding E, Mader P, Dubois D, Ineichen K, Boller T, Wiemken A. 2004. Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia, 138, 574–583.
Olsen S R. 1954. Estimation of Available Phosphorus in Soils by Extraction with Sodium Bicarbonate (No. 939). US Department of Agriculture, USA.
Ordoñez Y M, Fernandez B R, Lara L S, Rodriguez A, Uribe-Velez D, Sanders I R. 2016. Bacteria with phosphate solubilizing capacity alter mycorrhizal fungal growth both inside and outside the root and in the presence of native microbial communities. PLoS ONE, 11, e0154438.
Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij J M, Reier Ü, Zobel M. 2010. The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytologist, 188, 223–241.
Pearson J N, Jakobsen I. 1993. Symbiotic exchange of carbon and phosphorus between cucumber and three arbuscular mycorrhizal fungi. New phytologist, 124, 481–488.
Phillips J M, Hayman D S. 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, 158–161.
Püschel D, Janoušková M, Hujslová M, Slavíková R, Gryndlerová H, Jansa J. 2016. Plant–fungus competition for nitrogen erases mycorrhizal growth benefits of Andropogon gerardii under limited nitrogen supply. Ecology and Evolution, 6, 4332–4346.
Raymond N S, Gómez-Muñoz B, van der Bom F J T, Nybroe O, Jensen L S, Müller-Stöver D S, Oberson A, Richardson A E. 2020. Phosphate-solubilising microorganisms for improved crop productivity: A critical assessment. New Phytologist, 229, 1268–1277. 
Remy W, Taylor T N, Hass H, Kerp H. 1994. Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proceedings of the National Academy of Sciences of the United States of America, 91, 11841–11843.
Rillig M C, Aguilar-Trigueros C A, Bergmann J, Verbruggen E, Veresoglou S D, Lehmann A. 2015. Plant root and mycorrhizal fungal traits for understanding soil aggregation. New Phytologist, 205, 1385–1388.
Rillig M C, Mummey D L. 2006. Mycorrhizas and soil structure. New Phytologist, 171, 41–53.
Rouphael Y, Franken P, Schneider C, Schwarz D, Giovannetti M, Agnolucci M, De Pascale S, Bonini P, Colla G. 2015. Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. Scientia Horticulturae, 196, 91–108.
Sato K, Suyama Y, Saito M, Sugawara K. 2005. A new primer for discrimination of arbuscular mycorrhizal fungi with polymerase chain reaction-denature gradient gel electrophoresis. Grassland Science, 51, 179–181.
Schwarzott D, Schüßler A. 2001. A simple and reliable method for SSU rRNA gene DNA extraction, amplification, and cloning from single AM fungal spores. Mycorrhiza, 10, 203–207.
Sharma S B, Sayyed R Z, Trivedi M H, Gobi T A. 2013. Phosphate solubilizing microbes: Sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus, 2, 587.
Simon L, Lalonde M, Bruns T D. 1992. Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Applied and Environmental Microbiology, 58, 291–295.
Smith F, 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, 357–366.
Smith S E, Jakobsen I, Grønlund M, Smith F A. 2011. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: Interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiology, 156, 1050–1057.
Smith S E, Read D J. 2008. Mycorrhizal symbiosis. Quarterly Review of Biology, 3, 273–281.
Smith S E, Smith F A. 2011. Roles of arbuscular mycorrhizas in plant nutrition and growth: New paradigms from cellular to ecosystem scales. Annual Review of Plant Biology, 62, 227–250.
Smith S E, Smith F A, Jakobsen I. 2003. Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiology, 133, 16–20.
Soares C R F S, Siqueira J O. 2008. Mycorrhiza and phosphate protection of tropical grass species against heavy metal toxicity in multi-contaminated soil. Biology and Fertility of Soils, 44, 833–841. 
Soti P G, Rugg S, Racelis A. 2016. Potential of cover crops in promoting mycorrhizal diversity and soil quality in organic farms. Journal of Agricultural Science, 8, 42–47.
Staddon P L, Fitter A H, Graves J D. 1999. Effect of elevated atmospheric CO2 on mycorrhizal colonization, external mycorrhizal hyphal production and phosphorus inflow in Plantago lanceolata and Trifolium repens in association with the arbuscular mycorrhizal fungus Glomus mosseae. Global Change Biology, 5, 347–358.
Stewart L I, Hamel C, Hogue R, Moutoglis P. 2005. Response of strawberry to inoculation with arbuscular mycorrhizal fungi under very high soil phosphorus conditions. Mycorrhiza, 15, 612–619.
