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Role of Arbuscular Mycorrhiza in Amelioration of Salinity

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Salt Stress in Plants

Abstract

Soil salinity is world wide problem because it negatively affect plant productivity and yield of plants particularly in arid and semi-arid regions of the world. Excessive salts decline soil water availability for plants, inhibit plants metabolism and nutrients uptake and is also responsible for osmotic imbalance. All of these changes contribute to stunted growth and less productivity of plants. Exploitation of soil microorganisms for utilizing salt affected soils is of considerable interest to plant and soil scientists. Arbuscular mycorrhizal fungi (AMF) are ubiquitous soil microorganisms inhabiting the rhizosphere and establish a symbiotic relationship with the roots of many plants. Arbuscular mycorrhizal fungi are from integral components of all natural ecosystems and are known to occur in saline soils. Symbiotic association of a plant with AMF results in higher ability for taking up the immobile nutrients in nutrient-poor soils as well as improvement of tolerance to salinity. The possible mechanisms for alleviation of salinity stress by AMF include: (1) improvement of plant nutrient uptake, particularly P, (2) elevation of K:Na ratio, (3) providing higher accumulation of osmosolutes, and (4) maintaining higher antioxidant enzymatic activities. In addition, some aquaporin genes are up-regulated in mycorrhizal plants, causing significant increase in water absorption capacity of salt-affected plants. In contrast, expression of proline biosynthetic enzymes and LEA genes as stress indicators are maintained in mycorrhizal salt stressed plants suggesting that mycorrhizal plants are less susceptible to salinity because of salinity-avoidance mechanisms.

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References

  • Abbott LK, Robson AD (1984) Colonization of the root systems of subterranean clover by three species of vesicular-arbuscular mycorrhizal fungi. New Phytol 96:275–281

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Abdel-Latef AAH, Chaoxing H (2011) Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Sci Hort 127:228–233

    Article  CAS  Google Scholar 

  • Aguilera LE, Gutierrez JR, Moreno RJ (1998) Vesicular arbuscular mycorrhizae associated with saltbushes Atriplex spp. (Chenopodiaceae) in the Chilean arid zone. Rev Chil Hist Nat 71:291–302

    Google Scholar 

  • Aguin O, Mansilla JP, Vilarino A, Sainz MJ (2004) Effects of mycorrhizal inoculation on root morphology and nursery production of three grapevine rootstocks. Am J Enol Vitic 55:108–111

    Google Scholar 

  • Aharon R, Shahak Y, Wininger S, Bendov R, Kapulnik Y, Galili G (2003) Overexpression of plasma membrane aquaporins in transgenic tobacco improves plant vigour under favourable growth conditions but not under drought or salt stress. Plant Cell 15:439–447

    Article  PubMed  CAS  Google Scholar 

  • Alguacil MM, Kohler J, Caravaca F, Roldán A (2009) Differential effects of Pseudomonas mendocina and Glomus intraradices on lettuce plants physiological response and aquaporin PIP2 gene expression under elevated atmospheric CO2 and drought. Microb Ecol 58:942–951

    Article  CAS  Google Scholar 

  • Aliasgharzadeh N, Saleh Rastin N, Towfighi H, Alizadeh A (2001) Occurrence of arbuscular mycorrhizal fungi in saline soils of the Tabriz Plain of Iran in relation to some physical and chemical properties of soil. Mycorrhiza 11:119–122

    Article  CAS  Google Scholar 

  • Alkan N, Gadkar V, Yarden O, Kapulnik Y (2006) Analysis of quantitative interactions between two species of arbuscular mycorrhizal fungi, Glomus mosseae and G. intraradices, by real-time PCR. Appl Environ Microbiol 72:4192–4199

    Article  PubMed  CAS  Google Scholar 

  • Al-Karaki GN (2000) Growth of mycorrhizal tomato and mineral acquisition under salt stress. Mycorrhiza 10:51–54

    Article  CAS  Google Scholar 

  • Al-Karaki GN, Clark RB (1998) Growth, mineral acquisition, and water use by mycorrhizal wheat grown under water stress. J Plant Nutr 21:263–276

    Article  CAS  Google Scholar 

  • Al-Karaki GN, Hammad R, Rusan M (2001) Response of two tomato cultivars differing in salt tolerance to inoculation with mycorrhizal fungi under salt stress. Mycorrhiza 11:43–47

    Article  CAS  Google Scholar 

  • Allen MF (1983) Formation of vesicular-arbuscular mycorrhizae in Atriplex gardneri (Chenopodiaceae): seasonal response in a cold desert. Mycologia 75:773–776

    Article  Google Scholar 

  • Allen EB, Cunningham GL (1983) Effects of vesicular-arbuscular mycorrhizae on Distichlis spicata under three salinity levels. New Phytol 93:227–236

    Article  Google Scholar 

  • Allen MF, Smith WK, Moore TS, Christensen M (1981) Comparative water relations and photosynthesis of mycorrhizal and non-mycorrhizal Bouteloua gracilis H.B.K. Lag ex Steud. New Phytol 88:683–693

    Article  Google Scholar 

  • Amzallag GN (1997) Tolerance to salinity in plants: new concept for old problems. In: Jaiwal PK, Singh RP, Gulati A (eds) Strategies for improving salt tolerance in higher plants. Science, Enfield, pp 1–17

    Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  PubMed  CAS  Google Scholar 

  • Apse M, Aharon G, Snedden W, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258

    Article  PubMed  CAS  Google Scholar 

  • Arines J, Quintela M, Vilarino A, Palma JM (1994) Protein patterns and superoxide dismutase activity in non-mycorrhizal and arbuscular-mycorrhizal Pisum sativum L. plants. Plant Soil 166:37–45

    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 aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytol 173:808–816

    Article  PubMed  CAS  Google Scholar 

  • Asghari HR, Cavagnaro TR (2010) Mycorrhizal response of halophytes to plant growth in non-saline soil conditions. In proceedings book of the 19th world congress of soil science, soil solutions for a changing world, 1–6 Aug 2010, Brisbane

    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 273:245–256

    Article  CAS  Google Scholar 

  • Asghari HR, Amerian M, Gorbani H (2008) Soil salinity affects arbuscular mycorrhizal colonization of halophytes. Pak J Biol Sci 11:1909–1915

    Article  PubMed  CAS  Google Scholar 

  • Augé RM (2000) Stomatal behavior of arbuscular mycorrhizal plants. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: physiology and function. Kluwer, Dordrecht, pp 201–237

    Chapter  Google Scholar 

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

    Article  Google Scholar 

  • Augé RM, Toler HD, Sams CE, Nasim G (2008) Hydraulic conductance and water potential ­gradients in squash leaves showing mycorrhiza-induced increases in stomatal conductance. Mycorrhiza 18:115–121

