Isolation and characterization of rhizobia and plant growth-promoting rhizobacteria and their effects on growth of rice seedlings

American Journal of Agricultural and Biological Science

Volumn 9, Issue 3, 2014, Pages 342-360

  Tan, K Z ^a   Radziah, O ^a   Halimi, M S ^a   Khairuddin, A R ^b   Habib, S H ^a   Shamsuddin, Z H ^a  

^a UNIVERSITY PUTRA MALAYSIA   (Malaysia)

^b MALAYSIAN NUCLEAR AGENCY   (Malaysia)

Author keywords

Growth; PGPR; Rhizobia; Rice

Indexed keywords

EID: 84898654754     PISSN: 15574989     EISSN: 15574997     Source Type: Journal    
DOI: 10.3844/ajabssp.2014.342.360     Document Type: Article

References (82)

1. Adesemoye, A. O. and J. W. Kloepper, 2009. Plantmicrobes interactions in enhanced fertilizer-use efficiency. Applied Microbiol. Biotechnol., 85: 1-12. DOI: 10. 1007/s00248-009-9531-y.
2. Afzal, A. and B. Asghari, 2008. Rhizobium and phosphate solubilizing bacteria improve the yield and phosphorus uptake in wheat (Triticum aestivum L.). Int. J. Agri. Biol., 10: 1560-8530.
3. Ahmad, F., I. Ahmad and M. S. Khan, 2008. Screening of freeliving rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol. Res., 163: 173-181. DOI: 10. 1016/j. micres. 2006. 04. 001.
4. Ai'shah, O. N., H. G. Amir, C. L. Keng and A. R. Othman, 2010. Influence of various combinations of diazotrophs and chemical N fertilizer on plant growth and nitrogen fixation capacity of oil palm seedlings (Elaeis guineensis Jacq.). Thai J. Agric. Sci., 43: 139-149.
5. Alexander, D. B. and D. A. Zuberer, 1991. Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol. Fertil. Soil., 12: 39-45. DOI: 10. 1007/BF00369386.
6. Amir, H. G., Z. H. Shamsuddin, M. S. Halimi, M. F. Ramlan and M. Marziah, 1999. Potential use of rhizobacteria for sustainable oil palm seedling production. Malaysian J. Soil. Sci., 3: 39-50.
7. Amir, H. G., Z. H. Shamsuddin, M. S. Halimi, M. F. Ramlan and M. Marziah, 2003. Nitrogen fixation, nutrient accumulation and plant growth promotion by rhizobacteria in association with oil palm seedlings. Pak. J. Biol. Sci., 6: 1269-1272.
8. Amir, H. G., Z. H. Shamsuddin, M. S. Halimi, M. F. Ramlan and M. Marziah, 2005. Enhancement in nutrient accumulation and growth of oil palm seedlings caused by PGPR under field nursery conditions. Commun. Soil Sci. Plant Anal., 36: 2059-2066. DOI: 10. 1080/00103620500194270.
9. Anderson, F. N. and G. A. Peterson, 1978. Optimum starter fertilizer placement for sugarbeet seedlings as determined by uptake of radioactive 32P isotope. J. Am. Society Sugar Beet Technol., 20: 19-24.
10. Araujo, A. E. D. S., V. L. D. Baldani, P. D. S. Galisa, J. A. Pereira and J. I. Baldani, 2013. Response of traditional upland rice varieties to inoculation with selected diazotrophic bacteria isolated from rice cropped at the Northeast region of Brazil. Applied Soil. Ecol., 64: 49-55. DOI: 10. 1016/j. apsoil. 2012. 10. 004.
11. Asea, P. E. A., R. M. N. Kucey and J. W. B. Stewart, 1988. Inorganic phosphate solubilization by two Penicillium species in solution culture and soil. Soil Biol. Biochem., 20: 459-464. DOI: 10. 1016/0038-0717(88)90058-2.
