Abstract
At present, drought and soil salinity are among the most severe environmental stresses that affect the growth of plants through marked reduction of water uptake which lowers water potential, leading to osmotic stress. In general, osmotic stress causes a series of morphological, physiological, biochemical, and molecular changes that affect plant performance. Several studies have found that diverse types of soil microorganisms improve plant growth, especially when plants are under stressful conditions. Most important are the arbuscular mycorrhizal fungi (AMF) which form arbuscular mycorrhizas (AM) with approximately 80% of plant species and are present in almost all terrestrial ecosystems. Beyond the well-known role of AM in improving plant nutrient uptake, the contributions of AM to plants coping with osmotic stress merit analysis. With this review, we describe the principal direct and indirect mechanisms by which AM modify plant responses to osmotic stress, highlighting the role of AM in photosynthetic activity, water use efficiency, osmoprotectant production, antioxidant activities, and gene expression. We also discuss the potential for using AMF to improve plant performance under osmotic stress conditions and the lines of research needed to optimize AM use in plant production.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.References
Abd-El Baki BGK, Siefritz F, Man HM, Weiner H, Kaldenhoff R, Kaiser WM (2000) Nitrate reductase in Zea mays L. under salinity. Plant Cell Environ 23:515–521
Abdel-Latef A, Chaoxing H (2011) Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidiant enzymes activity and fruit yield of tomato grown under salinity stress. Sci Hortic 127:228–233
Abdel-Latef A, Chaoxing H (2014) Does the inoculation with Glomus mosseae improve salt tolerance in pepper plants? J Plant Growth Regulat 33(3):644–653
Abdul-Wasea AA, Khalid ME (2011) Alleviation of drought stress of marigold (Tagetes erecta) plants by using arbuscular mycorrhizal fungi. Saudi J Biol Sci 18(1):93–98
Abeer H, Abd-Allah EF, Alqarawi AA, Mona A, Alenazi MM, Dilfuza E, Ahmad P (2015) Arbuscular mycorrhizal fungi mitigates NaCl induced adverse effects on Solanum lycopersicum L. Pakistan J botany 47(1):327–340
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
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: signaling and communication in plants. Aluminum stress adaptation in plants. Editors: Sanjib Kumar Panda and Frantisek Baluska. pp 203–228
Al-Garni SMS (2006) Increasing NaCl-salt tolerance of a halophytic plant Phragmites australis by mycorrhizal symbiosis. American-Eurasian J Agric & Environ Sci 1:119–126
Al-Karaki GN (2006) Nursery inoculation of tomato with arbuscular mycorrhizal fungi and subsequent performance under irrigation with saline water. Scientia Horti 109:1–7
Allen MF (1982) Influence of vesicular-arbuscular mycorrhizae on water movement through Bouteloua gracilis Lag ex Steud. New Phytol 91:191–196
Allen DJ, Ort DR (2001) Impact of chilling temperatures on photosynthesis in warm climate plants. Trends Plant Sci 6:36–42
Allen DJ, Ratner K, Giller YE, Gussakovsky EE, Shahak Y, Ort DR (2000) An overnight chill induces a delayed inhibition of photosynthesis at midday in mango (Mangifera indica L.) J Exp Bot 51:1893–1902
Amiri R, Nikbakht A, Etemadi N (2015) Alleviation of drought stress on rose geranium (Pelargonium graveolens (L.) Herit.) in terms of antioxidant activity and secondary metabolites by mycorrhizal inoculation. Scientia Horti 197:373–380
Amiri R, Nikbakht A, Etemadi N, Reza Sabzalian M (2016) Nutritional status, essential oil changes and water-use efficiency of rose geranium in response to arbuscular mycorrhizal fungi and water deficiency stress. Symbiosis:1–11
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
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
Armada E, Azcon R, Lopez-Castillo OM, Calvo-Polanco M, Ruiz-Lozano JM (2015) Autochthonous arbuscular mycorrhizal fungi and Bacillus thuringiensis from a degraded Mediterranean area can be used to improve physiological traits and performance of a plant of agronomic interest under drought conditions. Plant Physiol Biochem 90:64–74
Aroca R, Porcel R, Ruiz-Lozano JM (2007) How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytol 173:808–816
Aroca R, Bago A, Sutka M, Paz JA, Cano C, Amodeo G, Ruiz-Lozano JM (2009) Expression analysis of the first arbuscular mycorrhizal fungi aquaporin described reveals concerted gene expression between salt-stressed and nonstressed mycelium. Mol Plant-Microbe Interact 22:1169–1178
Aroca R, Porcel R, Ruiz-Lozano MJ (2012) Regulation of root water uptake under abiotic stress conditions. J E Botany 63:43–57
Aroca R, Ruiz-Lozano JM, Zamarreño AM, Paz JA, García-Mina JM, Pozo MJ, López-Ráez JA (2013) Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J Plant Physiol 170(1):47–55
Asghari HR (2008) Vesicular-arbuscular (VA) mycorrhizae improve salinity tolerance in pre-inoculation subterranean clover (Trifolium subterraneum) seedlings. Inter J Plant Production 2(3):243–256
Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216
Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3543
Audet P (2012) AM symbiosis and other plant-soil interactions in relation to environmental stress. In: Ahmad P, Prasad MNV (eds) Environmental adaptations and stress tolerance of plants in the era of climate change. Springer, New York, pp 233–264
Augé RM (2001) Water relation, drought and VA mycorrhizal symbiosis. Mycorrhiza 11:3–42
Augé RM (2004) Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84:373–381
