Mechanisms of plant growth promoting rhizobacteria (PGPR) and mycorrhizae fungi to enhancement of plant growth under salinity stress: A review
Keywords:
PGPR, AMF, Nutrient uptake, Salt stressAbstract
Salinity is the major environmental factor limiting plant growth and productivity. Under salinity conditions, plant growth is affected by a number of factors such as hormonal and nutritional imbalance, ion toxicity, physiological disorders, susceptibility to diseases, etc. Plant growth under stress conditions may be enhanced by the application of microbial inoculation including plant growth promoting rhizobacteria (PGPR) and mycorrhizal fungi. These microbes can promote plant growth by regulating nutritional and hormonal balance, producing plant growth regulators, solubilizing nutrients and inducing resistance against plant pathogens. The present review comprehensively discusses on the effectiveness of PGPR and mycorrhizal fungi for enhancing plant growth under salinity stress. The mechanisms involved in plant salinity tolerance under stress conditions have been discussed at length in this review. Also the review discusses the role of rhizobacteria and mycorrhizae in combination in enhancing plant growth under stress conditions.
References
Adiku, G., Renger, M., Wessolek, G., Facklam, M., Hech-Bischoltz, C., 2001. Simulation of dry matter production and seed yield of common beans under varying soil water and salinity conditions. Agr. Water Manag., 47, 55–68.
Alghazali, R., Kmuhammad, S.H.M., Al-gzawl., 1986. Some observations on P solubilization by aerobic microorganisms isolated d from sediments of Al Khair River Baghdad (Iraq). J. Bio. Sci.Res., 47, 157-72.
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.N., 2006. Nursery inoculation of tomato with arbuscular mycorrhizal fungi and subsequent performance under irrigation with saline water. Sci. Hort., 109, 1–7.
Al-Karaki, G.N., Al-Raddad, A., 1997. Effect of arbuscular mycorrhizal fungi and drought stress on growth and nutrient uptake of two wheat genotypes differing in drought resistance. Mycorrhiza., 7, 83–88.
Antoun, H., Prevost, D., 2000. PGPR activity of Rhizobium with nonleguminous plants.http,//www.ag.auburn.ed/ ~mlowens/argentina/pdf%20manuscripts/prevost.pdf.
Ashraf, M., 1994. Breeding for salinity tolerance in plants. Crit. Rev. Plant Sci., 13, 17–42.
Ashraf, M., Berge, S.H., Mahmood, O.T., 2004. Inoculating wheat seedling with exopolysaccharideproducing bacteria restricts sodium uptake and stimulates plant growth under salt stress. Biol. Fertil. Soil., 40, 157–62.
Azcón-Aguilar, C., Azcón, R., Barea, J.M., 1997. Endomycorrhizal fungi and Rhizobium as biological fertilizers for Medicago sativa in normal cultivation. Nature., 279, 325–327.
Banik, S., Dey, B.K., 1982. Available phosphate content of an alluvial soil is influenced by inoculation of some isolated phosphate solubilizing microorganisms Plant Soil., 69, 353-364.
Barazani, O., Friedman, J., 1999. Is IAA the injury root growth factor secreted froin plant-growth-mediating bacteria. J. Chem. Ecol., 25, 2397-2406.
Bohnert, H.J., Jensen, R.G., 1996. Strategies for engineering water-stress tolerance in plants. Trends Biotechnol., 14, 89–97.
Boostani, H.M., Chorom, M., Moezi, A., Enayatizamir, N., 2014. Mechanisms of Plant Growth Promoting Rhizobacteria (PGPR) and Mycorrhizae Fungi to Enhancement of Plant Growth under salinity stress, A review.
Bouhmouch, I., Souad-Mouhsine, B., Brhada, F., Aurag, J., 2005. Influence of host cultivars and Rhizobium species on the growth and symbiotic performance of Phaseolus vulgaris under salt stress. J. Plant Physiol., 162, 1103–13.
Brown, M.E., 1974. Seed and root bacterization. Annu. Rev. Phytopathol., 12, 181–197.
Chabot, R., Beauchamp, C.J., Kloepper, J.W., Antoun, H., 1998. Effect of phosphorous on root colonization and growth promotion of maize by bioluminescent mutants of phosphate.
Colla, G., Rouphael, Y., Cardarelli, M., Tullio, M., Rivera, C.M., Rea, E., 2008. Alleviation of salt stress by arbuscular mycorrhizal in zucchini plants grown at low and high phosphorus concentration. Biol. Fertil. Soils., 44, 501–509.
Creus, C.M., Sueldo, R.J., Barassi, C.A., 1998. Water relations in Azospirillum inoculated wheat seedlings under osmotic stress. Canad. J. Bot., 76, 238–244.
