Arbuscular Mycorrhizal Fungi Improve Tolerance of Agricultural Plants to Cope Abiotic Stress Conditions

  • Pablo CornejoEmail author
  • Alex Seguel
  • Paula Aguilera
  • Sebastián Meier
  • John Larsen
  • Fernando Borie


Abiotic stresses have strong impact on agriculture, decreasing the stability of agroecosystems worldwide, due mainly to water and nutrient limitations and the presence of toxic elements. Several studies have demonstrated that soil microorganisms can improve plant growth, even more when plants are under stressful conditions, being probably the most important are the arbuscular mycorrhizal fungi (AMF). This kind of fungi forms symbiosis with approximately 80% of plant species, including the majority of agricultural plants, and is present in all terrestrial ecosystems. Via its extraradical mycelium, the AMF can improve the absorption of water and nutrients of their host plants under stress conditions, as well as contribute to cope with the presence of toxic elements such as phytotoxic aluminum and other toxic metal(loid)s, increasing plant growth and crop production. Moreover, several studies have determined that AMF strains isolated from agroecosystems affected by different abiotic limiting conditions enhance the growth of plants than those isolated from soils without such limiting condition. In this chapter we describe the main ways by which AMF contribute to the plant tolerance to cope the abovementioned abiotic stresses. Moreover, the physiological, biochemical, and molecular bases that explain the responses mediated by AMF in host plants are covered. Finally, biotechnological prospects of AMF present under stress conditions and their potential use as bio-inoculants are presented.


Acid soils Fungal diversity Nutrient limitations Osmotic stress Potentially toxic elements 



The authors thank the financial support of FONDECYT-CONICYT (Grants 1120890 P. Cornejo, 11160385 A. Seguel, 3150175 P. Aguilera, 11150480 S. Meier, and 1130541 F. Borie). P. Cornejo thanks the Associative Research Project Program of the Universidad de La Frontera, Grant N PIA16-0005, which allowed the interaction with Dr. J. Larsen (UNAM-IIES).


  1. Abdel-Lateif K, Bogusz D, Hocher V (2012) The role of flavonoids in the establishment of plant roots endosymbioses with arbuscular mycorrhiza fungi, rhizobia and Frankia bacteria. Plant Signal Behav 7:636–641PubMedPubMedCentralCrossRefGoogle Scholar
  2. Adiku G, Renger M, Wessolek G, Facklam M, Hech-Bischoltz C (2001) Simulation of dry matter production and seed yield of common beans under varying soil water and salinity conditions. Agric Water Manag 47:55–68CrossRefGoogle Scholar
  3. Adriano DC (2001) Trace elements in terrestrial environments: biogeochemistry, bioavailability, and risk of metals. Springer, New YorkCrossRefGoogle Scholar
  4. Adriano DC, Wenzel WW, Vangronsveld J, Bolan NS (2004) Role of assisted natural remediation in environmental cleanup. Geoderma 122:121–142CrossRefGoogle Scholar
  5. Aguilera P, Borie F, Seguel A, Cornejo P (2011) Fluorescence detection of aluminum in arbuscular mycorrhizal fungal structures and glomalin by using confocal laser scanning microscopy. Soil Biol Biochem 43:2417–2431CrossRefGoogle Scholar
  6. Aguilera P, Cornejo P, Borie F, Barea JM, von Baer E, Oehl F (2014) Diversity of arbuscular mycorrhizal fungi associated with Triticum aestivum L. plants growing in an Andosol with high aluminum level. Agric Ecosyst Environ 186:178–184CrossRefGoogle Scholar
  7. Aguilera P, Cumming J, Oehl F, Cornejo P, Borie F (2015) Diversity of arbuscular mycorrhizal fungi in acidic soils and their contribution to aluminum phytotoxicity alleviation. In: Panda SK, Baluska F (eds) Aluminum stress adaptation in plants, Signaling and communication in plants, vol 24. Springer International Publishing, Cham, pp 203–228CrossRefGoogle Scholar
  8. Al-Karaki G, McMichael B, Zak J (2004) Field response of wheat to arbuscular mycorrhizal fungi and drought stress. Mycorrhiza 14:263–269PubMedCrossRefGoogle Scholar
  9. Anjum SA, Wang LC, Farooq M, Hussain M, Xue LL, Zou CM (2011) Brassinolide application improves the drought tolerance in maize through modulation of enzymatic antioxidants and leaf gas exchange. J Agron Crop Sci 197:177–185CrossRefGoogle Scholar
  10. Aroca R, Porcel R, Ruiz-Lozano MJ (2012) Regulation of root water uptake under abiotic stress conditions. J Exp Bot 63:43–57PubMedCrossRefGoogle Scholar
  11. Arriagada C, Herrera M, Borie F, Ocampo J (2007) Contribution of arbuscular mycorrhizal and saprobe fungi to the aluminum resistance of Eucalyptus globulus. Water Air Soil Poll 182:383–394CrossRefGoogle Scholar
  12. Asghari HR, Marschner P, Smith SE, Smith FA (2005) Growth response of Atriplex nummularia to inoculation with arbuscular mycorrhizal fungi at different salinity levels. Plant Soil 373:245–256CrossRefGoogle Scholar
  13. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216CrossRefGoogle Scholar
  14. Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3543PubMedCrossRefGoogle Scholar
  15. Azcón-Aguilar C, Barea JM (2015) Nutrient cycling in the mycorrhizosphere. J Soil Sci Plant Nutr 15:372–396Google Scholar
  16. Babeanu C, Constantin C, Paunescu G, Popa D (2010) Effect of drought stress on some oxidoreductase enzymes in five varieties of wheat. J Environ Protect Ecol 11:1280–1284Google Scholar
  17. Barea JM (2015) Future challenges and perspectives for applying microbial biotechnology in sustainable agriculture based on a better understanding of plant-microbiome interactions. J Soil Sci Plant Nutr 15:261–282Google Scholar
