Abstract
Salinity is one of the major environmental threats for successful crop production, hampering plant growth due to the osmotic effect and nutritional and hormonal imbalances. The application of naturally occurring plant growth-promoting rhizobacteria (PGPR) is an emerging technology aimed at ameliorating the negative impact of salinity. However, the results obtained in the laboratory can sometimes not be reproduced in the field. The aim of the study reported here was to evaluate the effect of PGPR inoculation on seed germination in a saline environment under axenic conditions and on enhancement of the growth and yield of wheat under natural salt-affected field conditions. Wheat seeds were inoculated with pre-isolated strains of Pseudomonas putida, Enterobacter cloacae, Serratia ficaria, and Pseudomonas fluorescens and sown at different salinity levels (1, 2, 3, 6, 9, 12, 15 dS m-1). Inoculation with these strains was found to enhance the germination percentage, germination rate, and index of wheat seeds up to 43, 51, and 123 %, respectively, over the uninoculated control at the highest salinity level. The potential of these PGPR for improving the growth and yield of wheat was also evaluated at two natural salt-affected sites. Inoculation with PGPR resulted a significant increase in the growth and yield parameters of wheat at both sites. The inoculated plants also improved the nutrient status of the wheat plants. The inoculated plants had low sodium and high nitrogen, phosphorus, and potassium contents. Our results show that such rhizobacterial strains may be used as an effective tool for enhancing plant growth under salinity stress and for maximizing the utilization of salt-affected soils.
Similar content being viewed by others
References
Abbaspoor A, Zabihi HR, Movafegh S, Asl MHA (2009) The efficiency of plant growth promoting rhizobacteria (PGPR) on yield and yield components of two varieties of wheat in salinity condition. American–Eurasian J Sustainable Agric 3:824–828
Ahmad M, Zahir ZA, Asghar HN, Asghar M (2011a) Inducing salt tolerance in mung bean through coinoculation rhizobia and plant- growth- promoting rhizobacteria containing 1-aminocyclopropane-1-carboxylic acid deaminase. Can J Microbiol 57:578–589
Ahmad M, Zahir ZA, Asghar HN, Arshad M (2011b) The combined application of rhizobial strains and plant growth promoting rhizobacteria improves growth and productivity of mung bean (Vigna radiata L.) under salt-stressed conditions. Ann Microbiol. doi:10.1007/s13213-011-0380-9
AOSA (Association of Official Seed Analysts) (1983) Seed vigour testing handbook. AOSA, Lincoln
AOSA (Association of Official Seed Analysts) (2004) Rules for testing seeds. AOSA, Las Cruces
Arbona V, Marco AJ, Iglesias DJ, Lopez-Climent MF, Talon M, Gomez-Cadenas A (2005) Carbohydrate depletion in roots and leaves of salt-stressed potted Citrus clementina L. Plant Growth Regul 46:153–160
Ashraf M (1994) Breeding for salinity tolerance in plants. Crit Rev Plant Sci 13:17–17
Ashraf M (2004) Some important physiological selection criteria for salt tolerance in plants. Flora 199:361–376
Ashraf M, Foolad MR (2005) Pre-sowing seed treatment-A shotgun approach to improve germination, plant growth, and crop yield under saline and non-saline conditions. Adv Agron 88:223–271
Ashraf M, O’Leary JW (1996) Responses of some newly developed salt-tolerant genotypes of spring wheat to salt stress: 1. Yield components and ion distribution. J Agron Crop Sci 176:91–101
Ashraf M, O’Leary JM (1997) Ion distribution in leaves of salt-tolerant and salt-sensitive lines of spring wheat under salt stress. Acta Bot Neerl 46:207–218
Ashraf M, Zafar R, Ashraf MY (2003) Time-course changes in the inorganic and organic components of germinating sunflower achenes under salt (NaCl) stress. Flora 198:26–36
Ashraf M, Hasnain S, Berge O, Mahmood T (2004) Inoculating wheat seedling with exopolysaccharide-producing bacteria restricts sodium uptake and stimulates plant growth under salt stress. Biol Fertil Soils 40:157–162
Ayers RS, Westcot DW (1985) Water quality for agriculture. FAO Irrigation and Drainage Papers 29 (Rev. 1), FAO, Rome
Barassi CA, Ayrault G, Creus CM, Sueldo RJ, Sobrero MT (2006) Seed inoculation with Azospirillum mitigates NaCl effects on lettuce. Sci Hortic 109:8–14
Bernardo MA, Dieguez ET, Jones HG, Chairez FA, Ojanguren CLT, Cortes AL (2000) Path analysis of cowpea early seedling growth under saline conditions. Int J Exp Bot 67:85–92
Brockwell J, Bottomley PJ (1995) Recent advances in inoculant technology and prospects for the future. Soil Biol Biochem 27:683–697
