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BioMed Research International
Volume 2013, Article ID 248078, 13 pages
http://dx.doi.org/10.1155/2013/248078
Research Article

Potential for Plant Growth Promotion of Rhizobacteria Associated with Salicornia Growing in Tunisian Hypersaline Soils

1DeFENS, Department of Food, Environment and Nutritional Sciences (DeFENS), University of Milan, Via Celoria 2, 20133 Milan, Italy
2Laboratory of Microorganisms and Active Biomolecules, University of Tunis El Manar, Campus Universitaire, 2092 Tunis, Tunisia

Received 15 March 2013; Revised 30 April 2013; Accepted 3 May 2013

Academic Editor: George Tsiamis

Copyright © 2013 Francesca Mapelli et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Balloi, E. Rolli, R. Marasco et al., “The role of microorganisms in bioremediation and phytoremediation of polluted and stressed soils,” Agrochimica, vol. 54, no. 6, pp. 353–369, 2010. View at Google Scholar · View at Scopus
  2. L. E. de-Bashan, J. P. Hernandez, Y. Bashan, and R. M. Maier, “Bacillus pumilus ES4: candidate plant growth-promoting bacterium to enhance establishment of plants in mine tailings,” Environmental and Experimental Botany, vol. 69, no. 3, pp. 343–352, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. D. Egamberdieva, F. Kamilova, S. Validov, L. Gafurova, Z. Kucharova, and B. Lugtenberg, “High incidence of plant growth-stimulating bacteria associated with the rhizosphere of wheat grown on salinated soil in Uzbekistan,” Environmental Microbiology, vol. 10, no. 1, pp. 1–9, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. R. Hayat, S. Ali, U. Amara, R. Khalid, and I. Ahmed, “Soil beneficial bacteria and their role in plant growth promotion: a review,” Annals of Microbiology, vol. 60, no. 4, pp. 579–598, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. R. Marasco, E. Rolli, B. Ettoumi et al., “A drought resistance-promoting microbiome is selected by root system under desert farming,” PLoS ONE, vol. 7, no. 10, Article ID e48479, 2012. View at Google Scholar
  6. S. K. Upadhyay, D. P. Singh, and R. Saikia, “Genetic diversity of plant growth promoting rhizobacteria isolated from rhizospheric soil of wheat under saline condition,” Current Microbiology, vol. 59, no. 5, pp. 489–496, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Mayak, T. Tirosh, and B. R. Glick, “Plant growth-promoting bacteria confer resistance in tomato plants to salt stress,” Plant Physiology and Biochemistry, vol. 42, no. 6, pp. 565–572, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. K. C. Ravindran, K. Venkatesana, V. Balakrishnana, K. P. Chellappana, and T. Balasubramanian, “Restoration of saline land by halophytes for Indian soils,” Soil Biology and Biochemistry, vol. 39, pp. 2661–2664, 2007. View at Publisher · View at Google Scholar
  9. D. M. Al-Mailem, N. A. Sorkhoh, M. Marafie, H. Al-Awadhi, M. Eliyas, and S. S. Radwan, “Oil phytoremediation potential of hypersaline coasts of the Arabian Gulf using rhizosphere technology,” Bioresource Technology, vol. 101, no. 15, pp. 5786–5792, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. E. Manousaki and N. Kalogerakis, “Halophytes present new opportunities in phytoremediation of heavy metals and saline soils,” Industrial and Engineering Chemistry Research, vol. 50, no. 2, pp. 656–660, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. E. P. Glenn, J. W. O'Leary, M. C. Watson, T. L. Thompson, and R. O. Kuehl, “Salicornia bigelovii Torr.: an oilseed halophyte for seawater irrigation,” Science, vol. 251, no. 4997, pp. 1065–1067, 1991. View at Google Scholar · View at Scopus
  12. F. M. Attia, A. A. Alsobayel, M. S. Kriadees, M. Y. Al-Saiady, and M. S. Bayoumi, “Nutrient composition and feeding value of Salicornia bigelovii torr meal in broiler diets,” Animal Feed Science and Technology, vol. 65, no. 1–4, pp. 257–263, 1997. View at Google Scholar · View at Scopus
  13. United Nations Secretary-General’s High-level Panel on Global Sustainability, Resilient People, Resilient Planet: A Future Worth Choosing, United Nations, New York, NY, USA, 2012.