  18. Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778PubMedCrossRefGoogle Scholar
  19. Barea JM, Palenzuela J, Cornejo P, Sánchez-Castro I, Navarro-Fernández C, Lopéz-García A, Estrada B, Azcón R, Ferrol N, Azcón-Aguilar C (2011) Ecological and functional roles of mycorrhizas in semi-arid ecosystems of Southeast Spain. J Arid Environ 75:1292–1301CrossRefGoogle Scholar
  20. Bárzana G, Aroca R, Ruiz-Lozano JM (2015) Localized and non-localized effects of arbuscular mycorrhizal symbiosis on accumulation of osmolytes and aquaporins and on antioxidant systems in maize plants subjected to total or partial root drying. Plant Cell Environ 38:1613–1627PubMedCrossRefGoogle Scholar
  21. Bever J, Morton J, Antonovics J, Schultz P (1996) Host-dependent sporulation and species diversity of arbuscular mycorrhizal fungi in a mown grassland. J Ecol 84:71–82CrossRefGoogle Scholar
  22. Bhargava A, Clabaugh I, To JP, Maxwell BB, Chiang Y-H, Schaller GE, Loraine A, Kieber JJ (2013) Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-Seq in arabidopsis. Plant Physiol 162(1):272–294PubMedPubMedCentralCrossRefGoogle Scholar
  23. Bolan N, Naidu R, Syers JK, Tillman R (1999) Surface charge and solute interactions in soils. Adv Agron 67:87–140CrossRefGoogle Scholar
  24. Bolan N, Kunhikrishnan A, Thangarajan R, Kumpiene J, Park J, Makino T, Kirkham MB, Scheckel K (2014) Remediation of heavy metal(loid)s contaminated soils–to mobilize or to immobilize? J Hazard Mater 266:141–166PubMedCrossRefGoogle Scholar
  25. Bonfante P, Genre A (2015) Arbuscular mycorrhizal dialogues: do you speak ‘plantish’ or ‘fungish’? Trends Plant Sci 20:150–154PubMedCrossRefGoogle Scholar
  26. Borie F, Rubio R (1999) Effects of arbuscular mycorrhizae and liming on growth and mineral acquisition of aluminum-tolerant and aluminum-sensitive barley cultivars. J Plant Nutr 22:121–137CrossRefGoogle Scholar
  27. Borie F, Rubio R (2003) Total and organic phosphorus in Chilean volcanic soils. Gayana Botanica 60:69–78CrossRefGoogle Scholar
  28. Borie F, Zunino H (1983) Organic matter-phosphorus association as a sink in P fixation processes on allophanic soils of Chile. Soil Biol Biochem 15:599–603CrossRefGoogle Scholar
  29. Borie F, Rubio R, Morales A, Curaqueo G, Cornejo P (2010) Arbuscular mycorrhizae in agricultural and forest ecosystem in Chile. J Soil Sci Plant Nutr 10:185–206CrossRefGoogle Scholar
  30. Bray EA (2004) Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. J Exp Bot 55:2331–2341PubMedCrossRefGoogle Scholar
  31. Bûcking H, Kafle A (2015) Role of the arbuscular mycorrhizal fungi in the N uptake of plants. Current knowledge and research gaps. Agronomy 5:587–612CrossRefGoogle Scholar
  32. Calvo-Polanco M, Sánchez-Romera B, Aroca R, Asins MJ, Declerck S, Dodd IC, Martínez-Andújar C, Albacete A, Ruiz-Lozano JM (2016) Exploring the use of recombinant inbred lines in combination with beneficial microbial inoculants (AM fungus and PGPR) to improve drought stress tolerance in tomato. Environ Exp Bot 131:47–57CrossRefGoogle Scholar
  33. Cattivelli L, Rizza F, Badeck FW, Mazzucotelli E, Mastrangelo AM (2008) Drought tolerance improvement in crop plants: an integrated view from breeding to genomics. Field Crops Res 105:1–14CrossRefGoogle Scholar
  34. Cavallazzy JRP, Klauberg-Filho O, Stürmer SL, Rygiewicz PT, Mendonça MM (2007) Screening and selecting arbuscular mycorrhizal fungi for inoculating micropropagated apple rootstocks in acid soils. Plant Cell Tiss Org 90:117–129CrossRefGoogle Scholar
  35. Clark RB, Zeto SK (1996) Growth and root colonization of mycorrhizal maize grown on acid and alkaline soil. Soil Biol Biochem 28:1505–1511CrossRefGoogle Scholar
  36. Clark RB, Zeto SK, Zobel RW (1999a) Arbuscular mycorrhizal fungal isolate effectiveness on growth and root colonization of Panicum virgatum in acidic soil. Soil Biol Biochem 31:1757–1763CrossRefGoogle Scholar
  37. Clark RB, Zobel RW, Zeto SK (1999b) Effects of mycorrhizal fungus isolates on mineral acquisition by Panicum virgatum in acidic soil. Mycorrhiza 9:167–176CrossRefGoogle Scholar
  38. Cordell D, White S (2011) Peak phosphorus: clarifying the key issues of a vigorous debate about long-term phosphorus security. Sustainability 3:2027–2049CrossRefGoogle Scholar
  39. Cordell D, Drangert JO, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Change 19:292–305CrossRefGoogle Scholar
  40. Cornejo P, Borie F, Rubio R, Azcón R (2007) Influence of nitrogen source on the viability, functionality and persistence of Glomus etunicatum fungal propagules in an Andisol. Appl Soil Ecol 35:423–431CrossRefGoogle Scholar
  41. Cornejo P, Meier S, Borie G, Rillig M, Borie F (2008a) Glomalin-related soil protein in a Mediterranean ecosystem affected by a copper smelter and its contribution to Cu and Zn sequestration. Sci Total Environ 406:154–160PubMedCrossRefGoogle Scholar
  42. Cornejo P, Rubio R, Castillo C, Azcón R, Borie F (2008b) Mycorrhizal effectiveness on wheat nutrient acquisition in an acidic soil from southern Chile as affected by nitrogen sources. J Plant Nutr 31:1555–1569CrossRefGoogle Scholar
  43. Cornejo P, Pérez-Tienda J, Meier S, Valderas A, Borie F, Azcón-Aguilar C, Ferrol N (2013) Copper compartmentalization in spores as a survival strategy of arbuscular mycorrhizal fungi in Cu-polluted environments. Soil Biol Biochem 57:925–928CrossRefGoogle Scholar
  44. Cosme M, Ramireddy E, Franken P, Schmülling T, Wurst S (2016) Shoot- and root-borne cytokinin influences arbuscular mycorrhizal symbiosis. Mycorrhiza.
