Hostname: page-component-848d4c4894-xm8r8 Total loading time: 0 Render date: 2024-07-02T13:49:11.596Z Has data issue: false hasContentIssue false
  • English
  • Français

Mitigating the effects of water-deficit stress on potato growth and photosynthesis using mycorrhizal fungi and phosphate-solubilizing bacteria

Published online by Cambridge University Press:  06 March 2024

Ahmad Nemati ,
Mohammad Ali Aboutalebian Open the ORCID record for Mohammad Ali Aboutalebian [Opens in a new window]  and
Mehrdad Chaichi
Ahmad Nemati
Affiliation:
Department of Plant Production and Genetics, Faculty of Agriculture, Bu-Ali Sina University, Hamedan, Iran
Mohammad Ali Aboutalebian*
Affiliation:
Department of Plant Production and Genetics, Faculty of Agriculture, Bu-Ali Sina University, Hamedan, Iran
Mehrdad Chaichi
Affiliation:
Department of Seed and Plant Improvement Research, Agriculture Research, Education and Extension Organization, Hamedan, Iran
*
Corresponding author: Mohammad Ali Aboutalebian; Email: m.aboutalebian@basu.ac.ir
Get access Rights & Permissions [Opens in a new window]

Abstract

Biofertilizers, such as arbuscular mycorrhiza fungi and phosphate-solubilizing bacteria (PSB), have been reported to enhance plant growth under water stress conditions. This study aimed to investigate the effect of different biofertilizers on potato photosynthesis and growth under water deficit stress. The experiment was conducted over two crop years (2019 and 2020) using a randomized complete block design with three replications. Four irrigation intervals (70, 90, 110 and 130 mm of cumulative evaporation) and six biofertilizer treatments (PSB, Funneliformis mosseae [FM], Rhizoglomus fasciculatum [RF], PSB + FM, PSB + RF and no use) were applied. Severe moisture stress (130 mm evaporation) compared to no stress (70 mm evaporation) increased substomatal carbon dioxide concentration. The application of biofertilizers improved tuber yield under severe moisture stress, with FM showing the highest increase (62.9%), followed by RF (59.8%) and PSB (48.4%). The use of PSB along with mycorrhizae led to a significant decrease in mycorrhizal colonization percentage at all irrigation levels. The highest percentage of colonization and net photosynthesis was obtained from the application of both mycorrhizal species under irrigation conditions after 70 mm of evaporation. The application of PSB alone resulted in a 14.6% increase in the transpiration rate, additionally, the use of mycorrhiza led to an 18.7% increase in stomatal conductivity compared to no-biofertilizer. The results suggest that the simultaneous use of PSB and mycorrhizae can be effective in mild moisture stress, but in severe moisture stress, the use of mycorrhizal species alone is more effective.

Keywords

Funneliformis mosseaepercentage of colonizationRhizoglomus fasciculatumstomatal conductancetranspiration rate
Type
Crops and Soils Research Paper
Information
The Journal of Agricultural Science , Volume 162 , Issue 1 , February 2024 , pp. 46 - 58
Check for updates
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdel-Fattah, G and Shakry, W (2016) Application of mycorrhizal technology for improving yield production of common bean plants. International Journal of Applied Sciences and Biotechnology 4, 191–197. https://doi.org/10.3126/IJASBT.V4I2.15103CrossRefGoogle Scholar
Agricultural Statistics (2020) Ministry of Jihad Agriculture, Information and Communication Technology Center. Tehran, Iran: Agricultural Statistics.Google Scholar
