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Arbuscular Mycorrhizal Fungi and the Tolerance of Plants to Drought and Salinity

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Symbiotic Endophytes

Part of the book series: Soil Biology ((SOILBIOL,volume 37))

Abstract

Arbuscular mycorrhizal fungi are known to form symbiosis with plants in nature. From these symbioses, the fungi obtain carbon compounds from the plants and a niche to complete their life cycle, while the plants obtain access to unavailable nutrients and water resources. Arbuscular mycorrhizal fungi are usually considered to be beneficial for plants by improving different plant parameters as growth and photosynthetical rates. However, they are also believed to play a critical role in plant tolerance and resistance under different environmental stresses. In this chapter, we will focus on the effects of drought and salinity in plants and how the presence of arbuscular mycorrhizal fungi can affect plant responses to them. We will revise the current knowledge on the physiological, biochemical, and molecular plant–fungi responses to salt and drought and the different stress tolerance mechanisms involved in cell osmoregulation, ion balance, the role of aquaporins in water balance, and the plant antioxidant system and hormone regulation. The role of AM fungi in the resistance/tolerance of plants to salt and drought will be highlighted, as well as how the presence of AM fungi within the plant roots can determine the success of plants under salt- and/or drought-affected soils. Finally, new insights into the future role of AM fungi will be advised to help understand whole plant system responses to drought and salinity.

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References

  • Abbaspour H, Saeidi-Sar S, Abdel-Wahhab MA (2012) Improving drought tolerance of Pistacia vera L. Seedlings by arbuscular mycorrhiza under greenhouse conditions. J Plant Physiol 169:704–709

    Article  PubMed  CAS  Google Scholar 

  • Abdel-Fattah GM, Wasea A, Asrar A (2012) Arbuscular mycorrhizal fungal application to improve growth and tolerance of wheat (Triticum aestivum L.) plants grown in saline soil. Acta Physiol Plant 34:267–277

    Article  CAS  Google Scholar 

  • Agre P, Sasaki S, Chrispeels MJ (1993) Aquaporins: a family of water channel proteins. Am J Physiol Renal Physiol 265:F461

    CAS  Google Scholar 

  • Alguacil MM, Hernández JA, Caravaca F, Portillo B, Roldán A (2003) Antioxidant enzyme activities in shoots from three mycorrhizal shrub species afforested in a degraded semi-arid soil. Physiol Plant 118:562–570

    Article  CAS  Google Scholar 

  • Alleva K, Niemiets CM, Sutka M, Maurel C, Parasi M, Tyerman SD, Amodeo G (2006) Plasma membrane of Beta vulgaris storage root shows high water channel activity by cytoplasmic pH and a dual range of calcium concentrations. J Exp Bot 57:609–621

    Article  PubMed  CAS  Google Scholar 

  • Aral B, Kamoun P (1997) The proline biosynthesis in living organisms. Amino Acids 13:189–217

    Article  CAS  Google Scholar 

  • Aroca R, Ferrante A, Vernieri P, Chrispeels MJ (2006) Drought, abscisic acid and transpiration rate effects on the regulation of PIP aquaporin gene expression and abundance in Phaseolus vulgaris plants. Ann Bot 98:1301–1310

    Article  PubMed  CAS  Google Scholar 

  • Aroca R, Porcel R, Ruiz-Lozano JM (2007) How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporin in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytol 173:808–816

    Article  PubMed  CAS  Google Scholar 

  • Aroca R, Vernieri P, Ruiz-Lozano JM (2008) Mycorrhizal and nonmycorrhizal Lactuca sativa plants exhibit contrasting responses to exogenous ABA during drought stress and recovery. J Exp Bot 59:2029–2041

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 170:47–55

    Article  PubMed  CAS  Google Scholar 

  • Augé RM (2001) Water relations, drought and vesicular–arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Azcón R, Gómez M, Tobar RM (1996) Physiological and nutritional responses by Lacta sativa L. to nitrogen sources and mycorrhizal fungi under drought conditions. Biol Fertil Soils 22:156–161

    Article  Google Scholar 

  • Bago B, Azcón-Aguilar C (1997) Changes in the rhizospheric pH induced by arbuscular mycorrhiza formation in onion (Allium cepa L.). Z Pflanzenernaehr Bodenk 160:333–339