Storer K, Coggan A, Ineson P, Hodge A. 2018. Arbuscular mycorrhizal fungi reduce nitrous oxide emissions from N2O hotspots. New Phytologist, 220, 1285–1295.
Takeda M, Nakamoto T, Miyazawa K, Murayama T, Okada H. 2009. Phosphorus availability and soil biological activity in an Andosol under compost application and winter cover cropping. Applied Soil Ecology, 42, 86–95.
Tarafdar J C, Marschner H. 1994. Phosphatase activity in the rhizosphere and hyphosphere of VA mycorrhizal wheat supplied with inorganic and organic phosphorus. Soil Biology and Biochemistry, 26, 387–395.
Tawaraya K, Hirose R, Wagatsuma T. 2012. Inoculation of arbuscular mycorrhizal fungi can substantially reduce phosphate fertilizer application to Allium fistulosum L. and achieve marketable yield under field condition. Biology and Fertility of Soils, 48, 839–843.
Tian H, Drijber R A, Niu X S, Zhang J L, Li X L. 2011. Spatio-temporal dynamics of an indigenous arbuscular mycorrhizal fungal community in an intensively managed maize agroecosystem in North China. Applied Soil Ecology, 47, 141–152.
Torstensson L, Wessen B. 1984. Interactions between the fungicide benomyl and soil microorganisms. Soil Biology and Biochemistry, 16, 445–452.
Trouvelot A, Kough J L, Gianinazzi-Pearson V. 1986. Estimation of VA mycorhizal infection levels. Research for method having a functional significance. In: Physiological and Genetical Aspects of Mycorrhizae: Proceedings of the1st European Symposium on Mycorrhizae, Dijon. INRA. París, Francia. pp. 217–221.
Turner B L, Frossard E, Baldwin D S. 2005. Organic Phosphorus in the Environment. Commonwealth Agricultural Bureaux International Publishing, Cambridg. pp. 269–294.
Verbruggen E, van der Heijden M G A, Rillig M C, Kiers E T. 2013. Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New Phytologist, 197, 1104–1109.
Verstraete W, Voets J P. 1977. Soil microbial and biochemical characteristics in relation to soil management and fertility. Soil Biology and Biochemistry, 9, 253–258.
Vestberg M, Kahiluoto H, Wallius E. 2011. Arbuscular mycorrhizal fungal diversity and species dominance in a temperate soil with long-term conventional and low-input cropping systems. Mycorrhiza, 21, 351–361.
Walder F, van der Heijden M G A. 2015. Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nature Plants, 1, 15159.
Wang B, Liu H, Li Y H, Ma X W, Wang X H, Ma Y B. 2013. Phosphorus adsorption and desorption characteristics of gray desert soil under long-term fertilization. Acta Pedologica Sinica, 50, 727–733. (in Chinese)
Wang B, Liu H, Wang X H, Li J M, Ma Y B, Ma X W. 2015. Soil phosphorus accumulation model for an arid area of north-western China with 3-year rotation of wheat, maize and cotton. Journal of Agricultural Science, 153, 1247–1256.
Wang F, Shi N, Jiang R F, Zhang F S, Feng G. 2016. In situ stable isotope probing of phosphate-solubilizing bacteria in the hyphosphere. Journal of Experimental Botany, 6, 1689–1701.
Wang J P, Wang G G, Zhang B, Yuan Z M, Fu Z Y, Yuan Y D, Zhu L J, Ma S L, Zhang J C. 2019. Arbuscular mycorrhizal fungi associated with tree species in a planted forest of eastern China. Forests, 10, 424.
Wetzel K, Silva G, Matczinski U, Oehl F, Fester T. 2014. Superior differentiation of arbuscular mycorrhizal fungal communities from till and no-till plots by morphological spore identification when compared to T-RFLP. Soil Biology and Biochemistry, 72, 88–96.
Wilson G W T, Williamson M W. 2008. Topsin-M: The new benomyl for mycorrhizal-suppression experiments. Mycologia, 100, 548–554.
Zhang L, Fan J Q, Ding X D, He X H, Zhang F S, Feng G. 2014. Hyphosphere interactions between an arbuscular mycorrhizal fungus and a phosphate solubilizing bacterium promote phytate mineralization in soil. Soil Biology and Biochemistry, 74, 177–183.
Zhang L, Shi N, Fan J Q, Wang F, George T S, Feng G. 2018. Arbuscular mycorrhizal fungi stimulate organic phosphate mobilization associated with changing bacterial community structure under field conditions. Environmental Microbiology, 20, 2639–2651.
Zhang L, Xu M D, Liu Y, Zhang F S, Hodge A, Feng G. 2016. Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate-solubilizing bacterium. New Phytologist, 210, 1022–1032.

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