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

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Plant-Microbe Interactions in Agro-Ecological Perspectives

Abstract

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.

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References

  • 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 7:636–641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 47:55–68

    Article  Google Scholar 

  • Adriano DC (2001) Trace elements in terrestrial environments: biogeochemistry, bioavailability, and risk of metals. Springer, New York

    Book  Google Scholar 

  • Adriano DC, Wenzel WW, Vangronsveld J, Bolan NS (2004) Role of assisted natural remediation in environmental cleanup. Geoderma 122:121–142

    Article  CAS  Google Scholar 

  • 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 43:2417–2431

    Article  CAS  Google Scholar 

  • 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 186:178–184

    Article  CAS  Google Scholar 

  • 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 203–228

    Chapter  Google Scholar 

  • Al-Karaki G, McMichael B, Zak J (2004) Field response of wheat to arbuscular mycorrhizal fungi and drought stress. Mycorrhiza 14:263–269

    Article  PubMed  Google Scholar 

  • 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 197:177–185

    Article  CAS  Google Scholar 

  • Aroca R, Porcel R, Ruiz-Lozano MJ (2012) Regulation of root water uptake under abiotic stress conditions. J Exp Bot 63:43–57

    Article  CAS  PubMed  Google Scholar 

  • 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 182:383–394

    Article  CAS  Google Scholar 

  • 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 373:245–256

    Article  CAS  Google Scholar 

  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  • Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3543

    Article  CAS  PubMed  Google Scholar 

  • Azcón-Aguilar C, Barea JM (2015) Nutrient cycling in the mycorrhizosphere. J Soil Sci Plant Nutr 15:372–396

    Google Scholar 

  • 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 11:1280–1284

    CAS  Google Scholar 

  • 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 15:261–282

    CAS  Google Scholar 

  • Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778

    Article  CAS  PubMed  Google Scholar 

  • 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 75:1292–1301

    Article  Google Scholar 

  • 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 38:1613–1627

    Article  PubMed  CAS  Google Scholar 

  • 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 84:71–82

    Article  Google Scholar 

  • 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):272–294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bolan N, Naidu R, Syers JK, Tillman R (1999) Surface charge and solute interactions in soils. Adv Agron 67:87–140

    Article  CAS  Google Scholar 

  • 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 266:141–166

    Article  CAS  PubMed  Google Scholar 

  • Bonfante P, Genre A (2015) Arbuscular mycorrhizal dialogues: do you speak ‘plantish’ or ‘fungish’? Trends Plant Sci 20:150–154

    Article  CAS  PubMed  Google Scholar 

  • 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 22:121–137

    Article  CAS  Google Scholar 

  • Borie F, Rubio R (2003) Total and organic phosphorus in Chilean volcanic soils. Gayana Botanica 60:69–78

    Article  Google Scholar 

  • Borie F, Zunino H (1983) Organic matter-phosphorus association as a sink in P fixation processes on allophanic soils of Chile. Soil Biol Biochem 15:599–603

    Article  CAS  Google Scholar 

  • 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 10:185–206

    Article  Google Scholar 

  • Bray EA (2004) Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. J Exp Bot 55:2331–2341

    Article  CAS  PubMed  Google Scholar 

  • Bûcking H, Kafle A (2015) Role of the arbuscular mycorrhizal fungi in the N uptake of plants. Current knowledge and research gaps. Agronomy 5:587–612

    Article  Google Scholar 

  • 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 131:47–57

    Article  CAS  Google Scholar 

  • 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 105:1–14

    Article  Google Scholar 

  • 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 90:117–129

    Article  Google Scholar 

  • Clark RB, Zeto SK (1996) Growth and root colonization of mycorrhizal maize grown on acid and alkaline soil. Soil Biol Biochem 28:1505–1511

    Article  CAS  Google Scholar 

  • 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 31:1757–1763

    Article  CAS  Google Scholar 

  • Clark RB, Zobel RW, Zeto SK (1999b) Effects of mycorrhizal fungus isolates on mineral acquisition by Panicum virgatum in acidic soil. Mycorrhiza 9:167–176

    Article  CAS  Google Scholar 

  • Cordell D, White S (2011) Peak phosphorus: clarifying the key issues of a vigorous debate about long-term phosphorus security. Sustainability 3:2027–2049

    Article  Google Scholar 

  • Cordell D, Drangert JO, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Change 19:292–305