    Article  CAS  Google Scholar 

  • Bárzana G, Aroca R, Paz JA, Chaumont F, Martinez-Ballesta M, Carvajal M, Ruiz-Lozano JM (2012) Arbuscular mycorrhizal symbiosis increases relative apoplastic water flow in roots of the host plant under both well-watered and drought stress conditions. Ann Bot 109:1009–1017

    Article  PubMed  CAS  Google Scholar 

  • Benabdellah K, Merlos MA, Azcón-Aguilar C, Ferrol N (2009a) GintGRX1, the first characterized glomeromycotan glutaredoxin, is a multifunctional enzyme that responds to oxidative stress. Fungal Genet Biol 46:94–103

    Article  PubMed  CAS  Google Scholar 

  • Benabdellah K, Azcón-Aguilar C, Valderas A, Speziga D, Fitzpatrick TB, Ferrol N (2009b) GintPDX1 encodes a protein involved in vitamin B6 biosynthesis that is up-regulated by oxidative stress in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 184:682–693

    Article  PubMed  CAS  Google Scholar 

  • Bernstein L (1975) Effects of salinity and sodicity on plant growth. Annu Rev Phytopathol 13:295–312

    Article  Google Scholar 

  • Boursiac Y, Chen S, Luu DT, Sorieul M, Dries N, Maurel C (2005) Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol 139:790–805

    Article  PubMed  CAS  Google Scholar 

  • Bowler C, Slooten L, Vandenbranden S, De Rycke R, Botterman J, Sybesma C, Van Montagu M, Inze D (1991) Manganese superoxide dismutase can reduce cellular damage mediated by oxygen radicals in transgenic plants. EMBO J 10:1723–1732

    PubMed  CAS  Google Scholar 

  • Calvo-Polanco M, Zwiazek JJ, Jones MD, MacKinnon MD (2009) Effects of NaCl on responses of ectomycorrhizal black spruce (Picea mariana), white spruce (Picea glauca) and jack pine (Pinus banksiana) to fluoride. Physiol Plantarum 135:51–61

    Article  CAS  Google Scholar 

  • Chaumont F, Barrieu F, Jung R, Chrispeels MJ (2000) Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity. Plant Physiol 122:1025–1034

    Article  PubMed  CAS  Google Scholar 

  • Copeman RH, Martin CA, Stutz JC (1996) Tomato growth in response to salinity and mycorrhizal fungi from saline or nonsaline soils. Hortic Sci 31:341–344

    Google Scholar 

  • Corratgé C, Zimmermann S, Lambilliotte RRL, Plassard C, Marmeisse R, Thibaud JB, Lacombe B, Sentenac H (2007) Molecular and functional characterization of a Na+-K+ transporter from the Trk family in the ectomycorrhizal fungus Hebeloma cylindrosporum. J Biol Chem 282:26057–26066

    Article  PubMed  CAS  Google Scholar 

  • Ding M, Hou P, Shen X et al (2010) Salt-induced expression of genes related to Na(+)/K(+) and ROS homeostasis in leaves of salt resistant and salt-sensitive poplar species. Plant Mol Biol 73:251–269

    Article  PubMed  CAS  Google Scholar 

  • Dodd IC, Ruíz-Lozano JM (2012) Microbial enhancement of crop resource use efficiency. Curr Opin Biotechnol 23:236–242

    Article  PubMed  CAS  Google Scholar 

  • Doussan C, Vercambre G, Page L (1998) Modelling of the hydraulic architecture of root systems: an integrated approach to water absorption—distribution of axial and radial conductances in maize. Ann Bot 81:225–232

    Article  Google Scholar 

  • El-Mesbahi MN, Azcón R, Ruiz-Lozano JM, Aroca R (2012) Plant potassium content modifies the effects of arbuscular mycorrhizal symbiosis on root hydraulic properties in maize plants. Mycorrhiza 22:555–564

    Article  PubMed  CAS  Google Scholar 

  • Estrada B, Barea JM, Aroca R, Ruiz-Lozano JM (2013) A native Glomus intraradices strain from a Mediterranean saline area exhibits salt tolerance and enhanced symbiotic efficiency with maize plants under salt stress conditions. Plant Soil. doi:10.1007/s11104-012-1409-y

    Google Scholar 

  • Estrada-Luna AA, Davies FT (2003) Arbuscular mycorrhizal fungi influence water relations, gas Exchange, abscisic acid and growth of micropropagated chile ancho pepper (Capsicum annuum) plantlets during acclimatization and post-acclimatization. J Plant Physiol 160:1073–1083