  45. Cuenca G, De Andrade Z, Meneses E (2001) The presence of aluminum in arbuscular mycorrhizas of Clusia multiflora exposed to increased acidity. Plant Soil 231:233–241CrossRefGoogle Scholar
  46. Cumming J, Ning J (2003) Arbuscular mycorrhizal fungi enhance aluminium resistance of broomsedge (Andropogon virginicus L.) J Exp Bot 54:1447–1459PubMedCrossRefGoogle Scholar
  47. Curaqueo G, Acevedo E, Cornejo P, Seguel A, Rubio R, Borie F (2010) Tillage effect on soil organic matter, mycorrhizal hyphae and aggregates in a Mediterranean agroecosystem. J Soil Sci Plant Nutr 10:12–21Google Scholar
  48. Curaqueo G, Barea JM, Acevedo E, Rubio R, Cornejo P, Borie F (2011) Effects of different tillage system on arbuscular mycorrhizal fungal propagules and physical properties in a Mediterranean agroecosystem in central Chile. Soil Till Res 113:11–18CrossRefGoogle Scholar
  49. da Silva S, Siqueira JO, Soares CRFS (2006) Fungos micorrízicos no crescimento e na extração de metais pesados pela braquiária em solo contaminado. Pesq Agropec Bras 41:1749–1757CrossRefGoogle Scholar
  50. del Val C, Barea JM, Azcón-Aguilar C (1999) Diversity of arbuscular mycorrhizal fungus populations in heavy-metal-contaminated soils. Appl Environ Microbiol 65:718–723PubMedPubMedCentralGoogle Scholar
  51. Delhaize E, Ryan PR (1995) Aluminum Toxicity and Tolerance in Plants. Plant Physiol 107:315–321PubMedPubMedCentralCrossRefGoogle Scholar
  52. Dong D, Peng X, Yan X (2004) Organic acid exudation induced by phpshorus deficiency and/or aluminum toxicity in two contrasting soybean genotypes. Phisiol Plant 122:190–199CrossRefGoogle Scholar
  53. Elbon A, Whalen J (2015) Phosphorus supply to vegetable crops from arbuscular mycorrhizal fungi: a review. Biol Agric Hortic 31:73–90CrossRefGoogle Scholar
  54. Elser J, Bennett E (2011) Phosphorus cycle: a broken biogeochemical cycle. Nature 478:29–31PubMedCrossRefGoogle Scholar
  55. Escudey M, Galindo G, Förter JE, Briceño M, Diaz P, Chang A (2001) Chemical forms of phosphorus of volcanic ash-derived soils in Chile. Commun Soil Sci Plant Anal 32:601–616CrossRefGoogle Scholar
  56. Estrada B, Aroca R, Maathuis FJM, Barea JM, Ruiz-Lozano JM (2013) Arbuscular mycorrhizal fungi native from a Mediterranean saline area enhance maize tolerance to salinity through improved ion homeostasis. Plant Cell Environ 36:1771–1782PubMedCrossRefGoogle Scholar
  57. Etemadi M, Gutjahr C, Couzigou JM, Zouine M, Lauressergues D, Timmers A, Audran C, Bouzayen M, Bécard G, Combier JP (2014) Auxin perception is required for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Physiol 166:281–292PubMedPubMedCentralCrossRefGoogle Scholar
  58. Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1281PubMedPubMedCentralCrossRefGoogle Scholar
  59. 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 22:203–217PubMedCrossRefGoogle Scholar
  60. Evelin H, Giri B, Kapoor R (2013) Ultrastructural evidence for AMF mediated salt stress mitigation in Trigonella foenum-graecum. Mycorrhiza 23:71–86PubMedCrossRefGoogle Scholar
  61. Fernández-Bidondo L, Silvani V, Colombo R, Pérgola M, Bompadre J, Godeas A (2011) Pre-symbiotic and symbiotic interactions between the arbuscular mycorrhizal (AM) fungus Glomus intraradices and two Paenibacillus species associated with AM intraradical mycelia and spores. Soil Biol Biochem 43:1866–1872CrossRefGoogle Scholar
  62. Fernández-Bidondo L, Bompadre J, Pergola M, Silvani V, Colombo R, Bracamonte F, Godeas A (2012) Differential interaction between two Glomus intraradices strains with different extraradical mycelium architecture and a phosphate solubilizing bacterium in maize rhizosphere. Pedobiologia 55:227–232CrossRefGoogle Scholar
  63. Ferreira P, Ceretta C, Hildebrandt H, Tiecher T, Soares C, Rossato L, Nicoloso F, Brunetto G, Paranhos J, Cornejo P (2015) Rhizophagus clarus and phosphate alter the physiological responses of Crotalaria juncea cultivated in soil with a high Cu level. Appl Soil Ecol 91:37–47CrossRefGoogle Scholar
  64. Ferrol N, González Guerrero M, Valderas A, Benabdellah K, Azcón-Aguilar C (2009) Survival strategies of arbuscular mycorrhizal fungi in Cu-polluted environments. Phytochem Rev 8:551–559CrossRefGoogle Scholar
  65. Finlay RD (2008) Ecological aspects of mycorrhizal symbiosis with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot 59:1115–1126PubMedCrossRefGoogle Scholar
  66. Fischer EM, Knutti R (2015) Anthropogenic contribution to global occurrence of heavy-precipitation and high-temperature extremes. Nat Clim Chang 5:560–564CrossRefGoogle Scholar
  67. Fischlin A, Midgley GF, Price JT, Leemans R, Gopal B, Turley C, Rounsevell MDA, Dube OP, Tarazona J, Velichko AA (2007) Ecosystems, their properties, goods and services. In: Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE (eds) Climate change 2007: impacts, adaptation and vulnerability. contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel of Climate Change (IPCC). Cambridge University Press, Cambridge, pp 211–272Google Scholar
  68. Gadd GM (1993) Interaction of fungi with toxic metals. New Phytol 124:25–60CrossRefGoogle Scholar
  69. Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17:3489–3499PubMedPubMedCentralCrossRefGoogle Scholar