Augé RM, Toler HD, Saxton AM (2014) Arbuscular mycorrhizal symbiosis and osmotic adjustment in response to NaCl stress: a meta-analysis. Front Plant Sci 5:562. doi:10.3389/fpls.2014.00562
Bago B, Vierheiling H, Piche Y, Azcon-Aguilar C (1996) Nitrate depletion and pH changes by the extraradical myceliumof the arbuscular mycorrhizal fungus Glomus mosseae grown in monoxenic culture. New Phytol 133:273–280
Bago B, Pfeffer P, Shachar-Hill Y (2001) Could the urea cycle be translocating nitrogen in the arbuscular mycorrhizal symbiosis? New Phytol 149:4–8
Bago B, Pfeffer PE, Zipfe W, Lammers P, Shachar-Hill Y (2002) Tracking metabolism and imaging transport in arbuscular mycorrhizal fungi. Metabolism and transport in AM fungi. Plant Soil 244:189–197
Barea JM, Pozo MJ, Azcon R, Azcon-Aguilar C (2005) Microbial cooperation in the rhizosphere. J Exp Bot 56:1761–1778
Bárzana G, Aroca R, Bienert GP, Chaumont F, Ruíz-Lozano JM (2014) New insights into the regulation of aquaporins by the arbuscular mycorrhizal symbiosis in maize plants under drought stress and possible implications for plant performance. Mol Plant-Microbe Interact 27:349–363
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
Baslam M, Goicoechea N (2012) Water deficit improved the capacity of arbuscular mycorrhizal fungi (AMF) for inducing the accumulation of antioxidant compounds in lettuce leaves. Mycorrhiza 22:347–359
Behera SK, Srivastava P, Tripathi R, Singh JP, Singh N (2010) Evaluation of plant performance of Jatropha curcas L. under different agro-practices for optimizing biomass —a case study. Biomass Bioenergy 34:30–41
Bhoopander G, Mukerji K (2004) Mycorrhizal inoculant alleviates salt stress in Sesbania aegyptiaca and Sesbania grandiflora under field conditions: Evidence for reduced sodium and improved magnesium uptake. Mycorrhiza 14:307–312
Bonfante P, Genre A (2015) Arbuscular mycorrhizal dialogues: do you speak ‘plantish’ or ‘fungish’? Trends Plant Sci 20(3):150–154
Bowles TM, Felipe H, Barrios-Masias FH, Carlisle EA, Cavagnaro TR, Jackson LE (2016) Effects of arbuscular mycorrhizae on tomato yield, nutrient uptake, water relations, and soil carbon dynamics under deficit irrigation in field conditions. Sci Total Environ 566-567:1223–1234
Boyer LR, Brain P, Xu XM, 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(3):215–227
Bray EA (2004) Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. J Exp Bot 55:2331–2341
Bryla D, Koide R (1998) Mycorrhizal response of two tomato genotypes relates to their ability to acquire and utilize phosphorus. Ann Bot 82(6):849–857
Calvo-Polanco M, Sánchez-Romera B, Aroca R, Asins MJ, Declerck S, Dodd IC, Martínez-Andújar C, Albacete A, Ruiz-Lozano JM (2016a) Exploring the use of recombinant inbred lines in combination with beneficial microbial inoculants (AM fungus and PGPR) to improve drought stress tolerance in tomato. Env Exp Bot 131:47–57
Calvo-Polanco M, Sánchez-Castro I, Cantos M, García JL, Azcón R, Ruiz-Lozano JM, Beuzón CR, Aroca R (2016b) Effects of different arbuscular mycorrhizal fungal backgrounds and soils on olive plants growth and water relation properties under well-watered and drought conditions. Plant Cell Environ 39:2498–2514
Campanelli A, Ruta C, De Mastro G, Morone-Fortunato I (2012) The role of arbuscular mycorrhizal fungi in alleviating salt stress in Medicago sativa L. var. icon. Symbiosis 59(2):65–76
Cantrell IC, Linderman RG (2001) Preinoculation of lettuce and onion with VA mycorrhizal fungi reduces deleterious effects of soil salinity. Plant Soil 233:269–281
Casieri L, Lahmidi NA, Doidy J, Veneault-Fourrey C, Migeon A, Bonneau L, Courty PE, Garcia K, Charbonnier M, Delteil A, Brun A, Zimmermann S, Plassard C, Wipf D (2013) Biotrophic transportome in mutualistic plant fungal interactions. Mycorrhiza 23:597–625
Catford JG, Staehelin C, Larose G, Piché Y, Vierheilig H (2006) Systemically suppressed isoflavonoids and their stimulating effects on nodulation and mycorrhization in alfalfa split-root systems. Plant Soil 285:257–266
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
Cavagnaro TR, Gao LL, Smith FA, Smith SE (2001) Morphology of arbuscular mycorrhizas is influenced by fungal identity. New Phytol 151:469–475
Caverzan A, Passaia G, Rosa SB, Ribeiro CW, Lazzarotto F, Margis-Pinheiro M (2012) Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. Genet Mol Biol 35:1011–1019
Ceccarelli N, Curadi M, Martelloni L, Sbrana C, Picciarelli P, Giovannetti M (2010) Mycorrhizal colonization impacts on phenolic content and antioxidant properties of artichoke leaves and flower heads two years after field transplant. Plant Soil 335:311–323
Charpentier M, Sun J, Wen J, Mysore KS, Oldroyd G (2014) ABA promotion of arbuscular mycorrhizal colonization requires a component of the PP2A protein phosphatase complex. Plant Physiol 166:2077–2090
Chen S, Jin W, Liu A, Zhang S, Liu D, Wang F, Lin X, He C (2013) Arbuscular mycorrhizal fungi (AMF) increase growth and secondary metabolism in cucumber subjected to low temperature stress. Scie Horti 160:222–229
Chitarra W, Pagliarani C, Maserti B, Lumini E, Siciliano I, Cascone P, Schubert A, Gambino G, Balestrini R, Guerrieri E (2016) Insights on the impact of arbuscular mycorrhizal symbiosis on tomato tolerance to water stress. Plant Physiol 171(2):1009–1023
Chung IM, Kim JJ, Lim JD, Yu CY, Kim SH, Hahn SJ (2006) Comparison of resveratrol, SOD activity, phenolic compounds and free amino acids in Rehmannia glutinosa under temperature and water stress. Environ Exp Bot 56:44–53
Copeman RH, Martin CA, Stutz JC (1996) Tomato growth in response to salinity and mycorrhizal fungi from saline or non-saline soils. Hortic Sci 31:341–344
Cornejo P, Borie F, Rubio F, 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(2):423–431