    Article  PubMed  CAS  Google Scholar 

  • Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Farzaneh M, Vierheiling H, Lössl A, Kaul HP (2011) Arbuscular mycorrhiza enhances nutrient uptake in chickpea. Plant Soil Environ 57:465–470

    CAS  Google Scholar 

  • Feng G, Zhang FS, Li XL, Tian CY, Tang C, Rengel Z (2002) Improved tolerance of maize plants to salt stress by arbuscular mycorrhiza is related to higher accumulation of soluble sugars in roots. Mycorrhiza 12:185–190

    Article  PubMed  CAS  Google Scholar 

  • Fischer M, Kaldenhoff R (2008) On the pH regulation of plant aquaporins. J Biol Chem 283:33889–33892

    Article  PubMed  CAS  Google Scholar 

  • Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963

    Article  PubMed  CAS  Google Scholar 

  • Gao YX, Li Y, Yang XX, Li HJ, Shen QR, Guo SW (2010) Ammonium nutrition increases water absorption in rice seedlings (Oryza sativa L.) under water stress. Plant Soil 331:193–201

    Article  CAS  Google Scholar 

  • 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. (pigeon pea). J Agron Crop Sci 195:110–123

    Article  CAS  Google Scholar 

  • George E (2000) Nutrient uptake. In: Douds KY, Jr DD (eds) Arbuscular mycorrhizas: physiology and function. Kluwer Academic, Dordrecht

    Google Scholar 

  • Gerbeau P, Amodeo G, Henzler T, Santoni V, Ripoche P, Maurel C (2002) The water permeability of Arabidopsis plasma membrane is regulated by divalent cations and pH. Plant J 30:71–81

    Article  PubMed  CAS  Google Scholar 

  • Giri B, Mukerji KG (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

    Article  PubMed  Google Scholar 

  • Giri B, Kapoor R, Mukerji KG (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. Microb Ecol 54:753–760

    Article  PubMed  CAS  Google Scholar 

  • González-Guerrero M, Cano C, Azcón-Aguilar C, Ferrol N (2007) GintMT1 encodes a functional metallothionein in Glomus intraradices that responds to oxidative stress. Mycorrhiza 17:327–335

    Article  PubMed  CAS  Google Scholar 

  • González-Guerrero M, Oger E, Benabdellah K, Azcón-Aguilar C, Lanfranco L, Ferrol N (2010) Characterization of a CuZn superoxide dismutase gene in the arbuscular mycorrhizal fungus. Glomus intraradices. Curr Genet 56:265–274

    Article  PubMed  CAS  Google Scholar 

  • Graham JH, Syvertsen JP (1989) Vesicular-arbuscular mycorrhizas increase chloride concentration in citrus seedlings. New Phytol 113:29–36

    Article  Google Scholar 

  • Hajibagheri MA, Yeo AR, Flowers TJ, Collins JC (1989) Salinity resistance in Zea mays-fluxes of potassium, sodium and chloride, cytoplasmic concentrations and microsomal membrane lipids. Plant Cell Environ 12:753–757

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Halliwell B, Foyer CH (1976) Ascorbic acid, metal ions and the superoxide radical. Biochem J 155:697–700

    PubMed  CAS  Google Scholar 

  • Hammer EC, Nasr H, Pallon J, Olsson PA, Wallander H (2011) Elemental composition of arbuscular mycorrhizal fungi at high salinity. Mycorrhiza 21:117–129

    Article  PubMed  CAS  Google Scholar 

  • Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42

    Article  PubMed  CAS  Google Scholar 

  • Herrera-Medina MJ, Gagnon H, Piché Y, Ocampo JA, García-Garrido JM, Vierheilig H (2003) Root colonization by arbuscular mycorrhizal fungi is affected by the salicylic acid content of the plant. Plant Sci 164:993–998

    Article  CAS  Google Scholar 

  • Herrera-Medina MJ, Steinkellner S, Vierheilig H, Ocampo Bote JA, García Garrido JM (2007) Abscisic acid determines arbuscule development and functionality in the tomato arbuscular mycorrhiza. New Phytol 175:554–564

