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Arbuscular mycorrhizal fungi alleviate abiotic stresses in potato plants caused by low phosphorus and deficit irrigation/partial root-zone drying

Published online by Cambridge University Press:  05 February 2018

Caixia Liu*
Affiliation:
Department of Agroecology, Faculty of Science and Technology, Aarhus University, Blichers Allé 20, 8830 Tjele, Denmark
Sabine Ravnskov
Affiliation:
Department of Agroecology, Faculty of Science and Technology, Aarhus University, Blichers Allé 20, 8830 Tjele, Denmark
Fulai Liu
Affiliation:
Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Højbakkegård Allé 13, 2630 Tåstrup, Denmark
Gitte H. Rubæk
Affiliation:
Department of Agroecology, Faculty of Science and Technology, Aarhus University, Blichers Allé 20, 8830 Tjele, Denmark
Mathias N. Andersen
Affiliation:
Department of Agroecology, Faculty of Science and Technology, Aarhus University, Blichers Allé 20, 8830 Tjele, Denmark
*
Author for correspondence: Caixia Liu, E-mail: caixialiu21@hotmail.com

Abstract

Deficit irrigation (DI) improves water use efficiency (WUE), but the reduced water input often limits plant growth and nutrient uptake. The current study examined whether arbuscular mycorrhizal fungi (AMF) could alleviate abiotic stress caused by low phosphorus (P) fertilization and DI.

A greenhouse experiment was conducted with potato grown with (P1) or without (P0) P fertilization, with AMF (M1+: Rhizophagus irregularis or M2+: Glomus proliferum) or AMF-free control (M−) and subjected to full irrigation (FI), DI or partial root-zone drying (PRD).

Inoculation of M1+ and M2+ maintained or improved plant growth and P/nitrogen (N) uptake when subjected to DI/PRD and P0. However, the positive responses to AMF varied with P level and irrigation regime. Functional differences were found in ability of AMF species alleviating plant stress. The largest positive plant biomass response to M1+ and M2+ was found under FI, both at P1 and P0 (25% increase), while plant biomass response to M1+ and M2+ under DI/PRD (14% increase) was significantly smaller. The large growth response to AMF inoculation, particularly under FI, may relate to greater photosynthetic capacity and leaf area, probably caused by stimulation of plant P/N uptake and carbon partitioning toward roots and tubers. However, plant growth response to AMF was not related to the percentage of AMF root colonization. Arbuscular mycorrhizal fungi can maintain and improve P/N uptake, WUE and growth of plants both at high/low P levels and under FI/DI. If this is also the case under field conditions, it should be implemented for sustainable potato production.

Type
Crops and Soils Research Paper
Copyright
Copyright © Cambridge University Press 2018 

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References

Adholeya, A, Tiwari, P and Singh, R (2005) Large-scale inoculum production of arbuscular mycorrhizal fungi on root organs and inoculation strategies. In Declerck, S, Strullu, DG and Fortin, JA (eds). In Vitro Culture of Mycorrhizas. Berlin, Germany: Springer, pp. 315338.CrossRefGoogle Scholar
Ahmadi, SH, Andersen, MN, Plauborg, F, Poulsen, RT, Jensen, CR, Sepaskhah, AR and Hansen, S (2010) Effects of irrigation strategies and soils on field grown potatoes: yield and water productivity. Agricultural Water Management 97, 19231930.CrossRefGoogle Scholar
Aliasgharzad, N, Bolandnazar, SA, Neyshabouri, MR and Chaparzadeh, N (2009) Impact of soil sterilization and irrigation intervals on P and K acquisition by mycorrhizal onion (Allium cepa). Biologia 64, 512515.CrossRefGoogle Scholar
