Arbuscular mycorrhizal fungi (AMF) species and abundance exhibit different effects on saline-alkaline tolerance in Leymus chinensis

References

• Al-Karaki GN. 2006. Nursery inoculation of tomato with arbuscular mycorrhizal fungi and subsequent performance under irrigation with saline water. Sci Hortic. 109:1–7.
   Web of Science ®Google Scholar
• Aliasgharzadeh N, Rastin SN, Towfighi H, Alizadeh A. 2001. Occurrence of arbuscular mycorrhizal fungi in saline soils of the Tabriz Plain of Iran in relation to some physical and chemical properties of soil. Mycorrhiza. 11:119–122.
   PubMed Web of Science ®Google Scholar
• Asmelash F, Bekele T, Birhane E. 2016. The potential role of arbuscular mycorrhizal fungi in the restoration of degraded lands. Front Microbiol. 7:1095.
   PubMed Web of Science ®Google Scholar
• Asrar H, Hussain T, Hadi SMS, Gul B, Nielsen BL, Khan MA. 2017. Salinity induced changes in light harvesting and carbon assimilating complexes of Desmostachya bipinnata (L.) staph. Environ Exp Bot. 135:86–95.
   Web of Science ®Google Scholar
• Biermann B, Linderman RG. 1981. Quantifying vesicular-arbuscular mycorrhizae: A proposed method towards standardization. New Phytol. 87:63–67.
   Web of Science ®Google Scholar
• Boller T, Wiemken A, Sanders IR. 1998. Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology. 79:2082–2091.
   Web of Science ®Google Scholar
• Bompadre MJ, de Molina MR, Colombo RP, Bidondo LF, Silvani VA, Pardo AG, Ocampo JA, Godeas AM. 2013. Differential efficiency of two strains of the arbuscular mycorrhizal fungus Rhizophagus irregularis on olive (Olea europaea) plants under two water regimes. Symbiosis. 61:105–112.
   Web of Science ®Google Scholar
• Botella MA, Cerdá A, Lips SH. 1994. Kinetics of NO3− and NH4+ uptake by wheat seedlings. effect of salinity and nitrogen source. J Plant Physiol. 144:53–57.
   Web of Science ®Google Scholar
• Bremner JM. 1965. Organic forms of nitrogen. In: Black CA, editor. Methods of soils analysis. Madison: American Society of Agronomy; p. 1238–1255.
   Google Scholar
• Bücking H, Shachar-Hill Y. 2005. Phosphate uptake, transport and transfer by the arbuscular mycorrhizal fungus Glomus intraradices is stimulated by increased carbohydrate availability. New Phytol. 165:899–912.
   PubMed Web of Science ®Google Scholar
• Bui E. 2013. Soil salinity: a neglected factor in plant ecology and biogeography. J Arid Environ. 92:14–25.
   Web of Science ®Google Scholar
• Chen J, Zhang H, Zhang X, Tang M. 2017b. Arbuscular mycorrhizal symbiosis alleviates salt stress in black locust through improved photosynthesis, water status, and K+/Na+ homeostasis. Front Plant Sci. 8:1739.
   PubMed Web of Science ®Google Scholar
• Chen S, Zhao H, Zou C, Li Y, Chen Y, Wang Z, Jiang Y, Liu A, Zhao P, Wang M, Ahammed GJ. 2017a. Combined inoculation with multiple arbuscular mycorrhizal fungi improves growth, nutrient uptake and photosynthesis in cucumber seedlings. Front Microbiol. 8:2516.
   PubMed Web of Science ®Google Scholar
• Clark RB. 1997. Arbuscular mycorrhizal adaptation, spore germination, root colonization, and host plant growth and mineral acquisition at low pH. Plant Soil. 192:15–22.
   Web of Science ®Google Scholar
• Colla G, Rouphael Y, Cardarelli M, Tullio M, Rivera CM, Rea E. 2008. Alleviation of salt stress by arbuscular mycorrhizal in zucchini plants grown at low and high phosphorus concentration. Biol Fert Soils. 44:501–509.