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
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(9):1555–1569
Cornejo P, Rubio R, Borie F (2009) Mycorrhizal propagule persistence in a succession of cereals in a disturbed and undisturbed andisol fertilized with two nitrogen sources. Chilean J Agric Res 69(3):426–434
Cornejo P, Meier S, García S, Ferrol N, Durán P, Borie F, Seguel A (2017) Contribution of inoculation with arbuscular mycorrhizal fungi to the bioremediation of a copper polluted soil using Oenothera picensis. J Soil Sci Plant Nutr. doi:10.4067/S0718-95162016005000070
Cosme M, Ramireddy E, Franken P, Schmülling T, Wurst S (2016) Shoot- and root-borne cytokinin influences arbuscular mycorrhizal symbiosis. Mycorrhiza 26(7):709–720
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 Nut 10:12–21
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(1):11–18
Daei G, Ardakani M, Rejali F, Teimuri S, Miransari M (2009) Alleviation of salinity stress on wheat yield, yield components, and nutrient uptake using arbuscular mycorrhizal fungi under field conditions. J Plant Physiol 166:617–625
Delauney AJ, Verma DP (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223
Dickson S, Smith FA, Smith SE (2007) Structural differences in arbuscular mycorrhizal symbioses: more than 100 years after Gallaud, where next? Mycorrhiza 17:375–393
Eftekhari M, Alizadeh M, Ebrahimi P (2012) Evaluation of the total phenolics and quercetin content of foliage in mycorrhizal grape (Vitis vinifera L.) varieties and effect of postharvest drying on quercetin yield. Ind Crop Prod 38:160–165
Elhindi K, Sharaf El-din A, Elgorban A (2017) The impact of arbuscular mycorrhizal fungi in mitigating salt-induced adverse effects in sweet basil (Ocimum basilicum L.) Saudi J Biol Scie 24(1):170–179
Estrada B, Aroca R, Maathuis FJM, Barea JM, Ruiz-Lozano JM (2013a) Arbuscular mycorrhizal fungi native from a Mediterranean saline area enhance maize tolerance to salinity through improved ion homeostasis. Plant Cell Environ 36:1771–1782
Estrada B, Roca R, Barea JM, Ruiz-Lozano JM (2013b) Native arbuscular mycorrhizal fungi isolated from a saline habitat improved maize antioxidant systems and plant tolerance to salinity. Plant Sci 201:42–51
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
Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1281
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
Evelin H, Giri B, Kapoor R (2013) Ultrastructural evidence for AMF mediated salt stress mitigation in Trigonella foenum-graecum. Mycorrhiza 23:71–86
Ezz T, Nawar A (1994) Salinity and mycorrhizal association in relation to carbohydrate status, leaf chlorophyll and activity of peroxidase and polyphenol oxidase enzymes in sour orange seedlings. Alexandria J Agric Research 39:263–280
Faber BA, Zasoski RJ, Munns DN (1991) A method for measuring hyphal nutrient and water uptake in mycorrhizal plants. Can J Bot 69:87–94
Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2008) Plant drought stress: effects, mechanisms and management. In: Lichtfouse E, Navarrete M, Debaeke P, Véronique S, Alberola C (eds) Sustainable Agriculture. Springer, Berlín, pp 153–188
Fellbaum CR, Gachomo EW, Beesetty Y, Choudhari S, Strahan GD, Pfeffer PE, Kiers ET, Bucking H (2012) Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 109(7):2666–2671
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
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(12):227–232
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
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
Foyer CH, Lelandais M, Kunnert KJ (1994) Photooxidative stress in plants. Physiol Plantarum 92:696–717
Garg N, Bhandari P (2016) Silicon nutrition and mycorrhizal inoculations improve growth, nutrient status, K+/Na+ ratio and yield of Cicer arietinum L. genotypes under salinity stress. Plant Growth Regul 78(3):371–387
Garg N, Manchanda G (2008) Effect of arbuscular mycorrhizal inoculation on salt-induced nodule senescence in Cajanus cajan (pigeonpea). J Plant Growth Regul 27:115–124
Garg N, Manchanda G (2009) Role of arbuscular mycorrhizae in the alleviation of ionic, osmotic and oxidative stresses induced by salinity in Cajanus cajan (L.) Millsp. pigeonpea. J Agron Crop Sci 195:110–123
Gholamhoseini M, Ghalavand A, Dolatabadian A, Jamshidi E, Khodaei-Joghan A (2013) Effects of arbuscular mycorrhizal inoculation on growth, yield, nutrient uptake and irrigation water productivity of sunflowers grown under drought stress. Agric Water Manag 117:106–114
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
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
Giri B, Kapoor R, Mukerji K (2007) Improved tolerance of Acacia nilotica to salt stress by arbuscular mycorrhiza, Glomus fasciculatum, may be partly related to elevated K+/Na+ ratios in root and shoot tissues. Microbial Ecol 54:753–760
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
Govindarajulu M, Pfeffer P, Hairu J, Abubaker J, Douds D, Allen JW, Bücking H, Lammers P, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823
Graham JH, Abbott LK (2000) Wheat response to aggressive and non-aggressive arbuscular mycorrhizal fungi. Plant Soil 220:207–218
Hajiboland R, Aliasgharzadeh N, Laiegh SF, Poschenrieder C (2010) Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331:313–327
Hammer EC, Nasr H, Pallon J, Olsson PA, Wallander H (2011) Elemental composition of arbuscular mycorrhizal fungi at high salinity. Mycorrhiza 21:117–129
Hardie K (1985) The effect of removal of extraradical hyphae on water uptake by vesicular-arbuscular mycorrhizal plants. New Phytol 101:677–684
Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153:335–344