    Article  PubMed  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    Article  PubMed  CAS  Google Scholar 

  • Barea JM, Azcón-Aguilar C (1982) Production of plant growth-regulating substances by the vesicular-arbuscular mycorrhizal fungus Glomus mosseae. Appl Environ Microbiol 43:810–813

    PubMed  CAS  Google Scholar 

  • Barrow JR, Havstad KM, McCaslin BD (1997) Fungal root endophytes in fourwing saltbush, Atriplex canescens, on arid rangelands of southwestern USA. Arid Soil Res Rehabil 1:177–185

    Article  Google Scholar 

  • Bearden BN, Petersen L (2000) Influence of arbuscular mycorrhizal fungi on soil structure and aggregate stability of vertisols. Plant Soil 218:173–183

    Article  CAS  Google Scholar 

  • Beauchamp VB, Stromberg JC, Stutz JC (2005) Interactions between Tamarix ramosissima (saltcedar), Populus fremontii (cottonwood), and mycorrhizal fungi: effects on seedling growth and plant species coexistence. Plant Soil 275:221–231

    Article  CAS  Google Scholar 

  • Beauchamp VB, Walz C, Shafroth PB (2009) Salinity tolerance and mycorrhizal responsiveness of native xeroriparian plants in semi-arid western USA. Appl Soil Ecol 43:175–184

    Article  Google Scholar 

  • Becard G, Doner LW, Rolin DB, Douds DD, Pfeffer PE (1991) Identification and quantification of trehalose in vesicular arbuscular mycorrhizal fungi in vivo 13C NMR and HPLC analyses. New Phytol 108:547–552

    Article  Google Scholar 

  • Benavides MP, Marconi PL, Gallego SM, Comba ME, Tomaro ML (2000) Relationship between antioxidant defence systems and salt tolerance in Solanum tuberosum. Austr J Plant Physiol 27:273–278

    CAS  Google Scholar 

  • Bentivenga SP, Bever JD, Morton JB (1997) Genetic variation of morphological characters within a single isolate of the endomycorrhizal fungus Glomus clarum (Glomaceae). Am J Bot 84:1211–1216

    Article  PubMed  CAS  Google Scholar 

  • Berta G, Fusconi A, Trotta A (1993) VA mycorrhizal infection and the morphology and function of root systems. Environ Exp Bot 33:159–173

    Article  Google Scholar 

  • Bethlenfalvay GJ, Brown MS, Franson RL, Mihara KL (1989) The glycine-glomus-bradyrhizobium symbiosis. IX. Nutritional, morphological and physiological response of nodulated soybean to geographic isolates of the mycorrhizal fungus of Glomus mosseae. Physiol Plant 76:226–232

    Article  Google Scholar 

  • Bhardwaj S, Dudeja SS, Khurana AL (1997) Distribution of VAM fungi in the natural ecosystem. Fol Microbiol 42:589–594

    Article  CAS  Google Scholar 

  • Bhaskaran C, Selvaraj T (1997) Seasonal incidence and distribution of VAM fungi in native saline soils. J Environ Biol 18:209–212

    Google Scholar 

  • Biela A, Grote K, Otto B, Hoth S, Hedrich R, Kaldenho R (1999) The Nicotiana tabacum plasma membrane aquaporin NtAQP1 is mercury-insensitive and permeable for glycerol. Plant J 18:565–570

    Article  PubMed  CAS  Google Scholar 

  • Blilou I, Ocampo JA, García-Garrido JM (2000) Induction of Ltp (lipid transfer protein) and Pal (phenylalanine ammonia-lyase) gene expression in rice roots colonized by the arbuscular mycorrhizal fungus Glomus mosseae. J Exp Bot 51:1969–1977

    Article  PubMed  CAS  Google Scholar 

  • Bonfante P, Perotto S (2000) Outside and inside the roots: cell to cell interactions among arbuscular mycorrhizal fungi, bacteria and host plant. In: Podila GK, Douds DD (eds) Current advances in mycorrhizae research. The American Phytopathological Society, St. Paul, pp 141–155

    Google Scholar 

  • Borde M, Dudhane M, Jite P (2011) Growth photosynthetic activity and antioxidant responses of mycorrhizal and non-mycorrhizal bajra (Pennisetum glaucum) crop under salinity stress condition. Crop Prot 30:265–271

    Article  CAS  Google Scholar 

  • Bouchereau A, Aziz A, Larher F, Martin-Tanguy T (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125

    Article  CAS  Google Scholar 

  • Bowen G (1987) The biology and physiology of infection and its development. In: Safir GR (ed) Ecophysiology of VA mycorrhizal plants. CRC, Boca Raton, pp 27–57

    Google Scholar 

  • Brundrett M (1991) Mycorrhizas in natural ecosystems. Adv Ecol Res 21:300–313

    Google Scholar 

  • Camprubi A, Calvet C (1996) Isolation and screening of mycorrhizal fungi from citrus nurseries and orchards and inoculation studies. Hort Sci 31:363–369

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Caravaca F, Alguacil MM, Torres P, Roldán A (2005) Plant type mediates rhizospheric microbial activities and soil aggregation in a semiarid Mediterranean salt marsh. Geoderma 124:375–382

    Article  CAS  Google Scholar 

  • Carvajal M, Martínez V, Alcaraz CF (1999) Physiological function of water channels as affected by salinity in roots of paprika pepper. Physiol Plant 105:95–101

    Article  CAS  Google Scholar 

  • Carvajal M, Cerdá A, Martínez V (2000) Does calcium ameliorate the negative effect of NaCl on melon root water transport by regulating aquaporin activity? New Phytol 145:439–447

    Article  CAS  Google Scholar 

  • Carvalho LM, Cacador I, Martins-Loucão MA (2001) Temporal and spatial variation of arbuscular mycorrhizas in salt marsh plants of the Tagus estuary (Portugal). Mycorrhiza 11:303–309

    Article  Google Scholar 

  • Carvalho LM, Correia PM, Martins-Loucão MA (2004) Arbuscular mycorrhizal fungal propagules in a salt marsh. Mycorrhiza 14:165–170

    Article  PubMed  Google Scholar 

  • Chattopadhyay MK, Tiwari BS, Chattopadhyay G, Bose A, Sengupta DN, Ghosh B (2002) Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. Physiol Plant 116:192–199

    Article  PubMed  Google Scholar 

  • Chaves M, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560

    Article  PubMed  CAS  Google Scholar 

  • Chen G-P, Wilson ID, Kim SH, Grierson D (2001) Inhibiting expression of a tomato ripening-associated membrane protein increases organic acids and reduces sugar levels of fruit. Planta 212:799–807

