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Effect of Biofilm Forming Plant Growth Promoting Annals of Agricultural Science (2016) xxx(xx), xxx–xxx HOSTED BY Faculty of Agriculture, Ain Shams University Annals of Agricultural Science www.elsevier.com/locate/aoas Effect of biofilm forming plant growth promoting rhizobacteria on salinity tolerance in barley Wedad A. Kasim a,*, Reda M. Gaafar a, Rania M. Abou-Ali b, Mohamed N. Omar c, Heba M. Hewait c a Botany Department, Faculty of Science, Tanta University, Tanta, Egypt b Department of Nucleic Acid and Protein Structure, Agriculture Genetic Engineering Research Institute, Agriculture Research Centre, Giza, Egypt c Department of Microbiology, Soils Water and Environment Research Institute, Agriculture Research Centre, Giza, Egypt Received 21 May 2016; revised 13 July 2016; accepted 13 July 2016 KEYWORDS Abstract Formation of biofilm under varying stress conditions is a significant strategy adopted by Bacillus amyloliquifaciens; bacterial strains for their successful survival in plant rhizosphere. In this study, the activity of bio- Barley; film formation of 20 isolates and strains of plant growth promoting rhizobacteria (PGPR) was Biofilm; determined under different salt concentrations. The results indicated that all of the 20 PGPRs have Plant growth promoting rhi- the activity of biofilm formation under 0.0, 250, 500 or 1000 mM NaCl which was increased with zobacteria; increasing salt concentration. PGPR strains with the highest activity of biofilm formation were Salinity selected and used to coat barley grains. The coated grains were sown in clay/sandy soil and left to grow for 25 days. The results showed that bacterial inoculation was effective in alleviating the deleterious effect of salinity on some growth criteria (seedling length, fresh and dry masses as well as relative water content), compared with the control. The isolate HM6 (B6), which showed the highest activity of biofilm formation at all the studied NaCl concentrations, was identified using 16S ribosomal RNA gene amplification and sequencing of the PCR product. The similarity sequence analysis indicated that HM6 isolate has 97.4% similar sequence identity to Bacillus amyloliquifaciens. It could be speculated that the bacterial activity of biofilm formation is helpful for improving salt stress tolerance of barley. Ó 2016 Production and hosting by Elsevier B.V. on behalf of Faculty of Agriculture, Ain Shams University. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/4.0/). Introduction Barley (Hordeum vulgare L.) is a highly adaptable cereal grain and ranks 5th among all crops for dry matter production in the * Corresponding author. world. In addition, it is an important food source in many E-mail address: [email protected] (W.A. Kasim). parts of the world (Gupta et al., 2010). Although barley is Peer review under responsibility of Faculty of Agriculture, Ain-Shams regarded as salt tolerant among crop plants, its growth and University. http://dx.doi.org/10.1016/j.aoas.2016.07.003 0570-1783 Ó 2016 Production and hosting by Elsevier B.V. on behalf of Faculty of Agriculture, Ain Shams University. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Please cite this article in press as: Kasim, W.A. et al., Effect of biofilm forming plant growth promoting rhizobacteria on salinity tolerance in barley. Ann. Agric. Sci. (2016), http://dx.doi.org/10.1016/j.aoas.2016.07.003 2 W.A. Kasim et al. development are severely affected by ionic and osmotic stresses Plant growth promoting rhizobacterial isolates and strains in salt-affected soils (Mahmood, 2011). Saline soils are a major problem for agriculture because salt Twenty different plant growth promoting rhizobacteria (PGPR) turns agronomically useful lands into unproductive areas. The isolates and strains B (1–20) were used in this study (Table 1). United Nations Environment Program estimates that approx- From these 20 PGPRs eight bacterial isolates (isolates HM1- imately 20% of agricultural land and 50% of crop land in the HM8) were previously isolated from salinized rhizosphere of world are salt-stressed (Flowers and Yeo, 1995). Soil saliniza- wheat plant and characterized as salt tolerant isolates by tion is reducing the area that can be used for agriculture by 1– Hewait (2010) and Omar et al. (2013). The other twelve reference 2% every year, hitting hardest in the arid and semi-arid regions strains were obtained from Microbiology Department, Soil, (FAO, 2002). Soil salinity induces water stress, nutritional Water and Environment Research Institute (SWERI), imbalance, specific ion toxicity, hormonal imbalance and gen- Agricultural Research Center (ARC), Giza, Egypt. The isolates eration of reactive oxygen species which may cause membrane and reference strains were maintained for long-term storage at destabilization (Omar et al., 2009). Moreover, it decreases the À70 °C in Nutrient Broth (NB) with 30% glycerol. yield of many crops as salt inhibits plant photosynthesis, pro- tein synthesis and lipid metabolism (Paul and Lade, 2014). Soil Plant growth under stress conditions may be enhanced by the application