Hasegawa PM, Bressan RA, Zhu J, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499
Hause B, Schaarschmidt S (2009) The role of jasmonates in mutualistic symbioses between plants and soil-born microorganisms. Phytochemistry 70:1589–1599
He F, Zhang H, Tang M (2015) Aquaporin gene expression and physiological responses of Robinia pseudoacacia L. to the mycorrhizal fungus Rhizophagus irregularis and drought stress. Mycorrhiza 26(4):311–323
Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB (2001) Molecular evidence for the early colonization of land by fungi and plants. Science 293:1129–1133
Heidari Z, Nazari Deljou MJ (2014) Improvement of morpho-physiological traits and antioxidant capacity of zinnia (Zinnia elegance Dreamland Red) by arbuscular mycorrhizal fungi (Glomus mosseae) inoculation. Int J Adv Biol Biomed Res 2:2627–2631
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 andantioxidant activities of this species under non-saline and saline conditions. J Plant Physiol 201:28–41
Hill AE, Shachar-Hill B, Shachar-Hill Y (2004) What are aquaporins for? J Membr Biol 197:1–32
Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–299
Hodge A, Helgason T, Fitter AH (2010) Nutritional ecology of arbuscular mycorrhizal fungi. Fungal Ecol 3(4):267–273
Hu Y, Schimdhalter U (2005) Drought and salinity: a comparison of their effects on mineral nutrition of plants. J Plant Nutr Soil Sci 168:541–549
Huang Z, He C, He Z, Zou Z, Zhang Z (2010) The effects of arbuscular mycorrhizal fungi on reactive oxyradical scavenging system of tomato under salt tolerance. Agr Sci China 9:1150–1159
Inderjit DS (2003) Ecophysiological aspects of allelopathy. Planta 217(4):529–539
Jahromi F, Aroca R, Porcel R, Ruiz-Lozano JM (2008) Influence of salinity on the in vitro development of Glomus intraradices and on the in vivo physiological and molecular responses of mycorrhizal lettuce plants. Microb Ecol 55:45–53
Janos DP (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17:75–91
Jeffries P, Gianinazzi S, Perotto S, Turnau K, Barea J (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils 37:1–16
Juniper S, Abbott L (1993) Vesicular–arbuscular mycorrhizal and soil salinity. Mycorrhiza 4:45–57
Kapoor R, Sharma D, Bhatnagar A (2008) Arbuscular mycorrhizae in micropropagation systems and their potential applications. Sci Hortic 116:227–239
Kaya C, Higgs D, Kirnak H, Tas I (2003) Mycorrhizal colonisation improves fruit yield and water use efficiency in watermelon (Citrullus lanatus Thunb.) grown under well-watered and water-stressed conditions. Plant Soil 253:287–292
Kaya C, Ashraf M, Sonmez O (2009) The influence of arbuscular mycorrhizal colonisation on key growth parameters and fruit yield of pepper plants grown at high salinity. Sci Hortic 121:1–6
Khaled LB, Gomez AM, Ouarraqi EM, Oihabi A (2003) Physiological and biochemical responses to salt stress of mycorrhized and/or nodulated clover seedlings (Trifolium alexandrinum L.) Agronomie 23:571–580
Khalvati MA, Hu Y, Mozafar A, Schmidhalter U (2005) Quantification of water uptake by arbuscular mycorrhizal hyphae and its significance for leaf growth, water relations, and gas exchange of barley subjected to drought stress. Plant Biol 7:706–712
Kiani SP, Grieu P, Maury P, Hewezi T, Gentzbittel L, Sarrafi A (2007) Genetic variability for physiological traits under drought conditions and differential expression of water stress associated genes in sunflower (Helianthus annuus L.) Biomed Life Sci 114:193–207
Kikuchi Y, Hijikata N, Ohtomo R, Handa Y, Kawaguchi M, Saito K, Masuta C, Ezawa T (2016) Aquaporin-mediated long-distance polyphosphate translocation directed towards the host in arbuscular mycorrhizal symbiosis: application of virus-induced gene silencing. New Phytol 211:1202–1208
Kishor PB, Sreenivasulu N (2014) Is proline accumulation per se correlated with stress tolerance or is proline homeostasis a more critical issue? Plant Cell and Enviroment 37:300–311
Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301
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
Kobae Y, Tamura Y, Takai S, Banba M, Hata S (2010) Localized expression of arbuscular mycorrhiza-inducible ammonium transporters in soybean. Plant Cell Physiol 51:1411–1415
Kohlen W, Charnikhova T, Lammers M, Pollina T, Tóth P (2012) The tomato carotenoid cleavage dioxygenase8 (SICCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytol 196(2):535–547
Kohler J, Caravaca F, Roldán A (2010) An AM fungus and a PGPR intensify the adverse effects of salinity on the stability of rhizosphere soil aggregates of Lactuca sativa. Soil Biol Biochem 42:429–434
Kramer PJ, Boyer JS (1997) Water relations of plants and soils. Academic Press, London 495 p
Kruse E, Uehlein N, Kaldenhoff R (2006) The aquaporins. Genome Biol 7(2):206
Ksouri R, Megdiche W, Debez A, Falleh H, Grignon C, Abdelly C (2007) Salinity effects on polyphenol content and antioxidant activities in leaves of the halophyte Cakile maritima. Plant Physiol Biochem 45:244–249
Kumar A, Sharma S, Mishra S (2011) Influence of arbuscular mycorrhizal (AM) fungi and salinity on seedling growth, solute accumulation and mycorrhizal dependency of Jatropha curcas L. J Plant Growth Regul 29:297–306
Kumar A, Sharma S, Mishra S, Dames JF (2015) Arbuscular mycorrhizal inoculation improves growth and antioxidative response of Jatropha curcas (L.) under Na2SO4 salt stress. Plant Bios – Inter J D Aspects Plant Biol 149(2):260–269
Lambers H, Chapin FS, Pons TL (2008) Plant physiological ecology, 2nd edn. Springer, New York
Lehmann A, Rillig MC (2015) Arbuscular mycorrhizal contribution to copper, manganese and iron nutrient concentrations in crops: a meta-analysis. Soil Biol Biochem 81:147–158