12. Ashrafuzzaman, M., F. A. Hossen, M. R. Ismail, M. A. Hoque and M. Z. Islam et al., 2009. Efficiency of Plant Growth-Promoting Rhizobacteria (PGPR) for the enhancement of rice growth. African J. Biotechnol., 8: 1247-1252.
13. Barazani, O. Z. and J. Friedman, 1999. Is IAA the major root growth factor secreted from plant-growthmediating bacteria? J. Chemical Ecol., 10: 2397-2406. DOI: 10. 1023/A: 1020890311499.
14. Barton, C. J., 1948. Photometric analysis of phosphate rock. Anal. Chem., 20: 1068-1073. DOI: 10. 1021/ac60023a024.
15. Battacharjee, R. B., P. Jourand, C. Chaintreuil, B. Dreyfus, A. Singh and S. N. Mukhopadhyay, 2012. Indole acetic acid and ACC deaminase-producing Rhizobium leguminosarum bv. trifolii SN10 promote rice growth and in the process undergo colonization and chemotaxis. Biol. Fert. Soils, 48: 173-182. DOI: 10. 1007/s00374-011-0614-9.
16. Becker, M., K. H. Diekmann, J. K. Ladha, S. K. D. Datta and J. C. G. Ottow, 1991. Effect of NPK on growth and nitrogen fixation of Sesbania rostrata as a green manure for lowland rice (Oryza sativa L.). Plant Soil, 132: 149-158. DOI: 10. 1007/BF00011021.
17. Bhromsiri, C. and Bhromsiri, 2010. Isolation, screening of growth-promoting activities and diversity of rhizobacteria from vetiver grass and rice plants. Thai J. Agric. Sci., 43: 217-230.
18. Biswas, J. C., J. K. Ladha and F. B. Dazzo, 2000. Rhizobia inoculation improves nutrient uptake and growth of lowland rice. Soil Sci. Society Am. J., 64: 1644-1650. DOI: 10. 2136/sssaj2000. 6451644x.
19. Boddey, R. M., J. C. D. S. Moraes, B. J. R. Alves and S. Urquiaga, 1997. The contribution of biological nitrogen fixation for sustainable agricultural systems in the tropics. Soil Biol. Biochem., 29: 787-799. DOI: 10. 1016/S0038-0717(96)00221-0.
20. Boddey, R. M., O. C. D. Oliveira, S. Urquiga, V. M. Reis and F. L. D. Olivares et al., 1995. Biological nitrogen fixation associated with sugar cane and rice: Contributions and prospects for improvement. Plant Soil, 174: 195-209. DOI: 10. 1007/BF00032247.
21. Chabot, R., H. Antoun and M. P. Cescas, 1996. Growth promotion of maize and lettuce by phosphatesolubilizing Rhizobium leguminosarum biovar. phaseoli. Plant Soil, 184: 311-321. DOI: 10. 1007/BF00010460.
22. Chi, F., S. H. Shen, H. P. Cheng, Y. X. Jing and Y. G. Yanni et al., 2005. Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Applied Environ. Microbiol., 71: 7271-7278. DOI: 10. 1128/AEM. 71. 11. 7271-7278. 2005.
23. Dobereiner, J. and J. M. Day, 1975. Associative symbiosis in tropical grasses: Characterization of microorganisms and dinitrogen fixing sites. Proceedings of the 1st International Symposium on Nitrogen Fixation, (SNF' 75), Washington State University Press, Pullman, pp: 518-538.
24. Duangpaeng, A., P. Phetcharat, S. Chanthapho, N. Boonkantong and N. Okuda, 2012. The study and development of endophytic bacteria for enhancing organic rice growth. Procedia Eng., 32: 172-176. DOI: 10. 1016/j. proeng. 2012. 01. 1253.
25. Egamberdieva, D., F. Kamilova, S. Validov, L. Gafurova and Z. Kucharova et al., 2008. High incidence of plant growth-stimulating bacteria associated with the rhizosphere of wheat grown on salinated soil in Uzbekistan. Environ. Microbiol., 10: 1-9. DOI: 10. 1111/j. 1462-2920. 2007. 01424. x.