   Web of Science ®Google Scholar
• Crossay T, Majorel C, Redecker D, Gensous S, Medevielle V, Durrieu G, Cavaloc Y, Amir H. 2019. Is a mixture of arbuscular mycorrhizal fungi better for plant growth than single-species inoculants? Mycorrhiza. 29(4):325–339.
   PubMed Web of Science ®Google Scholar
• Elhindi KM, El-Din AS, Elgorban AM. 2017. The impact of arbuscular mycorrhizal fungi in mitigating salt-induced adverse effects in sweet basil (Ocimum basilicum L.). Saudi J Biol Sci. 24(1):170–179.
   PubMed Web of Science ®Google Scholar
• Estrada B, Aroca R, Barea JM, Ruiz-Lozano JM. 2013b. Native arbuscular mycorrhizal fungi isolated from a saline habitat improved maize antioxidant systems and plant tolerance to salinity. Plant Sci. 201:42–51.
   PubMed Web of Science ®Google Scholar
• Estrada B, Aroca R, Maathuis FJ, Barea JM, Ruiz-Lozano JM. 2013a. Arbuscular mycorrhizal fungi native from a Mediterranean saline area enhance maize tolerance to salinity through improved ion homeostasis. Plant Cell Environ. 36(10):1771–1782.
   PubMed Web of Science ®Google Scholar
• Evelin H, Devi TS, Gupta S, Kapoor R. 2019. Mitigation of salinity stress in plants by arbuscular mycorrhizal symbiosis: current understanding and new challenges. Front Plant Sci. 10:470.
   PubMed Web of Science ®Google Scholar
• Evelin H, Giri B, Kapoor R. 2012. Contribution of Glomus intraradices inoculation to nutrient acquisition and mitigation of ionic imbalance in NaCl-stressed Trigonella foenum-graecum. Mycorrhiza. 22(3):203–217.
   PubMed Web of Science ®Google Scholar
• Evelin H, Kapoor R, Giri B. 2009. Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot. 104:1263–1280.
   PubMed Web of Science ®Google Scholar
• FAO. 2008. Land and plant nutrition management service. http://www.fao.org/ag/agl/agll/spush.
   Google Scholar
• Feddermann N, Finlay R, Boller T, Elfstrand M. 2010. Functional diversity in arbuscular mycorrhiza–the role of gene expression, phosphorous nutrition and symbiotic efficiency. Fungal Eco. 3(1):1–8.
   Web of Science ®Google Scholar
• Gao Y, Wang D, Ba L, Bai Y, Liu B. 2008. Interactions between herbivory and resource availability on grazing tolerance of Leymus chinensis. Environ Exp Bot. 63:113–122.
   Web of Science ®Google Scholar
• Giri B, Kapoor R, Mukerji KG. 2007. Improved tolerance of Acacia nilotica to salt stress by arbuscular mycorrhiza, Glomus fasciculatum may be partly related to elevated K/Na ratios in root and shoot tissues. Microb Ecol. 54:753–760.
   PubMed Web of Science ®Google Scholar
• Gomathi R, Thandapani TV. 2005. Salt stress in relation to nutrient accumulation and quality of sugarcane genotypes. Sugar Tech. 7:39–47.
   Google Scholar
• Gong X, Zhang J, Liu JH. 2014. A stress responsive gene of Fortunella crassifolia FcSISP functions in salt stress resistance. Plant Physiol Bioch. 83:10–19.
   PubMed Web of Science ®Google Scholar
• Graham JH, Eissenstat DM, Drouillard DL. 1991. On the relationship between a plant’s mycorrhizal dependency and rate of vesicular-arbuscular mycorrhizal colonization. Funct Ecol. 5:773–779.