Lehmann S, Funck D, Szabados L, Rentsch D (2010) Proline metabolism and transport in plant development. Amino Acids 39:949–962
Lehmann A, Veresoglou SD, Leifheit EF, Rillig MC (2014) Arbuscular mycorrhizal influence on zinc nutrition in crop plants: A meta-analysis. Soil Biol Biochem 69:123–131
Levitt J (1980) Responses of plants to environmental stresses. In: Kozlowski TT (ed) Water, radiation, salt and other stresses, vol 2, 2nd edn. Academic, New York, pp 93–186
Li T, Hu YJ, Hao ZP, Li H, Wang YS, Chen BD (2013a) First cloning and characterization of two functional aquaporin genes from an arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 197:617–630
Li T, Hu YJ, Hao ZP, Li H, Chen BD (2013b) Aquaporin genes GintAQPF1 and GintAQPF2 from Glomus intraradices contribute to plant drought tolerance. Plant Sign Behav 8(5):e24030
Liu C, Muchhal US, Uthappa M, Kononowicz AK, Raghothama KG (1998) Tomato phosphate transporter genes are differentially regulated in plant tissues by phosphorus. Plant Physiol 116:91–99
Liu T, Li Z, Hui C, Tang M, Zhang H (2016) Effect of Rhizophagus irregularis on osmotic adjustment, antioxidation and aquaporin PIP genes expression of Populus × canadensis ‘Neva’ under drought stress. Acta Physiol Plant 38(8):191–191
Lopez D, Venisse JS, Fumanal B, Chaumont F, Guillot E, Daniels MJ, Cochard H, Julien JL, Gousset-Dupont A (2013) Aquaporins and leaf hydraulics: poplar sheds new light. Plant Cell Physiol 54(12):1963–1975
López-Pedrosa A, González-Guerrero M, Valderas A, Azcón-Aguilar C, Ferrol N (2006) GintAMT1 encodes a functional high-affinity ammonium transporter that is expressed in the extraradical mycelium of Glomus. Fungal Genet Biol 43:102–110
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
Løvdal T, Olsen KM, Slimestad R, Verheul M, Lillo C (2010) Synergetic effects of nitrogen depletion, temperature, and light on the content of phenolic compounds and gene expression in leaves of tomato. Phytochemistry 71:605–613
Ludwig-Muller J, Benett RN, García-Garrido JM, Piche Y, Vierheilig H (2002) Reduced arbuscular mycorrhizal root colonization in Tropaeolum majus and Carica papaya after jasmonic acid application can not be attributed to increased glucosinolate levels. J Plant Physiol 159:517–523
Maldonado-Mendoza IE, Dewbre GR, Harrison MJ (2001) A phosphate transporter gene from the extra-radical mycelium of an arbuscular mycorrhizal fungus Glomus intraradices is regulated in response to phosphate in the environment. Mol Plant-Microbe Interact 14(10):1140–1148
Manoharan PT, Shanmugaiah V, Balasubramanian N, Gomathinayagam S, Sharma MP, Muthuchelian K (2010) Influence of AM fungi on the growth and physiological status of Erythrina variegata Linn. grown under different water stress conditions. Eur J Soil Biol 46:151–156
Mansfield TJ, Atkinson CJ (1990) Stomatal behaviour in water stressed plants. In: Alscher RG, Cumming JR (eds) Stress responses in plants: adaptation and acclimation mechanisms. Wiley, New York, pp 241–264
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
Mardukhi B, Rejali F, Daei G, Ardakani MR, Malakouti M, Miransari M (2011) Arbuscular mycorrhizas enhance nutrient uptake in different wheat genotypes at high salinity levels under field and greenhouse conditions. Com Rend Biol 334:564–571
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
Marschner P, Crowley DE, Higashi RM (1997) Root exudation and physiological status of a root-colonizing fluorescent pseudomonad in mycorrhizal and non-mycorrhizal pepper (Capsicum annuum L.) Plant Soil 189:11–20
Martin SL, Mooney SJ, Dickinson MJ, West HM (2012) The effects of simultaneous root colonisation by three glomus species on soil pore characteristics. Soil Biol Biochem 49:167–173
Martín-Rodríguez JA, León-Morcillo R, Vierheilig H, Ocampo Bote JA, Ludwig-Müllerm J, García-Garrido JM (2010) Mycorrhization of the notabilis and sitiens tomato mutants in relation to abscisic acid and ethylene contents. J Plant Physiol 167:606–613
Martín-Rodríguez JA, Huertas R, Ho-Plágaro T, Ocampo JA, Turecková V, Tarkowská D, Ludwig-Müller J, García-Garrido JM (2016) Gibberellin–abscisic acid balances during arbuscular mycorrhiza formation in tomato. Front Plant Sci 7:1273. doi:10.3389/fpls.2016.01273
Marulanda A, Azcón R, Ruiz-Lozano JM (2003) Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa plants under drought stress. Physiol Plant 119:526–533
Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624
Maurel C, Santoni V, Luu DT, Wudick MM, Verdoucq L (2009) The cellular dynamics of plant aquaporin expression and functions. Curr Opin Plant Biol 12:690–698
Mikkelsen BL, Rosendahl S, Jakobsen I (2008) Underground resource allocation between individual networks of mycorrhizal fungi. New Phytol 180:890–898
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
Mo Y, Wang Y, Yang R, Zheng J, Liu C, Li H, Ma J, Zhang Y, Wei C, Zhang X (2016) Regulation of plant growth, photosynthesis, antioxidation and osmosis by an arbuscular mycorrhizal fungus in watermelon seedlings under well-watered and drought conditions. Front Plant Sci 7:644
Morgan JAW, Bending GD, White PJ (2005) Biological costs and benefits to plant–microbe interactions in the rhizosphere. J Exp Bot 56:1729–1739
Mosse B, Hepper CM (1975) Vesicular-arbuscular mycorrhizal infections in root organ cultures. Physiol Plant Pathol 5:215–233
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 Sign Behav 11(6):e1187356
Niu X, Bressan RA, Hasegawa PM, Pardo JM (1995) lon homeostasis in NaCl stress environments. Plant Physiol 109:735–742
