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http://dx.doi.org/10.4014/jmb.1101.01031

Genetic Diversity of Cultivable Plant Growth-Promoting Rhizobacteria in Korea  

Kim, Won-Il (Microbial Safety Division, National Academy of Agricultural Science, Rural Development Administration (RDA))
Cho, Won-Kyong (Department of Agricultural Biotechnology, College of Agriculture and Life Sciences, Seoul National University)
Kim, Su-Nam (Organic Agriculture Division, National Academy of Agricultural Science, Rural Development Administration (RDA))
Chu, Hyo-Sub (Bioindustrial Process Center, Jeonbuk Branch Institute of Korea Research Institute of Bioscience and Biotechnology (KRIBB))
Ryu, Kyoung-Yul (Microbial Safety Division, National Academy of Agricultural Science, Rural Development Administration (RDA))
Yun, Jong-Chul (Microbial Safety Division, National Academy of Agricultural Science, Rural Development Administration (RDA))
Park, Chang-Seuk (Department of Applied Biology and Environmental Sciences, Gyeongsang National University)
Publication Information
Journal of Microbiology and Biotechnology / v.21, no.8, 2011 , pp. 777-790 More about this Journal
Abstract
To elucidate the biodiversity of plant growth-promoting rhizobacteria (PGPR) in Korea, 7,638 bacteria isolated from the rhizosphere of plant species growing in many different regions were screened. A large number of PGPR were identified by testing the ability of each isolate to promote the growth of cucumber seedlings. After redundant rhizobacteria were removed via amplified rDNA restriction analysis, 90 strains were finally selected as PGPR. On the basis of 16S ribosomal RNA sequences, 68 Gram-positive (76%) and 22 Gram-negative (24%) isolates were assigned to 21 genera and 47 species. Of these genera, Bacillus (32 species) made up the largest complement, followed by Paenibacillus (19) and Pseudomonas (11). Phylogenetic analysis showed that most of the Grampositive PGPR fell into two categories: low- and high- G+C (Actinobacteria) strains. The Gram-negative PGPR were distributed in three categories: ${\alpha}$-proteobacteria, ${\beta}$- proteobacteria, and ${\gamma}$-proteobacteria. To our knowledge, this is the largest screening study designed to isolate diverse PGPR. The enlarged understanding of PGPR genetic diversity provided herein will expand the knowledge base regarding beneficial plant-microbe interactions. The outcome of this research may have a practical effect on crop production methodologies.
Keywords
PGPR; plant growth promotion; diversity; rhizobacteria; cucumber; rhizosphere;
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Times Cited By KSCI : 6  (Citation Analysis)
Times Cited By Web Of Science : 2  (Related Records In Web of Science)
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1 Adesemoye, A. O. and J. W. Kloepper. 2009. Plant-microbes interactions in enhanced fertilizer-use efficiency. Appl. Microbiol. Biotechnol. 85: 1-12.   DOI   ScienceOn
2 Lebeau, T., A. Braud, and K. Jézéquel. 2008. Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: A review. Environ. Pollut. 153: 497-522.   DOI   ScienceOn
3 Leon-Barrios, M., M. J. Lorite, J. Donate-Correa, and J. Sanjuan. 2009. Ensifer meliloti bv. lancerottense establishes nitrogenfixing symbiosis with Lotus endemic to the Canary Islands and shows distinctive symbiotic genotypes and host range. Syst. Appl. Microbiol. 32: 413-420.   DOI   ScienceOn
4 Caballero-Mellado, J., J. Onofre-Lemus, P. Estrada-de Los Santos, and L. Martinez-Aguilar. 2007. The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation. Appl. Environ. Microbiol. 73: 5308-5319.   DOI   ScienceOn
5 Caceres, E. A. R., G. G. Anta, J. R. Lopex, C. A. Di Ciocco, J. C. P. Basurco, and J. L. Parada. 1996. Response of field-grown wheat to inoculation with Azospirillum brasilense and Bacillus polymyxa in the semiarid region of Argentina. Arid Soil Res. Rehab. 10: 13-20.   DOI   ScienceOn
6 Choi, O., J. Kim, C. Ryu, and C. S. Park. 2004. Colonization and population changes of a biocontrol agent, Paenibacillus polymyxa E681, in seeds and roots. Plant Pathol. J. 20: 97-102.   DOI
7 Compant, S., B. Reiter, A. Sessitsch, J. Nowak, C. Clement, and E. Ait Barka. 2005. Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl. Environ. Microbiol. 71: 1685-1693.   DOI   ScienceOn
8 Dobereiner, J., S. Urquiaga, and R. M. Boddey. 1995. Alternatives for nitrogen nutrition of crops in tropical agriculture. Fertilizer Res. 42: 339-346.   DOI   ScienceOn
9 Dworkin, M. and J. Roster. 1958. Experiments with some microorganisms which utilize ethane and hydrogen. J. Bacteriol. 75: 592-601.