26. Egener, T., T. Hurek and B. Reinhold-Hurek, 1999. Endophytic expression of nif genes of Azoarcus sp. strain BH72 in rice roots. Molecular Plant-Microbe Interact., 12: 813-819. DOI: 10. 1094/MPMI. 1999. 12. 9. 813.
27. FAO., 2004. Food and Agriculture Organization. Rice is Life. Italy: FAO.
28. Farzana, Y., O. Radziah, S. Kamaruzaman and S. S. Mohd, 2007. Effect of PGPR inoculation on growth and yield of sweet potato. J. Biol. Sci., 7: 421-424. DOI: 10. 3923/jbs. 2007. 421. 424.
29. Farzana, Y., O. Radziah, S. Said and S. Kamaruzaman 2009. Growth and storage root development of sweetpotato inoculated with rhizobacteria under glasshouse conditions. Australian J. Basic Applied Sci., 3: 1461-1466.
30. Gordon, S. A. and R. P. Weber, 1951. Colorimetric estimation of indoleacetic acid. Plant Physiol., 26: 192-195. DOI: 10. 1104/pp. 26. 1. 192.
31. Halder, A. K. and P. K. Chakrabartty, 1993. Solubilization of inorganic phosphate by Rhizobium. Folia Microbiol., 38: 325-330. DOI: 10. 1007/BF02898602.
32. Hardy, R. W. F., R. D. Holsten, E. K. Jackson and R. C. Burns, 1968. The acetylene-ethylene assay for nitrogen fixation: Laboratory and field evaluation. Plant Physiol., 43: 1185-1207. DOI: 10. 1104/pp. 43. 8. 1185.
33. Hayat, R., R. A. Sheirdil, M. Iftikar-ul-Hassan and I. Ahmed, 2013. Characterization and identification of compost bacteria based on 16S rRNA gene sequencing. Ann. Microbiol., 63: 905-912. DOI: 10. 1007/s13213-012-0542-4.
34. Hu, X., J. Chen and J. Guo, 2006. Two phosphate-and potassium solubilizing bacteria isolated from Tianmu Mountain, Zhejiang, China. World J. Microbiol. Biotechnol., 22: 983-990. DOI: 10. 1007/s11274-006-9144-2.
35. Islam, M. R., T. Sultana, J. Cho, M. M. Joe and T. M. Sa, 2012. Diversity of free-living nitrogen-fixing bacteria associated with Korean paddy fields. Ann. Microbiol., 62: 1643-1650. DOI: 10. 1007/s13213-012-0421-z.
36. James, E. K., P. Gyaneshwar, N. Mathan, W. L. Barraquio and P. M. Reddy et al., 2002. Infection and colonization of rice seedlings by the plant growthpromoting bacterium Herbaspirillum seropedicae z67. Molecular Plant-Microbe Interact., 15: 894-906. DOI: 10. 1094/MPMI. 2002. 15. 9. 894.
37. Jha, Y. and R. B. Subramaniam, 2012. Isolation of root associated bacteria from the local variety of rice GJ-17. World Res. J. Geo Inform., 1: 21-26.
38. Kasana, R. C., R. Salwan, H. Dhar, S. Dutt and A. Gulati, 2008. A rapid and easy method for the detection of microbial cellulases on agar plates using Gram's iodine. Current Microbiol., 57: 503-507. DOI: 10. 1007/s00284-008-9276-8.
39. Katupitiya, S., J. Millet, M. Vesk, L. Viccars and A. Zeman et al., 1995. A mutant of Azospirillum brasilense Sp7 impaired in flocculation with a modified colonization pattern and superior nitrogen fixation in association with wheat. Applied Environ. Microbiol., 61: 1987-1995. PMID: 7646034.
40. Kennedy, I. R., A. T. M. A. Choudhury and M. L. Kecskes, 2004. Non-symbiotic bacterial diazotrophs in cropfarming systems: Can their potential for plant growth promotion be better exploited? Soil Biol. Biochem., 36: 1229-1244. DOI: 10. 1016/j. soilbio. 2004. 04. 006.