  70. Gildon A, Tinker PB (1983) Interactions of vesicular-arbuscular mycorrhizal infections and heavy metals in plants. II. The effects of infection on uptake of copper. New Phytol 95:263–268CrossRefGoogle Scholar
  71. Gill A, Bhadoria P, Sadana U (2013) Effect of mycorrhizal infection on phosphorus efficiency of maize (Zea mays L.) cultivars. Proc Nat Acad Sci India Sect A 83:147–157Google Scholar
  72. Giovannetti M, Sbrana C, Avio L, Citernesi AS, Logi C (1993) Differential hyphal morphogenesis in arbuscular mycorrhizal fungi during pre-infection stages. New Phytol 125:587–593CrossRefGoogle Scholar
  73. Gong M, van der Liut AH, Knight MR, Trewavas AJ (1998) Heat shock induced changes in intracellular Ca2+ level in tobacco seedlings in relation to thermo tolerance. Plant Physiol 116:429–437PubMedCentralCrossRefGoogle Scholar
  74. González-Chávez C, D’Haen J, Vangronsveld J, Dodd JC (2002) Copper sorption and accumulation by the extraradical mycelium of different Glomus spp. (arbuscular mycorrhizal fungi) isolated from the same polluted soil. Plant Soil 240:287–297CrossRefGoogle Scholar
  75. González-Chávez MC, Carrillo-González R, Wright SF, Nichols K (2004) The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environ Pollut 130:317–323PubMedCrossRefGoogle Scholar
  76. Guan XK, Song L, Wang TC, Turner NC, Li FM (2015) Effect of drought on the gas exchange, chlorophyll fluorescence and yield of six different-era Spring Wheat cultivars. J Agron Crop Sci 4:253–266CrossRefGoogle Scholar
  77. Guo CJ, Guo L, Li XJ, Gu JT, Zhao M, Duan WW, Ma CY, Lu WJ, Xiao K (2014) TaPT2, a high-affinity phosphate transporter gene in wheat (Triticum aestivum L.), is crucial in plant Pi uptake under phosphorus deprivation. Acta Physiol Plant 36:1373–1384CrossRefGoogle Scholar
  78. Hause B, Schaarschmidt S (2009) The role of jasmonates in mutualistic symbioses between plants and soil-born microorganisms. Phytochemistry 70:1589–1599PubMedCrossRefGoogle Scholar
  79. Hidri R, Barea JM, Metoui-Ben-Mahmoud O, Abdelly C, Azcón R (2016) Impact of microbial inoculation on biomass accumulation by Sulla carnosa provenances, and in regulating nutrition, physiological and antioxidant activities of this species under non-saline and saline conditions. J Plant Physiol 201:28–41PubMedCrossRefGoogle Scholar
  80. Hijikata N, Murase M, Tani C, Ohtomo R, Osaki M, Ezawa T (2010) Polyphosphate has a central role in the rapid and massive accumulation of phosphorus in extraradical mycelium of an arbuscular mycorrhizal fungus. New Phytol 186:285–289PubMedCrossRefGoogle Scholar
  81. Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68:139–146PubMedCrossRefGoogle Scholar
  82. Hove RM, Ziemann M, Bhave M (2015) Identification and expression analysis of the barley (Hordeum vulgare L.) Aquaporin Gene Family. PLoS One 10:e0128025PubMedPubMedCentralCrossRefGoogle Scholar
  83. Huseynova IM, Aliyeva DR, Mammadov AC, Aliyev JA (2015) Hydrogen peroxide generation and antioxidant enzyme activities in the leaves and roots of wheat cultivars subjected to long-term soil drought stress. Photosynth Res 125:279–289PubMedCrossRefGoogle Scholar
  84. Imadi S, Waseem S, Kazi A, Azooz MM, Ahmad P (2016) Aluminum toxicity in plants: an overview. In: Ahmed P (ed) Emerging remediation techniques. Elsevier Inc, Amsterdam, pp 1–20Google Scholar
  85. IPCC (2012) Managing the risk of extreme events and disasters to advance climate change adaptation, special report of the intergovernmental panel climate change. Cambridge University Press, New York, 582 ppGoogle Scholar
  86. Jeffries P, Gianinazzi S, Perotto S, Turnau K, Barea JM (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils 37:1–16Google Scholar
  87. Kahiluoto H, Vestberg M (1998) The effect of arbuscular mycorrhiza on biomass production and phosphorus uptake from sparingly soluble sources By Leek (Allium porrum L.) in finnish field soils helena. Biol Agric Hortic 16:65–85CrossRefGoogle Scholar
  88. Karandashov V, Nagy R, Amrhein N, Bucher M (2004) Evolutionary conservation of a phosphate transporter in the arbuscular mycorrhizal symbiosis. PNAS 101:6285–6290PubMedPubMedCentralCrossRefGoogle Scholar
  89. Kelly CN, Morton JB, Cumming JR (2005) Variation in aluminum resistance among arbuscular mycorrhizal fungi. Mycorrhiza 15:193–201PubMedCrossRefGoogle Scholar
  90. Klugh KR, Cumming JR (2007) Variations in organic acid exudation and aluminum resistance among arbuscular mycorrhizal species colonizing Liriodendron tulipifera. Tree Physiol 27:1103–1112PubMedCrossRefGoogle Scholar
  91. Klugh-Stewart K, Cumming JR (2009) Organic acid exudation by mycorrhizal Andropogon virginicus L. (broomsedge) roots in response to aluminum. Soil Biol Biochem 41:367–373CrossRefGoogle Scholar
  92. Knapp AK, Briggs JM, Koelliker JK (2001) Frequency and extent of water limitation to primary production in a mesic temperate grassland. Ecosystems 4:19–28CrossRefGoogle Scholar
  93. Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plan Mol Biol 46:237–260CrossRefGoogle Scholar
  94. Kochian L, Hoekenga OA, Pineros MA (2004) How do crop plants tolerate acid soils? – mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 55:459–493PubMedCrossRefGoogle Scholar