10 Gordon, S. A. and R. P. Weber. 1951. Colorimetric estimation of indole acetic acid. Plant Physiol. 26: 192-195.   DOI   ScienceOn
11 Gulati, A., P. Vyas, P. Rahi, and R. C. Kasana. 2009. Plant growth-promoting and rhizosphere-competent Acinetobacter rhizosphaerae strain BIHB 723 from the cold deserts of the Himalayas. Curr. Microbiol. 58: 371-377.   DOI   ScienceOn
12 Jaleel, C. A., P. Manivannan, B. Sankar, A. Kishorekumar, R. Gopi, R. Somasundaram, and R. Panneerselvam. 2007. Pseudomonas fluorescens enhances biomass yield and ajmalicine production in Catharanthus roseus under water deficit stress. Colloids Surf. B Biointerfaces 60: 7-11.   DOI   ScienceOn
13 Bloemberg, G. V. and B. J. Lugtenberg. 2001. Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr. Opin. Plant Biol. 4: 343-350.   DOI   ScienceOn
14 Barea, J. M., M. J. Pozo, R. Azcon, and C. Azcon-Aguilar. 2005. Microbial co-operation in the rhizosphere. J. Exp. Bot. 56: 1761-1778.   DOI   ScienceOn
15 Belimov, A. A., I. C. Dodd, N. Hontzeas, J. C. Theobald, V. I. Safronova, and W. J. Davies. 2009. Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signalling. New Phytol. 181: 413-423.   DOI   ScienceOn
16 Belimov, A. A., I. C. Dodd, V. I. Safronova, N. Hontzeas, and W. J. Davies. 2007. Pseudomonas brassicacearum strain Am3 containing 1-aminocyclopropane-1-carboxylate deaminase can show both pathogenic and growth-promoting properties in its interaction with tomato. J. Exp. Bot. 58: 1485-1495.   DOI   ScienceOn
17 Westerberg, K., A. M. Elvang, E. Stackebrandt, and J. K. Jansson. 2000. Arthrobacter chlorophenolicus sp. nov., a new species capable of degrading high concentrations of 4- chlorophenol. Int. J. Syst. Evol. Microbiol. 50: 2083-2092.   DOI   ScienceOn
18 Zhang, Z., S. Srichuwong, T. Kobayashi, M. Arakane, J. Y. Park, and K. Tokuyasu. 2010. Bioconversion of L-arabinose and other carbohydrates from plant cell walls to alpha-glucan by a soil bacterium, Sporosarcina sp. N52. Bioresour. Technol. 101: 9734-9741.   DOI   ScienceOn
19 Van Wees, S. C., S. Van der Ent, and C. M. Pieterse. 2008. Plant immune responses triggered by beneficial microbes. Curr. Opin. Plant Biol. 11: 443-448.   DOI   ScienceOn
20 Vivas, A., R. Azcon, B. Biro, J. M. Barea, and J. M. Ruiz- Lozano. 2003. Influence of bacterial strains isolated from leadpolluted soil and their interactions with arbuscular mycorrhizae on the growth of Trifolium pratense L. under lead toxicity. Can. J. Microbiol. 49: 577-588.   DOI   ScienceOn
21 Yadegari, M., H. A. Rahmani, G. Noormohammadi, and A. Ayneband. 2008. Evaluation of bean (Phaseolus vulgaris) seeds inoculation with Rhizobium phaseoli and plant growth promoting rhizobacteria on yield and yield components. Pak. J. Biol. Sci. 11: 1935-1939.   DOI   ScienceOn
22 Yan, Z., M. S. Reddy, and J. W. Kloepper. 2003. Survival and colonization of rhizobacteria in a tomato transplant system. Can. J. Microbiol. 49: 383-389.   DOI   ScienceOn
23 Yang, J., J. W. Kloepper, and C. M. Ryu. 2009. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 14: 1-4.   DOI   ScienceOn
24 Yeoung, S. B., S. J. Seung, S. P. Chang, and K. K. Hee. 1995. In vitro and greenhouse evaluation of cucumber growth enhanced by rhizosphere microorganisms. Plant Pathol. J. 11: 292-297.