Catroux G, Hartmann A, Revellin C (2001) Trends in rhizobial inoculant production and use. Plant Soil 230:21–30
Cuartero J, Fernandez-Munoz R (1999) Tomato and salinity. Sci Hortic 78:83–125
Dodd IC, Belimov AA (2009) Agricultural opportunities for ACC deaminase-containing rhizobacteria: a review. In: Int Conf on Positive Plant Microbial Interactions in Relation to Plant Performance and Ecosystem Function. Association of Applied Biologists, Wellesbourne, pp151–156
Duncan DB (1955) Multiple range and multiple F tests. Biometrics 11:1–42
Esashi Y (1991) Ethylene and seed germination. In: Matto AK, Suttle JC (eds) The plant hormone ethylene. CRC Press, Boca Raton, pp 133–157
Foolad MR (2000) Genetic basis of salt tolerance and cold tolerance in tomato. Curr Opin Plant Biol 2:35–49
Foolad MR (2004) Recent advances in genetics of salt tolerance in tomato. Plant Cell Tissue Organ Cult 76:101–119
Frankenberger WTJ, Arshad M (1995) Phytohormones in soils: microbial production and function. Marcel Dekker, New York
Glick BR, Liu C, Ghosh S, Dumbroff EB (1997) Early development of canola seedlings in the presence of the plant growth-promoting rhizobacterium Pseudomonas putida GR12-2. Soil Biol Biochem 29:1233–1239
Glick BR, Patten CL, Holgiun G, Penrose DM (1999) Biochemical and genetic mechanisms used by plant growth-promoting bacteria. Imperial College Press, London
Gorham J, Jones R, McDonnell E (1985) Some mechanisms of salt tolerance in crop plants. Plant Soil 89:15–40
Hamdia MAES, Shaddad MAK, Doaa MM (2004) Mechanisms of salt tolerance and interactive effects of Azospirillum brasilense inoculation on maize cultivars grown under salt stress conditions. Plant Growth Regul 44:165–174
Heidstra R, Yang WC, Yalcin Y, Peck S, Emons A, van Kammen A, Bisseling T (1997) Ethylene provides positional information on cortical cell division but is not involved in Nod factor-induced root hair tip growth in Rhizobium—legume interaction. Development 124:1781–1787
Jeschke WD, Wolf O (1988) External potassium supply is not required for root growth in saline conditions: experiments with Ricinus communis L. grown in a reciprocal split-root system. J Exp Bot 39:1149–1167
Jones RA, El-Abd SO (1989) Prevention of salt-induced epinasty by α-aminoacetic acid and cobalt. Plant Growth Regul 8:315–323
Kloepper JW, Lifshitz R, Zablotowicz RM (1989) Free-living bacterial inocula for enhancing crop productivity. Trends Biotechnol 7:39–44
Kohler J, Caravaca F, Carrasco L, Roldan A (2006) Contribution of Pseudomonas mendocina and Glomus intraradices to aggregate stabilization and promotion of biological fertility in rhizosphere soil of lettuce plants under field conditions. Soil Use Manag 22:298–304
Li FH, Benhur M, Keren R (2003) Effect of marginal water irrigation on soil salinity, sodicity and crop yield. Trans Chinese Soc Agric Eng 19:63–66
Ma W, Guinel FC, Glick BR (2003) Rhizobium leguminosarum biovar viciae 1-aminocyclopropane-1-carboxylate deaminase promotes nodulation of pea plants. Appl Environ Microbiol 69:4396–4402
Maguire JD (1962) Speed of germination-aid in slection and evaluation for seedling emergence and vigour. Crop Sci 2:176–177
Marschner H (1995) Mineral nutrition of higher plants. Academic Press, London
Mattoo AK, Suttle CS (1991) The plant hormone ethylene. CRS Press, Boca Raton
Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572
Mishra M, Kumar U, Mishra PK, Prakash V (2010) Efficiency of plant growth promoting rhizobacteria for the enhancement of Cicer arietinum L. growth and germination under salinity. Adv Biol Res 4:92–96
Nadeem SM, Zahir ZA, Naveed M, Arshad M (2009) Rhizobacteria containing ACC-deaminase confer salt tolerance in maize grown on salt-affected fields. Can J Microbiol 55:1302–1309
Nadeem SM, Zahir ZA, Naveed M, Asghar HN, Arshad M (2010) Rhizobacteria capable of producing ACC-deaminase may mitigate salt stress in wheat. Soil Sci Soc Am J 74:533–542
Nelson LM (2004) Plant growth promoting rhizobacteria (PGPR): Prospects for new inoculants. Online. Crop Manag. doi:10.1094/CM-2004-0301-05-RV
Richards LA (1954) Diagnosis and improvement of saline and alkali soils. U.S. Department of Agriculture, Washington, DC
Rueda-Puente EO, Garcia-Hernandez JL, Preciado-Rangel P, Murillo-Amador B, Tarazon-Herrera MA, Flores-Hernandez A, Holguin-Pena J, Aybar AN, Hoyos JMB, Weimers D (2007) Germination of Salicornia bigelovii ecotypes under stressing conditions of temperature and salinity and ameliorative effects of plant growth-promoting bacteria. J Agron Crop Sci 193:167–176
