Abstract
Responses of Puccinellia distans, a halophytic grass to low (50 mM) and high (200 mM) NaCl salinity, were studied in a sand culture experiment without or with inoculation by arbuscular mycorrhizal fungus (AMF), Claroideoglomus etunicatum isolated from its saline habitat. Plant biomass was not influenced by salinity levels, while a tendency to a higher biomass was observed in AMF plants under both control and saline conditions. Leaf photosynthesis increased by both salinity and AMF inoculation. Despite higher transpiration rate, AMF plants had higher water-use efficiency under sever saline conditions. AMF inoculation decreased proline concentration, but increased significantly leaf osmotic potential. Antioxidative enzymes responded differently to the salt and AMF treatments depending on the salt concentration and plant organ. Nonetheless, salt-induced malondialdehyde accumulation in the leaves diminished by AMF colonization. K and Ca contents were not affected by salt, while fungal colonization increased K in the roots and Ca in both leaves and roots. Our results indicated that enhancement of photosynthesis and ion homeostasis is involved in the tolerance of P. distans to both low and high salinity. AMF inoculation increased plants’ tolerance by augmentation of the above mechanisms accompanied by improvement of water relations and protection against oxidative damage in the leaves.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11738-014-1546-4/MediaObjects/11738_2014_1546_Fig1_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11738-014-1546-4/MediaObjects/11738_2014_1546_Fig2_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11738-014-1546-4/MediaObjects/11738_2014_1546_Fig3_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11738-014-1546-4/MediaObjects/11738_2014_1546_Fig4_HTML.gif)
Similar content being viewed by others
References
Akhani H (2006) Biodiversity of halophytic and Sabkha ecosystems of Iran. In: Khan MA, Barth H, Kust GC, Böer B (eds) Sabkha ecosystems, vol II., The southern and central Asian countriesSpringer, New York, pp 71–88
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
Al-Karaki G, McMichael B, Zak J (2004) Field response of wheat to arbuscular mycorrhizal fungi and drought stress. Mycorrhiza 14:263–269
Asghari HR, Amerian M, Gorbani H (2008) Soil salinity affects arbuscular mycorrhizal colonization of halophytes. Pak J Biol Sci 11:1909–1915
Augé RM (2000) Stomatal behavior of arbuscular mycorrhizal plants. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: physiology and function. Kluwer Academic, Dordrecht, pp 201–237
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
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
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
Clayton WD, Vorontsova MS, Harman KT, Williamson H (2013) Grass base—the online world grass flora. http://www.kew.org/data/grasses-db.html. Accessed 20 Nov 2013
Eimanifar A, Mohebbi F (2007) Urmia Lake (Northwest Iran): a brief review. Saline Syst 3:5. doi:10.1186/1746-1448-3-5
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963
Füzy A, Tóth T, Biró B (2008) Soil-plant factors, other than the type of salt-specific anions are affecting the mycorrhiza colonization of some halophytes. Commun Ecol 9:1–8
Giovanetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol 84:489–500
Giri B, Kapoor R, Mukerji KG (2003) Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass and maineral nutrition of Acacia auriculiformis. Biol Fertil Soils 38:170–175
Hajiboland R (2013) Role of arbuscular mycorrhiza in amelioration of salinity. In: Ahmad P, Azzoz MM, Prasad MNV (eds) Salt stress in plants, singnaling, omics and adaptations. Springer, New York, pp 301–354
Hajiboland R, Aliasgharzad N, Laiegh SF, Poschenrieder C (2010) Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331:313–327
Hammer EC, Nasr H, Pallon J, Olsson PA, Wallander H (2011) Elemental composition of arbuscular mycorrhizal fungi at high salinity. Mycorrhiza 21:117–129
Hasegawa PM, Bressan RA, Zhu J-K, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499
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