  95. Kochian L, Piñeros M, Hoekenga O (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175–195CrossRefGoogle Scholar
  96. Kohlen W, Charnikhova T, Lammers M, Pollina T, Tóth P (2012) The tomato carotenoid cleavage dioxygenase8 (SLCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytol 196:535–547PubMedCrossRefGoogle Scholar
  97. Koslowsky S, Boener R (1989) Interactive effects of aluminum, phosphorus and mycorrhizae on growth and nutrient uptake of Panicum virgatum L. (Poaceae). Environ Pollut 61:107–125PubMedCrossRefGoogle Scholar
  98. Kraemer U (2003) Phytoremediation to phytochelatin – plant trace metal homeostasis. New Phytol 158:4–6CrossRefGoogle Scholar
  99. Kramer PJ, Boyer JS (1995) Water relations of plants and soils. Academic, London, 495 pGoogle Scholar
  100. Krikun J, Haas JH, Dodd J, Kinsbursky R (1990) Mycorrhizal dependence of four crops in a P-sorbing soil. Plant Soil 122:213–217CrossRefGoogle Scholar
  101. Krishnamoorthy R, Kim K, Subramanian P, Senthilkumar M, Anandham R, Sa T (2016) Arbuscular mycorrhizal fungi and associated bacteria isolated from salt-affected soil enhances the tolerance of maize to salinity in coastal reclamation soil. Agric Ecosys Environ 231:233–239CrossRefGoogle Scholar
  102. Lambers H, Chapin FS, Pons TL (2008) Plant physiological ecology, 2nd edn. Springer, New YorkCrossRefGoogle Scholar
  103. Lehmann J, Pereira da Silva J, Steiner C, Nehls T, Zech W, Glaser B (2003) Nutrient availability and leaching in an archaeological Anthrosol and a Ferralsol of the Central Amazon basin: fertilizer, manure and charcoal amendments. Plant Soil 249:343–357CrossRefGoogle Scholar
  104. Leigh J, Hodge A, Fitter AH (2009) Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol 181:199–207PubMedCrossRefGoogle Scholar
  105. Leung HM, Ye ZH, Wong MH (2007) Survival strategies of plants associated with arbuscular mycorrhizal fungi on toxic mine tailings. Chemosphere 66:905–915PubMedCrossRefGoogle Scholar
  106. Levitt J (1980) Responses of plants to environmental stresses. In: Kozlowski TT (ed) Water, radiation, salt and other stresses, 2nd ed, vol 2. Academic, New York, pp 93–186Google Scholar
  107. Li XF, Ma JF, Matsumoto H (2000) Pattern of aluminum-induced secretion of organic acids differs between rye and wheat. Plant Physiol 123:1537–1543PubMedPubMedCentralCrossRefGoogle Scholar
  108. Liao H, Wan H, Shaff J, Wang X, Yan X, Kochian LV (2006) Phosphorus and aluminum interactions in soybean in relation to aluminum tolerance. Exudation of specific organic acids from different regions of the intact root system. Plant Physiol 141:674–684PubMedPubMedCentralCrossRefGoogle Scholar
  109. Ligaba A, Yamaguchi M, Shen H, Sasaki T, Yamamoto Y, Matsumoto H (2004) Phosphorus deficiency enhances plasma membrane H+-ATP ase activity and citrate exudation in greater purple lupin (Lupinus pilosus). Func Plant Biol 31:1075–1083CrossRefGoogle Scholar
  110. Liu A, Hamel C, Hamilton RI, Ma BL, Smith DL (2000) Acquisition of Cu, Zn, Mn and Fe by mycorrhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels. Mycorrhiza 9:331–336CrossRefGoogle Scholar
  111. López-Ráez JA, Charnikhova T, Fernández I, Bouwmeester H, Pozo MJ (2011) Arbuscular mycorrhizal symbiosis decreases strigolactone production in tomato. J Plant Physiol 168:294–297PubMedCrossRefGoogle Scholar
  112. Luthria D, Lu Y, Maria-John KM (2015) Bioactive phytochemicals in wheat: extraction, analysis, processing, and functional properties. J Funct Foods 18:910–925CrossRefGoogle Scholar
  113. Lux HB, Cumming JR (2001) Mycorrhizae confer aluminum resistance to tulip-poplar seedlings. Can J For Res 31:694–702CrossRefGoogle Scholar
  114. Ma JF (2000) Role of organic acids in detoxification of Al in higher plants. Plant Cell Physiol 41:383–390PubMedCrossRefGoogle Scholar
  115. Ma JF, Zheng SJ, Matsumoto H (1997) Specific secretion of citric acid induced by Al stress in Cassia tora L. Plant Cell Physiol 348:1019–1025CrossRefGoogle Scholar
  116. Ma D, Sun D, Wang C, Li Y, Guo T (2014) Expression of flavonoid biosynthesis genes and accumulation of flavonoid in wheat leaves in response to drought stress. Plant Physiol Biochem 80:60–66PubMedCrossRefGoogle Scholar
  117. Manchanda G, Garg N (2011) Alleviation of salt-induced ionic, osmotic and oxidative stresses in Cajanus cajan nodules by AM inoculation. Plant Biosys 145:88–97CrossRefGoogle Scholar
  118. Mardhiah U, Caruso T, Gurnell A, Rillig M (2016) Arbuscular mycorrhizal fungal hyphae reduce soil erosion by surface water flow in a greenhouse experiment. Appl Soil Ecol 99:137–140CrossRefGoogle Scholar
  119. Marschner P, Timonen S (2005) Interactions between plant species and mycorrhizal colonization on the bacterial community composition in the rhizosphere. Appl Soil Ecol 28:23–36CrossRefGoogle Scholar
  120. Martini D, Grazia D, Egidio M, Nicoletti I, Corradini D, Taddei F (2015) Effects of durum wheat debranning on total antioxidant capacity and on content and profile of phenolic acids. J Funct Foods 17:83–92CrossRefGoogle Scholar
  121. Martín-Rodríguez J, Huertas R, Ho-Plágaro T, Ocampo J, Turečková V, Tarkowská D, Ludwig-Müller J, García-Garrido JM (2016) Gibberellin – abscisic acid balances during arbuscular mycorrhiza formation in tomato. Front Plant Sci.