Aroca, R, Vernieri, P and Ruiz-Lozano, JM (2008) Mycorrhizal and non-mycorrhizal Lactuca sativa plants exhibit contrasting responses to exogenous ABA during drought stress and recovery. Journal of Experimental Botany 59, 20292041.CrossRefGoogle ScholarPubMed
Auge, RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11, 342.Google Scholar
Bago, B, Vierheilig, H, Piché, Y and Azcón-Aguilar, C (1996) Nitrate depletion and pH changes induced by the extraradical mycelium of the arbuscular mycorrhizal fungus Glomus intraradices grown in monoxenic culture. New Phytologist 133, 273280.CrossRefGoogle ScholarPubMed
Balemi, T (2009) Effect of phosphorus nutrition on growth of potato genotypes with contrasting phosphorus efficiency. African Crop Science Journal 17, 199212.Google Scholar
Balzergue, C, Puech-Pages, V, Becard, G and Rochange, SF (2011) The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signalling events. Journal of Experimental Botany 62, 10491060.CrossRefGoogle ScholarPubMed
Bates, D, Maechler, M, Bolker, B and Walker, S (2014) lme4: Linear Mixed-effects Models Using Eigen and S4. R package version 1.1-7. Available at http://CRAN.R-project.org/package=lme4 (Accessed 11 December 2017).Google Scholar
Biemond, H, Vos, J and Struik, PC (1995) Effects of nitrogen on development and growth of the leaves of vegetables. 1. Appearance, expansion growth and life span of leaves of Brussels sprouts plants. Netherlands Journal of Agricultural Science 43, 217232.CrossRefGoogle Scholar
Birhane, E, Sterck, FJ, Fetene, M, Bongers, F and Kuyper, TW (2012) Arbuscular mycorrhizal fungi enhance photosynthesis, water use efficiency, and growth of frankincense seedlings under pulsed water availability conditions. Oecologia 169, 895904.CrossRefGoogle ScholarPubMed
Black, KG, Mitchell, DT and Osborne, BA (2000) Effect of mycorrhizal-enhanced leaf phosphate status on carbon partitioning, translocation and photosynthesis in cucumber. Plant, Cell and Environment 23, 797809.CrossRefGoogle Scholar
Black, RLB and Tinker, PB (1977) Interaction between effects of vesicular-arbuscular mycorrhiza and fertilizer phosphorus on yields of potatoes in field. Nature 267, 510511.CrossRefGoogle Scholar
Boyer, LR, Brain, P, Xu, XM and Jeffries, P (2015) Inoculation of drought-stressed strawberry with a mixed inoculum of two arbuscular mycorrhizal fungi: effects on population dynamics of fungal species in roots and consequential plant tolerance to water deficiency. Mycorrhiza 25, 215227.CrossRefGoogle ScholarPubMed
Brachmann, A and Parniske, M (2006) The most widespread symbiosis on earth. PLoS Biology 4, 11111112.CrossRefGoogle Scholar
Ceballos, I, Ruiz, M, Fernandez, C, Pena, R, Rodriguez, A and Sanders, IR (2013) The in vitro mass-produced model mycorrhizal fungus, rhizophagus irregularis, significantly increases yields of the globally important food security crop cassava. PLoS ONE 8, e70633. Available at https://doi.org/10.1371/journal.pone.0070633 CrossRefGoogle ScholarPubMed
Cesaro, P, van Tuinen, D, Copetta, A, Chatagnier, O, Berta, G, Gianinazzi, S and Lingua, G (2008) Preferential colonization of Solanum tuberosum L. roots by the fungus Glomus intraradices in arable soil of a potato farming area. Applied and Environmental Microbiology 74, 57765783.CrossRefGoogle ScholarPubMed
Davies, FT, Calderon, CM and Huaman, Z (2005) Influence of arbuscular mycorrhizae indigenous to Peru and a flavonoid on growth, yield, and leaf elemental concentration of ‘Yungay’ potatoes. Hortscience 40, 381385.CrossRefGoogle Scholar