  14. C. J. Ruan, J. A. T. da Silva, S. Mopper, Q. Pei, and S. Lutts, “Halophyte improvement for a salinized world,” Critical Reviews in Plant Sciences, vol. 29, no. 6, pp. 329–359, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. D. Ramadoss, V. K. Lakkineni, P. Bose, S. Ali, and K. Annapurna, “Mitigation of salt stress in wheat seedlings by halotolerant bacteria isolated from saline habitats,” SpringerPlus, vol. 2, no. 1, article 6, 2013. View at Google Scholar
  16. S. Tiwari, P. Singh, R. Tiwari et al., “Salt-tolerant rhizobacteria-mediated induced tolerance in wheat (Triticum aestivum) and chemical diversity in rhizosphere enhance plant growth,” Biology and Fertility of Soils, vol. 47, no. 8, pp. 907–916, 2011. View at Publisher · View at Google Scholar
  17. M. Argandoña, R. Fernández-Carazo, I. Llamas et al., “The moderately halophilic bacterium Halomonas maura is a free-living diazotroph,” FEMS Microbiology Letters, vol. 244, no. 1, pp. 69–74, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. Y. Bashan, M. Moreno, and E. Troyo, “Growth promotion of the seawater-irrigated oilseed halophyte Salicornia bigelovii inoculated with mangrove rhizosphere bacteria and halotolerant Azospirillum spp.,” Biology and Fertility of Soils, vol. 32, no. 4, pp. 265–272, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. I. Gontia, K. Kavita, M. Schmid, A. Hartmann, and B. Jha, “Brachybacterium saurashtrense sp. nov., a halotolerant root-associated bacterium with plant growth-promoting potential,” International Journal of Systematic and Evolutionary Microbiology, vol. 61, part 12, pp. 2799–2804, 2011. View at Publisher · View at Google Scholar
  20. T. Ozawa, J. Wu, and S. Fujii, “Effect of inoculation with a strain of Pseudomonas pseudoalcaligenes isolated from the endorhizosphere of Salicornia europea on salt tolerance of the glasswort,” Soil Science and Plant Nutrition, vol. 53, no. 1, pp. 12–16, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. E. Rueda-Puente, T. Castellanos, E. Troyo-Diéguez, J. L. D. de León-Alvarez, and B. Murillo-Amador, “Effects of a nitrogen-fixing indigenous bacterium (Klebsiella pneumoniae) on the growth and development of the halophyte Salicornia bigelovii as a new crop for saline environments,” Journal of Agronomy and Crop Science, vol. 189, no. 5, pp. 323–332, 2003. View at Publisher · View at Google Scholar · View at Scopus
  22. B. Jha, I. Gontia, and A. Hartmann, “The roots of the halophyte Salicornia brachiata are a source of new halotolerant diazotrophic bacteria with plant growth-promoting potential,” Plant and Soil, vol. 356, no. 1-2, pp. 265–277, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. Forssk, Fl. Aeg. Arab. 2. 1775.
  24. E. Le Floc’h, L. Boulos, and E. Vela, Catalogue synonymique commenté de la flore de Tunisie, République tunisienne ministère de l’environnement et du développement durable banque nationale de genes, 2010.
