Abstract
Understanding how nutrient absorption processes in plants are related to arbuscular mycorrhizal (AM) association is critical for predicting the effects of AM symbiosis on elemental cycling for plants. Both mulberry (Morus alba) and Chinese prickly ash (Zanthoxylum bungeanum) are AM-associated plants, widely distributed in southwest China. It was hypothesized that if the nutrient absorption processes were efficiently associated with AM symbiosis in both mulberry and Chinese prickly ash, foliar nutrient concentrations—especially calcium (Ca)—would be primarily determined by the soil conditions in different regions. To investigate this, AM colonization levels of soils, nutrient levels in soils and leaves, and δ13C values of leaves were analyzed for mulberry and Chinese prickly ash. In this study, spore density in soils with low pH was higher than that in soils with high pH. The average concentrations of sugar delivered to roots in both mulberry and Chinese prickly ash in soil with relatively low pH and soil extractable cations were higher than those in other areas. The values of foliar δ13C in both mulberry and Chinese prickly ash in low soil-pH and soil extractable cations were lower than those in contrast areas, indicating that water availability was impacted by soil characteristics. The efficiency in AM-mediated processes might play an important role in translocation between soil nutrients and plant tissue. The results suggest uptake and translocation of nutrients, especially Ca, in AM-associated plants may be affected by an efficiency of AM-mediated processes. Since Sr does not appear to be similarly affected, expressing Ca and other nutrient concentrations relative to Sr could be used to evaluate whether the uptake and translocation of Ca and other nutrients are affected by AM-mediated processes.
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Aliasgharzadeh N, Rastin NS, 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
Al-Karaki GN, Al-Omoush M (2002) Wheat response to phosphogypsum and mycorrhizal fungi in alkaline soil. J Plant Nutr 25(4):873–883
An G-H, Miyakawa S, Kawahara A, Osaki M, Ezawa T (2008) Community structure of arbuscular mycorrhizal fungi associated with pioneer grass species Miscanthus sinensis in acid sulfate soils: habitat segregation along pH gradients. Soil Sci Plant Nutr 54:517–528
Baes AU, Bloom PR (1988) Exchange of alkaline earth cations in soil organic matter. Soil Sci 146:6–14
Bárcenas-Moreno G, Rousk J, Bååth E (2011) Fungal and bacterial recolonisation of acid and alkaline forest soils following artificial heat treatments. Soil Biol Biochem 43:1023–1033
Bárzana G, Aroca R, Paz JA, Chaumont F, Martinez-Ballesta MC, Carvajal M, Ruiz-Lozano JM (2012) Arbuscular mycorrhizal symbiosis increases relative apoplastic water flow in roots of the host plant under both well-watered and drought stress conditions. Ann Bot 109:1009–1017
Blum JD, Dasch AA, Hamburg SP, Yanai RD, Arthur MA (2008) Use of foliar Ca/Sr discrimination and 87Sr/86Sr ratios to determine soil Ca sources to sugar maple foliage in a northern hardwood forest. Biogeochemistry 87:287–296
Blum JD, Hamburg SP, Yanai RD, Arthur MA (2012) Determination of foliar Ca/Sr discrimination factors for six tree species and implications for Ca sources in northern hardwood forests. Plant Soil 356:303–314
Caines AM, Shennan C (1999) Growth and nutrient composition of Ca2+ use efficient and Ca2+ use inefficient genotypes of tomato. Plant Physiol Biochem 37:559–567
Chinnasamy G, Bal AK (2003) Seasonal changes in carbohydrates of perennial root nodules of beach pea. J Plant Physiol 160:1185–1192