41. Keyeo, F., O. N. Ai'shah and H. G. Amir, 2011. The effects of nitrogen fixation activity and phytohormone production of diazotroph in promoting growth of rice seedlings. Biotechnology, 10: 267-273. DOI: 10. 3923/biotech. 2011. 267. 273.
42. Kloepper, J. W., C. Ryu and S. Zhang, 2004. Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology, 94: 1259-1266. DOI: 10. 1094/PHYTO. 2004. 94. 11. 1259, PMID: 18944464.
43. Kloepper, J. W., J. Leong, M. Teintze and M. N. Schroth, 1980. Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature, 286: 885-886. DOI: 10. 1038/286885a0.
44. Klonowska, A., C. Chaintreuil, P. Tisseyre, L. Miche, R. Melkonian and M. Ducousso et al., 2012. Biodiversity of Mimosa pudica rhizobial symbionts (Cupriavidus taiwanensis, Rhizobium mesoamericanum) in New Caledonia and their adaptation to heavy metal-rich soils. Microbiol. Ecol., 81: 618-635. DOI: 10. 1111/j. 1574-6941. 2012. 01393. x.
45. Kumar, K. V., S. Srivastava, N. Singh and H. M. Behl, 2009. Role of metal resistant plant growth promoting bacteria in ameliorating fly ash to the growth of Brassica juncea. J. Hazardous Materials, 170: 51-57. DOI: 10. 1016/j. jhazmat. 2009. 04. 132.
46. Liu, Y., L. Feng, H. Hu, G. Jiang and Z. Cai et al., 2012. Phosphorus release from low-grade phosphate rocks by low molecular weight organic acids. J. Food, Agric. Environ., 10: 1001-1007.
47. Lucy, M., E. Reed and B. R. Glick, 2004. Applications of free living plant growth-promoting rhizobacteria. Antonie Van Leeuwenhoek, 86: 1-25. DOI: 10. 1023/B: ANTO. 0000024903. 10757. 6e.
48. Lugtenberg, B. and F. Kamilova, 2009. Plant-growthpromoting rhizobacteria. Annual Rev. Microbiol., 63: 541-556. DOI: 10. 1146/annurev. micro. 62. 081307. 162918.
49. Malik, K. A., R. Bilal, S. Mehnaz, G. Rasul and M. S. Mirza et al., 1997. Association of nitrogen-fixing, Plant-Growth-Promoting Rhizobacteria (PGPR) with kallar grass and rice. Plant Soil, 194: 37-44. DOI: 10. 1023/A: 1004295714181.
50. Mia, M. A. B., Z. H. Shamsuddin and M. Mahmood, 2012. Effects of rhizobia and plant growth promoting bacteria inoculation on germination and seedling vigor of lowland rice. African J. Biotechnol., 11: 3758-3765. DOI: 10. 5897/AJB09. 1337.
51. Mia, M. A. B., Z. H. Shamsuddin, Z. Wahab and M. Marziah 2010a. Rhizobacteria as bioenhancer and biofertilizer for growth and yield of banana (Musa spp. cv. 'Berangan'). Scientia Horticulturae, 126: 80-87. DOI: 10. 1016/j. scienta. 2010. 06. 005.
52. Mia, M. A. B., Z. H. Shamsuddin, Z. Wahab and M. Marziah, 2009. The effect of rhizobacterial inoculation on growth and nutrient accumulation of tissue-cultured banana plantlets under low Nfertilizer regime. African J. Biotechnol., 8: 5855-5866.
53. Mia, M. A. B., Z. H. Shamsuddin, Z. Wahab and M. Marziah, 2010b. Effect of Plant Growth Promoting Rhizobacterial (PGPR) inoculation on growth and nitrogen incorporation of tissue-cultured Musa plantlets under nitrogen-free hydroponics condition. Aus. J. Crop Sci., 4: 85-90.
54. Naher, U. A., O. Radziah, Z. H. Shamsuddin, M. S. Halimi and I. M. Razi, 2009. Isolation of diazotrophs from different soils of Tanjong Karang rice growing area in Malaysia. Int. J. Agric. Biol., 11: 547-552.