Olsson PA, Baath E, Jakobsen I, Söderström B (1995) The use of phospholipid and neutral lipid fatty acids to estimate biomass of arbuscular mycorrhizal fungi in soil. Mycol Res 99:623–629
Omirou M, Ioannides IM, Ehaliotis C (2013) Mycorrhizal inoculation affects arbuscular mycorrhizal diversity in watermelon roots, but leads to improved colonization and plant response underwater stress only. Appl Soil Ecol 63:112–119
Ortiz N, Armada E, Duque E, Roldán A, Azcón R (2015) Contribution of arbuscular mycorrhizal fungi and/or bacteria to enhancing plant drought tolerance under natural soil conditions: Effectiveness of autochthonous or allochthonous strains. J Plant Physiol 174:87–96
Ouziad F, Wilde P, Schmelzer E, Hildebrandt U, Bothe H (2006) Analysis of expression of aquaporins and Na+/H+ transporters in tomato colonized by arbuscular mycorrhizal fungi and affected by salt stress. Environ Exp Bot 57:177–186
Ozkur O, Ozdemir F, Bor M, Turkan I (2009) Physiochemical and antioxidant responses of the perennial xerophyte Capparis ovate Desf to drought. Environ Exp Bot 66:487–492
Palacio S, Escudero A, Montserrat-Martí G, Maestro M, Milla R, Albert MJ (2007) Plants living on gypsum: beyond the specialist model. Ann Bot 99(2):333–343
Pearson JN, Jakobsen I (1993) Symbiotic exchange of carbon and phosphorus between cucumber and three arbuscular mycorrhizal fungi. New Phytol 124:481–488
Pedranzani H, Rodríguez-Rivera M, Gutiérrez M, Porcel R, Hause B, Ruiz-Lozano JM (2016) Arbuscular mycorrhizal symbiosis regulates physiology and performance of Digitaria eriantha plants subjected to abiotic stresses by modulating antioxidant and jasmonate levels. Mycorrhiza 26(2):141–152
Perez-Perez JG, Robles JM, Tovar JC, Botia P (2009) Response to drought and salt stress of lemon ‘Fino 49’ under field conditions: water relations, osmotic adjustment and gas exchange. Sci Hort 122:83–90
Peterson RL, Massicotte HB, Melville LH (2004) Mycorrhizas: anatomy and cell biology. NRC Research Press, Ottawa 173 pp
Porcel R, Ruiz-Lozano JM (2004) Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. J Exp Bot 55:1743–1750
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
Porcel R, Aroca R, Azcon R, Ruiz-Lozano JM (2016) Regulation of cation transporter genes by the arbuscular mycorrhizal symbiosis in rice plants subjected to salinity suggests improved salt tolerance due to reduced Na+ root-to-shoot distribution. Mycorrhiza 26(7):673–684
Porras-Soriano A, Soriano-Martin ML, Porras-Piedra A, Azcón R (2009) Arbuscular mycorrhizal fungi increased growth, nutrient uptake and tolerance to salinity in olive trees under nursery conditions. J Plant Physiol 166(13):1350–1359
Rabie GH, Almadini AM (2005) Role of bioinoculants in development of salt-tolerance of Vicia faba plants under salinity stress. Afr J Biotechnol 4:210–222
Ramoliya P, Patel H, Pandey AN (2004) Effect of salinization of soil on growth and macro- and micro-nutrient accumulation in seedlings of Salvadora pérsica (Salvadoraceae). Forest Ecol Manag 2002:181–193
Rapti-Caputo D (2010) Influence of climatic changes and human activities on the salinization process of coastal aquifer systems. Ital J Agron 5(3):67–79
Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161(11):1189–1202
Redecker D, Morton JB, Bruns TD (2000) Ancestral lineages of arbuscular mycorrhizal fungi (Glomales). Mol Phylogen Evol 14:276–284
Redecker D, Schüßler A, Stockinger H, Stürmer SL, Morton JB, Walker C (2013) An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23:515–531
Regvar M, Gogala N, Zalar P (1996) Effects of jasmonic acid on mycorrhizal Allium sativum. New Phytol 134:703–707
Rice-Evans CA, Miller NJ, Paganga G (1996) Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic Biol Med 20:933–956
Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53
Rillig MC, Wright SF, Nichols KA, Schmidt WF, Torn MS (2001) Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils. Plant Soil 233:167–177
Robert M, Augé RM, Heather D, Carl F, Sams EA, Ghazala N (2008) Hydraulic conductance and water potential gradients in squash leaves showing mycorrhiza-induced increases in stomatal conductance. Mycorrhiza 18:115–121
Rozpadek P, Rąpała-Kozik M, Wężowicz K, Grandin A, Karlsson S, Ważny R, Anielska T, Turnau K (2016) Arbuscular mycorrhiza improves yield and nutritional properties of onion (Allium cepa). P Physiol Biochem 107:264–272
Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13(6):309–317
Ruiz-Lozano JM, Aroca R (2010) Host response to osmotic stresses: stomatal behaviour and water use efficiency of arbuscular mycorrhizal plants. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function, second edn. Springer Science + Business Media, Berlin, pp 239–256
Ruiz-Lozano JM, Azcón R (1995) Hyphal contribution to water uptake in mycorrhizal plants as affected by the fungal species and water status. Phys Plantarum 95:472–478
Ruiz-Lozano JM, Gomez M, Azcon R (1995) Influence of different Glomus species on the time course of physiological responses of lettuce to progressive drought stress periods. Plant Sci 110:37–44
Ruíz-Lozano JM, Perálvarez MC, Aroca R, Azcón R (2011) The application of a treated sugar beet waste residue to soil modifies the responses of mycorrhizal and non mycorrhizal lettuce plants to drought stress. Plant Soil 346:153–166
Ruiz-Lozano JM, Porcel R, Azcón R, Aroca R (2012) Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. J Exp Botany 63(11):4033–4044
Ruiz-Lozano JM, Aroca R, Zamarreño AM, Molina S, Andreo-Jiménez B, Porcel R, García-Mina JM, Ruyter-Spira C, López-Ráez JA (2015) Arbuscular mycorrhizal symbiosis induces strigolactone biosynthesis under drought and improves drought tolerance in lettuce and tomato. Plant Cell Environ 39(2):441–452