De salmon, I.E.G., Hynes, R.K., Nelson, L.M., 2001. Cytokenin production by plant growth promoting rhizobacteria and selected mutants. Can. J. Microbal., 47,404-411.
Dehne, H.W., 1982. Interaction between vesicular-arbuscular mycorrhizal fungi and plant pathogens. Phytopathol., 72, 1115–1119.
Evelin, H., Kapoor, R., Giri, B., 2009. Arbuscular mycorrhizal fungi in alleviation of salt stress, a review. Ann. Bot., 104, 1263–80.
Fasim, F., Ahmed, N., Parsons, R., Gadd, G.M., 2002. Solubilization of zinc salts by bacterium isolated by the air environment of tannery. FEMS Microbiol. Lett., 213, 1-6.
Frechill, S., Lasa, B., Ibarretxe, L., Lamsfus, C., Aparicio Trejo, P., 2001. Pea response to saline stress is affected by the source of nitrogen nutrition (ammonium or nitrate) Plant Growth Regulators., 35, 171–179.
Fuzy, A., Biro, B., Toth, 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.
Gamalero, E., Berta, G., Massa, N., Glick, B.R., Lingua, G., 2010. Interactions between Pseudomonas putida UW4 and Gigaspora rosea BEG9 and their consequences on the growth of cucumber under salt stress conditions. J. Appl. Microbiol., 108, 236–245.
Garg, N., Chandel, S., 2011. Effect of mycorrhizal inoculation on growth, nitrogenfixation, and nutrient uptake inCicer arietinum(L.) under salt stress. Turk. J. Agr. For., 35, 205–214.
Garg, N., Manchanda, G., 2008. Effect of arbuscular mycorrhizal inoculation of salt-induced nodule senescence in Cajanus cajan (pigeonpea). J. Plant Growth Regul., 27, 115–124.
Gaur, A.C., Gaind, S., 1999. Phosphate solubilizing microorganisms-An overview. Agromicrobes. Current trends in life sciences, Today and tomorrows publishers, New Delhi. India., 23, 151-164.
Geddie, J.L., Sutherland, I.W., 1993. Uptake of metals by bacterial polysaccharides. J. Appl. Bacteriol., 74, 467–72.
Giri, B., Kapoor, R., Mukerji, K.G., 2003. Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass and mineral nutrition of Acacia auriculiformis. Biol. Fertil. Soils., 38, 170–175.
Giri, B., Mukerji, K.G., 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.
Glick, B.R., Pasternak, J.J., 2003. Plant growth promoting bacteria. In, BR Glick & JJ Pasternak (eds) Molecular Biotechnology – Princ. Appl. Recomb., DNA. ASM Press, Washington, DC, 3rd edn, pp. 436–454.
Glick, B.R., Pasternak, J.J., 2003. Plant growth promoting bacteria. In, BR Glick & JJ Pasternak (eds)Molecular Biotechnology – Princ. Appl. Recomb. DNA. ASM Press, Washington, DC, 3rd edn, pp. 436–454.
Govindarajulu, M., Pfeffer, P.E., Jin, H.R., et al., 2005. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature., 435, 819–823.
Gutierrez-Manero, F.J., Ramos-Solano, B., Probanza, A., Mehouachi, J., Tadeo, F.R., Talon, M., 2001.The plant-growth-promoting rhizobacteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active gibberellins. Physiol Plant., 111, 206–211.
Halder, A.K., Chakrabartty, P.K., 1993. Solubilization of inorganic phosphate by Rhizobium. Folia Microbiol., 38, 325–30.
Halder, A.K., Mishra, A.K., Bhattacharyya, P., Chakrabartty, P.K., 1990. Solubilization of rock phosphate by Rhizhobium and Bradyrhizobium, J. Gen. Appl. Microbiol., 36, 81–92.
Hamdia, M.A., Shaddad, M.A.K., Doaa, M.M., 2004. Mechanism of salt tolerance and interactive effect of Azospirillum bransilense inoculation on maize cultivars grown under salt stress conditions. Plant Growth Regul., 44, 165–74.
Han, H.S., Lee, K.D., 2005. Physiological responses of soybean-inoculation of Bradyrhizobium japonicum with PGPR in Saline soil conditions. Res. J. Agr. Biol. Sci., 1, 216–221.
Igual, J.M., Valverde, A., Cervantes, E., Velásquez, E., 2001. Phosphate solubilizing bacteria as inoculants for agriculture, use of updated molecular techniques in their study. Agr., 2, 561–568.
Illmer, P., Schineer, F., 1992. Solubilization of insoluble phosphates by microrganisms isolated from forest soils. Soil biol. biochem., 24, 389-395.