Alizade, A (2001) Plant, Water and Soil Realationship. Mashhad, Iran: Razavi Qods Astan Press.Google Scholar
Arnon, AN (1967) Method of extraction of chlorophyll in the plants. Agronomy Journal 23, 112–121.Google Scholar
Bago, B, Pfeffer, PE and Shachar-Hill, Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiology 124, 949–957. https://doi.org/10.1104/pp.124.3.949CrossRefGoogle ScholarPubMed
Balzergue, C, Chabauud, M, David, GB, Guillaume, B and Soizic, FR (2013) High phosphate reduces host ability to develop arbuscular mycorrhizal symbiosis without affecting root calcium spiking responses to the fungus. Frontiers in Plant Science 4, 426. https://doi.org/10.3389/fpls.2013.00426CrossRefGoogle Scholar
Bambara, S and Ndakidemi, PA (2009) Effects of rhizobium inoculation, lime and molybdenum on photosynthesis and chlorophyll content of Phaseolus vulgaris L. African Journal of Microbiology Research 3, 791–798. https://doi.org/10.5897/AJMR.9000276Google Scholar
Bashir, Z, Zargar, MY, Mohit, H, Mohiddin, FA, Shaheen, K, Syed Berjes, Z, Asif, A and Jagdeesh, PR (2017) Phosphorus solubilizing microorganisms: mechanism and diversity. International Journal of Chemical Studies 5, 666–673. http://doi.org/10.18782/2320-7051.5446Google Scholar
Batool, T, Ali, S, Mahmoud, FS, Naima, HN, Aamir, A, Khurshid, A, Muhammad, A, Muhammad, R, Muhammad, RS, Majed, A, Ibrahim, A-A and Muhammad, M (2020) Plant growth promoting rhizobacteria alleviates drought stress in potato in response to suppressive oxidative stress and antioxidant enzymes activities. Scientific Reports 10, 16975. https://doi.org/10.1038/s41598-020-73489-zCrossRefGoogle ScholarPubMed
Bayrami, S, Mirshekari, B and Farahvash, F (2012) Response of potato (Solanum tuberosum) to seed inoculation with mycorrhiza strains in different phosphorus fertilization. Journal of Food, Agriculture and Environment 10, 726–728.Google Scholar
Begum, N, Qin, C, Muhammad, AA, Sajjad, R, Muhammad, IK, Muhammad, A, Nadeem, A and Lixin, Z (2019) Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Frontiers in Plant Science 10, 1068. https://doi.org/10.3389/fpls.2019.01068CrossRefGoogle ScholarPubMed
Bonneau, L, Huguet, S, Daniel, W, Nicolas, P and Hoai-Nam, T (2013) Combined phosphate and nitrogen limitation generates a nutrient stress transcriptome favorable for arbuscular mycorrhizal symbiosis in Medicago truncatula. New Phytologist 199, 188–202. https://doi.org/10.1111/nph.12234CrossRefGoogle ScholarPubMed
Briggs, LJ and Shantz, HL (1913) The water requirement of plants. In Taylor, W (ed.), Bureau of Plant Industry Bulletin. Washington, DC: US Department of Agriculture, pp. 282–285. https://doi.org/10.5962/bhl.title.119193Google Scholar
Chen, YP, Rekha, PD, Arun, AB, Shen, FT, Lai, WA and Young, CC (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Applied Soil Ecology 34, 33–41. https://doi.org/10.1016/j.apsoil.2005.12.002CrossRefGoogle Scholar
Chen, S, Zhao, H, Chenchen, Z, Yongsheng, L, Yifei, CH, Zhonghong, W, Yan, J, Airong, L, Puyan, ZH, Mengmeng, W and Golam, JA (2017) Combined inoculation with multiple arbuscular mycorrhizal fungi improves growth, nutrient uptake and photosynthesis in cucumber seedlings. Frontiers in Microbiology 8, 2516. https://doi.org/10.3389/fmicb.2017.02516CrossRefGoogle ScholarPubMed
Dadrasi, A, Torabi, B, Rahimi, A, Soltani, A and Zeinali, E (2022 a) Modeling potential production and yield gap of potato using modelling and GIS approaches. Ecological Modelling 471, 110050. https://doi.org/10.1016/j.ecolmodel.2022.110050CrossRefGoogle Scholar