Ruiz-Sanchez M, Aroca R, Muñoz Y, Polón R, Ruiz-Lozano JM (2010) The arbuscular mycorrhizal simbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. J Plant Physiol 167:862–869
Ruth B, Khalvati M, Schmidhalter U (2011) Quantification of mycorrhizal water uptake via high-resolution on-line water content sensors. Plant Soil 342:459–468
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
Safir GR, Boyer JS, Gerdemann JW (1971) Mycorrhizal enhancement of water transport in soybean. Science 172:581–583
Safir GR, Boyer JS, Gerdemann JW (1972) Nutrient status and mycorrhizal enhancement of water transport in soybean. Plant Physiol 49:700–703
Saibo NJM, Lourenço T, Oliveira MM (2009) Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Ann Bot 103:609–623
Samarah NH, Alqudah AM, Amayreh JA, McAndrews GM (2009) The effect of late-terminal drought stress on yield components of four barley cultivars. J Agron Crop Sci 195:427–441
Sánchez-Blanco MJ, Conejero W, Navarro A, Ortuño MF, Alarcón JJ, Torrecillas A, Morte A, García-Mina JM, López LF (2004) Implementation of a new mycorrhizal inoculant fluid through drip irrigation on lettuce. Agric Murcia 3:14–15
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(189):89–96
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 Nutri 61(2):269–274
Schüβler A (2000) Glomus claroideum forms an arbuscular mycorrhiza-like symbiosis with the hornwort Anthoceros punctatus. Mycorrhiza 10:15–21
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 Biotech 14:194–199
Sharifi M, Ghorbanli M, Ebrahimzadeh H (2007) Improved growth of salinity-stressed soybean after inoculation with pre-treated mycorrhizal fungi. J Plant Physiol 164:1144–1151
Sheng M, Tang M, Chen H, Yang B, Zhang F, Huang Y (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18:287–296
Sheng M, Tang M, Zhang F, Huang Y (2011) Influence of arbuscular mycorrhiza on organic solutes in maize leaves under salt stress. Mycorrhiza 21:423–430
Shokri S, Maadi B (2009) Effects of arbuscular mycorrhizal fungus on the mineral nutrition and yield of Trifolium alexandrium plants under salinity stress. J Agron 8:79–83
Simon L, Bousquet J, Levesque RC, Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular plants. Nature 363:67–69
Singh S, Gupta AK, Kaur N (2012) Differential responses of antioxidative defence system to long-term field drought in wheat (Triticum aestivum L.) genotypes differing in drought tolerance. J Agron Crop Sci 198:185–189
Sircelj 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
Sjöberg J (2005) Arbuscular mycorrhizal fungi-occurrence in Sweden and interaction with a pathogenic fungus in barley. PhD dissertation, Swedish University of Agricultural Sciences
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, Cambridge
Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250
Smith FW, Mudge SR, Rae AL, Glassop D (2003) Phosphate transport in plants. P Soil 248:71–83
Smith SE, Smith FA, 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 Phytol 162:511–524
Smith S, Facelli E, Pope S, Smith A (2010) Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant Soil 326:3–20
Soka G, Ritchie M (2014) Arbuscular mycorrhizal symbiosis, ecosystem processes and environmental changes in tropical soils. Open J Ecol 4(1):11–22
Solaiman MZ, Saito M (1997) Use of sugars by intraradical hyphae of arbuscular mycorrhizal fungi revealed by rediorespirometry. New Phytol 136:533–538
Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev I, Gryganskyi A, James TY, O'Donnell K, Roberson RW, Taylor TN, Uehling J, Vilgalys R, White MM, Stajich JE (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108(5):1028–1046
Sreenivasulu N, Grimm B, Wobus U, Weschke W (2000) Differential response of antioxidant compounds to salinity stress in salt tolerant and salt sensitive seedlings of foxtail millet (Setaria italica). Physiol Plant 109:435–442
Subramanian KS, Charest C (1995) Influence of arbuscular mycorrhizae on the metabolism of maize under drought stress. Mycorrhiza 5:273–278
Subramanian KS, Charest C (1998) Arbuscular mycorrhizae and nitrogen assimilation in maize after drought and recovery. Physiol Plantarum 102:285–296
Sylvia DM, William SE, (1992) Vesicular-arbuscular mycorrhizae in sustainable agriculture. In: G.J. Bethlenfalvag and R.G. Linderman, (Eds.) American Society of Agronomy, Madison: 101–124
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
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
Talaat NB, Shawky BT (2011) Influence of arbuscular mycorrhizae on yield, nutrients, organic solutes, and antioxidant enzymes of two wheat cultivars under salt stress. J Plant Nutri Soil Sci 174:283–291
Talaat NB, Shawky BT (2013) Modulation of nutrient acquisition and polyamine pool in salt-stressed wheat (Triticum aestivum L.) plants inoculated with arbuscular mycorrhizal fungi. Acta Physiol Plant 35:2601–2610
Tanaka Y, Yano K (2005) Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant Cell Environ 28:1247–1254
Tejeda-Sartorius M, de la Vega OM, Delano-Frier JP (2008) Jasmonic acid influences mycorrhizal colonization in tomato plants by modifying the expression of genes involved in carbohydrate partitioning. Physiol Plant 133:339–353
Tisdall JM, Oades JM (1982) Organic matter and water-stable aggregates in soils. J Soil Sci 33:141–163
Tisserant E, Kohler A, Dozolme-Seddas P, Balestrini R, Benabdellah K, Colard A, Croll D, Da Silva C, Gomez SK, Koul R, Ferrol N, Fiorilli V, Formey D, Franken P, Helber N, Hijri M, Lanfranco L, Lindquist E, Liu Y, Malbreil M, Mori E, Poulain J, Shapiro H, van Tuinen D, Waschke A, Azcón-Aguilar C, Bécard G, Bonfante P, Harrison MJ, Küster H, Lammers P, Paszkowski U, Requena N, Rensing SA, Roux C, Sanders IR, Shachar-Hill Y, Tuskan G, Young JPW, Gianinazzi-Pearson V, Martin F (2012) The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytol 193:755–769