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Jagendorf A, Zhu JK (2005) Understanding and improving salt tolerance in plants. Crop Sci 45:437–448

    Article  CAS  Google Scholar 

  • Chulan HA, Martin K (1992) The vesicular-arbuscular (VA) mycorrhiza and its effects on growth of vegetatively propagated Theobroma cacao L. Plant Soil 144:227–233

    Article  Google Scholar 

  • Clapp JP, Young JPW, Merryweather JW, Fitter AH (1995) Diversity of fungal symbionts in arbuscular mycorrhizas from a natural community. New Phytol 130:259–265

    Article  PubMed  CAS  Google Scholar 

  • Colla G, Rouphael Y, Cardarelli M, Tullio M, Rivera CM, Rea E (2008) Alleviation of salt stress by arbuscular mycorrhizal in zucchini plants grown at low and high phosphorus concentration. Biol Fert Soils 44:501–509

    Article  CAS  Google Scholar 

  • Cook JC, Butler RH, Madol T (1993) Some observations on the vertical distribution of VAM in roots of salt marsh grasses growing in saturated soils. Mycologia 85:547–550

    Article  Google Scholar 

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

    Google Scholar 

  • Cramer G (2004) Sodium–calcium interactions under salinity stress. In: Läuchli A, Lüttge S (eds) Salinity: environment–plants–molecules. Springer, Netherlands, pp 205–227

    Chapter  Google Scholar 

  • Daei G, Ardekani MR, 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

    Article  PubMed  CAS  Google Scholar 

  • Daniels BA, Graham SO (1976) Effects of nutrition and soil extracts on germination of Glomus mosseae spores. Mycologia 68:108–116

    Article  Google Scholar 

  • Daniels BA, Trappe JM (1980) Factors affecting spore germination of the vesicular-arbuscular mycorrhizal fungus Glomus epigaeus. Mycologia 72:457–471

    Article  CAS  Google Scholar 

  • Davies HA, Dow JM (1997) Induction of extracellular matrix glycoproteins in Brassica petioles bywounding and in response to Xanthomonas campestris. Mol Plant-Microb Interact 10:812–820

    Article  CAS  Google Scholar 

  • Davies WJ, Zhang J (1991) Root signals and the regulation of growth and development of plants in drying soil. Annu Rev Plant Physiol 42:55–73

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Dixon RK, Garg VK, Rao MV (1993) Inoculation of Leucaena and Prosopis seedlings with Glomus and Rhizobium species in saline soil: rhizosphere relations and seedling growth. Arid Soil Res Rehabil 7:133–144

    Google Scholar 

  • Dodd JC, Thomson BD (1994) The screening and selection of inoculant arbuscular-mycorrhizal and ectomycorrhizal fungi. Plant Soil 159:149–158

    Google Scholar 

  • Douds DD Jr, Millner PD (1999) Biodiversity of arbuscular mycorrhizal fungi in agroecosystems. Agric Ecosyst Environ 74:183–193

    Article  Google Scholar 

  • Duke ER, Johnson CR, Koch KE (1986) Accumulation of phosphorus, dry matter and betaine during NaC1 stress of split-root citrus seedlings colonized with vesicular-arbuscular mycorrhizal fungi on zero, one or two halves. New Phytol 104:583–590

    Article  CAS  Google Scholar 

  • Estaun MV (1989) Effect of sodium chloride and mannitol on germination and hyphal growth of the vesicular-arbuscular mycorrhizal fungus Glomus mosseae. Agric Ecosyst Environ 29:123–129

    Article  Google Scholar 

  • Estaun MV (1991) Effect of NaC1 and mannitol on the germination of two isolates of the vesicular-arbuscular mycorrhizal fungus Glomus mosseae. In: Proceedings book of 3rd European symposium on mycorrhizas. University of Sheffield, Sheffield

    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 

  • Ezawa T, Smith SE, Smith FA (2002) P metabolism and transport in AM fungi. Plant Soil 244:221–230

    Article  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 

  • Fornalé S, Sarjala T, Bagni N (1999) Endogenous polyamine content and metabolism in the ectomycorrhizal fungus Paxillus involutus. New Phytol 143:581–587

    Article  Google Scholar 

  • Francoise F, Daniel LR, John G (1991) Effects of salt stress on amino acid, organic acid and carbohydrate composition of root, bacteroids, and cytosol of alfalfa (Medicago sativa L.). Plant Physiol 96:1228–1236

    Article  Google Scholar 

  • Fukuda A, Nakamura A, Tanaka Y (1999) Molecular cloning and expression of the Na+/H+ exchanger gene in Oryza sativa. Biochim Biophys Acta 1446:149–155

    Article  PubMed  CAS  Google Scholar 

  • Füzy A, Biró B, Tóth T, Hildebrandt U, Bothe H (2008) Drought, but not salinity, determines the apparent effectiveness of halophytes colonized by arbuscular mycorrhizal fungi. J Plant Physiol 165:1181–1192

    Article  PubMed  CAS  Google Scholar 

  • Gadkar V, Rillig M (2006) The arbuscular mycorrhizal fungal protein glomalin is a putative homolog of heat shock protein 60. FEMS Microbiol Lett 263:93–101

    Article  PubMed  CAS  Google Scholar 

  • Garg N, Chandel S (2011) The effects of salinity on nitrogen fixation and trehalose metabolism in mycorrhizal Cajanus cajan (L.) Millsp. plants. J Plant Growth Regul 30:490–503

    Article  CAS  Google Scholar 

  • Garratt LC, Janagoudar BS, Lowe KC (2002) Salinity tolerance and antioxidant status in cotton culture. Free Radic Biol Med 33:502–511

    Article  PubMed  CAS  Google Scholar 

  • Gaxiola RA, Rao R, Sherman A, Grisafi P, Alper SL, Fink GR (1999) The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proc Natl Acad Sci USA 96:1480–1485

    Article  PubMed  CAS  Google Scholar 

  • Ghachtouli NE, Paynot M, Morandi D, Martintanguy J, Gianinazzi S (1995) The effect of polyamines on endomycorrhizal infection of wild-type Pisum sativum, cv. Frisson (nod  +  myc+) and 2 mutants (nod– myc  +  and nod–myc–). Mycorrhiza 5:189–192

    CAS  Google Scholar 

  • Gianinazzi-Pearson V (1996) Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis. Plant Cell 8:1871–1883

    PubMed  Google Scholar 

  • Giri M, 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 (2003) Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass, and mineral nutrition of Acacia auriculiformis. Biol Fertil Soil 38:170–175

    Article  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. Microbiol Ecol 54:753–760