Clarholm M, Skyllberg U (2013) Translocation of metals by trees and fungi regulates pH, soil organic matter turnover and nitrogen availability in acidic forest soils. Soil Biol Biochem 63:142–153
Clarkson DT (1984) Calcium transport between tissues and its distribution in the plant. Plant Cell Environ 7:449–456
Dasch AA, Blum JD, Eagar C, Fahey TJ, Driscoll CT, Siccama TG (2006) The relative uptake of Ca and Sr into tree foliage using a whole-watershed calcium addition. Biogeochemistry 80:21–41
De Beenhouwer M, Van Geel M, Ceulemans T, Muleta D, Lievens B, Honnay O (2015) Changing soil characteristics alter arbuscular mycorrhizal fungi communities of Arabica coffee (Coffea Arabica) in Ethiopia across a management gradient. Soil Biol Biochem 91:133–139
Doubková P, Suda J, Sudová R (2012) Arbuscular mycorrhizal symbiosis on serpentine soils: the effect of native fungal communities on different Knautia arvensis ecotypes. Plant Soil 345:325–338
Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280
Farquhar GD, Hubick KT, Condon AG, Richards RA (1988) Carbon isotope fractionation and plant water-use efficiency. Ecol Stud 68:21–40
Funk JL, Amatangelo KL (2013) Physiological mechanisms drive differing foliar calcium content in ferns and angiosperms. Oecologia 173:23–32
George E, Haussler K, Vetterlein G, Gorgus E, Marschner H (1992) Water and nutrient translocation by hyphae of Glomus mosseae. Can J Bot 70:2130–2137
Gosling P, Hodge A, Goodlass G, Bending GD (2006) Arbuscular mycorrhizal fungi and organic farming. Agric Ecosyst Environ 113:17–35
Graetz DA, Nair VD, Portier KM, Voss RL (1999) Phosphorus accumulation in manure-impacted Spodosols of Florida. Agric Ecosyst Environ 75:31–40
Grant OM, Davies MJ, James CM, Johnson AW, Leinonen I, Simpson DW (2012) Thermal imaging and carbon isotope composition indicate variation amongst strawberry (Fragaria x ananassa) cultivars in stomatal conductance and water use efficiency. Environ Exp Bot 76:7–15
Guha A, Sengupta D, Rasineni GK, Reddy AR (2012) Non-enzymatic antioxidative defence in drought-stressed mulberry (Morus indica L.) genotypes. Trees 26:903–918
Guo YJ, Ni Y, Raman H, Wilson AL, Ash GJ, Wang AS, Li GD (2012) Arbuscular mycorrhizal fungal diversity in perennial pastures; responses to long-term lime application. Plant Soil 351:389–403
Hawkins H-J, George E (2001) Reduced 15N-nitrogen transport through arbuscular mycorrhizal hyphae to Triticum aestivum L. supplied with ammonium vs. nitrate nutrition. Ann Bot 87:303–311
Huang XH, Liu Y, Li JX, Xiong XZ, Chen Y, Yin XH, Feng DL (2013) The response of mulberry trees after seedling hardening to summer drought in the hydro-fluctuation belt of three Gorges reservoir areas. Environ Sci Pollut Res 20:7103–7111
Hubick KT, Farquhar GD, Shorter R (1986) Correlation between water-use efficiency and carbon isotope discrimination in diverse peanut (Arachis) germplasm. Aust J Plant Physiol 13:803–816
Jiang YB, Ji HB (2011) Sr fluxes and 87Sr/86Sr characterization of river waters from a karstic versus granitic watershed in the Yangtze River. J Geochem Explor 110:202–215
Karley AJ, Leigh RA, Sanders D (2000) Where do all the ions go? The cellular basis of differential ion accumulation in leaf cells. Trends Plant Sci 5:465–470
Karpova EA, Gomonova NF (2006) Strontium in an agrocenosis on a soddy-podzolic soil under conditions of the long-term effect and aftereffect of fertilizers. Eur J Soil Sci 39:779–784