Davies, WJ and Hartung, W (2004) Has extrapolation from biochemistry to crop functioning worked to sustain plant production under water scarcity? In Fischer, T, Turner, N, Angus, J, McIntyre, L, Robertson, M, Borrell, A and Lloyd, D (eds). Proceedings of the Fourth International Crop Science Congress, Brisbane, Australia. Gosford, Australia: The Regional Institute Ltd. Available at http://agronomyaustraliaproceedings.org/index.php/26-2004-conference-information/122-physiology (Accessed 8 January 2018).Google Scholar
Davies, WJ, Wilkinson, S and Loveys, B (2002) Stomatal control by chemical signalling and the exploitation of this mechanism to increase water use efficiency in agriculture. New Phytologist 153, 449460.CrossRefGoogle ScholarPubMed
Declerck, S, Cranenbrouck, S, Dalpé, Y, Séguin, S, Grandmougin-Ferjani, A, Fontaine, J and Sancholle, M (2000) Glomus proliferum sp. nov.:a description based on morphological, biochemical, molecular and monoxenic cultivation data. Mycologia 92, 11781187.CrossRefGoogle Scholar
Douds, DD, Nagahashi, G, Reider, C and Hepperly, PR (2007) Inoculation with arbuscular mycorrhizal fungi increases the yield of potatoes in a high P soil. Biological Agriculture & Horticulture 25, 6778.CrossRefGoogle Scholar
Dry, PR, Loveys, BR, Botting, D and During, H (1996) Effects of partial rootzone drying on grapevine vigour, yield, composition of fruit and use of water. In Stockley, CS, Sas, AN, Johnstone, RS and Lee, TH (eds). Proceedings of the 9th Australian Wine Industry Technical Conference. Adelaide, Australia: Winetitles, pp. 126131.Google Scholar
English, MJ, Musick, JT and Murty, VVN (1990) Deficit irrigation. In Hoffman, GJ, Howell, TA and Solomon, KH (eds). Management of Farm Irrigation System. St. Joseph, MI: American Society of Agricultural Engineers, pp. 631663.Google Scholar
Feddermann, N, Finlay, R, Boller, T and Elfstrand, M (2010) Functional diversity in arbuscular mycorrhiza – the role of gene expression, phosphorous nutrition and symbiotic efficiency. Fungal Ecology 3, 18.CrossRefGoogle Scholar
Fellbaum, CR, Gachomo, EW, Beesetty, Y, Choudhari, S, Strahan, GD, Pfeffer, PE, Kiers, ET and Bücking, H (2012) Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences of the USA 109, 26662671.CrossRefGoogle ScholarPubMed
Fohse, D, Claassen, N and Jungk, A (1988) Phosphorus efficiency of plants. 1. External and internal P requirement and P uptake efficiency of different plant species. Plant and Soil 110, 101109.Google Scholar
Freeman, KL, Franz, PR and De Jong, RW (1998) Effect of phosphorus on the yield, quality, and petiolar phosphorus concentration of potatoes (cvs. Russet Burbank and Kennebec) grown in the krasnozem and duplex soils of Victoria. Australian Journal of Experimental Agriculture 38, 8393.CrossRefGoogle Scholar
Frossard, E, Condron, LM, Oberson, A, Sinaj, S and Fardeau, JC (2000) Processes governing phosphorus availability in temperate soils. Journal of Environmental Quality 29, 1523.CrossRefGoogle Scholar
Gahoonia, TS, Raza, S and Nielsen, NE (1994) Phosphorus depletion in the rhizosphere as influenced by soil-moisture. Plant and Soil 159, 213218.CrossRefGoogle Scholar
Gaur, A, Adholeya, A and Mukerji, KG (1998) A comparison of AM fungi inoculants using capsicum and Polianthes in marginal soil amended with organic matter. Mycorrhiza 7, 307312.CrossRefGoogle Scholar
Giovannetti, M and Mosse, B (1980) An evaluation of techniques for measuring vesicular-arbuscular infection in roots. New Phytologist 84, 489500.CrossRefGoogle Scholar
Gordon, H, Haygarth, PM and Bardgett, RD (2008) Drying and rewetting effects on soil microbial community composition and nutrient leaching. Soil Biology and Biochemistry 40, 302311.CrossRefGoogle Scholar