    Article  CAS  Google Scholar 

  • Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45

    Article  PubMed  CAS  Google Scholar 

  • Guo LQ, Shi DC, Wang DL (2010) The key physiological response to alkali stress by the alkali-resistant halophyte Puccinellia tenuiflora is the accumulation of large quantities of organic acids and into the rhizosphere. J Agron Crop Sci 196:123–135

    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 

  • Hajlaoui H, Ayeb NE, Garrec JP, Denden M (2010) Differential effects of salt stress on osmotic adjustment and solutes allocation on the basis of root and leaf tissue senescence of two silage maize (Zea mays L.) varieties. Ind Crops Prod 31:122–130

    Article  CAS  Google Scholar 

  • Hammer EC, Rillig MC (2011) The influence of different stresses on glomalin levels in an arbuscular mycorrhizal fungus-salinity increases glomalin content. PLoS One 6(12):e28426

    Article  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 

  • Harinasut P, Poonsopa D, Roengmongkol K, Charoensataporn R (2003) Salinity effects on antioxidant enzymes in mulberry cultivar. Sci Asia 29:109–113

    Article  CAS  Google Scholar 

  • Harley JL, Harley EL (1987) A check-list of mycorrhiza in the British flora. New Phytol 10:1–102

    Article  Google Scholar 

  • Hartmond U, Schaesberg NV, Graham JH, Syvertsen JP (1987) Salinity and flooding stress effects on mycorrhizal and nonmycorrhizal citrus rootstock seedlings. Plant Soil 104:37–43

    Article  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  PubMed  CAS  Google Scholar 

  • Hatzig S, Kumar A, Neubert A, Schubert S (2010) PEP-carboxylase activity: a comparison of its role in a C4 and a C3 species under salt stress. J Agron Crop Sci 196:185–192

    Article  CAS  Google Scholar 

  • He XL, Mouratov S, Steinberger Y (2002) Spatial distribution and colonization of arbuscular mycorrhizal fungi under the canopies of desert halophytes. Arid Land Res Manag 16:149–160

    Article  Google Scholar 

  • He ZQ, He CX, Zhang ZB, Zou ZR, Wang HS (2007) Changes of antioxidative enzymes and cell membrane osmosis in tomato colonized by arbuscular mycorrhizae under NaCl stress. Colloids Surf B Biointerfaces 59:128–133

    Article  PubMed  CAS  Google Scholar 

  • Hepper CM (1979) Germination and growth of Glomus caledonius spores: the effects of inhibitors and nutrients. Soil Biol Biochem 11:269–277

    Article  CAS  Google Scholar 

  • Hetrick BAD, Bockus WW, Bloom J (1984) The role of vesicular-arbuscular mycorrhizal fungi in the growth of Kansas winter wheat. Can J Bot 62:735–740

    Article  Google Scholar 

  • Hildebrandt U, Janetta K, Ouziad F, Renne B, Nawrath K, Bothe H (2001) Arbuscular mycorrhizal colonization of halophytes in Central European salt marshes. Mycorrhiza 10:175–183

    Article  CAS  Google Scholar 

  • Hill AE, Shachar-Hill B, Shachar-Hill Y (2004) What are aquaporins for? J Membr Biol 197:1–32

    Article  PubMed  CAS  Google Scholar 

  • Hirrel MC (1981) The effect of sodium and chloride salts on the germination of Gigaspora margarita. Mycologia 73:610–617

    Article  CAS  Google Scholar 

  • Hirrel MC, Gerdemann JW (1980) Improved growth of onion and bell pepper in saline soils by two vesicular–arbuscular mycorrhizal fungi. Soil Sci Soc Am J 44:654–655

    Article  CAS  Google Scholar 

  • Hirrel MC, Mehravaran H, Gerdemann JW (1978) Vesiculararbuscular mycorrhiza in the Chenopodiaceae and Cruciferae: do they occur? Can J Bot 56:2813–2817

    Article  Google Scholar 

  • Ho I (1987) Vesicular-arbuscular mycorrhizae of halophytic grasses in the Alvard desert of Oregon. Northwest Sci 61:148–151

    Google Scholar 

  • Hoefnagels MH, Broome SW, Shafer SR (1993) Vesicular-arbuscular mycorrhizae in salt marshes in North Carolina. Estuaries 16:851–858

    Article  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. Microbial Ecol 55:45–53

    Article  Google Scholar 

  • Jakobsen I, Abbott LK, Robson AD (1992) External hyphae of vesicular-mycorrhizal fungi associated with Trifolium subterraneum L. New Phytol 120:371–380

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Janos DP (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17:75–91

    Article  PubMed  Google Scholar 

  • Javot H, Lauvergeat V, Santoni V, Martin-Laurent F, Guclu J, Vinh J, Heyes J, Franck KI, Schaffner AR, Bouchez D, Maurel C (2003) Role of a single aquaporin isoform in root water uptake. Plant Cell 15:509–522

    Article  PubMed  CAS  Google Scholar 

  • Johansson I, Larsson C, Ek B, Kjellbom P (1996) The major integral proteins of spinach leaf plasma membranes are putative aquaporins and are phosphorylated in response to Ca2+ and apoplastic water potential. Plant Cell 8:1181–1191

    PubMed  CAS  Google Scholar 

  • Johansson I, Karlsson M, Johanson U, Larsson C, Kjellbom P (2000) The role of aquaporins in cellular and whole plant water balance. Biochim Biophys Acta 1465:324–342

    Article  PubMed  CAS  Google Scholar 

  • Johnson WC (1992) Dams and riparian forests: case study from the upper Missouri River. Rivers 3:229–242

    Google Scholar 

  • Johnson GPC, Kenkel NC, Booth T (1995) The distribution and phenology of arbuscular mycorrhizae along an inland salinity gradient. Can J Bot 73:1318–1327

    Article  Google Scholar 

  • Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytol 135:574–586

    Article  Google Scholar 

  • Juniper S, Abbott LK (1993) Vesicular-arbuscular mycorrhizas and soil salinity. Mycorrhiza 4:45–57

    Article  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 

  • Kapoor R, Sharma D, Bhatnagar AK (2008) Arbuscular mycorrhizae in micropropagation systems and their potential applications. Sci Hort 116:227–239

    Article  Google Scholar 

  • Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45:712–722

    Article  PubMed  CAS  Google Scholar 

  • Kaya C, Ashraf M, Sonmez O, Aydemir S, Tuna LA, Cullu AM (2009) The influence of arbuscular mycorrhizal colonization on key growth parameters and fruit yield of pepper plants grown at high salinity. Sci Hort 12:1–6

    Article  CAS  Google Scholar 

  • Khaled LB, Gõmez 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

    Article  CAS  Google Scholar 

  • Khalil HA, Eissa AM, El-Shazly SM, Aboul-Nasr AM (2011) Improved growth of salinity-stressed citrus after inoculation with mycorrhizal fungi. Sci Hort 130:624–632