    Article  PubMed  CAS  Google Scholar 

  • Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6:431–438

    Article  PubMed  CAS  Google Scholar 

  • Jacoby B (1994) Mechanisms involved in salt tolerance by plants. In: Pessarakli M (ed) Handbook of plant and crop stress. Dekker, New York, NY

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Jang JY, Kim DG, Kim YO, Kim JS, Kang H (2004) An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol Biol 54:713–725

    Article  PubMed  CAS  Google Scholar 

  • Jang JY, Lee SH, Rhee JY, Chung GC, Ahn SJ, Kang H (2007) Transgenic Arabidopsis and tobacco plants overexpressing an aquaporin respond differently to various abiotic stresses. Plant Mol Biol 64:621–632

    Article  PubMed  CAS  Google Scholar 

  • Johansson I, Karlsson M, Shukla VK, Chrispeels MJ, Larsson C, Kjellbom P (1998) Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 10:451–459

    PubMed  CAS  Google Scholar 

  • Juniper S, Abbott LK (2006) Soil salinity delays germination and limits growth of hyphae from propagules of arbuscular mycorrhizal fungi. Mycorrhiza 16:371–379

    Article  PubMed  CAS  Google Scholar 

  • Kamaluddin M, Zwiazek JJ (2004) Effects of root medium pH on water transport in paper birch (Betula papyrifera) seedlings in relation to root temperature and abscisic acid treatments. Tree Physiol 24:1173–1180

    Article  PubMed  CAS  Google Scholar 

  • Keskin BC, Sarikaya AT, Yuksel B, Memon AR (2010) Abscisic acid regulated gene expression in bread wheat. Aust J Crop Sci 4:617–625

    CAS  Google Scholar 

  • Kishor PB, Hong Z, Miao GH, Hu CA, Verma DPS (1995) Overexpression of Δ1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108:1387–1394

    PubMed  CAS  Google Scholar 

  • Kline KG, Barrett-Wilt GA, Sussman MR (2010) In planta changes in protein phosphorylation induced by the plant hormone abscisic acid. Proc Natl Acad Sci USA 107:15986–15991

    Article  PubMed  CAS  Google Scholar 

  • Koch K (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47:509–540

    Article  PubMed  CAS  Google Scholar 

  • Kramer PJ, Boyer JS (1997) Water relations of plants and soils. Academic, San Diego, CA

    Google Scholar 

  • Lanfranco L, Novero M, Bonfante P (2005) The mycorrhizal fungus Gigaspora margarita possesses a CuZn superoxide dismutase that is up-regulated during symbiosis with legume hosts. Plant Physiol 137:1319–1330

    Article  PubMed  CAS  Google Scholar 

  • Läuchli A, Luttge U (eds) (2002) Salinity: environment-plants-molecules. Kluwer Academic, Dordrecht

    Google Scholar 

  • Lee BR, Muneer S, Avice JC, Jung WJ, Kim TH (2012) Mycorrhizal colonisation and P-supplement effects on N uptake and N assimilation in perennial ryegrass under well-watered and drought-stressed conditions. Mycorrhiza 22:525–534

    Article  PubMed  CAS  Google Scholar 

  • Lehto T, Zwiazek JJ (2011) Ectomycorrhizas and water relations of trees: a review. Mycorrhiza 21:71–90

    Article  PubMed  Google Scholar 

  • Leslie CA, Romani RJ (1988) Inhibition of ethylene biosynthesis by salicylic acid. Plant Physiol 88:833–837

    Article  PubMed  CAS  Google Scholar 

  • Li T, Hu YJ, Hao ZP, Li H, Wang YS, Chen BD (2013) First cloning and characterization of two functional aquaporin genes from an arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 197:617–630

    Article  PubMed  CAS  Google Scholar 

  • Mahdieh M, Mostejaran A (2009) Abscisic acid regulates root hydraulic conductance via aquaporin expression in Nicotiana tabacum. J Plant Physiol 166:1993–2003

    Article  PubMed  CAS  Google Scholar 

  • Martínez-Ballesta MC, Martínez V, Carvajal M (2003) Aquaporin functionality in relation to H+-ATPase activity in root cells of Capsicum annuum grown under salinity. Physiol Plantarum 117:413–420

    Article  Google Scholar 

  • Martín-Rodríguez JA, León-Morcillo R, Vierheilig H, Ocampo JA, Ludwig-Müller J, García-Garrido JM (2011) Ethylene-dependent/ethylene-independent ABA regulation of tomato plants colonized by arbuscular mycorrhiza fungi. New Phytol 190:193–205