   Web of Science ®Google Scholar
• Guissou T, Ba AM, Ouadba JM, Guinko S, Duponnois R. 1998. Responses of Parkia biglobosa (Jacq.) Benth, Tamarindus indica L. and Zizyphus mauritiana Lam. to arbuscular mycorrhizal fungi in a phosphorus-deficient sandy soil. Biol Fer Soils. 26:194–198.
   Web of Science ®Google Scholar
• Harrison MJ, Dewbre GR, Liu J. 2002. A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell. 14:2413–2429.
   PubMed Web of Science ®Google Scholar
• Heike B, Arjun K. 2015. Role of arbuscular mycorrhizal fungi in the nitrogen uptake of plants: current knowledge and research gaps. Agron J. 5:587–612.
   Google Scholar
• Heydari S, Pirzad A. 2020. Mycorrhizal fungi and Thiobacillus co-inoculation improve the physiological indices of Lallemantia iberica under salinity stress. Curr Microbiol. doi:10.1007/s00284-020-02034-y.
   PubMed Web of Science ®Google Scholar
• Hoagland DR, Arnon DI. 1950. The water-culture method for growing plants without soil. California Agricultural Experiment Station, Circular-347.
   Google Scholar
• Kaschuk G, Kuyper TW, Leffelaar PA, Hungria M, Giller KE. 2009. Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol Biochem. 41:1233–1244.
   Web of Science ®Google Scholar
• Kitson RE, Mellon MG. 1944. Colorimetric determination of phosphorus as molybdivanadophosphoric acid. Ind Eng Chem. 16:379–383.
   Google Scholar
• Klironomos JN, Hart MM. 2002. Colonization of roots by arbuscular mycorrhizal fungi using different sources of inoculum. Mycorrhiza. 12:181–184.
   PubMed Web of Science ®Google Scholar
• Kong L, Gong X, Zhang X, Zhang W, Sun J, Chen B. 2020. Effects of arbuscular mycorrhizal fungi on photosynthesis, ion balance of tomato plants under saline-alkali soil condition. J Plant Nutr. 43(5):682–698.
   Web of Science ®Google Scholar
• Kong D, Wu H, Wang M, Simmons M, Lü X, Yu Q, Han X. 2010. Structural and chemical differences between shoot-and root-derived roots of three perennial grasses in a typical steppe in Inner Mongolia China. Plant Soil. 336:209–217.
   Web of Science ®Google Scholar
• Lin J, Wang Y, Sun S, Mu C, Yan X. 2017. Effects of arbuscular mycorrhizal fungi on the growth, photosynthesis and photosynthetic pigments of Leymus chinensis seedlings under salt-alkali stress and nitrogen deposition. Sci Total Environ. 576:234–241.
   PubMed Web of Science ®Google Scholar
• Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Ann Rev Plant Biol. 59:651–681.
   PubMed Web of Science ®Google Scholar
• Muranaka S, Shimizu K, Kato M. 2002. A salt-tolerant cultivar of wheat maintains photosynthetic activity by suppressing sodium uptake. Photosynthetica. 40:505–515.
   Web of Science ®Google Scholar
• Navarro JM, Pérez-Tornero O, Morte A. 2014. Alleviation of salt stress in citrus seedlings inoculated with arbuscular mycorrhizal fungi depends on the rootstock salt tolerance. J Plant Physiol. 171(1):76–85.
   PubMed Web of Science ®Google Scholar
• Oehl F, Laczko E, Bogenrieder A, Stahr K, Bösch R, van der Heijden M, Sieverding E. 2010. Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biol Biochem. 42:724–738.
   Web of Science ®Google Scholar
• Parvin S, Van Geel M, Yeasmin T, Verbruggen E, Honnay O. 2020. Effects of single and multiple species inocula of arbuscular mycorrhizal fungi on the salinity tolerance of a Bangladeshi rice (Oryza sativa L.) cultivar. Mycorrhiza. 30:431–444.
   PubMed Web of Science ®Google Scholar
• Phillips JM, Hayman DS. 1970. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. T Brit Mycol Soc. 55:158–161.