    Article  Google Scholar 

  • 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 35:423–431

    Article  Google Scholar 

  • 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 406:154–160

    Article  CAS  PubMed  Google Scholar 

  • 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 31:1555–1569

    Article  CAS  Google Scholar 

  • 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 57:925–928

    Article  CAS  Google Scholar 

  • Cosme M, Ramireddy E, Franken P, Schmülling T, Wurst S (2016) Shoot- and root-borne cytokinin influences arbuscular mycorrhizal symbiosis. Mycorrhiza. https://doi.org/10.1007/s00572-016-0706-3

  • Cuenca G, De Andrade Z, Meneses E (2001) The presence of aluminum in arbuscular mycorrhizas of Clusia multiflora exposed to increased acidity. Plant Soil 231:233–241

    Article  CAS  Google Scholar 

  • Cumming J, Ning J (2003) Arbuscular mycorrhizal fungi enhance aluminium resistance of broomsedge (Andropogon virginicus L.) J Exp Bot 54:1447–1459

    Article  CAS  PubMed  Google Scholar 

  • 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 10:12–21

    Google Scholar 

  • 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 113:11–18

    Article  Google Scholar 

  • 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 41:1749–1757

    Article  Google Scholar 

  • del Val C, Barea JM, Azcón-Aguilar C (1999) Diversity of arbuscular mycorrhizal fungus populations in heavy-metal-contaminated soils. Appl Environ Microbiol 65:718–723

    CAS  PubMed  PubMed Central  Google Scholar 

  • Delhaize E, Ryan PR (1995) Aluminum Toxicity and Tolerance in Plants. Plant Physiol 107:315–321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 122:190–199

    Article  CAS  Google Scholar 

  • Elbon A, Whalen J (2015) Phosphorus supply to vegetable crops from arbuscular mycorrhizal fungi: a review. Biol Agric Hortic 31:73–90

    Article  Google Scholar 

  • Elser J, Bennett E (2011) Phosphorus cycle: a broken biogeochemical cycle. Nature 478:29–31

    Article  CAS  PubMed  Google Scholar 

  • 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 32:601–616

    Article  CAS  Google Scholar 

  • 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 36:1771–1782

    Article  CAS  PubMed  Google Scholar 

  • 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 166:281–292

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evelin H, Giri B, Kapoor R (2012) Contribution of Glomus intraradices inoculation to nutrient acquisition and mitigation of ionic imbalance in NaCl-stressed Trigonella foenum-graecum. Mycorrhiza 22:203–217

    Article  CAS  PubMed  Google Scholar 

  • Evelin H, Giri B, Kapoor R (2013) Ultrastructural evidence for AMF mediated salt stress mitigation in Trigonella foenum-graecum. Mycorrhiza 23:71–86

    Article  CAS  PubMed  Google Scholar 

  • 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 43:1866–1872

    Article  CAS  Google Scholar 

  • 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 55:227–232

    Article  Google Scholar 

  • 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 91:37–47

    Article  Google Scholar 

  • 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 8:551–559

    Article  CAS  Google Scholar 

  • Finlay RD (2008) Ecological aspects of mycorrhizal symbiosis with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot 59:1115–1126

    Article  CAS  PubMed  Google Scholar 

  • Fischer EM, Knutti R (2015) Anthropogenic contribution to global occurrence of heavy-precipitation and high-temperature extremes. Nat Clim Chang 5:560–564

    Article  Google Scholar 

  • 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 211–272

    Google Scholar 

  • Gadd GM (1993) Interaction of fungi with toxic metals. New Phytol 124:25–60

    Article  CAS  Google Scholar 

  • 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 17:3489–3499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 95:263–268

    Article  CAS  Google Scholar 

  • 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 83:147–157

    Google Scholar 

  • Giovannetti M, Sbrana C, Avio L, Citernesi AS, Logi C (1993) Differential hyphal morphogenesis in arbuscular mycorrhizal fungi during pre-infection stages. New Phytol 125:587–593

    Article  Google Scholar 

  • 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 116:429–437

    Article  CAS  PubMed Central  Google Scholar 

  • 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 240:287–297

    Article  Google Scholar 

  • 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 130:317–323

    Article  PubMed  CAS  Google Scholar 

  • 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 4:253–266

    Article  CAS  Google Scholar 

  • 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 36:1373–1384

    Article  CAS  Google Scholar 

  • Hause B, Schaarschmidt S (2009) The role of jasmonates in mutualistic symbioses between plants and soil-born microorganisms. Phytochemistry 70:1589–1599