  122. McGrath SP, Zhao FJ (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opin Biotechnol 14:277–282PubMedCrossRefGoogle Scholar
  123. Meier S, Azcón R, Cartes P, Borie F, Cornejo P (2011) Alleviation of Cu toxicity in Oenothera picensis by copper-adapted arbuscular mycorrhizal fungi and treated agrowaste residue. Appl Soil Ecol 48:117–124CrossRefGoogle Scholar
  124. Meier S, Alvear A, Aguilera P, Ginocchio R, Borie F, Cornejo P (2012a) Influence of copper on root exudate patterns in some metallophytes and agricultural plants. Ecotoxicol Environ Safe 75:8–15CrossRefGoogle Scholar
  125. Meier S, Borie F, Bolan N, Cornejo P (2012b) Phytoremediation of metal-polluted soils by arbuscular mycorrhizal fungi. Crit Rev Environ Sci Technol 42:741–775CrossRefGoogle Scholar
  126. Meier S, Borie F, Curaqueo G, Nolan N, Cornejo P (2012c) Effects of arbuscular mycorrhizal inoculation on metallophyte and agricultural plants growing at increasing copper levels. Appl Soil Ecol 61:280–287CrossRefGoogle Scholar
  127. Meier S, Cornejo P, Cartes P, Borie F, Medina J, Azcón R (2015) Interactive effect between Cu-adapted arbuscular mycorrhizal fungi and biotreated agrowaste residue to improve the nutritional status of Oenothera picensis growing in Cu-polluted soils. J Plant Nutr Soil Sci 178:126–135CrossRefGoogle Scholar
  128. Meier S, Curaqueo G, Khan N, Bolan N, Cea M, González ME, Cornejo P, Ok Y, Borie F (2016) Chicken manure-derived biochar reduce the bioavailability of copper in a contaminated soil. J Soil Sed. doi: (in press)
  129. Mendoza J, Borie F (1998) Effect of Glomus etunicatum inoculation on aluminum, phosphorus, calcium, and magnesium uptake of two barley genotypes with different aluminum tolerance. Commun Soil Sci Plant Anal 29:681–695CrossRefGoogle Scholar
  130. Mikkelsen BL, Rosendahl S, Jakobsen I (2008) Underground resource allocation between individual networks of mycorrhizal fungi. New Phytol 180:890–898PubMedCrossRefGoogle Scholar
  131. Miller RM, Jastrow JD (2000) Mycorrhizal fungi influence soil structure. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: molecular biology and physiology. Kluwer Academic, Dordrecht, pp 3–18CrossRefGoogle Scholar
  132. Miyasaka SC, Buta JG, Howell RK, Foy CD (1991) Mechanism of aluminum tolerance in snapbean: root exudation of citric acid. Plant Physiol 96:737–743PubMedPubMedCentralCrossRefGoogle Scholar
  133. Mora ML, Demanet R, Vistoso E, Gallardo F (2005) Influence of sulfate concentration in mineral solution on ryegrass grown at different pH and aluminium levels. J Plant Nutr 28:1–16CrossRefGoogle Scholar
  134. Nagata M, Yamamoto N, Miyamoto T, Shimomura A, Arima S, Hirsch A, Suzuki A (2016) Enhanced hyphal growth of arbuscular mycorrhizae by root exudates derived from high R/FR treated Lotus japonicus. Plant Signal Behav 2 11(6):e1187356CrossRefGoogle Scholar
  135. Nakagawa T, Mori S, Yoshimura E (2003) Amelioration of aluminum toxicity by pretreatment with phosphate in aluminum-tolerant rice cultivar. J Plant Nutr 26:619–628CrossRefGoogle Scholar
  136. Olsen J, Schaefer J, Edwards J, Hunter M, Galea V, Muller L (1999) Effects of a network of mycorrhizae on capsicum (Capsicum annuum L.) grown in the field with five rates of applied phosphorus. Aust J Agric Res 50:239–252CrossRefGoogle Scholar
  137. Oono Y, Kobayashi F, Kawahara Y, Yazawa T, Handa H, Itoh T, Matsumoto T (2013) Characterisation of the wheat (Triticum aestivum L.) transcriptome by de novo assembly for the discovery of phosphate starvation-responsive genes: gene expression in Pi-stressed wheat. BMC Genomics 14:77PubMedPubMedCentralCrossRefGoogle Scholar
  138. Pellet DM, Papernik LA, Kochian LV (1996) Multiple aluminum resistance mechanisms in wheat: roles of root apical phosphate and malate exudation. Plant Physiol 112:591–597PubMedPubMedCentralCrossRefGoogle Scholar
  139. Pérez-Tienda J, Valderas A, Camañes G, Garcia-Agustin P, Ferrol N (2012) Kinetics of NH4 + uptake by the arbuscular fungus Rhizophagus irregularis. Mycorrhiza 22:485–491PubMedCrossRefGoogle Scholar
  140. Peterson RL, Massicotte HB, Melville LH (2004) Mycorrhizas: anatomy and cell biology. NRC Research Press, Ottawa, 173 ppGoogle Scholar
  141. Plenchette C, Morel C (1996) External phosphorus requirement of mycorrhizal and non-mycorrhizal barley and soybean plants. Biol Fertil Soils 21(4):303–308CrossRefGoogle Scholar
  142. Pinior A, Grunewaldt-Stöcker G, von Alten H, Strasser R (2005) Mycorrhizal impact on drought stress tolerance of rose plants probed by chlorophyll a fluorescence, proline content and visual scoring. Mycorrhiza 15:596–605PubMedCrossRefGoogle Scholar
  143. Pinochet D, Epple G, Mac Donald R (2001) Fracciones de fósforo orgánico e inorgánico en un transecto de suelos de origen volcánico y metamórfico. R C Suelo Nutr Veg 1:58–69Google Scholar
  144. Porcel R, Aroca R, Azcón R, Ruiz-Lozano JM (2006) PIP aquaporin gene expression in arbuscular mycorrhizal Glycine max and Lactuca sativa plants in relation to drought stress tolerance. Plant Molec Biol 60:389–404CrossRefGoogle Scholar
