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

  • Caixia Liu (a1), Sabine Ravnskov (a1), Fulai Liu (a2), Gitte H. Rubæk (a1) and Mathias N. Andersen (a1)...


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.


Corresponding author

Author for correspondence: Caixia Liu, E-mail:


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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.
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.
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.
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.
Auge, RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11, 342.
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.
Balemi, T (2009) Effect of phosphorus nutrition on growth of potato genotypes with contrasting phosphorus efficiency. African Crop Science Journal 17, 199212.
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.
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 (Accessed 11 December 2017).
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.
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.
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.
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.
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.
Brachmann, A and Parniske, M (2006) The most widespread symbiosis on earth. PLoS Biology 4, 11111112.
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
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.
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.
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 (Accessed 8 January 2018).
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Gahoonia, TS, Raza, S and Nielsen, NE (1994) Phosphorus depletion in the rhizosphere as influenced by soil-moisture. Plant and Soil 159, 213218.
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.
Giovannetti, M and Mosse, B (1980) An evaluation of techniques for measuring vesicular-arbuscular infection in roots. New Phytologist 84, 489500.
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.
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 (Accessed 11 December 2017).
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.
Hijri, M (2016) Analysis of a large dataset of mycorrhiza inoculation field trials on potato shows highly significant increases in yield. Mycorrhiza 26, 209214.
Hodge, A and Storer, K (2015) Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant and Soil 386, 119.
Jakobsen, I and Rosendahl, L (1990) Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytologist 115, 7783.
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.
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.
Jenkins, PD and Ali, H (1999) Growth of potato cultivars in response to application of phosphate fertiliser. Annals of Applied Biology 135, 431438.
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.
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.
Lawlor, DW (2002) Limitation to photosynthesis in water-stressed leaves: stomata vs. metabolism and the role of ATP. Annals of Botany 89, 871885.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Paul, MJ and Foyer, CH (2001) Sink regulation of photosynthesis. Journal of Experimental Botany 52, 13831400.
Plaxton, WC and Tran, HT (2011) Metabolic adaptations of phosphate-starved plants. Plant Physiology 156, 10061015.
Prummel, J and Von Barnau-Sijthoff, PA (1984) Optimum phosphate and potassium levels in potato tops. Fertilizer Research 5, 203211.
R Core Team (2014) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
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.
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.
Schachtman, DP, Reid, RJ and Ayling, SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiology 116, 447453.
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.
Sharkey, TD (1985) Photosynthesis in intact leaves of C3 plants: physics, physiology and rate limitations. Botanical Review 51, 53105.
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.
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.
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.
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.
Smith, SE and Smith, FA (2012) Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia 104, 113.
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.
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.
Stuffins, CB (1967) Determination of phosphate and calcium in feeding stuffs. The Analyst 92, 107111.
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.
Tabatabai, MA and Bremner, JM (1969) Use of p-nitrophenylphosphate for assay of soil phosphatase activity. Soil Biology and Biochemistry 1, 301307.
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.
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.
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.
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.
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.
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.
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.
Wu, QS, Srivastava, AK and Zou, YN (2013) AMF-induced tolerance to drought stress in citrus: a review. Scientia Horticulturae 164, 7787.
Yamaguchi, J (2002) Measurement of root diameter in field-grown crops under a microscope without washing. Soil Science and Plant Nutrition 48, 625629.
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.
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.
Zhao, B (2014) Determining of a critical dilution curve for plant nitrogen concentration in winter barley. Field Crops Research 160, 6472.
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.
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.


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

  • Caixia Liu (a1), Sabine Ravnskov (a1), Fulai Liu (a2), Gitte H. Rubæk (a1) and Mathias N. Andersen (a1)...


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