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kim CK, Weber DJ (1985) Distribution of VA mycorrhiza on halophytes on inland salt playas. Plant Soil 83:207–214

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Kohler J, Hernández JA, Caravaca F, Roldán A (2009) Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environ Exp Bot 65:245–252

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Koide RT (2000) Functional complementarity in the arbuscular mycorrhizal symbiosis. New Phytol 147:233–235

    Article  Google Scholar 

  • Krajinski F, Biela A, Schubert D, Gianinazzi-Pearson V, Kaldenhoff R, Franken P (2000) Arbuscular mycorrhiza development regulates the mRNA abundance of Mtaqp1 encoding a mercury-insensitive aquaporin of Medicago truncatula. Planta 211:85–90

    Article  PubMed  CAS  Google Scholar 

  • Lambais MR, Ríos-Ruiz WF, Andrade RM (2003) Antioxidant responses in bean (Phaseolus vulgaris) roots colonized by arbuscular mycorrhizal fungi. New Phytol 160:421–428

    Article  CAS  Google Scholar 

  • Landwehr M, Hildebrandt U, Wilde P, Nawrath K, Tóth T, Biró B, Bothe H (2002) The arbuscular mycorrhizal fungus Glomus geosporum in European saline, sodic and gypsum soils. Mycorrhiza 12:199–211

    Article  PubMed  CAS  Google Scholar 

  • Lerat S, Lapointe L, Gutjahr S, Piché Y, Vierheilig H (2003) Carbon partitioning in a split-root system of arbuscular mycorrhizal plants is fungal and plant species dependent. New Phytol 157:589–595

    Article  Google Scholar 

  • Locatelli LM, Vitovski CA, Lovato PE (2002) Root architecture of apple rootstocks inoculated with arbuscular mycorrhizal fungi. Pesq Agropec Bras 37:1239–1245

    Article  Google Scholar 

  • López-Bucio J, Nieto-Jacobo MF, Ramírez-Rodríguez V, Herrera-Estrella L (2000) Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. Plant Sci 160:1–13

    Article  PubMed  Google Scholar 

  • Luu DT, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 28:85–96

    Article  CAS  Google Scholar 

  • Mamatha G, Bagyaraj DJ, Jaganath S (2002) Inoculation of field-established mulberry and papaya with arbuscular mycorrhizal fungi and a mycorrhiza helper bacterium. Mycorrhiza 12:313–316

    Article  PubMed  CAS  Google Scholar 

  • Mardukhi B, Rejali F, Daei G, Ardakani MR, Malakouti MJ, 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

    Article  CAS  Google Scholar 

  • Marschner P (2012) Rhizosphere biology. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants, 3rd edn. Academic Press, USA, pp 369–388

    Chapter  Google Scholar 

  • Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102

    CAS  Google Scholar 

  • Martinčič A, Wraber T, Jogan N, Podobnik A, Turk B, Vreš B, Ravnik V, Frajman B, Strgulc-Krajšek S, Trčak B, Bačič T, Fischer MA, Eler K, Surina B (2007) Mala Flora Slovenije: Ključ Za Določanje Praprotnic in Semenk. Tehniška založba Slovenije, Ljubljana

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Mathur N, Singh J, Bohra S, Vyas A (2007) Arbuscular mycorrhizal status of medicinal halophytes in saline areas of Indian Thar desert. Int J Soil Sci 2:119–127

    Article  Google Scholar 

  • Maurel C, Kado RT, Guern J, Chrispeels MJ (1995) Phosphorylation regulates the water channel activity of the seed-specific aquaporin alpha-TIP. EMBO J 14:3028–3035

    PubMed  CAS  Google Scholar 

  • Maurel C, Chrispeels M, Lurin C, Tacnet F, Geelen D, Ripoche P, Guern J (1997) Function and regulation of seed aquaporins. J Exp Bot 48:421–430

    Article  PubMed  CAS  Google Scholar 

  • McMillen BG, Juniper S, Abbott LK (1998) Inhibition of hyphal growth of a VA mycorrhizal fungus in soil containing sodium chloride limits the spread of infection from spores. Soil Biol Biochem 30:1639–1646

    Article  CAS  Google Scholar 

  • Mehdy MC, Sharma YK, Sathasivan K, Bays NW (1996) The role of activated oxygen species in plant disease resistance. Physiol Plant 98:365–374

    Article  CAS  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, Dordrecht, pp 3–18

    Chapter  Google Scholar 

  • Miranda D, Fischer G, Ulrichs C (2011) The influence of arbuscular mycorrhizal colonization on the growth parameters of cape gooseberry (Physalis peruviana L.) plants grown in a saline soil. J Soil Sci Plant Nutr 1:18–30

    Article  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 

  • Miransari M (2011) Arbuscular mycorrhizal fungi and nitrogen uptake. Arch Microbiol 193:77–81

    Article  PubMed  CAS  Google Scholar 

  • Miransari M, Smith DL (2007) Overcoming the stressful effects of salinity and acidity on soybean [Glycine max (L.) Merr.] nodulation and yields using signal molecule genistein under field conditions. J Plant Nutr 30:1967–1992

    Article  CAS  Google Scholar 

  • Miransari M, Smith DL (2008) Using signal molecule genistein to alleviate the stress of suboptimal root zone temperature on soybean-Bradyrhizobium symbiosis under different soil textures. J Plant Interact 3:287–295

    Article  Google Scholar 

  • Miransari M, Bahrami HA, Rejali F, Malakouti MJ, Torabi H (2007) Using arbuscular mycorrhiza to reduce the stressful effects of soil compaction on corn (Zea mays L.) growth. Soil Biol Biochem 39:2014–2026

    Article  CAS  Google Scholar 

  • Miransari M, Bahrami HA, Rejali F, Malakouti MJ (2008) Using arbuscular mycorrhiza to reduce the stressful effects of soil compaction on wheat (Triticum aestivum L.) growth. Soil Biol Biochem 40:1197–1206

    Article  CAS  Google Scholar 

  • Mittova V, Tal M, Volokita M, Guy M (2002) Salt stress induces up-regulation of an efficient chloroplast antioxidant system in the salt-tolerant wild tomato species Lycopersicon pennellii but not in the cultivated species. Physiol Plant 115:393–400

    Article  PubMed  CAS  Google Scholar 

  • Mosse B, Hepper C (1975) Vesicular-arbuscular mycorrhizal infections in root organ cultures. Physiol Plant Pathol 5:215–223

    Article  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681

    Article  CAS  Google Scholar 

  • Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043

    Article  PubMed  CAS  Google Scholar 

  • Murkute AA, Sharma S, Singh SK (2006) Studies on salt stress tolerance of citrus rootstock genotypes with arbuscular mycorrhizal fungi. Hort Sci 33:70–76