Dadrasi, A, Torabi, B, Rahimi, A, Soltani, A, Salmani, F, Nehbandani, A, Nourbakhsh, F and Ullah, Z (2022 b) Evaluation of water productivity in the main areas of potato cultivation in Iran. Potato Research 66, 905–963. https://doi.org/10.1007/s11540-022-09603-7CrossRefGoogle Scholar
Dalp, Y (1993) Vesicular arbuscular mycorrhiza. In Carter, MR (ed.), Soil Sampling and Methods of Analysis. Boca Raton, FL, USA: Lewis Publisher, pp. 287–301.Google Scholar
Dash, SN and Jena, RC (2015) Biofertilizer options in nutrient management of potato. International Journal of Scientific Research 4, 420–421. https://www.doi.org/10.36106/ijsrGoogle Scholar
Dawwam, GE, Elbeltagy, A, Emara, HM, Abbas, IH and Hassan, MM (2013) Beneficial effect of plant growth promoting bacteria isolated from the roots of potato plant. Annals of Agricultural Sciences 58, 195–201. https://doi.org/10.1016/j.aoas.2013.07.007CrossRefGoogle Scholar
Dibenedetto, NA, Corbo, MR, Daniela, C, Mariagrazia, PC, Antonio, B, Milena, S and Zina, F (2017) The role of plant growth promoting bacteria in improving nitrogen use efficiency for sustainable crop production: a focus on wheat. AIMS Microbiology 3, 413–434. https://doi.org/10.3934/microbiol.2017.3.413Google Scholar
Elliott, AJ, Daniell, TJ, Duncan, D and Katie, JF (2021) A commercial arbuscular mycorrhizal inoculum increases root colonization across wheat cultivars but does not increase assimilation of mycorrhiza-acquired nutrients. Plants People Planet 3, 588–599. https://doi.org/10.1002/ppp3.10094CrossRefGoogle Scholar
Evelin, H, Kapoor, R and Bhoopander, G (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Annals of Botany 104, 1263–1280. https://doi.org/10.1093/aob/mcp251CrossRefGoogle ScholarPubMed
FAO (2020) World Corp Production Statistics. Available at http://faostat.fao.org/ (accessed 26 May 2020).Google Scholar
Farzana, Y and Radizah, O (2005) Influence of rhizobacterial inoculation on growth of the sweet potato cultivar. Online Journal of Biological Sciences 1, 176–179. https://doi.org/10.3844/AJBBSP.2005.176.179Google Scholar
Fischer, R, Rees, D, Sayre, Z, Lu, M, Condon, AG and Larque, SA (1998) Wheat yield progress associated with higher stomatal conductance and photosynthetic rate, and cooler canopies. Crop Science 38, 1467–1475. http://doi.org/10.2135/cropsci1998.0011183X003800060011xCrossRefGoogle Scholar
Gai, JP, Feng, G, Christie, P and Li, XL (2006) Screening of arbuscular mycorrhizal fungi for symbiotic efficiency with sweet potato. Journal of Plant Nutrition 29, 1085–1094. https://doi.org/10.1080/01904160600689225CrossRefGoogle Scholar
Ghobadi, M, Movahhedi Dehnavi, M, Yadavi, AR, Parvizi, KH and Zafari, D (2020) Reduced P fertilization improves Fe and Zn uptake in potato when inoculated with AMF in P, Fe and Zn deficient soil. Rhizosphere 15, 100239. https://doi.org/10.1016/j.rhisph.2020.100239CrossRefGoogle Scholar
Ghorbanli, M, Gafarabad, M, Amirkian, T and Mamaghani, BA (2013) Investigation of proline, total protein, chlorophyll, ascorbate and dehydro ascorbate changes under drought stress in Akria and Mobil tomato cultivars. Iranian Journal of Plant Physiology 3, 651–658.Google Scholar
Hajiboland, R, Aliasgharzadeh, N, Farsad Laiegh, SH and Poschenrieder, CH (2010) Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant and Soil 331, 313–327. https://doi.org/10.1007/s11104-009-0255-zCrossRefGoogle Scholar