Jahromi, F., Aroca, R., Porcel, R., Ruiz-Lozano, J.M., 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.
Juniper, S., Abbott, L.K., 1993. Vesicular-arbuscular mycorrhizas and soil salinity. Mycorrhiza., 4, 45–57.
Kapoor, R., Sharma, D., Bhatnagar, A.K., 2008. Arbuscular mycorrhizae in micropropagation systems and their potential applications. Sci. Hort., 116, 227–239.
Khodair, T.A., Galal, G.F., El-Tayeb, T.S., 2008. Effect of inoculating wheat seedlings with exopolysaccharide-producing bacteria in saline soil. J. Appl. Sci Res., 4, 2065–2070.
Kim, K.Y., Jordan, D., Krishnan, H.B., 1997. Rahnella aqualitis, bacterium isolated from soybean rhizosphere, can solubilize hydroxyapatite. FEMS Microbiol. Lett., 153, 273–277.
Kohler, J., Caravaca, F., Roldan, 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.
Kothari, S.K., Marschner, H., George, E., 1990. Effect of VA mycorrhizal fungi and rhizosphere microorganism on root and shoot morphology, growth and water relations of maize. New Phytolog., 116, 303–311.
Kumar, A., Sharma, S., Mishra, S., 2010. Influence of arbuscular mycorrhizal (AM) fungi and salinity on seedling growth, solute accumulation and mycorrhizal dependency of Jatropha curcas L. J. Plant Growth Regul., 29, 297–306.
Lesueur, D., Sarr, A., 2008. Effects of single and dual inoculation with selected microsymbionts (rhizobia and arbuscular mycorrhizal fungi) on field growth and nitrogenfixation of Calliandra calothyrsusMeissn. Agr. Syst., 73, 37–45
Levy, Y., Dodd, J., Krikun, J., 1983. Effect of irrigation water salinity and rootstock on the vertical distribution of vesicular-arbuscular mycorrhiza in citrus roots. New Phytolog., 95, 397–403.
Lindermann, R.G., 1994. Role of VAM in biocontrol. In, Pfleger FL, Linderman RG, editors. Mycorrhizae and plant health. St. Paul, American Phytopatholog. Soc., pp. 1–26.
Mardukhi, B., Rejali, F., Daei, G., Ardakani, M., Malakuti, M.A., Miransari, M., 2011. Arbuscular mycorrhizaes enhance nutrient uptake in different wheat genotype at high salinity levels under field and greenhouse conditions. C. R. Biologies., 334, 564-571.
Marschner, H., 1995. Mineral nutrition of higher plants. 2nd edn. New York, NY, Academic Press;
Matamoros, M.A., Baird, L.M., Escuredo, P.R., et al., 1999. Stress-induced legume root nodule senescence, physiological, biochemical and structural alterations. Plant Physiol., 121, 97–111.
Meyer, J.R., Linderman, R.G., 1986. Response of subterranean clover todual inoculation with vesicular– arbuscular mycorrhizal fungi and a plant growth-promoting bacterium, Pseudomonas putida. Soil. Biol. Biochem., 18, 185–90
Munns, R., 2002. Comparative physiology of salt and water stress. Plant Cell Env., 25, 239–50
Najafi, A., Ardakani, M.R., Rejali, F., Sajedi, N., 2012. Response of winter barley to co-inoculation with Azotobacter and Mycorrhiza fungi influenced by plant growth promoting rhizobacteria. Ann. Biol. Res., 3, 4002–4006.
Parks, E.J., Olson, G.J., Brinckman, F.E., Baldi, F., 1990. Characterization by high performance liquid chromatography (HPLC) of solubilization of phosphorus in iron ore by a fungus. J. Ind. Microbiol., 5,183-190.
Puente, M.E., Bashan, Y., Li, C.Y., Lebsky, V.K., 2004. Microbial populations and activities in the rhizoplane of rock weathering desert plants root colonization and weathering of igneous rocks. Plant Biol., 6, 629-642.
Qurashi, A.W., Sabri, A.N., 2012. Bacterial exopolysaccharide and biofilm formation stimulate chickpea growth and soil aggregation under salt stress. Braz J. Microbiol., 11, 83–91.
Rabie, G.H., Aboul-Nasr, M.B., Al-Humiany, A., 2005. Increased salinity tolerance of cowpea plants by dual inoculation of an arbuscular mycorrhizal fungusGlomus clarumand a nitrogen-fixer Azospirillum brasilense. Microbiol., 33, 51–60.
Rai, A.K., Tiwari, S.P., 1999. Response to NaCl of nitrate assimilation and nitrogenase activity in the cyanobacterium Anabaena sp. PCC 7120 and its mutants. J. Appl. Microbiol., 87, 877–83.