of microbial inoculation including plant growth The soil used in the present experiment was clay-sandy soil (2:1 promoting rhizobacteria (PGPR). These microbes can promote w/w). Its characters and composition are illustrated in Table 2. plant growth by regulating nutritional and hormonal balance, A mineral fertilizer (N, P, K) was applied according to the rec- producing plant growth regulators, solubilizing nutrients and ommendations of the Egyptian Ministry of Agriculture. inducing resistance against plant pathogens (Boostani et al., 2014). Certain strains of PGPR belonging to Bacillus, Enter- obacter, Burkholderia, Acinetobacter, Alcaligenes, Arthrobacter, Methods Azospirillum, Azotobacter, Beijerinckia, Erwinia, Flavobac- terium, Rhizobium and Serratia are now being used worldwide Selection of the best biofilm forming PGPR under different salt with the aim to enhance crop productivity (Bharti et al., 2013). concentrations There has been a great interest in eco-friendly and sustainable agriculture with emphasis on the use of beneficial microorgan- The 20 PGPR strains and isolates were screened for their isms. The benefits of PGPR for plants growing in saline soils potency of biofilm formation in nutrient broth (NB) which were reported as an enhancer of root and shoot growth, nutrient was prepared according to Difco (1985). The qualitative and uptake, hydration, chlorophyll content, and resistance to dis- quantitative biofilm formation assays were carried out as eases (Qurashi and Sabri, 2012). These PGPRs stimulate plant follows: growth and enhance plant biomass and their beneficial effects have been demonstrated in many agricultural crop species such Qualitative assay as wheat, tobacco, Brassica juncea, tomatoes, bell peppers, Bacterial cultures of 20 PGPR B (1–20) were grown in NB cucumbers and barley as reviewed by Kang et al. (2014). medium with different NaCl concentrations (0.0, 250, 500 PGPRs are effective in colonizing the plant root and further and 1000 mM) for 24 h without agitation. Thereafter, the multiply into microcolonies and/or produce biofilm as a result of a successful plant-microbe interaction. The plant associated biofilms are highly capable of providing protection from exter- Table 1 Names and codes of 20 PGPR isolates and strains (B nal stress, decreasing microbial competition, and giving pro- 1–20). tecting effects to the host plant supporting growth, yield and crop quality (Asari, 2015). Code PGPR The present study aims to do the following: (a) determine B1 Isolate HM1 the best biofilm forming PGPR isolates and strains by deter- B2 Isolate HM2 mining their activity of biofilm formation under several salt B3 Isolate HM3 concentrations, and (b) evaluate the effect of these PGPRs B4 Isolate HM4 B5 Isolate HM5 on the growth of two barley cultivars (Giza 123 as salt sensitive B6 Isolate HM6 and Giza 2000 as salt tolerant) growing under different levels B7 Isolate HM7 of salinity. B8 Isolate HM8 B9 Bacillus megatherium B10 Pseudomonas fluorescens Material and methods B11 Bacillus circulans B12 Paenibacillus polymyxa Material B13 Azotobacter chroococcum B14 Azospirillum sp. Barley cultivars B15 Paenibacillus polymyxa2 B16 Azospirillum brasilense NO40 Grains of two barley cultivars (H. vulgare L.), cv. Giza 123, as B17 Hyderella sp. B18 V1B1C1 salt sensitive (cv.1) and Giza 2000, as salt tolerant (cv.2) were B19 Mr16 obtained from Barley Department, Agricultural Research B20 Ssbr Center, Giza, Egypt. Please cite this article in press as: Kasim, W.A. et al., Effect of biofilm forming plant growth promoting rhizobacteria on salinity tolerance in barley. Ann. Agric. Sci. (2016), http://dx.doi.org/10.1016/j.aoas.2016.07.003 Effect of rhizobacterial biofilm on barley growth 3 Table 2 Physical and chemical properties of the soil. Table 3 List of the best biofilm forming PGPR, B (5–13) at Textural class Clay Loam 500 mM NaCl. Organic materials (%) 1.43 Code PGPR CaCO3 (%) 0.43 B5 Isolate HM5 PH (1 soil: 2.5 water) 7.66 B6 Isolate HM6 À EC (dS m 1) 36.50 B7 Isolate HM7 B8 Isolate HM8 Anions (cmol/kg) B9 Bacillus megatherium Ca2+ 41.82 B10 Pseudomonas fluorescens Mg2+ 16.46 B11 Bacillus circulans K+ 0.58 B12 Paenibacillus polymyxa Na+ 62.0 B13 Azotobacter chroococcum Cations (cmol/kg) 2À SO4 59.48 ClÀ 58.85 À HCO3 2.55 2À CO3 Nil medium and left to grow overnight at 30 °C with shaking. This Macro elements (g/kg) culture was used for coating barley grains and as liquid inocu- N 1.441 lation. Barley grains were selected for uniformity and size and P 0.644 grouped in equal numbers. Each group was coated with 26 ml K 10.782 of each culture which was loaded on definite vermiculite carrier Micro elements (g/kg) in small plastic bag (30 g/bag) and incubated for 24 h at 37 °C. S 0.0196 To improve the adhesion of the carrier particles to the grains, Fe 12.561 5 ml of the Arabian gum solution was added and the mixture Mn 0.185 was left to dry for 2 h, and then six of these coated grains were Zn 0.131 sown in each plastic pot (9 cm depth  8 cm width), which was Cu 0.0742 previously filled with 300 g of clay-sandy soil.
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