Han, H and Lee, K (2005) Plant growth promoting rhizobacteria effect on antioxidant status, photosynthesis, mineral uptake and growth of lettuce under soil salinity. Journal of Agricultural and Biological Sciences 1, 210–215.Google Scholar
James, E, Gyaneshwar, K, Natarajan, M, Wilfredo, LB, Pallavolu, MR, Pietro, PMI, Fabio, LO and Jagdish, KL (2002) Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z 67. Molecular Plant-Microbe Interactions 15, 894–906. https://doi.org/10.1094/mpmi.2002.15.9.894CrossRefGoogle Scholar
Jarosław, P, Dominika, BM and Waldemar, M (2020) Relations between photosynthetic parameters and drought-induced tuber yield decrease in Katahdin-derived potato cultivars. Potato Research 63, 463–477. https://doi.org/10.1007/s11540-020-09451-3Google Scholar
Kacheyo, OC, van Dijk, LCM, de Vrie, ME and Strui, PC (2020) Augmented descriptions of growth and development stages of potato (Solanum tuberosum L.) grown from different types of planting material. Annals of Applied Biology 178, 549–566. https://doi.org/10.1111/aab.12661CrossRefGoogle Scholar
Khan, N, Ali, S, Shahid, MA, Mustafa, A, Sayyed, RZ and Curá, JA (2021) Insights into the interactions among roots, rhizosphere, and rhizobacteria for improving plant growth and tolerance to abiotic stresses: a review. Cells 10, 1551. https://doi.org/10.3390/cells10061551CrossRefGoogle ScholarPubMed
Khosravifar, S, Farahvash, F, Aliasgharzad, N, Yarnia, M and Rahimzadeh khoei, F (2020) Effects of different irrigation regimes and two arbuscular mycorrhizal fungi on some physiological characteristics and yield of potato under field conditions. Journal of Plant Nutrition 43, 2067–2079. https://doi.org/10.1080/01904167.2020.1758133CrossRefGoogle Scholar
Kim, YS, Lee, KS, Kim, HG and Lee, GJ (2022) Biocontrol of large patch disease in zoysiagrass (Zoysia japonica) by Bacillus subtilis SA-15: identification of active compounds and synergism with a fungicide. Horticulturae 8, 34. https://doi.org/10.3390/horticulturae8010034CrossRefGoogle Scholar
Leigh, J, Fitter, A and Hodge, A (2011) Growth and symbiotic effectiveness of an arbuscular mycorrhizal fungus in organic matter in competition with soil bacteria. FEMS Microbiology Ecology 76, 428–438. https://doi.org/10.1111/j.1574-6941.2011.01066.xCrossRefGoogle ScholarPubMed
Leventis, G, Tsiknia, M, Feka, M, Ladikou, EV, Papadakis, IE, Chatzipavlidis, I, Papadopoulou, K and Ehaliotis, C (2021) Arbuscular mycorrhizal fungi enhance growth of tomato under normal and drought conditions, via different water regulation mechanisms. Rhizosphere 19, 100394. https://doi.org/10.1016/j.rhisph.2021.100394CrossRefGoogle Scholar
Luziatelli, F, Melini, F, Bonini, P, Melini, V, Cirino, V and Ruzzi, M (2021) Production of indole auxins by Enterobacter sp. Strain P-36 under submerged conditions. Fermentation 7, 138. https://doi.org/10.3390/fermentation7030138CrossRefGoogle Scholar
Mai, W, Xue, X, Gu, F and Changyan, T (2018) Simultaneously maximizing root mycorrhizal growth and phosphorus uptake by cotton plants by optimizing water and phosphorus management. BMC Plant Biology 18, 334. https://doi.org/10.1186/s12870-018-1550-8CrossRefGoogle ScholarPubMed
Marcińska, I, Czyczyło-Mysza, I, Edyta, S, Maria, F, Stanisław, G, Maciej, TG, Franciszek, J, Tomasz, H, Michał, D, Kinga, D, Agata, N and Steve, AQ (2013) Impact of osmotic stress on physiological and biochemical characteristics in drought-susceptible and drought-resistant wheat genotypes. Acta Physiologiae Plantarum 35, 451–461. https://doi.org/10.1007/s11738-012-1088-6CrossRefGoogle Scholar