Reyes, I., Bernier, L., Simard, R., Antoun, H., 1999. Effect of nitrogen source on solubilization of different inorganic phosphates by bacterial strain of Pencillium rugulosum and two UVinduced mutants. FEMS Microbiol. Ecol., 28, 281–290.
Rodríguez, H., Fraga, R., 1999. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Adv., 17, 319–339.
Ruiz-lozano J.M., Azcon, R., 2000. Symbiotic efficiency and infectivity of an autochthonous arbuscular mycorrhizal Glumus Sp. From saline soils and Glumus deserticola under salinity. Mycorrhizae., 10, 137-143.
Ryu, C.M., Farag, M.A., Hu, C.H., Reddy, M.S., Kloepper, J.W., Pare, P.W., 2004. Plant physiol., 134, 1017-1026.
Salisbury, F.B., 1994. The role of plant hormones. In, Wilkinson RE (eds) Plant–Environment Interactions. Marcel Dekker, New York., USA, 39-81.
Salisbury, F.B., 2002. The role of plant hormones. In, Wilkinson RE (eds) Plant–Environment Feng, G., Zhang, F.S., Li, X.l., Tian, C.Y., Tang, C., Rengel, Z., 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.
Sandhya, V., Ali, S.K.Z., Grover, M., Reddy, G., Venkateswarlu, B., 2009. Alleviation of drought stress effects in sunflower seedlings by the exopolysaccharides producing Pseudomonas putida strain GAP-P45. Biol. Fertil. Soils., 46, 17–26.
Sannazzaro, A.I., Ruiz, O.A., Alberto, E.O., Menendez AB. 2006. Alleviation of salt stress inLotus glaber by Glomus intraradices. Plant Soil., 285, 279–287.
Sannazzaro, A.I., Ruiz, O.A., Albetró, E.O., Menéndez, A.B., 2006. Alleviation of salt stress in Lotus glaber by Glomus intraradies. Plant Soil., 285, 279–287.
Selvakumar, G., Thamizhiniyan, P., 2011. The effect of the arbuscular mycorrhizal (AM) fungus Glomus intraradices on the growth and yield of chilli (Capsicum annuum L.) under salinity stress. World Appl. Sci. J., 14, 1209–1214.
Sharifi, M., Ghorbanli, M., Ebrahimzadeh, H., 2007. Improved growth of salinity-stressed soybean after inoculation with pre-treated mycorrhizal fungi. J. Plant Physiol., 164, 1144–1151.
Sheng, M., Tang, M., Chan, H., Yang, B., Zhang, F., Huang, Y., 2008. Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza., 18, 287–296.
Shirmardi, M., Savaghebi, G.R., Khavazi, K., Akbarzadeh, A., Farahbakhsh, M., Rejali, F., et al., 2010. Effect of microbial inoculants on uptake of nutrient elements in two cultivars of sunflower (Helianthus annuus L.) in saline soils. Not. Sci. Biol., 2, 57–66.
Smith, S.E., Read, D.J., 1995. Mycorrhizal symbiosis. New York, NY, Academic Press., pp. 105–160.
Tester, M., Davenport, R., 2003. Na+ tolerance and Na+ transport in higher plants. Ann. Bot., 91, 503–527.
Torre, L., Vegli, F., Terreri, M., Ercole, C., Lepidi, A., 1993. Manganese bioleaching from pyrolusite, Bacterial properties reliable for the process .FEMS Microbiol. Rev., 11, 103-108.
Tripathi, A.K., Nagarajan, T., Verma, S.C., Le Rudulier, D., 2002. Inhibition of biosynthesis and activity of nitrogenase in Azospirillum brasilense Sp7 under salinity stress. Curr Microbiol., 44, 363–367.
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.
Yokoi, S., Quintero, F.J., Cubero, B., Ruiz, M.T., Bressan, R.A.,Hasegawa, P.M., Pardo, J.M. 2002. Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response. Plant J., 30, 529–539.
Zhang, Y.F., Wang, P., Yang, Y.F., Bi, Q., Tian, S.Y., Shi, X.W., 2011. Arbuscular mycorrhizal fungi improve re establishment of Leymus chinensisin bare saline–alkaline soil, Implication on vegetation restoration of extremely degraded land. J. Arid. Environ., 75, 773–778.
Zhifang, G., Loescher, W.H., 2003. Expression of a celery mannose 6-phosphate reductase in Arabidopsis thalianaenhances salt tolerance and induces biosynthesis of both mannitol and a glucosyl-mannitol dimmer. Plant Cell Environ., 26, 275–283.
Zuccarini, P., 2007. Mycorrhizal infection ameliorates chlorophyll content and nutrient uptake of lettuce exposed to saline irrigation. Plant, Soil Env., 53, 283–286.
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