    Article  CAS  Google Scholar 

  • Marulanda A, Azcón R, Ruíz-Lozano JM (2003) Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa L. plants under drought stress. Physiol Plantarum 119:526–533

    Article  CAS  Google Scholar 

  • Maurel C (2007) Plant aquaporins: novel functions and regulation properties. FEBS Lett 581:2227–2236

    Article  PubMed  CAS  Google Scholar 

  • Maurel C, Verdoucq L, Luu D-T, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624

    Article  PubMed  CAS  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stress. Plant Cell Environ 33:453–467

    Article  PubMed  CAS  Google Scholar 

  • Miransari M (2010) Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol 1:563–569

    Google Scholar 

  • Navarro GA, Del P, Bañón AS, Morte A, Sánchez-Blanco MJ (2011) Effects of nursery pre-conditioning through mycorrhizal inoculation and drought in Arbutus unedo L. plants. Mycorrhiza 21:53–64

    Article  Google Scholar 

  • Navarro-Ródenas A, Ruíz-Lozano JM, Kaldenhoff R, Morte A (2012) The aquaporin TcAQP1 of the desert truffle Terfezia claveryi is a membrane pore for water and CO2 transport. Mol Plant Microbe Interact 25:259–266

    Article  PubMed  CAS  Google Scholar 

  • Németh-Cahalan KL, Hall JE (2000) pH and calcium regulate the water permeability of aquaporin 0. J Biol Chem 275:6777–6782

    Article  PubMed  Google Scholar 

  • Olías R, Eljakaoui Z, Pardo JM, Belver A (2009) The Na+/H+ exchanger SOS1 controls extrusion and distribution of Na+ in tomato plants under salinity conditions. Plant Signal Behav 4:973–976

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Parent B, Hachez C, Redondo E, Simonneau T, Chaumont F, Tardieu F (2009) Drought and abscisic acid effects on aquaporin content translate into changes in hydraulic conductivity and leaf growth rate: a trans-scale approach. Plant Physiol 149:2000–2012

    Article  PubMed  CAS  Google Scholar 

  • Park W, Scheffler E, Bauer PJ, Campbell BT (2010) Identification of the family of aquaporin genes and their expression in upland cotton (Gossypium hirsutum L.). BMC Plant Biol 10:142

    Article  PubMed  CAS  Google Scholar 

  • Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Porcel R, Azcón R, Ruiz-Lozano JM (2004) Evaluation of the role of genes encoding for Δ1-pyrroline-5-carboxylate synthetase (P5CS) during drought stress in arbuscular mycorrhizal Glycine max and Lactuca sativa plants. Physiol Mol Plant Pathol 65:211–221

    Article  CAS  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 Mol Biol 2006:389–404

    Article  CAS  Google Scholar 

  • Porcel R, Aroca R, Ruiz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. Agron Sustain Dev 32:181–200

    Article  CAS  Google Scholar 

  • Porras-Soriano A, Soriano-Martin ML, Porras-Piedra A, Azcon R (2009) Arbuscular mycorrhizal fungi increased growth, nutrient uptake and tolerance to salinity in olive trees under nursery conditions. J Plant Physiol 166:1350–1359

    Article  PubMed  CAS  Google Scholar 

  • Pozo MJ, Azcón-Aguilar C (2007) Unravelling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398

    Article  PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401

    Article  PubMed  CAS  Google Scholar 

  • Ramos AC, Façanha AR, Feijó JA (2008) A proton (H+) flux signature of the presymbiotic development of the arbuscular mycorrhizal fungi. New Phytol 178:177–188

    Article  PubMed  CAS  Google Scholar 

  • Riedel T, Groten K, Baldwin IT (2008) Symbiosis between Nicotiana attenuate and Glomus intraradices: ethylene plays a role, jasmonic acid does not. Plant Cell Environ 31:1203–1213

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Lozano JM, Aroca R (2010) Modulation of aquaporin genes by the arbuscular mycorrhizal symbiosis in relation to osmotic stress tolerance. In: Sechback J, Grube M (eds) Symbiosis and stress. Springer, Berlin

    Google Scholar 

  • Ruiz-Lozano JM, Porcel R, Aroca R (2006) Does the enhanced tolerance of arbuscular mycorrhizal plants to water deficit involve modulation of drought-induced plant genes? New Phytol 171:693–698