55. Nautiyal, C. S., 1999. An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol. Lett., 170: 265-270. DOI: 10. 1111/j. 1574-6968. 1999. tb13383. x.
56. Ng, L. C., M. Sariah, O. Sariam, O. Radziah and M. A. Z. Abidin, 2012. Rice seed bacterization for promoting germination and seedling growth under aerobic cultivation system. Australian J. Crop Sci., 6: 170-175.
57. Nguyen, T. H. N., L. Brechenmacher, J. T. Aldrich, T. R. Clauss and M. A. Gritsenko et al., 2012. Quantitative phosphoproteomic analysis of soybean root hairs inoculated with bradyrhizobium japonicum. Molecular Cellular Proteom., 11: 1140-1155. DOI: 10. 1074/mcp. M112. 018028.
58. Panhwar, Q. A., O. Radziah, A. R. Zaharah, M. Sariah and I. M. Razi, 2012. Isolation and characterization of phosphate-solubilizing bacteria from aerobic rice. African J. Biotech., 11: 2711-2719. DOI: 10. 5897/AJB10. 2218.
59. Patten, C. L. and B. R. Glick, 2002. Role of Pseudomonas putida indoleaccetic acid in development of the host plant root system. Applied Environ. Microbiol., 68: 3795-3801. DOI: 10. 1128/AEM. 68. 8. 3795-3801. 2002.
60. Peng, S., J. C. Biswas, J. K. Ladha, P. Gyaneshwar and Y. Chen, 2002. Influence of rhizobial inoculation on photosynthesis and grain yield of rice. Agron. J., 94: 925-929. DOI: 10. 2134/agronj2002. 9250.
61. Perez, E., M. Sulbaran, M. M. Ball and L. A. Yarzabal, 2007. Isolation and characterization of mineral phosphate-solubilizing bacteria naturally colonizing a limonitic crust in the south-eastern Venezuelan region. Soil Biol. Biochem., 39: 2905-2914. DOI: 10. 1016/j. soilbio. 2007. 06. 017.
62. Pikovskaya, R. I., 1948. Mobilization of phosphorus in soil in connection with vital activity by some microbial species. Microbiologica, 17: 362-370.
63. Premalatha, P., 2006. Colonization of oryza sativa roots by plant growth-promoting rhizobacterium, Bacillus sphaericus UPMB10 and subsequent inoculant formulation. PhD Thesis, Universiti Putra Malaysia.
64. Ramachandran, K., V. Srinivasan, S. Hamza and M. Anandaraj, 2005. Phosphate solubilising bacteria isolated from the rhizosphere soil and its growth promotion on black pepper (Piper nigrum L.) cuttings. Proceedings of the 1st International Meeting on Microbial Phosphate Solubilization, (MPS' 03), Springer Netherlands, pp: 325-331. DOI: 10. 1007/978-1-4020-5765-6_51.
65. Ramamoorthy, V., R. Viswanathan, T. Raguchander, V. Prakasam and R. Samiyappan, 2001. Induction of systemic resistance by plant growth promoting rhizobacteria in crop plants against pests and diseases. Crop Protect., 20: 1-11. DOI: 10. 1016/S0261-2194(00)00056-9.
66. Rashid, M., S. Khalil, N. Ayub, S. Alam and F. Latif, 2004. Organic acids production and phosphate solubilization By Phosphate-Solubilizing Microorganisms (PSM) under in vitro conditions. Pak. J. Biol. Sci., 7: 187-196.
67. Reinhold-Hurek, B. and T. Hurek 1998. Life in grasses: Diazotrophic endophytes. Trend Microbiol., 6: 139-144. DOI: 10. 1016/S0966-842X(98)01229-3.
68. Ribeiro, C. M. and E. J. B. N. Cardoso, 2012. Isolation, selection and characterization of root-associated growth promoting bacteria in Brazil Pine (Araucaria angustifolia). Microbiol. Res., 167: 69-78. DOI: 10. 1016/j. micres. 2011. 03. 003.