    Google Scholar 

  • Nemec S (1981) Histochemical characterization of Glomus etunicatum infection of Citrus limon roots. Can J Bot 59:609–617

    Article  Google Scholar 

  • Neto ADA, Prisco JT, Gomes-Filho E (2009) Changes in soluble amino-N, soluble proteins and free amino acids in leaves and roots of salt-stressed maize genotypes. J Plant Interact 4:137–144

    Article  CAS  Google Scholar 

  • Niki T, Mitsuhara I, Ohtsubo S, Ohashi Y (1998) Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiol 39:500–507

    Article  CAS  Google Scholar 

  • O’Connor PJ, Smith SE, Smith FA (2001) Arbuscular mycorrhizal associations in the southern Simpson desert. Aust J Bot 49:493–499

    Article  Google Scholar 

  • Ocón A, Hampp R, Requena N (2007) Trehalose turnover during abiotic stress in arbuscular mycorrhizal fungi. New Phytol 174:879–891

    Article  PubMed  CAS  Google Scholar 

  • Ojala JC, Jarrell WM, Menge JA, Johnson ELV (1983) Influence of mycorrhizal fungi on the mineral nutrition and yield of onion in saline soil. Agron J 75:255–259

    Article  CAS  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 

  • Pacovsky RS, De Silva P, Carvalho MTV, Tsai SM (1991) Growth and nutrient allocation in Phaseolus vulgaris L. colonized with endomycorrhizae or Rhizobium. Plant Soil 132:127–137

    Article  CAS  Google Scholar 

  • Palma JM, Longa MA, del Rio LA, Arines J (1993) Superoxide dismutase in vesicular-arbuscular red clover plants. Physiol Plant 87:77–83

    Article  CAS  Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349

    Article  PubMed  CAS  Google Scholar 

  • Paul MJ, Primavesi LF, Jhurreea D, Zhang Y (2008) Trehalose metabolism and signaling. Annu Rev Plant Biol 59:417–441

    Article  PubMed  CAS  Google Scholar 

  • Peng J, Li Y, Shi P, Chen X, Lin H, Zhao B (2011) The differential behavior of arbuscular mycorrhizal fungi in interaction with Astragalus sinicus L. under salt stress. Mycorrhiza 21:27–33

    Article  PubMed  CAS  Google Scholar 

  • Pfeiffer CM, Bloss HE (1988) Growth and nutrition of guayule (Parthenium argentatum) in a saline soil as influenced by vesicular- arbuscular mycorrhiza and phosphorus fertilization. New Phytol 108:315–321

    Article  Google Scholar 

  • Pitman M, Läuchli A (2004) Global impact of salinity and agricultural ecosystems. In: Läuchli A, Lüttge S (eds) Salinity: environment–plants–molecules. Springer, Dordrecht, pp 3–20

    Chapter  Google Scholar 

  • Plenchette C, Duponnois R (2005) Growth response of the saltbush Atriplex nummularia L. to inoculation with the arbuscular mycorrhizal fungus Glomus intraradices. J Arid Environ 61:535–540

    Article  Google Scholar 

  • Pond EC, Menge JA, Jarrell WM (1984) Improved growth of tomato in salinized soil by vesicular-arbuscular mycorrhizal fungi collected from saline soils. Mycologia 76:74–84

    Article  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, Gómez M, Kaldenhoff R, Ruiz-Lozano JM (2005) Impairment of NtAQP1 gene expression in tobacco plants does not affect root colonisation pattern by arbuscular mycorrhizal fungi but decreases their symbiotic efficiency under drought. Mycorrhiza 15:417–423

    Article  PubMed  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 60:389–404

    Article  PubMed  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-Martín 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 166:1350–1359

    Article  PubMed  CAS  Google Scholar 

  • Poss JA, Pond E, Menge JA, Harrell WM (1985) Effect of salinity on mycorrhizal onion and tomato in soil with and without additional phosphate. Plant Soil 88:307–319

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Rabie GH (2005) Influence of arbuscular mycorrhizal fungi and kinetin on the response of mungbean plants to irrigation with seawater. Mycorrhiza 15:225–230

    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 

  • Rao DLN (1998) Biological amelioration of salt affected soils. In: Microbial interactions in agriculture and forestry, 1st edn. Science, Enfield, pp 21–238

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Reeves FB, Wagner D, Moorman T, Kiel J (1979) The role of endomycorrhizae in revegetation practices in the semi-arid west. I. A comparison of incidence of mycorrhizae in severely disturbed vs. natural environments. Am J Bot 66:6–13

    Article  Google Scholar 

  • Rhodes D, Nadolska-Orczyk A, Rich PJ (2004) Salinity, osmolytes and compatible solutes. In: Läuchli A, Lüttge S (eds) Salinity: environment–plants–molecules. Springer, Dordrecht, pp 181–204

    Chapter  Google Scholar 

  • Rillig MC (2004) Arbuscular mycorrhizae, glomalin, and soil aggregation. Can J Soil Sci 84:355–363

    Article  Google Scholar 

  • Rovira AD (1969) Plant root exudates. Bot Rev 35:35–57

    Article  CAS  Google Scholar 

  • Rozema J, Arp W, Van Diggelen J, Van Esbroek M, Broekma R, Punt H (1986) Occurrence and ecological significance of vesicular-arbuscular mycorrhiza in the salt marsh environment. Acta Bot Neerl 35:457–467

    Google Scholar 

  • Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress new perspectives for molecular studies. Mycorrhiza 13:309–317

    Article  PubMed  Google Scholar 

  • Ruiz-Lozano JM, Aroca R (2010) Modulation of aquaporin genes by the arbuscular mycorrhizal symbiosis in relation to osmotic stress tolerance. In: Seckbach J, Grube M (eds) Symbioses and stress, vol 17, Cellular origin, life in extreme habitats and astrobiology. Springer, Berlin, pp 357–374

    Chapter  Google Scholar 

  • Ruiz-Lozano JM, Azcón R (2000) Symbiotic efficiency and infectivity of an autochthonous arbuscular mycorrhizal Glomus sp. from saline soils and Glomus deserticola under salinity. Mycorrhiza 10:137–143

    Article  CAS  Google Scholar 

  • Ruiz-Lozano JM, Azcón R, Goméz M (1996) Alleviation of salt stress by arbuscular-mycorrhizal Glomus species in Lactuca sativa plants. Physiol Plant 98:767–772

    Article  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(11):4033–4044

    Article  PubMed  CAS  Google Scholar 

  • Rush DW, Epstein E (1976) Genotypic responses to salinity: differences between salt-sensitive and salt-tolerant genotypes of tomato. Plant Physiol 57:162–166