   Web of Science ®Google Scholar
• Plenchette C, Fortin JA, Furlan V. 1983. Growth responses of several plant species to mycorrhizae in a soil of moderate P-fertility: II. Soil fumigation induced stunting of plants corrected by reintroduction of the wild endomycorrhizal flora. Plant Soil. 1:211–217.
   Google Scholar
• Porcel R, Aroca R, Azcon R, Ruiz-Lozano JM. 2016. Regulation of cation transporter genes by the arbuscular mycorrhizal symbiosis in rice plants subjected to salinity suggests improved salt tolerance due to reduced Na+ root-to-shoot distribution. Mycorrhiza. 26(7):673–684.
   PubMed Web of Science ®Google Scholar
• Porcel R, Redondo-Gómez S, Mateos-Naranjo E, Aroca R, Garcia R, Ruiz-Lozano JM. 2015. Arbuscular mycorrhizal symbiosis ameliorates the optimum quantum yield of photosystem II and reduces non-photochemical quenching in rice plants subjected to salt stress. J Plant Physiol. 185:75–83.
   PubMed Web of Science ®Google Scholar
• Porras-Soriano A, Soriano-Martín ML, Porras-Piedra A, Azcón R. 2009. Arbuscular mycorrhizal fungi increased growth, nutrient uptake and tolerance to salinity in olive trees under nursery conditions. J Plant Physiol. 166(13):1350–1359.
   PubMed Web of Science ®Google Scholar
• Rao PS, Mishra B, Gupta SR. 2013. Effects of soil salinity and alkalinity on grain quality of tolerant, semi-tolerant and sensitive rice genotypes. Rice Sci. 20:284–291.
   Google Scholar
• Reynolds HL, Vogelsang KM, Hartley AE, Bever JD, Schultz PA. 2006. Variable responses of old-field perennials to arbuscular mycorrhizal fungi and phosphorus source. Oecologia. 147:348–358.
   PubMed Web of Science ®Google Scholar
• 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. Sci Hortic. 196:91–108.
   Web of Science ®Google Scholar
• Rubinigg M, Posthumus F, Ferschke M, Elzenga JTM, Stulen I. 2003. Effects of NaCl salinity on 15N-nitrate fluxes and specific root length in the halophyte Plantago maritima L. Plant Soil. 250:201–213.
   Web of Science ®Google Scholar
• Santander C, Sanhueza M, Olave J, Borie F, Valentine A, Cornejo P. 2019. Arbuscular mycorrhizal colonization promotes the tolerance to salt stress in lettuce plants through an efficient modification of ionic balance. J Soil Sci Plant Nut. 19(2):321–331.
   Google Scholar
• Schnepf A, Roose T, Schweiger P. 2008. Impact of growth and uptake patterns of arbuscular mycorrhizal fungi on plant phosphorus uptake-a modelling study. Plant Soil. 312:85–99.
   Web of Science ®Google Scholar
• Sheng M, Tang M, Chen H, Yang B, Zhang F, Huang Y. 2008. Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza. 18:287–296.
   PubMed Web of Science ®Google Scholar
• Shi-chu L, Yong J, Ma-bo L, Wen-xu Z, Nan X, Hui-hui Z. 2019. Improving plant growth and alleviating photosynthetic inhibition from salt stress using AMF in alfalfa seedlings. J Plant Interact. 14(1):482–491.
   Web of Science ®Google Scholar
• Shrivastava P, Kumar R. 2015. Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci. 22:123–131.
   PubMed Web of Science ®Google Scholar
• Siebielec G, Ukalska-Jaruga A, Kidd P. 2015. Bioavailability of trace elements in soils amended with high-phosphate materials. In: Phosphate in soils: interaction with micronutrients, radionuclides and heavy metals. Boca Raton: CRC Press; p. 237–260.
   Google Scholar
• Smith SE, Read DJ. 2008. Mycorrhizal symbiosis. New York, NY: Academic Press.