    Article  CAS  PubMed  Google Scholar 

  • 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 201:28–41

    Article  CAS  PubMed  Google Scholar 

  • 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 186:285–289

    Article  CAS  PubMed  Google Scholar 

  • Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68:139–146

    Article  CAS  PubMed  Google Scholar 

  • Hove RM, Ziemann M, Bhave M (2015) Identification and expression analysis of the barley (Hordeum vulgare L.) Aquaporin Gene Family. PLoS One 10:e0128025

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 125:279–289

    Article  CAS  PubMed  Google Scholar 

  • 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 1–20

    Google Scholar 

  • 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 pp

    Google Scholar 

  • 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 37:1–16

    Google Scholar 

  • 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 16:65–85

    Article  Google Scholar 

  • Karandashov V, Nagy R, Amrhein N, Bucher M (2004) Evolutionary conservation of a phosphate transporter in the arbuscular mycorrhizal symbiosis. PNAS 101:6285–6290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelly CN, Morton JB, Cumming JR (2005) Variation in aluminum resistance among arbuscular mycorrhizal fungi. Mycorrhiza 15:193–201

    Article  CAS  PubMed  Google Scholar 

  • Klugh KR, Cumming JR (2007) Variations in organic acid exudation and aluminum resistance among arbuscular mycorrhizal species colonizing Liriodendron tulipifera. Tree Physiol 27:1103–1112

    Article  CAS  PubMed  Google Scholar 

  • Klugh-Stewart K, Cumming JR (2009) Organic acid exudation by mycorrhizal Andropogon virginicus L. (broomsedge) roots in response to aluminum. Soil Biol Biochem 41:367–373

    Article  CAS  Google Scholar 

  • Knapp AK, Briggs JM, Koelliker JK (2001) Frequency and extent of water limitation to primary production in a mesic temperate grassland. Ecosystems 4:19–28

    Article  Google Scholar 

  • Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plan Mol Biol 46:237–260

    Article  CAS  Google Scholar 

  • 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 55:459–493

    Article  CAS  PubMed  Google Scholar 

  • Kochian L, Piñeros M, Hoekenga O (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175–195

    Article  CAS  Google Scholar 

  • 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 196:535–547

    Article  CAS  PubMed  Google Scholar 

  • Koslowsky S, Boener R (1989) Interactive effects of aluminum, phosphorus and mycorrhizae on growth and nutrient uptake of Panicum virgatum L. (Poaceae). Environ Pollut 61:107–125

    Article  CAS  PubMed  Google Scholar 

  • Kraemer U (2003) Phytoremediation to phytochelatin – plant trace metal homeostasis. New Phytol 158:4–6

    Article  Google Scholar 

  • Kramer PJ, Boyer JS (1995) Water relations of plants and soils. Academic, London, 495 p

    Google Scholar 

  • Krikun J, Haas JH, Dodd J, Kinsbursky R (1990) Mycorrhizal dependence of four crops in a P-sorbing soil. Plant Soil 122:213–217

    Article  CAS  Google Scholar 

  • 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 231:233–239

    Article  CAS  Google Scholar 

  • Lambers H, Chapin FS, Pons TL (2008) Plant physiological ecology, 2nd edn. Springer, New York

    Book  Google Scholar 

  • 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 249:343–357

    Article  CAS  Google Scholar 

  • 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 181:199–207

    Article  CAS  PubMed  Google Scholar 

  • Leung HM, Ye ZH, Wong MH (2007) Survival strategies of plants associated with arbuscular mycorrhizal fungi on toxic mine tailings. Chemosphere 66:905–915

    Article  CAS  PubMed  Google Scholar 

  • 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 93–186

    Google Scholar 

  • Li XF, Ma JF, Matsumoto H (2000) Pattern of aluminum-induced secretion of organic acids differs between rye and wheat. Plant Physiol 123:1537–1543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 141:674–684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 31:1075–1083

    Article  CAS  Google Scholar 

  • 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 9:331–336

    Article  CAS  Google Scholar 

  • López-Ráez JA, Charnikhova T, Fernández I, Bouwmeester H, Pozo MJ (2011) Arbuscular mycorrhizal symbiosis decreases strigolactone production in tomato. J Plant Physiol 168:294–297

    Article  PubMed  CAS  Google Scholar 

  • Luthria D, Lu Y, Maria-John KM (2015) Bioactive phytochemicals in wheat: extraction, analysis, processing, and functional properties. J Funct Foods 18:910–925