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 Chan 4:17–22
Valliyodan B, Nguyen HT (2006) Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curr Opin Plant Biol 9:1–7
Verbruggen E, Jansa J, Hammer EC, Rillig MC (2016) Do arbuscular mycorrhizal fungi stabilize litter-derived carbon in soil? J Ecol 104:261–269
Viereck N, Hansen PE, Jakobsen I (2004) Phosphate pool dynamics in the arbuscular mycorrhizal fungus Glomus intraradices studied by in vivo 31P NMR spectroscopy. New Phytol 162:783–794
Wahid A, Rasul E (2005) Photosynthesis in leaf, stem, flower and fruit. In: Pessarakli M (ed) Handbook of photosynthesis, 2nd edn. CRC Press, Florida, pp 479–497
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
Wright SF, Upadhyaya A, Buyer JS (1998) Comparison of N-linked oligosaccharides of glomalin from arbuscular mycorrhizal fungi and soils by capillary electrophoresis. Soil Biol Biochem 30:1853–1857
Wu QS, Xia RX (2006) Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. J Plant Physiol 163:417–425
Wu QS, Zou YN, Xia RX (2006) Effects of water stress and arbuscular mycorrhizal fungi on reactive oxygen metabolism and antioxidant production by citrus (Citrus tangerine) roots. Eur J Soil Biol 42:166–172
Wu QS, Xia RX, Zou YN (2008) Improved soil structure and citrus growth after inoculation with three arbuscular mycorrhizal fungi under drought stress. Eur J Soil Biol 44:122–128
Wu QS, Zou YN, He XH (2010) Contributions of arbuscular mycorrhizal fungi to growth, photosynthesis, root morphology and ionic balance of citrus seedlings under salt stress. Acta Physiol Plant 32:297–304
Wu QS, Zou YN, Abd-Allah EF (2014) Mycorrhizal association and ROS in plants. In: Ahmad P (ed) Oxidative damage to plants antioxid. Academic Press, Cambridge, pp 53–475
Xie X, Wenga BD, Cai B, Dong Y, Yan C (2014) Effects of arbuscular mycorrhizal inoculation and phosphorus supply on the growth and nutrient uptake of Kandelia obovata seedlings in autoclaved soil. App Soil Ecol 75:162–171
Yang CW, Chong JN, Kim CM, Li CY, Shi DC, Wang DL (2007) Osmotic adjustment and ion balance traits of an alkali resistant halophyte Kochia sieversiana during adaptation to salt and alkali conditions. Plant Soil 294:263–276
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
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. Envi Sci Pollution Research 23(17):17840–17849
Yokota A, Kawasaki S, Iwano M, Nakamura C, Miyake C, Akashi K (2002) Citrulline and DRIP-1 protein (Arge homologue) in drought tolerance of wild watermelon. Ann Bot 89:825–832
Yooyongwech S, Phaukinsang N, Cha-Um S, 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 Regul 69:285–293
Yooyongwech S, Samphumphuang T, Tisarum R, Theerawitaya C, Cha-Um S (2016) Arbuscular mycorrhizal fungi (AMF) improved water deficit tolerance in two different sweet potato genotypes involves osmotic adjustments via soluble sugar and free proline. Sci Hortic 198:107–117
Zarei M, Paymaneh Z (2014) Effect of salinity and arbuscular mycorrhizal fungi on growth and some physiological parameters of Citrus jambheri. Arch Agron Soil Sci 60(7):993–1004
Zhang YC, Wangc P, Wud QH, Zoua YN, Baoa Q, Wua QS (2016) Arbuscular mycorrhizas improve plant growth and soil structure in trifoliate orange under salt stress. Arch Agron Soil Sci 63(4):491–500
Zhao R, Guo W, Bi N, Guo J, Wang L, Zhao J, Zhang J (2015) Arbuscular mycorrhizal fungi affect the growth, nutrient uptake and water status of maize (Zea mays L.) grown in two types of coal mine spoils under drought stress. Appl Soil Ecol 88:41–49
Zhi H, Chao-Xing H, Zhong-Qun H, Zhi-Rong Z, Zhi-Bin Z (2010) The effects of arbuscular mycorrhizal fungi on reactive oxyradical scavenging system of tomato under salt tolerance. Agric Sci China 9(8):1150–1159
Zhu YG, Miller RM (2003) Carbon cycling by arbuscular mycorrhizal fungi in soil-plant systems. Trends Plant Sci 8:407–409
Zhu JK, Hasegawa PM, Bressan RA (1997) Molecular aspects of osmotic stress in plants. Crit Rev Plant Sci 16:253–277
Zhu JK, Liu J, Xiong L (1998) Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. Plant Cell 10:1181–1191
Zhu XC, Song FB, Liu SQ, Liu TD, Zhou X (2012) Arbuscular mycorrhizae improves photosynthesis and water status of Zea mays L. under drought stress. Plant Soil Environ 58(4):186–191
Zou YN, Srivastava AK, Wu QS, Huang YM (2014) Glomalin related soil protein and water relations in mycorrhizal citrus (Citrus tangerina) during soil water deficit. Arch Agron Soil Sci 60:1103–1114
Zubek S, Rola K, Szewczyk A, Majewska ML, Turnau K (2015) Enhanced concentrations of elements and secondary metabolites in Viola tricolor L. induced by arbuscular mycorrhizal fungi. Plant Soil 390:129–142
Zuccarini P (2007) Mycorrhizal infection ameliorates chlorophyll content and nutrient uptake of lettuce exposed to saline irrigation. Plant Soil Environ 7:283–289
Acknowledgements
The authors thank CONICYT, Chile, for the financial support through FONDECYT 1170264 (P. Cornejo), FONDECYT 1161326 (P. Cartes) and scholarship for Doctoral Thesis, Grant No. 21161211 (C. Santander). The authors also thank the highly valuable contribution of anonymous reviewers and the Editor of this review.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Santander, C., Aroca, R., Ruiz-Lozano, J.M. et al. Arbuscular mycorrhiza effects on plant performance under osmotic stress. Mycorrhiza 27, 639–657 (2017). https://doi.org/10.1007/s00572-017-0784-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-017-0784-x