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Lozano JM, Alguacil MM, Bárzana G, Vernieri P, Aroca R (2009) Exogenous ABA accentuates the differences in root hydraulic properties between mycorrhizal and non mycorrhizal maize plants through regulation of PIP aquaporins. Plant Mol Biol 70:565–579

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Lozano JM, Porcel R, Azcón C, 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 Bot 63:4033–4044

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Sanchez M, Aroca R, Munoz Y, Polon R, Ruiz-Lozano JM (2010) The arbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. J Plant Physiol 167:862–869

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sakurai J, Ishikawa F, Yamaguchi T, Uemura M, Maeshima M (2005) Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol 46:1568–1577

    Article  PubMed  CAS  Google Scholar 

  • Samaras Y, Bressan RA, Csonka LN, Garcia-Rios M, Paino D’Urzo M, Rhodes D (1995) Proline accumulation during water deficit. In: Smirnoff N (ed) Environment and plant metabolism. Flexibility and acclimation. Bios Scientific, Oxford

    Google Scholar 

  • Schachtman DP, Goodger JQD (2008) Chemical root to shoot signaling under drought. Trends Plant Sci 13:281–287

    Article  PubMed  CAS  Google Scholar 

  • Scheibe R, Beck E (2011) Drought, desiccation, and oxidative stress. In: Lüttge U, Bech E, Bartels D (eds) Plant desiccation tolerance. Ecological studies, vol 215. Springer, Berlin

    Google Scholar 

  • Shao HB, Chu LY, Shao MA, Jaleel CA, Mi HM (2008) Higher plant antioxidants and redox signaling under environmental stresses. C R Biol 331:433–441

    Article  PubMed  CAS  Google Scholar 

  • Sharifi M, Ghorbanli M, Ebrahimzadeh H (2007) Improved growth of salinity-stressed soybean after inoculation with salt pre-treated mycorrhizal fungi. J Plant Physiol 164:1144–1151

    Article  PubMed  CAS  Google Scholar 

  • Shaterian J, Waterer D, De Jong H, Tanino KK (2005) Differential stress responses to NaCl salt application in early- and late maturing diploid potato (Solanum sp.) clones. Environ Exp Bot 54:202–212

    Article  CAS  Google Scholar 

  • Sheen J, Zhou L, Jang JC (1999) Sugars as signaling molecules. Curr Opin Plant Biol 2:410–418

    Article  PubMed  CAS  Google Scholar 

  • Sheng M, Tang M, Chen H, Yang BW, Zhang FF, Huang YH (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18:287–296

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Shokri S, Maadi B (2009) Effect of arbuscular mycorrhizal fungus on the mineral nutrition and yield of Trifolium alexandrinum plants under salinity stress. J Agron 8:79–83

    Article  CAS  Google Scholar 

  • Smeekens S (2000) Sugar-induced signal transduction in plants. Annu Rev Plant Biol 51:49–81

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (eds) (2008) Mycorrhizal symbiosis. Academic, San Diego, CA

    Google Scholar 

  • Steudle E, Peterson CA (1998) How does water get through roots? J Exp Bot 49:775–788

    CAS  Google Scholar 

  • Sutka M, Alleva K, Parisi M, Amodeo G (2005) Tonoplast vesicles of Beta vulgaris storage root show functional aquaporins regulated by protons. Biol Cell 97:837–846

    Article  PubMed  CAS  Google Scholar 

  • 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 Nutr Soil Sci 174:283–291

    Article  CAS  Google Scholar 

  • Tang C, Cobley BT, Mokhtara S, Wilson CE, Greenway H (1993) High pH in the nutrient solution impairs water uptake in Lupinus angustifolius L. Plant Soil 155–156:517–519

    Article  Google Scholar 

  • Tavakkoli E, Rengasamy P, McDonald GK (2010) High concentrations of Na+ and Cl ions in soil solution have simultaneous detrimental effects on growth of faba bean under salinity stress. J Exp Bot 61:4449–4459

    Article  PubMed  CAS  Google Scholar 

  • Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    Article  PubMed  CAS  Google Scholar 

  • Tisserant E, Kohler A, Dozolme-Seddas P et al (2012) The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytol 193:755–769