    Article  CAS  Google Scholar 

  • Lux HB, Cumming JR (2001) Mycorrhizae confer aluminum resistance to tulip-poplar seedlings. Can J For Res 31:694–702

    Article  CAS  Google Scholar 

  • Ma JF (2000) Role of organic acids in detoxification of Al in higher plants. Plant Cell Physiol 41:383–390

    Article  CAS  PubMed  Google Scholar 

  • Ma JF, Zheng SJ, Matsumoto H (1997) Specific secretion of citric acid induced by Al stress in Cassia tora L. Plant Cell Physiol 348:1019–1025

    Article  Google Scholar 

  • 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 80:60–66

    Article  CAS  PubMed  Google Scholar 

  • Manchanda G, Garg N (2011) Alleviation of salt-induced ionic, osmotic and oxidative stresses in Cajanus cajan nodules by AM inoculation. Plant Biosys 145:88–97

    Article  Google Scholar 

  • 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 99:137–140

    Article  Google Scholar 

  • Marschner P, Timonen S (2005) Interactions between plant species and mycorrhizal colonization on the bacterial community composition in the rhizosphere. Appl Soil Ecol 28:23–36

    Article  Google Scholar 

  • 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 17:83–92

    Article  CAS  Google Scholar 

  • 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. https://doi.org/10.3389/fpls.2016.01273

  • McGrath SP, Zhao FJ (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opin Biotechnol 14:277–282

    Article  CAS  PubMed  Google Scholar 

  • 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 48:117–124

    Article  Google Scholar 

  • 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 75:8–15

    Article  CAS  Google Scholar 

  • Meier S, Borie F, Bolan N, Cornejo P (2012b) Phytoremediation of metal-polluted soils by arbuscular mycorrhizal fungi. Crit Rev Environ Sci Technol 42:741–775

    Article  CAS  Google Scholar 

  • 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 61:280–287

    Article  Google Scholar 

  • 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 178:126–135

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.1007/s11368-015-1256-6 (in press)

  • 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 29:681–695

    Article  CAS  Google Scholar 

  • Mikkelsen BL, Rosendahl S, Jakobsen I (2008) Underground resource allocation between individual networks of mycorrhizal fungi. New Phytol 180:890–898

    Article  PubMed  Google Scholar 

  • 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 3–18

    Chapter  Google Scholar 

  • Miyasaka SC, Buta JG, Howell RK, Foy CD (1991) Mechanism of aluminum tolerance in snapbean: root exudation of citric acid. Plant Physiol 96:737–743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 28:1–16

    Article  CAS  Google Scholar 

  • 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):e1187356

    Article  CAS  Google Scholar 

  • Nakagawa T, Mori S, Yoshimura E (2003) Amelioration of aluminum toxicity by pretreatment with phosphate in aluminum-tolerant rice cultivar. J Plant Nutr 26:619–628

    Article  CAS  Google Scholar 

  • 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 50:239–252

    Article  Google Scholar 

  • 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 14:77

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pellet DM, Papernik LA, Kochian LV (1996) Multiple aluminum resistance mechanisms in wheat: roles of root apical phosphate and malate exudation. Plant Physiol 112:591–597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez-Tienda J, Valderas A, Camañes G, Garcia-Agustin P, Ferrol N (2012) Kinetics of NH4 + uptake by the arbuscular fungus Rhizophagus irregularis. Mycorrhiza 22:485–491

    Article  PubMed  CAS  Google Scholar 

  • Peterson RL, Massicotte HB, Melville LH (2004) Mycorrhizas: anatomy and cell biology. NRC Research Press, Ottawa, 173 pp

    Google Scholar 

  • Plenchette C, Morel C (1996) External phosphorus requirement of mycorrhizal and non-mycorrhizal barley and soybean plants. Biol Fertil Soils 21(4):303–308

    Article  Google Scholar 

  • 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 15:596–605

    Article  CAS  PubMed  Google Scholar 

  • 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 1:58–69

    Google Scholar 

  • 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 60:389–404

    Article  CAS  Google Scholar 

  • 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 185:75–83

    Article  CAS  PubMed  Google Scholar 

  • Rapti-Caputo D (2010) Influence of climatic changes and human activities on the salinization process of coastal aquifer systems. Ital J Agron 5:67–79

    Article  Google Scholar 

  • Redecker D, Morton JB, Bruns TD (2000) Ancestral lineages of arbuscular mycorrhizal fungi (Glomales). Mol Phylogen Evol 14:276–284