  25. C. Schbereiter-Gurtner, G. Piñar, W. Lubitz, and S. Rölleke, “An advanced molecular strategy to identify bacterial communities on art objects,” Journal of Microbiological Methods, vol. 45, no. 2, pp. 77–87, 2001. View at Publisher · View at Google Scholar
  26. G. Muyzer, E. C. de Waal, and A. G. Uitterlinden, “Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA,” Applied and Environmental Microbiology, vol. 59, no. 3, pp. 695–700, 1993. View at Google Scholar · View at Scopus
  27. M. Cardinale, L. Brusetti, P. Quatrini et al., “Comparison of different primer sets for use in automated ribosomal intergenic spacer analysis of complex bacterial communities,” Applied and Environmental Microbiology, vol. 70, no. 10, pp. 6147–6156, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. D. Daffonchio, S. Borin, G. Frova, P. L. Manachini, and C. Sorlini, “PCR fingerprinting of whole genomes, the spacers between the 16S and 23S rRNA genes and of intergenic tRNA gene regions reveal a different intraspecific genomic variability of Bacillus cereus and Bacillus licheniformis,” International Journal of Systematic Bacteriology, vol. 48, pp. 107–116, 1998. View at Google Scholar · View at Scopus
  29. J. M. Bric, R. M. Bostock, and S. E. Silverstone, “Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane,” Applied and Environmental Microbiology, vol. 57, no. 2, pp. 535–538, 1991. View at Google Scholar · View at Scopus
  30. F. Ahmad, I. Ahmad, and M. S. Khan, “Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities,” Microbiological Research, vol. 163, no. 2, pp. 173–181, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. J. C. Cappuccino and N. Sherman, “Negative staining,” in Microbiology: A Laboratory Manual, J. C. Cappuccino and N. Sherman, Eds., pp. 125–179, Benjamin/Cummings, Redwood City, Calif, USA, 3rd edition, 1992. View at Google Scholar
  32. P. Nielsen and J. Sørensen, “Multi-target and medium-independent fungal antagonism by hydrolytic enzymes in Paenibacillus polymyxa and Bacillus pumilus strains from barley rhizosphere,” FEMS Microbiology Ecology, vol. 22, no. 3, pp. 183–192, 1997. View at Publisher · View at Google Scholar · View at Scopus
  33. D. M. Penrose and B. R. Glick, “Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria,” Physiologia Plantarum, vol. 118, no. 1, pp. 10–15, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. F. Poly, L. J. Monrozier, and R. Bally, “Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil,” Research in Microbiology, vol. 152, no. 1, pp. 95–103, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. L. Lambertsen, C. Sternberg, and S. Molin, “Mini-Tn7 transposons for site-specific tagging of bacteria with fluorescent proteins,” Environmental Microbiology, vol. 6, no. 7, pp. 726–732, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. W. T. Liu, T. L. Marsh, H. Cheng, and L. J. Forney, “Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA,” Applied and Environmental Microbiology, vol. 63, no. 11, pp. 4516–4522, 1997. View at Google Scholar · View at Scopus
  37. M. M. Fisher and E. W. Triplett, “Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities,” Applied and Environmental Microbiology, vol. 65, no. 10, pp. 4630–4636, 1999. View at Google Scholar · View at Scopus
  38. C. A. Lozupone and R. Knight, “Global patterns in bacterial diversity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 27, pp. 11436–11440, 2007. View at Google Scholar
  39. K. Smalla, G. Wieland, A. Buchner et al., “Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed,” Applied and Environmental Microbiology, vol. 67, no. 10, pp. 4742–4751, 2001. View at Publisher · View at Google Scholar · View at Scopus
  40. T. M. Caton, L. R. Witte, H. D. Ngyuen, J. A. Buchheim, M. A. Buchheim, and M. A. Schneegurt, “Halotolerant aerobic heterotrophic bacteria from the Great Salt Plains of Oklahoma,” Microbial Ecology, vol. 48, no. 4, pp. 449–462, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. J. Tang, A. P. Zheng, E. S. P. Bromfield et al., “16S rRNA gene sequence analysis of halophilic and halotolerant bacteria isolated from a hypersaline pond in Sichuan, China,” Annals of Microbiology, vol. 61, no. 2, pp. 375–381, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. R. R. de la Haba, D. R. Arahal, M. C. Márquez, and A. Ventosa, “Phylogenetic relationships within the family Halomonadaceae based on comparative 23S and 16S rRNA gene sequence analysis,” International Journal of Systematic and Evolutionary Microbiology, vol. 60, no. 4, pp. 737–748, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. A. C. F. Dias, F. D. Andreote, F. Dini-Andreote et al., “Diversity and biotechnological potential of culturable bacteria from Brazilian mangrove sediment,” World Journal of Microbiology and Biotechnology, vol. 25, no. 7, pp. 1305–1311, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. K. A. El-Tarabily and T. Youssef, “Enhancement of morphological, anatomical and physiological characteristics of seedlings of the mangrove Avicennia marina inoculated with a native phosphate-solubilizing isolate of Oceanobacillus picturae under greenhouse conditions,” Plant and Soil, vol. 332, no. 1, pp. 147–162, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. B. E. Michel and M. R. Kaufmann, “The osmotic potential of polyethylene glycol 6000,” Plant Physiology, vol. 51, no. 5, pp. 914–917, 1973. View at Publisher · View at Google Scholar