Kerley SJ (2000) Changes in root morphology of white lupin (Lupinus albus L.) and its adaptation to soils with heterogeneous alkaline/acid profiles. Plant Soil 218(1–2):197–205
Khabou W, Hajji B, Zouari M, Rigane H, Abdallah FB (2014) Arbuscular mycorrhizal fungi improve growth and mineral uptake of olive tree under gypsum substrate. Ecol Eng 73:290–296
Labidi S, Jeddi FB, Tisserant B, Debiane D, Rezgui S, Grandmougin-Ferjani A, Sahraoui AL-H (2012) Role of arbuscular mycorrhizal symbiosis in root mineral uptake under CaCO3 stress. Mycorrhiza 22:337–345
Ladeyn I, Plassard C, Staunton S (2008) Mycorrhizal association of maritime pine, Pinus pinaster, with Rhizopogon roseolus has contrasting effects on the uptake from soil and root-to-shoot trasfer of 137Cs, 85Sr and 95mTc. J Environ Radioact 99:853–863
Li LF, Yang AN, Zhao ZW (2005) Seasonality of arbuscular mycorrhizal symbiosis and dark septate endophytes in a grassland site in southwest China. FEMS Microbiol Ecol 54:367–373
Li S-L, Liu C-Q, Li J, Xue Z, Guan J, Lang Y, Ding H, Li L (2013) Evaluation of nitrate source in surface water of southwestern China based on stable isotopes. Environ Earth Sci 68:219–228
Liu C-Q (2007) Biogeochemical processes and cycling of nutrients in the Earth’s surface: chemical erosion and nutrient cycling in Karstic catchments, Southwest China. Science Press, Beijing, p 608
Mårtensson L-M, Schnoor TK, Olsson PA (2012) Allocation of carbon to mycorrhiza in the grasses Koeleria glauca and Corynephorus canescens in sandy grasslands. Appl Soil Ecol 54:55–62
McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501
Meding SM, Zasoski RJ (2008) Hyphal-mediated transfer of nitrate, arsenic, cesium, rubidium, and strontium between arbuscular mycorrhizal forbs and grasses from a California oak woodland. Soil Biol Biochem 40:126–134
Moody PW, Aitken RL (1997) Soil acidification under some tropical agricultural systems: rates of acidification and contributing factors. Aust J Soil Res 35:163–173
Müller A, George E, Gabriel-Neumann E (2013) The symbiotic recapture of nitrogen from dead mycorrhizal and non-mycorrhizal roots of tomato plants. Plant Soil 364:341–355
Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circ. 939, Washington
Olsson PA, Schnoor TK, Hanson S-A (2010) pH preferences of red-listed gasteromycetes in calcareous sandy grasslands: implications for conservation and restoration. Fungal Ecol 3:357–365
Orozco-Patiño F, Medina-Sierra M (2013) Effects of arbuscular mycorrhizal fungal species and the medium pH on the growth of Pueraria phaseoloides (Roxb.) Benth. Symbiosis 60:65–71
Parekh NR, Poskitt JM, Dodd BA, Potter ED, Sanchez A (2008) Soil microorganisms determine the sorption of radionuclides within organic soil systems. J Environ Radioact 99:841–852
Pascual M, Lordan J, Villar JM, Fonseca F, Rufat J (2013) Stable carbon and nitrogen isotope ratios as indicators of water status and nitrogen effects on peach trees. Sci Hortic 157:99–107
Piao H-C, Liu C-Q (2011) Variations in nitrogen, zinc and sugar concentrations in Chinese fir seedlings grown on shrubland and ploughed soils in response to arbuscular mycorrhizae-mediated process. Biol Fertil Soils 47:721–727
Piao H-C, Liu C-Q (2012) Response of biomass accumulation and nodulation by Vicia villosa to soil conditions: evidence from δ13C and δ15N isotopes. Chin J Geochem 31:119
Piao H-C, Liu C-Q, Wang S-J (2012) Isotopic evaluation of the role of arbuscular mycorrhizae in the nitrogen preference in Chinese fir seedlings. Pedobiologia 55:167–174
Poszwa A, Dambrine E, Pollier B, Atteia O (2000) A comparison between Ca and Sr cycling in forest ecosystems. Plant Soil 225:299–310