  145. Porcel R, Redondo-Gómez S, Mateos-Naranjo E, Aroca R, García 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 185:75–83PubMedCrossRefGoogle Scholar
  146. Rapti-Caputo D (2010) Influence of climatic changes and human activities on the salinization process of coastal aquifer systems. Ital J Agron 5:67–79CrossRefGoogle Scholar
  147. Redecker D, Morton JB, Bruns TD (2000) Ancestral lineages of arbuscular mycorrhizal fungi (Glomales). Mol Phylogen Evol 14:276–284CrossRefGoogle Scholar
  148. Requena N, Serrano E, Ocon A, Breuninger J (2007) Plant signals and fungal perception during arbuscular mycorrhiza establishment. Phytochemistry 68:33–40PubMedCrossRefGoogle Scholar
  149. Rohyadi A, Smith FA, Murray RS, Smith SE (2004) Effects of pH on mycorrhizal colonization and nutrient uptake in cowpea under conditions that minimize confounding effects of elevated available aluminium. Plant Soil 260:283–290CrossRefGoogle Scholar
  150. Ryan PR, Delhaize E, Randall PJ (1995) Characterization of Aluminum-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196:788–795CrossRefGoogle Scholar
  151. Sade D, Brotman Y, Eybishtz A, Cuadros-Inostroza A, Fernie AR, Willmitzer L, Czosnek H (2013) Involvement of the hexose transporter gene LeHT1 and of sugars in resistance of tomato to tomato yellow leaf curl virus. Mol Plant 6:1707–1710PubMedCrossRefGoogle Scholar
  152. Sánchez-Rodríguez E, Rubio-Wilhelmi M, Blasco B, Leyva R, Romero L, Ruiz JM (2012) Antioxidant response resides in the shoot in reciprocal grafts of drought-tolerant and drought-sensitive cultivars in tomato under water stress. Plant Sci 188:89–96PubMedCrossRefGoogle Scholar
  153. Sato T, Ezawa T, Cheng W, Tawaraya K (2015) Release of acid phosphatase from extraradical hyphae of arbuscular mycorrhizal fungus Rhizophagus clarus. Soil Sci Plant Nutr 61:269–274CrossRefGoogle Scholar
  154. Schijlen E, Ric de Vos CH, van Tunen A, Bovy AG (2004) Modification of flavonoid biosynthesis in crop plants. Phytochemistry 19:2631–2648CrossRefGoogle Scholar
  155. Schwitzguébel JP (2001) Hype or hope: the potential of phytoremediation as an emerging green technology. Remediat J 11:63–78CrossRefGoogle Scholar
  156. Seguel A, Medina J, Rubio R, Cornejo P, Borie F (2012) Effects of soil aluminum on early arbuscular mycorrhizal colonization of wheat and barley cultivars growing in an andisol. Chil J Agr Res 72:449–455CrossRefGoogle Scholar
  157. Seguel A, Cumming J, Klugh-Stewart K, Cornejo P, Borie F (2013) The role of arbuscular mycorrhizas in decreasing Al phytotoxicity in acidic soils: a review. Mycorrhiza 23:167–183PubMedCrossRefGoogle Scholar
  158. Seguel A, Barea JM, Cornejo P, Borie F (2015) Role of arbuscular mycorrhizal symbiosis in phosphorus-uptake efficiency and aluminium tolerance in barley growing in acid soils. Crop Pasture Sci 66:696–705CrossRefGoogle Scholar
  159. Seguel A, Castillo GC, Morales A, Campos P, Cornejo P, Borie F (2016a) Arbuscular Mycorrhizal symbiosis in four Al-tolerant wheat genotypes grown in an acidic Andisols. J Soil Sci Plant Nutr 16:164–173Google Scholar
  160. Seguel A, Cumming J, Cornejo P, Borie F (2016b) Aluminum tolerance of wheat cultivars and relation to arbuscular mycorrhizal colonization in a non-limed and limed andisol. Appl Soil Ecol 108:228–237CrossRefGoogle Scholar
  161. Seki M, Kamei A, Yamaguchi-Shinozaki K, Shinozaki K (2003) Molecular responses to drought, salinity and frost: common and different paths for plant protection. Curr Opin Biotechnol 14:194–199PubMedCrossRefGoogle Scholar
  162. Silva WP, Precker JW, Silva CMDPS, Silva DDPS (2009) Determination of the effective diffusivity via minimization of the objective function by scanning: application to drying of cowpea. J Food Eng 95:298–304CrossRefGoogle Scholar
  163. Simon L, Bousquet J, Levesque RC, Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular plants. Nature 363:67–69CrossRefGoogle Scholar
  164. Šircelj HM, Tausz M, Grill D, Batic F (2005) Biochemical responses in leaves of two apple tree cultivars subjected to progressing drought. J Plant Physiol 162:1308–1318PubMedCrossRefGoogle Scholar
  165. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, LondonGoogle Scholar
  166. Smith SE, Smith FA (2011) Role of the arbuscular mycorrhizal symbiosis in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250PubMedCrossRefGoogle Scholar
  167. Smith S, Manjarrez M, Stonor R, McNeill R, Acdonald L (2015) Indigenous arbuscular mycorrhizal (AM) fungi contribute to wheat phosphate uptake in a semi-arid field environment, shown by tracking with radioactive phosphorus. Appl Soil Ecol 96:68–74CrossRefGoogle Scholar
  168. Soja G, Soja AM (2005) Recognizing the sources of stress in wheat and bean by using chlorophyll fluorescence induction parameters as inputs for neural network models. Phyton 45:157–168Google Scholar
  169. Soka G, Ritchie M (2014) Arbuscular mycorrhizal symbiosis, ecosystem processes and environmental changes in tropical soils. Open J Ecol 4:11–22CrossRefGoogle Scholar