   Google Scholar
• Tisarum R, Theerawitaya C, Samphumphuang T, Polispitak K, Thongpoem P, Singh HP, Cha-um S. 2020. Alleviation of salt stress in upland rice (Oryza sativa L. ssp. indica cv. Leum Pua) using arbuscular mycorrhizal fungi inoculation. Front Plant Sci. 11:348.
   PubMed Web of Science ®Google Scholar
• Tisserant B, Gianinazzi-Pearson V, Gianinazzi S, Gollotte A. 1993. In planta histochemical staining of fungal alkaline phosphatase activity for analysis of efficient arbuscular mycorrhizal infections. Mycol Res. 97:245–250.
   Web of Science ®Google Scholar
• van der Heijden MGA. 2002. Arbuscular mycorrhizal fungi as a determinant of plant diversity. In: Search of underlying mechanisms and general principles. Berlin: Springer; p. 243–265.
   Google Scholar
• Wang D, Ba L. 2008. Ecology of meadow steppe in northeast China. Rangeland J. 30:247–254.
   Web of Science ®Google Scholar
• Wang D, Du J, Zhang B, Ba L, Hodgkinson KC. 2017. Grazing intensity and phenotypic plasticity in the clonal grass Leymus chinensis. Rangeland Ecol Manag. 70:740–747.
   Web of Science ®Google Scholar
• Wang C, Li X, Zhou J, Wang G, Dong Y. 2008. Effects of arbuscular mycorrhizal fungi on growth and yield of cucumber plants. Commun Soil Sci Plan. 39:499–509.
   Web of Science ®Google Scholar
• Wang L, Seki K, Miyazaki T, Ishihama Y. 2009. The causes of soil alkalinization in the Songnen Plain of Northeast China. Paddy Water Environ. 7:259–270.
   Web of Science ®Google Scholar
• Wang X, Wang J, Liu H, Zou D, Zhao H. 2013. Influence of natural saline-alkali stress on chlorophyll content and chloroplast ultrastructure of two contrasting rice (Oryza sativa L. japonica) cultivars. Aust J Crop Sci. 7:289–292.
   Google Scholar
• Wellburn AR. 1994. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol. 144:307–313.
   Web of Science ®Google Scholar
• Wu QS, Liu CY, Zhang DJ, Zou YN, He XH, Wu QH. 2016. Mycorrhiza alters the profile of root hairs in trifoliate orange. Mycorrhiza. 26:237–247.
   PubMed Web of Science ®Google Scholar
• Xu X, Xu H, Wang Y, Wang X, Qiu Y, Xu B. 2008. The effect of salt stress on the chlorophyll level of the main sand-binding plants in the shelterbelt along the Tarim Desert Highway. Chinese Sci Bull. 53:109–111.
   Web of Science ®Google Scholar
• Yang Y, Tang M, Sulpice R, Chen H, Tian S, Ban Y. 2014. Arbuscular mycorrhizal fungi alter fractal dimension characteristics of Robinia pseudoacacia L. seedlings through regulating plant growth, leaf water status, photosynthesis, and nutrient concentration under drought stress. J Plant Growth Regul. 33:612–625.
   Web of Science ®Google Scholar
• Yang CW, Wang P, Li CY, Shi DC, Wang DL. 2008. Comparison of effects of salt and alkali stresses on the growth and photosynthesis of wheat. Photosynthetica. 46:107–114.
   Web of Science ®Google Scholar
• Yang C, Xu H, Wang L, Liu J, Shi D, Wang D. 2009. Comparative effects of salt-stress and alkali-stress on the growth, photosynthesis, solute accumulation, and ion balance of barley plants. Photosynthetica. 47:79–86.
   Web of Science ®Google Scholar
• Zhu XQ, Wang CY, Chen H, Tang M. 2014. Effects of arbuscular mycorrhizal fungi on photosynthesis, carbon content, and calorific value of black locust seedlings. Photosynthetica. 52:247–252.
   Web of Science ®Google Scholar