    Article  PubMed  CAS  Google Scholar 

  • Sannazzaro AI, Alvarez CL, Menéndez AB, Pieckenstain FL, Albertó EO, Ruiz OA (2004) Ornithine and arginine decarboxilase activities and effect of some polyamine biosynthesis inhibitors on Gigaspora rosea germinating spores. FEMS Microbiol Lett 230:115–121

    Article  PubMed  CAS  Google Scholar 

  • Sannazzaro AI, Ruíz OA, Alberto EO, Menendez AB (2006) Alleviation of salt stress in Lotus glaber by Glomus intraradices. Plant Soil 285:279–287

    Article  CAS  Google Scholar 

  • Sannazzaro AI, Echeverría M, Albertó EO, Ruiz OA, Menéndez AB (2007) Modulation of polyamine balance in Lotus glaber by salinity and arbuscular mycorrhiza. Plant Physiol Biochem 45:39–46

    Article  PubMed  CAS  Google Scholar 

  • Sarda X, Tousch D, Ferrare K, Cellier F, Alcon C, Dupuis JM, Casse F, Lamaze T (1999) Characterization of closely related delta- TIP genes encoding aquaporins which are differentially expressed in sunflower upon water deprivation through exposure to air. Plant Mol Biol 40:179–191

    Article  PubMed  CAS  Google Scholar 

  • Sawers RJ, Gutjahr C, Paszkowski U (2008) Cereal mycorrhiza: an ancient symbiosis in modern agriculture. Trends Plant Sci 13:93–97

    Article  PubMed  CAS  Google Scholar 

  • Scheublin TR, Ridgway KP, Young PW, van der Heijden MGA (2004) Non legumes, legumes, and root nodules harbor different arbuscular mycorrhizal fungal communities. Appl Environ Microbiol 70:6240–6246

    Article  PubMed  CAS  Google Scholar 

  • Schroeder MS, Janos DP (2005) Plant growth, phosphorus nutrition, and root morphological responses to arbuscular mycorrhizas, phosphorus fertilization, and intraspecific density. Mycorrhiza 15:203–216

    Article  PubMed  CAS  Google Scholar 

  • Schubert A, Wyss P, Wiekman A (1992) Occurrence of trehalose in vesicular-arbuscular mycorrhizal fungi and in mycorrhizal roots. J Plant Physiol 140:41–45

    Article  CAS  Google Scholar 

  • Sengupta A, Chaudhuri S (1990) Vesicular-arbuscular mycorrhiza in pioneer salt marsh plants of the Ganges river delta in West Bengal (India). Plant Soil 122:111–113

    Article  Google Scholar 

  • Shalata A, Tal M (1998) The effect of salt stress on lipid peroxidation and antioxidants in the leaf of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii. Physiol Plant 104:169–174

    Article  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 

  • 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 

  • Shi H, Ishitani M, Kim C, Zhu J-K (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97:6896–6901

    Article  PubMed  CAS  Google Scholar 

  • Shi ZY, Zhang L, Feng G, Christie P, Tian CY, Li XL (2006) Diversity of arbuscular mycorrhizal fungi associated with desert ephemerals growing under and beyond the canopies of Tamarisk shrubs. Chinese Sci Bull 51:132–139

    Article  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 

  • Smart LB, Moskal WA, Cameron KD, Bennett AB (2001) MIP genes are down-regulated under drought stress in Nicotiana glauca. Plant Cell Physiol 42:686–693

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Smith FA, Smith SE (1997) Structural diversity in (vesicular)-arbuscular mycorrhizal symbioses. New Phytol 137:373–388

    Article  Google Scholar 

  • Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20

    Article  PubMed  CAS  Google Scholar 

  • Sonjak S, Udovič M, Wraber T, Likar M, Regvar M (2009) Diversity of halophytes and identification of arbuscular mycorrhizal fungi colonising their roots in an abandoned and sustained part of Sečovlje salterns. Soil Biol Biochem 41:1847–1856

    Article  CAS  Google Scholar 

  • Sottosanto JB, Gell A, Blumwald E (2004) DNA array analyses of Arabidopsis thaliana lacking a vacuolar Na+/H+ antiporter: impact of AtNHX1 on gene expression. Plant J 40:752–771

    Article  PubMed  CAS  Google Scholar 

  • Spanu P, Bonfante-Fasolo P (1988) Cell-wall-bound peroxidase activity in roots of mycorrhizal Allium porrum. New Phytol 109:119–124

    Article  CAS  Google Scholar 

  • Sreenivasulu N, Ramanjulu S, Ramachandra-Kini K, Prakash HS, Shekar-Shetty H, Savithri HS, Sudhakar C (1999) Total peroxidase activity and peroxidase isoforms as modified by salt stress in two cultivars of fox-tail millet with differential salt tolerance. Plant Sci 141:1–9

    Article  CAS  Google Scholar 

  • Strack D, Fester T, Hause B, Schliemann W, Walter MH (2003) Arbuscular mycorrhiza: biological, chemical, and molecular aspects. J Chem Ecol 29:1955–1979

    Article  PubMed  CAS  Google Scholar 

  • Sylvia DM, Fuhrmann JJ, Hartel PG, Zuberer D (1998) Principles and applications of soil microbiology. Prentice, Upper Saddle River

    Google Scholar 

  • Szalai G, Janda T (2009) Effect of salt stress on the salicylic acid synthesis in young maize (Zea mays L.) plants. J Agric Crop Sci 195:165–171

    Article  CAS  Google Scholar 

  • Tal M, Katz A, Heikin H, Dehan K (1979) Salt tolerance in the wild relatives of the cultivated tomato: proline accumulation in Lycopersicon esculentum Mill., L., Peruvianum Mill. and Solanum pennelli Cor. Treated with NaCl and polyethylene glycol. New Phytol 82:349–355

    Article  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 

  • Tian CY, Feng G, Li XL, Zhang FS (2004) Different effects of arbuscular mycorrhizal fungal isolates from saline or non-saline soil on salinity tolerance of plants. Appl Soil Ecol 26:143–148

    Article  Google Scholar 

  • Titus JH, Titus PJ, Nowak RS, Smith SD (2002) Arbuscular mycorrhizae of Mojave desert plants. West North Am Naturalist 62:327–334

    Google Scholar 

  • Tommerup IC (1984) Effect of soil water potential on spore germination by vesicular-arbuscular fungi. Trans Br Mycol Soc 83:193–202

    Article  Google Scholar 

  • Tonin C, Vandenkoornhuyse P, Joner E, Straczek J, Leyval C (2001) Diversity of AM fungi in the rhizosphere of Viola calaminaria and effect of these fungi on heavy metal uptake by clover. Mycorrhiza 10:161–168