    Article  PubMed  CAS  Google Scholar 

  • Törnroth-Horsefield S, Wang Y, Hedfalk K, Johanson U, Karlsson M, Tajkhorshid E, Neutze R, Kjellbom P (2006) Structural mechanism of plant aquaporin gating. Nature 439:688–694

    Article  PubMed  CAS  Google Scholar 

  • Tournaire-Roux C, Sutka M, Javot H, Gout E, Gerbeau P, Luu DT, Bligny R, Maurel C (2003) Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425:393–397

    Article  PubMed  CAS  Google Scholar 

  • Trotel-Aziz P, Niogret MF, Larher F (2000) Proline level is partly under the control of abscisic acid in canola leaf discs recovery from hyper-osmotic stress. Physiol Plantarum 110:376–383

    Article  CAS  Google Scholar 

  • Türkan I, Demiral T (2009) Recent developments in understanding salinity tolerance. Environ Exp Bot 67:2–9

    Article  CAS  Google Scholar 

  • Tyerman SD, Skerrett IM (1999) Root ion channels and salinity. Sci Hortic 78:175–235

    Article  CAS  Google Scholar 

  • Wan X (2010) Osmotic effects of NaCl on cell hydraulic conductivity of corn roots. Acta Biochim Biophys Sin 42:351–357

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Mopper S, Hasentein KH (2001) Effects of salinity on endogenous ABA, IAA, JA and SA in Iris hexagona. J Chem Ecol 27:327–342

    Article  PubMed  CAS  Google Scholar 

  • Wang KLC, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14:S131–S151

    PubMed  CAS  Google Scholar 

  • Wang FY, Liu RJ, Lin XG, Zhou JM (2004) Arbuscular mycorrhizal status of wild plants in saline-alkaline soils of the Yellow River Delta. Mycorrhiza 14:133–137

    Article  PubMed  Google Scholar 

  • White PJ, Broadley MR (2001) Chloride in soils and its uptake and movement within the plant: a review. Ann Bot 88:967–988

    Article  CAS  Google Scholar 

  • Wilkinson S, Davies WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ 33:510–525

    Article  PubMed  CAS  Google Scholar 

  • Wolters H, Jürgens G (2009) Survival of the flexible: hormonal growth control and adaptation in plant development. Nat Rev Genet 10:305–317

    Article  PubMed  CAS  Google Scholar 

  • Wu QS, Zou YN (2009) Mycorrhiza has a direct effect on reactive oxygen metabolism of drought-stressed citrus. Plant Soil Environ 55:436–442

    CAS  Google Scholar 

  • Wu QS, Zou YN, Xia RX, Wang MY (2007) Five Glomus species affect water relations of Citrus tangerine during drought stress. Bot Stud 48:147–154

    Google Scholar 

  • Wu QS, Zou YN, Liu W, Ye XF, Zai HF, Zhao LJ (2010) Alleviation of salt stress in citrus seedlings inoculated with mycorrhiza: changes in leaf antioxidant defense systems. Plant Soil Environ 56:470–475

    CAS  Google Scholar 

  • Xu G, Magen H, Tarchitzky J, Kafkaki U (2000) Advances in chloride nutrition. Adv Agr 68:96–150

    Google Scholar 

  • Yang HM, Zhang JH, Zhang XY (2005) Regulation mechanisms of stomatal oscillation. J Integr Plant Biol 47:1159–1172

    Article  CAS  Google Scholar 

  • Zelenina M, Bondar AA, Zelenin S, Aperia A (2003) Nickel and extracellular acidification inhibit the water permeability of human aquaporin-3 in lung epithelial cells. J Biol Chem 278:30037–30043

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crop Res 97:111–119

    Article  Google Scholar 

  • Zhang Y, Zhu H, Zhang Q, Li M, Yan M, Wang R, Wang L, Welti R, Zhang W, Wang X (2009) Phospholipase Dα1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21:2357–2377

    Article  PubMed  CAS  Google Scholar 

  • Zuccarini P, Okurowska P (2008) Effects of mycorrhizal colonization and fertilization on growth and photosynthesis of sweet basil under salt stress. J Plant Nutr 31:497–513

    Article  CAS  Google Scholar 

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Calvo-Polanco, M., Sánchez-Romera, B., Aroca, R. (2013). Arbuscular Mycorrhizal Fungi and the Tolerance of Plants to Drought and Salinity. In: Aroca, R. (eds) Symbiotic Endophytes. Soil Biology, vol 37. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-39317-4_14

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