Richardson AE, Barea J-M, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339
Rillig MC (2004) Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecol Lett 7:740–754
Shtangeeva I, Steinnes E, Lierhagen S (2011) Macronutrients and trace elements in rye and wheat: similarities and differences in uptake and relationships between elements. Environ Exp Bot 70:259–265
Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, San Diego
Smith SE, Facelli E, Pope S, Smith FA (2010) Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant Soil 326:3–20
Stark S, EsKelinen A, Männistö MK (2011) Regulation of microbial community composition and activity by soil nutrient availability, soil pH, and herbivory in the tundra. Ecosystems 15:18–33
Suárez N (2010) Leaf lifetime photosynthetic rate and leaf demography in whole plants of Ipomoea pes-caprae growing with a low supply of calcium, a ‘non-mobile’ nutrient. J Exp Bot 61:843–855
Taylor J, Harrier LA (2001) A comparison of development and mineral nutrition of micropropagated Fragaria X ananassa cv. Elvira (strawberry) when colonised by nine species of arbuscular mycorrhizal fungi. Appl Soil Ecol 18:205–215
Theuerl S, Buscot F (2010) Laccases: toward disentangling their diversity and functions in relation to soil organic mater cycling. Biol Fertil Soils 46:215–225
Thomas GW (1982) Exchangeable cations. In: Page AL, Miller RH, Keeney (eds) Methods of soil analysis, Part 2. Chemical and microbiological properties-agronomy monograph no. 9, 2nd edn. ASA-SSSA, Madison, pp 159–165
Van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310
Van der Heijden G, Dambrine E, Pollier B, Zeller B, Ranger J, Legout A (2015) Mg and Ca uptake by roots in relation to depth and allocation to aboveground tissues: results from an isotopic labeling study in a beech forest on base-poor soil. Biogeochemistry 122:375–393
Veresoglou SD, Shaw LJ, Sen RB (2011) Glomus intraradices and Gigaspora margarita arbuscular mycorrhizal associations differentially affect nitrogen and potassium nutrition of Plantago lanceolata in a low fertility dune soil. Plant Soil 340:481–490
Wang S-J, Liu Q-M, Zhang D-F (2004) Karst rocky desertification in southwestern China: geomorphology, landuse, impact and rehabilitation. Land Degrad Dev 15:115–121
Wang P, Shu B, Wang Y, Zhang DJ, Liu JF, Xia JF (2013) Diversity of arbuscular mycorrhizal fungi in red tangerine (Citrus reticulate Blanco) rootstock rhizospheric soils from hillside citrus orchads. Pedobiologia 56:161–167
Xiao JX, Hu CY, Chen YY, Yang B, Hua J (2014) Effects of low magnesium and an arbuscular mycorrhizal fungus on the growth, magnesium distribution and photosynthesis of two citrus cultivars. Sci Hortic 177:14–20
Zhu Y-G, Miller RM (2003) Carbon cycling by arbuscular mycorrhizal fungi in soil-plant systems. Trends Plant Sci 8:407–409
Acknowledgments
The authors wish to thank Dr. Z. W. Zhao, from the Key Laboratory for Conservation and Utilization of Bio-resources of Yunnan University for assistance in determining arbuscular mycorrhizal colonization levels. This study was financially supported by the National Natural Science Foundation of China (Grant no. 4121004), and water project of MEP (2012ZX07503003001).
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Piao, H., Li, S. & Wang, S. Nutrient uptake by mulberry and Chinese prickly ash associated with arbuscular mycorrhizal fungi. Acta Geochim 35, 120–129 (2016). https://doi.org/10.1007/s11631-016-0097-3
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DOI: https://doi.org/10.1007/s11631-016-0097-3