Hack, H, Gall, H, Klemke, T, Klose, R, Meier, U, Stauss, R and Witzenberger, A (2001) The BBCH scale for phonological growth stages of potato (Solanum tuberosum L.). In Meier, U (ed.). Growth Stages of Mono and Dicotyledonous Plants BBCH Monograph. Berlin, Germany: Federal Biological Research Centre for Agriculture and Forestry. Available at https://www.politicheagricole.it/flex/AppData/WebLive/Agrometeo/MIEPFY800/BBCHengl2001.pdf (Accessed 11 December 2017).Google Scholar
Hawkins, HJ, Johansen, A and George, E (2000) Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant and Soil 226, 275285.CrossRefGoogle Scholar
Hijri, M (2016) Analysis of a large dataset of mycorrhiza inoculation field trials on potato shows highly significant increases in yield. Mycorrhiza 26, 209214.CrossRefGoogle ScholarPubMed
Hodge, A and Storer, K (2015) Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant and Soil 386, 119.CrossRefGoogle Scholar
Jakobsen, I and Rosendahl, L (1990) Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytologist 115, 7783.CrossRefGoogle Scholar
Jakobsen, I, Abbott, LK and Robson, AD (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium-subterraneum L. 1 spread of hyphae and phosphorus inflow into roots. New Phytologist 120, 371380.CrossRefGoogle Scholar
Jayne, B and Quigley, M (2014) Influence of arbuscular mycorrhiza on growth and reproductive response of plants under water deficit: a meta-analysis. Mycorrhiza 24, 109119.CrossRefGoogle ScholarPubMed
Jenkins, PD and Ali, H (1999) Growth of potato cultivars in response to application of phosphate fertiliser. Annals of Applied Biology 135, 431438.CrossRefGoogle Scholar
Kaschuk, G, Kuyper, TW, Leffelaar, PA, Hungria, M and Giller, KE (2009) Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biology and Biochemistry 41, 12331244.CrossRefGoogle Scholar
Kuo, CG and Huang, RS (1982) Effect of vesicular-arbuscular mycorrhizae on the growth and yield of rice-stubble cultured soybeans. Plant and Soil 64, 325330.CrossRefGoogle Scholar
Lawlor, DW (2002) Limitation to photosynthesis in water-stressed leaves: stomata vs. metabolism and the role of ATP. Annals of Botany 89, 871885.CrossRefGoogle ScholarPubMed
Liu, CX, Rubæk, GH, Liu, FL and Andersen, MN (2015 a) Effect of partial root zone drying and deficit irrigation on nitrogen and phosphorus uptake in potato. Agricultural Water Management 159, 6676.CrossRefGoogle Scholar
Liu, CX, Liu, FL, Ravnskov, S, Rubæk, GH, Sun, ZC and Andersen, MN (2017) Impact of wood biochar and its interactions with mycorrhizal fungi, phosphorus fertilization and irrigation strategies on potato growth. Journal of Agronomy and Crop Science 203, 131145.CrossRefGoogle Scholar
Liu, FL, Shahnazari, A, Andersen, MN, Jacobsen, SE and Jensen, CR (2006) Effects of deficit irrigation (DI) and partial root drying (PRD) on gas exchange, biomass partitioning, and water use efficiency in potato. Scientia Horticulturae 109, 113117.CrossRefGoogle Scholar
Liu, FL, Song, R, Zhang, XY, Shahnazari, A, Andersen, MN, Plauborg, F, Jacobsen, SE and Jensen, CR (2008) Measurement and modelling of ABA signalling in potato (Solanum tuberosum L.) during partial root-zone drying. Environmental and Experimental Botany 63, 385391.CrossRefGoogle Scholar
Liu, Z, Li, Y, Wang, J, He, XY and Tian, CJ (2015 b) Different respiration metabolism between mycorrhizal and non-mycorrhizal rice under low-temperature stress: a cry for help from the host. Journal of Agricultural Science, Cambridge 153, 602614.CrossRefGoogle Scholar
McArthur, DAJ and Knowles, NR (1993 a) Influence of species of vesicular-arbuscular mycorrhizal fungi and phosphorus-nutrition on growth, development, and mineral-nutrition of potato (Solanum-tuberosum L). Plant Physiology 102, 771782.CrossRefGoogle ScholarPubMed