Marschner, H (2011) Rhizosphere biology. In Marschner, P (ed.), Marschner's Mineral Nutrition of Higher Plants. Cambridge, MA, USA: Academic Press, pp. 369–388.Google Scholar
Muhammad, AA, Naveed, M, Adnan, M and Amjad, A (2017) The good, the bad, and the ugly of rhizosphere microbiome. In Kumar, V, Kumar, M, Sharma, S and Prasad, R (eds), Probiotics and Plant Health. Singapore: Springer, pp. 253–290. http://doi.org/10.1007/978-981-10-3473-2_11Google Scholar
Murphy, J and Riley, JP (1962) A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta 27, 31–36.10.1016/S0003-2670(00)88444-5CrossRefGoogle Scholar
Mustafa, A, Naveed, M, Saeed, Q, Ashraf, MN, Hussain, A, Abbas, T, Kamran, M, Nan-Sun, N and Minggang, X (2019) Application Potentials of Plant Growth Promoting Rhizobacteria and Fungi as an Alternative to Conventional Weed Control Methods, Sustainable Crop Production. London, UK: IntechOpen [Online]. Available at https://www.intechopen.com/chapters/67546. https://doi.org/10.5772/intechopen.86339Google Scholar
Nacoon, S, Jogloy, S, Nuntavun, R, Wiyada, M, Thomas, WK and Sophon, B (2020) Interaction between phosphate solubilizing bacteria and arbuscular mycorrhizal fungi on growth promotion and tuber inulin content of Helianthus tuberosus L. Scientific Reports 10, 4916. https://doi.org/10.1038/s41598-020-61846-xCrossRefGoogle ScholarPubMed
Nagy, R, Drissner, D, Nikolaus, A, Iver, J and Marcel, B (2009) Mycorrhizal phosphate uptake pathway in tomato is phosphorus-repressible and transcriptionally regulated. New Phytologist 181, 950–959. https://doi.org/10.1111/j.1469-8137.2008.02721.xCrossRefGoogle ScholarPubMed
Nautiyal, CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiology Letters 170, 265–270. https://doi.org/10.1111/j.1574-6968.1999.tb13383.xCrossRefGoogle ScholarPubMed
Ordoñez, YM, Fernandez, BR, Lidia, SL, Alia, R, Daniel, UV and Ian, RS (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, 1–18. https://doi.org/10.1371/journal.pone.0154438CrossRefGoogle ScholarPubMed
Ortas, I (2012) The effect of mycorrhizal fungal inoculation on plant yield, nutrient uptake and inoculation effectiveness under long-term field conditions. Field Crops Research 125, 35–48. https://doi.org/10.1016/j.fcr.2011.08.005CrossRefGoogle Scholar
Pande, A, Pandey, P, Simmi, M, Mritunjay, S and Suresh, K (2017) Phenotypic and genotypic characterization of phosphate solubilizing bacteria and their efficiency on the growth of maize. Journal of Genetic Engineering and Biotechnology 15, 379391. https://doi.org/10.1016/j.jgeb.2017.06.005CrossRefGoogle ScholarPubMed
Phillips, JM and Hayman, D (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, 118–158. http://doi.org/10.1016/S0007-1536(70)80110-3CrossRefGoogle Scholar
Ray, P and Lakshmanan, V (2020) Microbe to microbiome: a paradigm shift in the application of microorganisms for sustainable agriculture. Frontiers in Microbiology 11, 3323. https://doi.org/10.3389/fmicb.2020.622926CrossRefGoogle ScholarPubMed
Retuerto, R, Fernández-Lema, B and Obeso, JR (2006) Changes in photochemical efficiency in response to herbivory and experimental defoliation in the dioecious tree Ilex aquifolium. International Journal of Plant Sciences 167, 279–289. https://doi.org/10.1086/498919CrossRefGoogle Scholar
Rossi, M, Borromeo, I, Capo, C, Glick, BR, Del Gallo, M, Pietrini, F and Forni, C (2021) PGPB improve photosynthetic activity and tolerance to oxidative stress in Brassica napus grown on salinized soils. Applied Sciences 11, 11442. http://doi.org/10.3390/app112311442CrossRefGoogle Scholar