  46. N. P. Hua, A. Hamza-Chaffai, R. H. Vreeland, H. Isoda, and T. Naganuma, “Virgibacillus salarius sp. nov., a halophilic bacterium isolated from a Saharan salt lake,” International Journal of Systematic and Evolutionary Microbiology, vol. 58, no. 10, pp. 2409–2414, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. T. Quesada, M. Aguilera, J. A. Morillo, A. Ramos-Cormenzana, and M. Monteoliva-Sánchez, “Virgibacillus olivae sp. nov., isolated from waste wash-water from processing of Spanish-style green olives,” International Journal of Systematic and Evolutionary Microbiology, vol. 57, no. 5, pp. 906–910, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. I. Romano, L. Lama, P. Orlando, B. Nicolaus, A. Giordano, and A. Gambacorta, “Halomonas sinaiensis sp. nov., a novel halophilic bacterium isolated from a salt lake inside Ras Muhammad Park, Egypt,” Extremophiles, vol. 11, no. 6, pp. 789–796, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. C. Sánchez-Porro, R. R. de la Haba, N. Soto-Ramírez, M. C. Márquez, R. Montalvo-Rodríguez, and A. Ventosa, “Description of Kushneria aurantia gen. nov., sp. nov., a novel member of the family Halomonadaceae, and a proposal for reclassification of Halomonas marisflavi as Kushneria marisflavi comb. nov., of Halomonas indalinina as Kushneria indalinina comb. nov. and of Halomonas avicenniae as Kushneria avicenniae comb. nov,” International Journal of Systematic and Evolutionary Microbiology, vol. 59, no. 2, pp. 397–405, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. N. Soto-Ramírez, C. Sánchez-Porro, S. Rosas et al., “Halomonas avicenniae sp. nov., isolated from the salty leaves of the black mangrove Avicennia germinans in Puerto Rico,” International Journal of Systematic and Evolutionary Microbiology, vol. 57, no. 5, pp. 900–905, 2007. View at Publisher · View at Google Scholar
  51. S. Compant, B. Duffy, J. Nowak, C. Clément, and E. A. Barka, “Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects,” Applied and Environmental Microbiology, vol. 71, no. 9, pp. 4951–4959, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Compant, C. Clément, and A. Sessitsch, “Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization,” Soil Biology and Biochemistry, vol. 42, no. 5, pp. 669–678, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. R. S. Redman, Y. O. Kim, C. J. D. A. Woodward et al., “Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change,” PLoS ONE, vol. 6, no. 7, Article ID e14823, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. S. Timmusk, V. Paalme, T. Pavlicek et al., “Bacterial distribution in the rhizosphere of wild barley under contrasting microclimates,” PLoS ONE, vol. 6, no. 3, Article ID e17968, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. M. A. Siddikee, P. S. Chauhan, R. Anandham, G. H. Han, and T. Sa, “Isolation, characterization, and use for plant growth promotion under salt stress, of ACC deaminase-producing halotolerant bacteria derived from coastal soil,” Journal of Microbiology and Biotechnology, vol. 20, no. 11, pp. 1577–1584, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. V. Sgroy, F. Cassán, O. Masciarelli, M. F. del Papa, A. Lagares, and V. Luna, “Isolation and characterization of endophytic plant growth-promoting (PGPB) or stress homeostasis-regulating (PSHB) bacteria associated to the halophyte Prosopis strombulifera,” Applied Microbiology and Biotechnology, vol. 85, no. 2, pp. 371–381, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Bacilio, H. Rodriguez, M. Moreno, J. P. Hernandez, and Y. Bashan, “Mitigation of salt stress in wheat seedlings by a gfp-tagged Azospirillum lipoferum,” Biology and Fertility of Soils, vol. 40, no. 3, pp. 188–193, 2004. View at Publisher · View at Google Scholar · View at Scopus
  58. B. Fan, X. H. Chen, A. Budiharjo, W. Bleiss, J. Vater, and R. Borriss, “Efficient colonization of plant roots by the plant growth promoting bacterium Bacillus amyloliquefaciens FZB42, engineered to express green fluorescent protein,” Journal of Biotechnology, vol. 151, no. 4, pp. 303–311, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. B. Fan, R. Borriss, W. Bleiss, and X. Wu, “Gram-positive rhizobacterium Bacillus amyloliquefaciens FZB42 colonizes three types of plants in different patterns,” Journal of Microbiology, vol. 50, no. 1, pp. 38–44, 2012. View at Publisher · View at Google Scholar