    Article  CAS  Google Scholar 

  • Requena N, Serrano E, Ocon A, Breuninger J (2007) Plant signals and fungal perception during arbuscular mycorrhiza establishment. Phytochemistry 68:33–40

    Article  CAS  PubMed  Google Scholar 

  • 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 260:283–290

    Article  CAS  Google Scholar 

  • Ryan PR, Delhaize E, Randall PJ (1995) Characterization of Aluminum-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196:788–795

    Article  Google Scholar 

  • 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 6:1707–1710

    Article  CAS  PubMed  Google Scholar 

  • 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 188:89–96

    Article  PubMed  CAS  Google Scholar 

  • 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 61:269–274

    Article  CAS  Google Scholar 

  • Schijlen E, Ric de Vos CH, van Tunen A, Bovy AG (2004) Modification of flavonoid biosynthesis in crop plants. Phytochemistry 19:2631–2648

    Article  CAS  Google Scholar 

  • Schwitzguébel JP (2001) Hype or hope: the potential of phytoremediation as an emerging green technology. Remediat J 11:63–78

    Article  Google Scholar 

  • 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 72:449–455

    Article  Google Scholar 

  • 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 23:167–183

    Article  CAS  PubMed  Google Scholar 

  • 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 66:696–705

    Article  CAS  Google Scholar 

  • 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 16:164–173

    Google Scholar 

  • 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 108:228–237

    Article  Google Scholar 

  • 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 14:194–199

    Article  CAS  PubMed  Google Scholar 

  • 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 95:298–304

    Article  Google Scholar 

  • Simon L, Bousquet J, Levesque RC, Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular plants. Nature 363:67–69

    Article  Google Scholar 

  • 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 162:1308–1318

    Article  PubMed  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, London

    Google Scholar 

  • 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 62:227–250

    Article  CAS  PubMed  Google Scholar 

  • 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 96:68–74

    Article  Google Scholar 

  • 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 45:157–168

    Google Scholar 

  • Soka G, Ritchie M (2014) Arbuscular mycorrhizal symbiosis, ecosystem processes and environmental changes in tropical soils. Open J Ecol 4:11–22

    Article  Google Scholar 

  • 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 102:795–804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 167:545–557

    Article  CAS  PubMed  Google Scholar 

  • 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):e1028706

    Article  CAS  Google Scholar 

  • 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 48:839–843

    Article  Google Scholar 

  • 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 38:1699–1712

    Article  PubMed  Google Scholar 

  • 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 4:17–22

    Article  Google Scholar 

  • 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 71:34–40

    Article  Google Scholar 

  • 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 33:1247–1260

    Article  CAS  Google Scholar 

  • 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 73:73–83

    Article  Google Scholar 

  • Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecol 2011:1–20

    Google Scholar 

  • Yano K, Takaki M (2005) Mycorrhizal alleviation of acid soil stress in the sweet potato (Ipomoea batatas). Soil Biol Biochem 37:1569–1572

    Article  CAS  Google Scholar 

  • 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 90:26–34

    Article  Google Scholar 

  • 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 23:17840–17849

    Article  CAS  Google Scholar 

  • 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 61:359–368

    Article  CAS  Google Scholar 

  • Zhao Z, Ma JF, Sato K, Takeda K (2003) Differential Al resistance and citrate secretion in barley (Hordeum vulgare L.) Planta 217:794–800

    Article  CAS  PubMed  Google Scholar 

  • 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 8:1158–1161

    CAS  Google Scholar 

  • 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 138:297–303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e52439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu YG, Miller RM (2003) Carbon cycling by arbuscular mycorrhizal fungi in soil-plant systems. Trends Plant Sci 8:407–409

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK, Hasegawa PM, Bressan RA (1997) Molecular aspects of osmotic stress in plants. Crit Rev Plant Sci 16:253–277

    Article  CAS  Google Scholar 

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Acknowledgments

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).

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Cornejo, P., Seguel, A., Aguilera, P., Meier, S., Larsen, J., Borie, F. (2017). Arbuscular Mycorrhizal Fungi Improve Tolerance of Agricultural Plants to Cope Abiotic Stress Conditions. In: Singh, D., Singh, H., Prabha, R. (eds) Plant-Microbe Interactions in Agro-Ecological Perspectives. Springer, Singapore. https://doi.org/10.1007/978-981-10-6593-4_3

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