Sadeghipour, O and Aghaei, P (2012) Response of common bean (Phaseolus vulgaris L.) to exogenous application of salicylic acid (SA) under water stress conditions. Advances in Environmental Biology 6, 1160–1168.Google Scholar
Sakha, M and Jefwa, J (2019) Effects of arbuscular mycorrhizal fungal inoculation on growth and yield of two sweet potato varieties. Journal of Agriculture and Ecology Research International 18, 1–8. http://doi.ir-library.ku.ac.ke/handle/123456789/22027CrossRefGoogle Scholar
Salimpour, S, Khavazi, K, Nadian, HA and Besharati, H (2010) Effect of rock phosphate along with sulfur and microorganisms on yield chemical composition of canola. Iranian Journal of Soil Research 24, 9–19 (in Persian). https://doi.org/10.22092/ijsr.2010.126525Google Scholar
Simard, SW (2018) Mycorrhizal networks facilitate tree communication, learning, and memory. In Baluska, F, Gagliano, M and Witzany, G (eds), Memory and Learning in Plants. Berlin, Germany: Springer, pp. 191–213. https://doi.org/10.1007/978-3-319-75596-0_10CrossRefGoogle Scholar
Singh, S and Kapoor, KK (1998) Effects of inoculation of phosphate solubilizing microorganisms and an arbuscular mycorrhizal fungus on mungbean grown under natural soil conditions. Mycorrhiza 7, 249–253. https://doi.org/10.1007/s005720050188CrossRefGoogle Scholar
Smith, SE and Read, DJ (2008) Mycorrhizal Symbiosis, 3rd Edn. London: Academic Press.Google Scholar
Song, H (2005) Effects of VAM on host plant in condition of drought stress and its mechanisms. Electronic Journal of Biology 3, 44–48.Google Scholar
Steyn, JM, Franke, AC, vander Waals, JE and Haverkort, AJ (2016) Resource use efficiencies as indicators of ecological sustainability in potato production: a South African case study. Field Crops Research 199, 136–149. https://doi.org/10.1016/j.fcr.2016.09.020CrossRefGoogle Scholar
Vacheron, J, Desbrosses, G, Marie-Lara, B, Bruno, T, Yvan, ML, Daniel, M, Laurent, L, Florence, WD and Claire, PC (2013) Plant growth-promoting rhizobacteria and root system functioning. Frontiers in Plant Science 4, 356. https://doi.org/10.3389/fpls.2013.00356CrossRefGoogle ScholarPubMed
Villa, PM, Rodrigues, AC and Rada, F (2017) Leaf area index of potato (Solanum tuberosum L.) crop under three nitrogen fertilization treatments. Agronomía Colombiana 35, 171–175.10.15446/agron.colomb.v35n2.62110CrossRefGoogle Scholar
Watson, DJ (1947) Comparative physiological studies in the growth of field crops. I. Variation in net assimilation rate and leaf area between species and varieties, and within and between years. Annals of Botany 11, 41–76. https://doi.org/10.1093/oxfordjournals.aob.a083148CrossRefGoogle Scholar
Wegener, CB, Jurgens, HU and Jansen, G (2017) Drought stress affects nutritional and bioactive compounds in € potatoes (Solanum tuberosum L.) relevant to human health. FFHD 7, 17–35. https://doi.org/10.31989/ffhd.v7i1.279CrossRefGoogle Scholar
Yujie, F and Lizhong, X (2015) General mechanisms of drought response and their application in drought resistance improvement in plants. Cellular and Molecular Life Sciences 72, 673–689. https://doi.org/10.1007/s00018-014-1767-0Google Scholar
Zhang, L, Xu, M, Liu, Y, Zhang, F, Hodge, A and 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. https://doi.org/10.1111/nph.13838CrossRefGoogle Scholar
Zhao, R, Guo, W, Fu, R, Bi, N, Wang, L, Zhao, W, Guo, J and Zhang, J (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. http://doi.org/10.1016/j.apsoil.2014.11.016CrossRefGoogle Scholar