  170. Sun QB, Shen RF, Zhao XQ, Chen RF, Dong XY (2008) Phosphorus enhances Al resistance in Al-resistant Lespedeza bicolor but not in Al-sensitive L. cuneata under relatively high Al stress. Ann Bot 102:795–804PubMedPubMedCentralCrossRefGoogle Scholar
  171. Takeda N, Handa Y, Tsuzuki S, Kojima M, Sakakibara H, Kawaguchi M (2015) Gibberellins interfere with symbiosis signaling and gene expression, and alter colonization by arbuscular mycorrhizal fungi in Lotus japonicus. Plant Physiol 167:545–557PubMedCrossRefGoogle Scholar
  172. Takeda N, Handa Y, Tsuzuki S, Kojima M, Sakakibara H, Kawaguchi M (2016) Gibberellin regulates infection and colonization of host roots by arbuscular mycorrhizal fungi. Plant Signal Behav 10(6):e1028706CrossRefGoogle Scholar
  173. Tawaraya K, Hirose R, Wagatsuma T (2012) Inoculation of arbuscular mycorrhizal fungi can substantially reduce phosphate fertilizer application to Allium fistulosum L. and achieve marketable yield under field condition. Biol Fert Soils 48:839–843CrossRefGoogle Scholar
  174. Teskey R, Wertin T, Bauweraerts I, Ameye M, McGuire MA, Steppe K (2015) Responses of tree species to heat waves and extreme heat events. Plant Cell Environ 38:1699–1712PubMedCrossRefGoogle Scholar
  175. Trenberth KE, Dai A, Van Der Schrier G, Jones PD, Barichivich J, Briffa KR, Sheffield J (2014) Global warming and changes in drought. Nature Clim Chang 4:17–22CrossRefGoogle Scholar
  176. Walter J, Nagy L, Hein R, Rascher U, Beierkuhnlein C, Willner E (2010) Do plants remember drought? Hints towards a drought-memory in grasses. Environ Exp Bot 71:34–40CrossRefGoogle Scholar
  177. Watanabe T, Osaki M (2002) Mechanisms of adaptation to high aluminum condition in native plant species growing in acid soils: a review. Commun Soil Sci Plant Anal 33:1247–1260CrossRefGoogle Scholar
  178. Wery J, Silim SN, Knights EJ, Malhotra RS, Cousin R (1994) Screening techniques and sources and tolerance to extremes of moisture and air temperature in cool season food legumes. Euphytica 73:73–83CrossRefGoogle Scholar
  179. Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecol 2011:1–20Google Scholar
  180. Yano K, Takaki M (2005) Mycorrhizal alleviation of acid soil stress in the sweet potato (Ipomoea batatas). Soil Biol Biochem 37:1569–1572CrossRefGoogle Scholar
  181. Ye S, Yanga Y, Xin G, Wang Y, Ruan L, Ye G (2015) Studies of the Italian ryegrass–rice rotation system in southern China: Arbuscular mycorrhizal symbiosis affects soil microorganisms and enzyme activities in the Lolium mutiflorum L. rhizosphere. Appl Soil Ecol 90:26–34CrossRefGoogle Scholar
  182. Yin N, Zhang Z, Wang L, Qian K (2016) Variations in organic carbon, aggregation, and enzyme activities of gangue-fly ash-reconstructed soils with sludge and arbuscular mycorrhizal fungi during 6-year reclamation. Environ Sci Pollut Res 23:17840–17849CrossRefGoogle Scholar
  183. Zhang X, Chen B, Ohtomo R (2015) Mycorrhizal effects on growth, P uptake and Cd tolerance of the host plant vary among different AM fungal species. Soil Sci Plant Nutr 61:359–368CrossRefGoogle Scholar
  184. Zhao Z, Ma JF, Sato K, Takeda K (2003) Differential Al resistance and citrate secretion in barley (Hordeum vulgare L.) Planta 217:794–800PubMedCrossRefGoogle Scholar
  185. Zhao H, Zhang ZB, Xu P (2010) Enhanced aquaporin activity of two different genotypes of drought-resistant wheat (Triticum aestivum L.) cultivars facilitate their adaptation to drought stress. J Food Agric Environ 8:1158–1161Google Scholar
  186. Zheng SJ, Yang JL, He YF, Yu XH, Zhang L, You JF, Shen RF, Matsumoto H (2005) Immobilization of aluminum with phosphorus in roots is associated with high Al resistance in buckwheat. Plant Physiol 138:297–303PubMedPubMedCentralCrossRefGoogle Scholar
  187. Zhou S, Hu W, Deng X, Ma Z, Chen L, Huang C, Wang C, Wang J, He Y, Yang G, He G (2012) Overexpression of the wheat aquaporin gene, TaAQP7, enhances drought tolerance in transgenic tobacco. PLoS One 7:e52439PubMedPubMedCentralCrossRefGoogle Scholar
  188. Zhu YG, Miller RM (2003) Carbon cycling by arbuscular mycorrhizal fungi in soil-plant systems. Trends Plant Sci 8:407–409PubMedCrossRefGoogle Scholar
  189. Zhu JK, Hasegawa PM, Bressan RA (1997) Molecular aspects of osmotic stress in plants. Crit Rev Plant Sci 16:253–277CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • Pablo Cornejo
    • 1
    Email author
  • Alex Seguel
    • 1
  • Paula Aguilera
    • 1
  • Sebastián Meier
    • 1
    • 2
  • John Larsen
    • 3
  • Fernando Borie
    • 1
  1. 1.Departamento de Ciencias Químicas y Recursos NaturalesCenter of Amelioration and Sustainability of Volcanic Soils, Scientific and Technological Bioresource Nucleus, BIOREN-UFRO, Universidad de La FronteraTemucoChile
  2. 2.Instituto Nacional de Investigaciones Agropecuarias. INIA CarillancaTemucoChile
  3. 3.Laboratorio de AgroecologíaInstituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de MéxicoMoreliaMexico

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