Hwang M, Ederer GM (1975) Rapid hippurate hydrolysis method for presumptive identification of group B streptococci. J Clin Microbiol 1:114–115
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
Johnson-Green P, Kenkel NC, Boot T (2001) Soil salinity and arbuscular mycorrhizal colonization of Puccinellia nuttalliana. Mycol Res 105:1094–1110
Kronzucker HJ, Coskun D, Schulze LM, Wong JR, Britto DT (2013) Sodium as nutrient and toxicant. Plant Soil 369:1–23
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
Lichtenthaler HK, Wellburn AR (1985) Determination of total carotenoids and chlorophylls a and b of leaf in different solvents. Biol Soc Trans 11:591–592
M’Rah S, Ouerghi Z, Eymery F, Rey P, Hajji M, Grignon C, Lachaal M (2007) Efficiency of biochemical protection against toxic effects of accumulated salt differentiates Thellungiella halophila from Arabidopsis thaliana. J Plant Physiol 164:375–384
Magné C, Saladin G, Clément C (2006) Transient effect of the herbicide flazasulfuron on carbohydrate physiology in Vitis vinifera. Chemosphere 62:650–657
Mansour MMF (2013) Plasma membrane permeability as an indicator of salt tolerance in plants. Biol Plant 57:1–10
Merryweather JW, Fitter AH (1991) Techniques in arbuscular mycorrhiza research. York Mycorrhiza Research Group, UK
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
Ozgur R, Uzilday B, Sekmen AH, Turkan I (2013) Reactive oxygen species regulation and antioxidant defence in halophytes. Func Plant Biol 40:832–884
Parida AK, Jha B (2010) Antioxidative defense potential to salinity in the euhalophyte Salicornia brachiata. J Plant Growth Regul 29:137–148
Peng YH, Zhu YF, Mao YQ, Wang SM, Su WA, Tang ZC (2004) Alkali grass resists salt stress through high [K+] and an endodermis barrier to Na+. J Exp Bot 55:939–949
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
Porcel R, Aroca R, Ruiz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron Sustain Dev 32:181–200
Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress: new perspectives for molecular studies. Mycorrhiza 13:309–317
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
Sannazzaro AI, Ruíz OA, Alberto EO, Menendez AB (2006) Alleviation of salt stress in Lotus glaber by Glomus intraradices. Plant Soil 285:279–287
Shabala SN, Mackay A (2011) Ion transport in halophytes. In: Kader JC, Delseny M (eds) Advances in botanical research. Elsevier, Burlington, pp 151–199
Sharifi M, Ghorbanli M, Ebrahimzadeh H (2007) Improved growth of salinity-stressed soybean after inoculation with pre-treated mycorrhizal fungi. J Plant Physiol 164:1144–1151
Stelzer R, Läuchli A (1978) Salt- and flooding tolerance of Puccinellia peisonis. III. Distribution and localization of ions in the plant. Z Pflanzenphysiol 88:437–448
Subbarao GV, Ito O, Berry WL, Wheeler RM (2003) Sodium-a functional plant nutrient. Crit Rev Plant Sci 22:391–416
Szabados L, Savouré A (2010) Proline: a multifunctional amino acid L. Trends Plant Sci 15:89–97
Talaat NB, Shawky BT (2013) Modulation of nutrient acquisition and polyamine pool in salt-stressed wheat (Triticum aestivum L.) plants inoculated with arbuscular mycorrhizal fungi. Acta Physiol Plant 35:2601–2610
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
Yamato M, Ikeda S, Iwase K (2008) Community of arbuscular mycorrhizal fungi in coastal vegetation on Okinawa Island and effect of the isolated fungi on growth of sorghum under salt-treated conditions. Mycorrhiza 18:241–249
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
Acknowledgments
The authors greatly appreciate Dr H. Akhani, University of Tehran who suggested using P. distans for our physiological studies.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. H. Walter.
Rights and permissions
About this article
Cite this article
Dashtebani, F., Hajiboland, R. & Aliasgharzad, N. Characterization of salt-tolerance mechanisms in mycorrhizal (Claroideoglomus etunicatum) halophytic grass, Puccinellia distans . Acta Physiol Plant 36, 1713–1726 (2014). https://doi.org/10.1007/s11738-014-1546-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11738-014-1546-4