    Article  CAS  Google Scholar 

  • Tressner HD, Hayes JA (1971) Sodium chloride tolerance of terrestrial fungi. Appl Microbiol 22:210–213

    Google Scholar 

  • Usha K, Saxena A, Singh B (2004) Rhizosphere dynamics influenced by arbuscular mycorrhizal fungus (Glomus deserticola) and related changes in leaf nutrient status and yield of Kinnow mandarin [King (Citrus nobilis)  ×  Willow Leaf (Citrus deliciosa)]. Aust J Agric Res 55:571–576

    Article  Google Scholar 

  • van der Heijden MGA, Boller T, Wiemken A, Sanders IR (1998a) Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79:2082–2091

    Article  Google Scholar 

  • van Der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998b) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72

    Article  CAS  Google Scholar 

  • Vogel-Mikuš K, Drobne D, Regvar M (2005) Zn, Cd and Pb accumulation and arbuscular mycorrhizal colonization of pennycress Thlaspi praecox Wulf Brassicaceae from the vicinity of a lead mine and smelter in Slovenia. Environ Pollut 133:232–242

    Google Scholar 

  • Wang B, Qiu Y-L (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363

    Article  PubMed  CAS  Google Scholar 

  • Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

    Article  PubMed  CAS  Google Scholar 

  • Wang F, Zeng B, Sun ZX, Zhu C (2009) Relationship between proline and Hg2+-induced oxidative stress in a tolerant rice mutant. Arch Environ Contam Toxicol 56:723–731

    Article  PubMed  CAS  Google Scholar 

  • Watad AEA, Reinhold L, Lerner HR (1983) Comparison between a stable NaCl-selected Nicotiana cell line and the wild type: K+, Na+, and proline pools as a function of salinity. Plant Physiol 73:624–629

    Article  PubMed  CAS  Google Scholar 

  • Weig A, Deswarte C, Chrispeels MJ (1997) The major intrinsic protein family of Arabidopsis has 23 members that form three distinct groups with functional aquaporins in each group. Plant Physiol 114:1347–1357

    Article  PubMed  CAS  Google Scholar 

  • Williams SE, Wollum AG II, Aldon FE (1974) Growth of Atriplex canescens (Pursh.) Nutt. improved by formation of vesicular-arbuscular mycorrhizae. Proc Soil Sci Soc Am 38:962–965

    Article  Google Scholar 

  • Wilson JM (1984) Comparative development of infection by three vesicular-arbuscular mycorrhizal fungi. New Phytol 97:413–426

    Article  Google Scholar 

  • Wilson GWT, Hartnett DC (1998) Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie. Am J Bot 85:1732–1738

    Article  PubMed  CAS  Google Scholar 

  • Wright DP, Read DJ, Scholes JD (1998) Mycorrhizal sink strength influences whole-plant carbon balance of Trifolium repens L. Plant Cell Environ 21:881–891

    Article  Google Scholar 

  • Wu QS, Xia RX, Zou YN, Wang GY (2007) Osmotic solute responses of mycorrhizal citrus (Poncirus trifoliata) seedlings to drought stress. Acta Physiol Plant 29:543–549

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Xia T, Apse MP, Aharon GS, Blumwald E (2002) Identification and characterization of a NaCl-inducible vacuolar Na+/H+antiporter in Beta vulgaris. Physiol Plant 116:206–212

    Article  PubMed  CAS  Google Scholar 

  • Yamada S, Katsuhara M, Kelly WB, Michalowski CB, Bohnert HJ (1995) A family of transcripts enpoding water channel proteins: tissue-specific expression in the common ice plant. Plant Cell 7:1129–1142

    PubMed  CAS  Google Scholar 

  • Yamada S, Komori T, Myers PN, Kuwata S, Kubo T, Imaseki H (1997) Expression of plasma membrane water channel genes under water stress in Nicotiana excelsior. Plant Cell Physiol 38:1226–1231

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Yano-Melo AM, Saggin OJ, Maia LC (2003) Tolerance of mycorrhized banana (Musa sp. cv. Pacovan) plantlets to saline stress. Agric Ecosyst Environ 95:343–348

    Article  Google Scholar 

  • Zai XM, Qin P, Wan SW, Zhao FG, Wang G, Yan DL, Zhou J (2007) Effects of arbuscular mycorrhizal fungi on the rooting and growth of beach plum (Prunus maritima) cuttings. J Hortic Sci Biotechnol 82:863–866

    CAS  Google Scholar 

  • Zeuthen T (2001) How water molecules pass through aquaporins. Trends Biochem Sci 26:77–81

    Article  PubMed  CAS  Google Scholar 

  • Zhang X-H, Hodson I, Williams JP, Blumwald E (2001) Engineering salt-tolerant Brassica plants: characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation. Proc Natl Acad Sci USA 98:12832–12836

    Article  PubMed  CAS  Google Scholar 

  • Zhang YF, Feng G, Li XL (2003) The effect of arbuscular mycorrhizal fungi on the components and concentrations of organic acids in the exudates of mycorrhizal red clover. Acta Ecol Sin 23:30–37

    Google Scholar 

  • Zhang H, Wu X, Li G, Qin P (2011) Interactions between arbuscular mycorrhizal fungi and phosphate-solubilizing fungus (Mortierella sp.) and their effects on Kostelelzkya virginica growth and enzyme activities of rhizosphere and bulk soils at different salinities. Biol Fertil Soil 47:543–554

    Article  CAS  Google Scholar 

  • Zhi H, He CX, He ZQ, Zou ZR, Zhang ZB (2010) The effects of arbuscular mycorrhizal fungi on reactive oxyradical scavenging system of tomato under salt tolerance. Agric Sci China 9:1150–1159

    Article  CAS  Google Scholar 

  • Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445

    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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Authors and Affiliations

  1. Plant Science Department, University of Tabriz, 51666-14779, Tabriz, Iran

    R. Hajiboland

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  1. R. Hajiboland
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Correspondence to R. Hajiboland .

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Editors and Affiliations

  1. Department of Botany A.S. College, University of Kashmir, Srinagar, India

    Parvaiz Ahmad

  2. Department of Botany Faculty of Science, South Valley University, Qena, Egypt

    M. M. Azooz

  3. Department of Biological Sciences Faculty of Science, King Faisal University, Al Hassa, Saudi Arabia

    M. M. Azooz

  4. Department of Plant Sciences, University of Hyderabad, Hyderabad, India

    M. N. V. Prasad

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Hajiboland, R. (2013). Role of Arbuscular Mycorrhiza in Amelioration of Salinity. In: Ahmad, P., Azooz, M.M., Prasad, M.N.V. (eds) Salt Stress in Plants. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-6108-1_13

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