McArthur, DAJ and Knowles, NR (1993 b) Influence of vesicular-arbuscular mycorrhizal fungi on the response of potato to phosphorus deficiency. Plant Physiology 101, 147160.CrossRefGoogle ScholarPubMed
Neumann, E, Schmid, B, Romheld, V and George, E (2009) Extraradical development and contribution to plant performance of an arbuscular mycorrhizal symbiosis exposed to complete or partial rootzone drying. Mycorrhiza 20, 1323.CrossRefGoogle ScholarPubMed
Niemira, BA, Safir, GR, Hammerschmidt, R and Bird, GW (1995) Production of prenuclear minitubers of potato with feat-based arbuscular mycorrhizal fungal inoculum. Agronomy Journal 87, 942946.CrossRefGoogle Scholar
Olsen, S, Cole, C, Watanabe, F and Dean, L (1954) Estimation of Available Phosphorus in Soils by Extraction with Sodium Bicarbonate. USDA Circular Nr 939. Washington, DC: USDA.Google Scholar
Park, M, Singvilay, A, Shin, W, Kim, E, Chung, J and Sa, T (2004) Effects of long-term compost and fertilizer application on soil phosphorus status under paddy cropping system. Communications in Soil Science and Plant Analysis 35, 16351644.CrossRefGoogle Scholar
Paul, MJ and Foyer, CH (2001) Sink regulation of photosynthesis. Journal of Experimental Botany 52, 13831400.CrossRefGoogle ScholarPubMed
Plaxton, WC and Tran, HT (2011) Metabolic adaptations of phosphate-starved plants. Plant Physiology 156, 10061015.CrossRefGoogle ScholarPubMed
Prummel, J and Von Barnau-Sijthoff, PA (1984) Optimum phosphate and potassium levels in potato tops. Fertilizer Research 5, 203211.CrossRefGoogle Scholar
R Core Team (2014) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Ruiz-Lozano, JM and Azcon, R (1995) Hyphal contribution to water uptake in mycorrhizal plants as affected by the fungal species and water status. Physiologia Plantarum 95, 472478.CrossRefGoogle Scholar
Ruiz-Sanchez, M, Armada, E, Munoz, Y, de Salamone, IEG, Aroca, R, Ruiz-Lozano, JM and Azcon, R (2011) Azospirillum and arbuscular mycorrhizal colonization enhance rice growth and physiological traits under well-watered and drought conditions. Journal of Plant Physiology 168, 10311037.CrossRefGoogle ScholarPubMed
Schachtman, DP, Reid, RJ and Ayling, SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiology 116, 447453.CrossRefGoogle ScholarPubMed
Schreiner, RP, Tarara, JM and Smithyman, RP (2007) Deficit irrigation promotes arbuscular colonization of fine roots by mycorrhizal fungi in grapevines (Vitis vinifera L.) in an arid climate. Mycorrhiza 17, 551562.CrossRefGoogle Scholar
Sharkey, TD (1985) Photosynthesis in intact leaves of C3 plants: physics, physiology and rate limitations. Botanical Review 51, 53105.CrossRefGoogle Scholar
Sharma, MP, Gaur, A, Bhatia, NP and Adholeya, A (1996) Growth responses and dependence of Acacia nilotica var cupriciformis on the indigenous arbuscular mycorrhizal consortium of a marginal wasteland soil. Mycorrhiza 6, 441446.CrossRefGoogle Scholar
Sibbesen, E and Runge-Metzger, A (1995) Phosphorus balance in European agriculture – status and policy options. In Tiessen, H (ed.). Phosphorus in the Global Environment – Transfers, Cycles and Management. SCOPE 54. Chichester, UK: John Wiley and Sons, pp. 4357.Google Scholar
Sissingh, HA (1971) Analytical technique of Pw method, used for assessment of phosphate status of arable soils in the Netherlands. Plant and Soil 34, 483486.CrossRefGoogle Scholar
Smith, SE and Smith, FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annual Review of Plant Biology 62, 227250.CrossRefGoogle ScholarPubMed
Smith, SE and Smith, FA (2012) Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia 104, 113.CrossRefGoogle ScholarPubMed