Ruiz D, Martinez V, Cerda A (1995) Citrus response to salinity: growth and nutrient uptake. Tree Physiol 17:141–150
Ryan J, Estefan G, Rashid A (2001) Soil and plant analysis: laboratory manual. International Centre for Agricultural Research in Dry Areas (ICARDA), Aleppo
Saharan BS, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res 2011: LSMR-21
Sairam RK, Tyagi A (2004) Physiology and molecular biology of salinity stress tolerance in plants. Curr Sci 86:407–421
Saleem M, Arshad M, Hussain S, Bhatti AS (2007) Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J Ind Microbiol Biotechnol 34:635–648
Sallam HA (1999) Effect of some seed-soaking treatments on growth and chemical components on faba bean plants under saline conditions. Ann Agric Sci 44:159–171
Saravanakumar D, Samiyappan R (2007) ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J Appl Microbiol 102:1283–1292
Sarquis JI, Jordan WR, Morgan PW (1991) Ethylene evolution from maize (Zea mays L.) seedling roots and shoots in response to mechanical impedance. Plant Physiol 96:1171–1176
Shakirova FM, Sakhabutdinova AR, Bezrukova MV, Fatkhutdinova RA, Fatkhutdinova DR (2003) Changes in the hormonal status of wheat seedlings induced by salicylic acid and salinity. Plant Sci 164:317–322
Sidari M, Mallamaci C, Muscolo A (2008) Drought, salinity and heat differently affect seed germination of Pinus pinea. J For Res 13:326–330
Siddikee MA, Chauhan PS, Anandham R, Han G, Sa T (2010) Isolation, characterization and use for plant growth promotion under salt stress, of ACC deaminase-producing halotolerant derived from coastal soil. J Microbiol Biotechnol 20:1577–1584
Siddikee MA, Glick BR, Chauhan PS, Yim W, Sa T (2011) Enhancement of growth and salt tolerance of red pepper seedlings (Capsicum annuum L.) by regulating stress ethylene synthesis with halotolerant bacteria containing 1-aminocyclopropane-1-carboxylic acid deaminase activity. Plant Physiol Biochem 49:427–434
Smyth EM, McCarthy J, Nevin R, Khan MR, Dow JM, O’Gara F, Doohan FM (2011) In vitro analyses are not reliable predictors of the plant growth promotion capability of bacteria; a Pseudomonas fluorescens strain that promotes the growth and yield of wheat. J Appl Microbiol 111:683–692
Sobeih WY, Dodd IC, Bacon MA, Grierson D, Davies WJ (2004) Long-distance signals regulating stomatal conductance and leaf growth in tomato (Lycopersicon esculentum) plants subjected to partial root-zone drying. J Exp Bot 55:2353–2363
Steel RGD, Torrie JH, Dicky DA (1997) Principles and procedures of statistics—a biometrical approach. McGraw Hill Book, Singapore
Suarez N, Medina E (2005) Salinity effect on plant growth and leaf demography of the mangrove, Avicennia germinans L. Trees 19:721–727
Tank N, Saraf M (2010) Salinity-resistant plant growth promoting rhizobacteria ameliorates sodium chloride stress on tomato plants. J Plant Interact 5:51–58
Wolf B (1982) A comprehensive system of leaf analyses and its use for diagnosing crop nutrient status. Commun Soil Sci Plant Anal 13:1035–1059
Xu G, Magen H, Tarchitzky J, Kafkafi U (2000) Advances in chloride nutrition of plants. Adv Agron 68:97–110
Zabihi HR, Savaghebi GR, Khavazi A, Ganjali A, Miransari M (2010) Pseudomonas bacteria and phosphorous fertilization, affecting wheat (Triticum aestivum L.) yield and P uptake under greenhouse and field conditions. Acta Physiol Plant 33:145–152
Zahir ZA, Ghani U, Naveed M, Nadeem SM, Asghar HN (2009) Comparative effectiveness of Pseudomonas and Serratia sp. containing ACC-deaminase for improving growth and yield of wheat (Triticum aestivum L.) under salt-stressed conditions. Arch Microbiol 191:415–424
Zapata PJ, Botella MÁ, Pretel MT, Serrano M (2007) Responses of ethylene biosynthesis to saline stress in seedlings of eight plant species. Plant Growth Regul 53:97–106
Zhender GW, Yao C, Murphy JF, Sikora ER, Kloepper JW, Schuster DJ, Polston JE (1999) Microbe-induced resistance against pathogens and herbivores: evidence of effectiveness in agriculture. In: Agarwal AA, Tuzun S, Bent E (eds) Induced plant defenses against pathogens and herbivores: biochemistry, ecology agriculture. APS Press, St Paul, p 33
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Nadeem, S.M., Zahir, Z.A., Naveed, M. et al. Mitigation of salinity-induced negative impact on the growth and yield of wheat by plant growth-promoting rhizobacteria in naturally saline conditions. Ann Microbiol 63, 225–232 (2013). https://doi.org/10.1007/s13213-012-0465-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13213-012-0465-0