69. Rodriguez, H. and R. Fraga, 1999. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Adv., 17: 319-339. DOI: 10. 1016/S0734-9750(99)00014-2.
70. Saharan, B. S. and V. Nehra, 2011. Plant growth promoting rhizobacteria: A critical review. Life Sci. Med. Res., 21: 1-29.
71. Schwyn, B. and J. B. Neilands, 1987. Universal chemical assay for the detection and determination of siderophores. Analytical Biochem., 160: 47-56. DOI: 10. 1016/0003-2697(87)90612-9.
72. Sitepu, I. R., Y. Hashidoko, E. Santoso and S. Tahara, 2007. Potent phosphate-solubilizing bacteria isolated from dipterocarps grown in peat swamp forest in central Kalimantan and their possible utilization for biorehabilitation of degraded peat swamp forest in Central Kalimantan. Proceedings of the International Symposium and Workshop on Tropical Peatland. Aug. 27-29, Yogyakarta, Indonesia.
73. Somasegaran, P. and H. J. Hoben, 1985. Methods in Legume-Rhizobium Technology. 1st Edn., University of Hawaii NifTAL Project and MIRCEN, pp: 367.
74. Sugumaran, P. and B. Janarthanam, 2007. Solubilization of potassium containing minerals by bacteria and their effect on plant growth. World J. Agric. Sci., 3: 350-355.
75. Suzuki, Y., D. Adhikari, K. Itoh and K. Suyama, 2014. Effects of temperature on competition and relative dominance of bradyrhizobium japonicum and bradyrhizobium elkanii in the process of soybean nodulation. Plant Soil, 374: 915-924. DOI: 10. 1007/s11104-013-1924-5.
76. Vargas, L., T. L. G. D. Carvalho, P. C. G. Ferreira, V. L. D. Baldani and J. I. Baldani et al., 2012. Early responses of rice (Oryza sativa L.) seedlings to inoculation with beneficial diazotrophic bacteria are dependent on plant and bacterial genotypes. Plant Soil, 356: 127-137. DOI: 10. 1007/s11104-012-1274-8.
77. Verma, S. C., J. K. Ladha and A. K. Tripathi, 2001. Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. J. Biotechnol., 91: 127-141. DOI: 10. 1016/S0168-1656(01)00333-9.
78. Vessey, J. K., 2003. Plant growth promoting rhizobacteria as biofertilizers. Plant Soil, 255: 571-586. DOI: 10. 1023/A: 1026037216893.
79. Yanni, Y. G., R. Y. Rizk, V. Corich, A. Squartini and K. Ninke et al., 1997. Natural endophytic association between Rhizobium leguminosarumbv. trifolii and rice roots and assessment of its potential to promote rice growth. Plant Soil, 194: 99-114. DOI: 10. 1023/A: 1004269902246.
80. Yogesh, K., K. K. Vamsi, B. Amol, G. Nikhil and T. Soham et al., 2009. Study of pectinase production in submerged fermentation using different isolates of Aspergillus Niger. Int. J. Microbiol. Res., 1: 13-17.
81. Zakry, F. A. A., M. S. Halimi, K. B. A. Rahim, H. A. Osumanu and S. K. Wong et al., 2010. Isolation and plant growth-promoting properties of rhizobacterial diazotrophs from pepper vine (Piper nigrum L.). Malays. Appl. Biol., 39: 41-45.
82. Zakry, F. A. A., Z. H. Shamsuddin, K. A. Rahim, Z. Z. Zakaria and A. A. Rahim, 2012. Inoculation of Bacillus sphaerichus UPMB-10 to young oil palm and measurement of its uptake of fixed nitrogen using the 15N isotope dilution technique. Microbes Environ., 27: 257-262. DOI: 10. 1264/jsme2. ME11309.