Smith, SE, Smith, FA and Jakobsen, I (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytologist 162, 511524.CrossRefGoogle Scholar
Smith, SE, Jakobsen, I, Gronlund, M and Smith, FA (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, 10501057.CrossRefGoogle ScholarPubMed
Stuffins, CB (1967) Determination of phosphate and calcium in feeding stuffs. The Analyst 92, 107111.CrossRefGoogle ScholarPubMed
Sun, YQ, Cui, XY and Liu, FL (2015) Effect of irrigation regimes and phosphorus rates on water and phosphorus use efficiencies in potato. Scientia Horticulturae 190, 6469.CrossRefGoogle Scholar
Tabatabai, MA and Bremner, JM (1969) Use of p-nitrophenylphosphate for assay of soil phosphatase activity. Soil Biology and Biochemistry 1, 301307.CrossRefGoogle Scholar
Tarkalson, DD, Jolley, VD, Robbins, CW and Terry, RE (1998) Mycorrhizal colonization and nutrient uptake of dry bean in manure and compost manure treated subsoil and untreated topsoil and subsoil. Journal of Plant Nutrition 21, 18671878.CrossRefGoogle Scholar
Turner, BL, Driessen, JP, Haygarth, PM and Mckelvie, ID (2003) Potential contribution of lysed bacterial cells to phosphorus solubilisation in two rewetted Australian pasture soils. Soil Biology and Biochemistry 35, 187189.CrossRefGoogle Scholar
Vierheilig, H, Coughlan, AP, Wyss, U and Piche, Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Applied and Environmental Microbiology 64, 50045007.CrossRefGoogle Scholar
Wang, YS, Liu, FL, Jensen, LS, De Neergaard, A and Jensen, CR (2013) Alternate partial root-zone irrigation improves fertilizer-N use efficiency in tomatoes. Irrigation Science 31, 589598.CrossRefGoogle Scholar
Weisz, R, Kaminski, J and Smilowitz, Z (1994) Water-deficit effects on potato leaf growth and transpiration – utilizing fraction extractable soil-water for comparison with other crops. American Potato Journal 71, 829840.CrossRefGoogle Scholar
White, PJ, Broadley, MR, Hammond, JP and Thompson, AJ (2005) Optimising the potato root system for phosphorus and water acquisition in low-input growing systems. Aspects of Applied Biology 73, 111118.Google Scholar
Wright, DP, Read, DJ and Scholes, JD (1998) Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L. Plant, Cell and Environment 21, 881891.CrossRefGoogle Scholar
Wu, QS, Srivastava, AK and Zou, YN (2013) AMF-induced tolerance to drought stress in citrus: a review. Scientia Horticulturae 164, 7787.CrossRefGoogle Scholar
Yamaguchi, J (2002) Measurement of root diameter in field-grown crops under a microscope without washing. Soil Science and Plant Nutrition 48, 625629.CrossRefGoogle Scholar
Yooyongwech, S, Phaukinsang, N, Cha-um, S and Supaibulwatana, K (2013) Arbuscular mycorrhiza improved growth performance in Macadamia tetraphylla L. grown under water deficit stress involves soluble sugar and proline accumulation. Plant Growth Regulation 69, 285293.CrossRefGoogle Scholar
Yu, GR, Zhuang, J, Nakayama, K and Jin, Y (2007) Root water uptake and profile soil water as affected by vertical root distribution. Plant Ecology 189, 1530.CrossRefGoogle Scholar
Zhao, B (2014) Determining of a critical dilution curve for plant nitrogen concentration in winter barley. Field Crops Research 160, 6472.CrossRefGoogle Scholar
Zhou, Q, Ravnskov, S, Jiang, D and Wollenweber, B (2014) Changes in carbon and nitrogen allocation, growth and grain yield induced by arbuscular mycorrhizal fungi in wheat (Triticum aestivum L.) subjected to a period of water deficit. Plant Growth Regulation 75, 751760.CrossRefGoogle Scholar
Zhu, XC, Song, FB, Liu, SQ and Liu, FL (2016) Arbuscular mycorrhiza improve growth, nitrogen uptake, and nitrogen use efficiency in wheat grown under elevated CO2 . Mycorrhiza 26, 133140.CrossRefGoogle ScholarPubMed