25 Sheng, X. F., J. J. Xia, C. Y. Jiang, L. Y. He, and M. Qian. 2008. Characterization of heavy metal-resistant endophytic bacteria from rape (Brassica napus) roots and their potential in promoting the growth and lead accumulation of rape. Environ. Pollut. 156: 1164-1170.   DOI   ScienceOn
26 Zaidi, A., M. S. Khan, M. Ahemad, and M. Oves. 2009. Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiol. Immunol. Hung. 56: 263-284.   DOI   ScienceOn
27 Shaharoona, B., G. M. Jamro, Z. A. Zahir, M. Arshad, and K. S. Memon. 2007. Effectiveness of various Pseudomonas spp. and Burkholderia caryophylli containing ACC-deaminase for improving growth and yield of wheat (Triticum aestivum L.). J. Microbiol. Biotechnol. 17: 1300-1307.
28 Shen, Shun-Shan, Sin-Hyo Park, and Chang-Seuk Park. 2005. Enhancement of biocontrol efficacy of Serratia plymuthica A21-4 against phytophthora blight of pepper by improvement of inoculation buffer solution. Plant Pathol. J. 21: 68-72.   DOI
29 Shoebitz, M., C. M. Ribaudo, M. A. Pardo, M. L. Cantore, L. Ciampi, and J. A. Cura. 2009. Plant growth promoting properties of a strain of Enterobacter ludwigii isolated from Lolium perenne rhizosphere. Soil Biol. Biochem. 41: 1768-1774.   DOI   ScienceOn
30 Silby, M. W., A. M. Cerdeno-Tarraga, G. S. Vernikos, S. R. Giddens, R. W. Jackson, G. M. Preston, et al. 2009. Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens. Genome Biol. 10: R51.   DOI
31 Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599.   DOI   ScienceOn
32 Timmusk, S., V. Paalme, U. Lagercrantz, and E. Nevo. 2009. Detection and quantification of Paenibacillus polymyxa in the rhizosphere of wild barley (Hordeum spontaneum) with realtime PCR. J. Appl. Microbiol. 107: 736-745.   DOI   ScienceOn
33 Ryu, C. M., J. F. Murphy, K. S. Mysore, and J. W. Kloepper. 2004. Plant growth-promoting rhizobacteria systemically protect Arabidopsis thaliana against Cucumber Mosaic Virus by a salicylic acid and NPR1-independent and jasmonic aciddependent signaling pathway. Plant J. 39: 381-392.   DOI   ScienceOn
34 Trivedi, P., A. Pandey, and T. Sa. 2007. Chromate reducing and plant growth promoting activities of psychrotrophic Rhodococcus erythropolis MtCC 7905. J. Basic Microbiol. 47: 513-517.   DOI   ScienceOn
35 Ryan, R. P., S. Monchy, M. Cardinale, S. Taghavi, L. Crossman, M. B. Avison, G. Berg, D. van der Lelie, and J. M. Dow. 2009. The versatility and adaptation of bacteria from the genus Stenotrophomonas. Nat. Rev. Microbiol. 7: 514-525.   DOI   ScienceOn
36 Ryan, R. P., K. Germaine, A. Franks, D. J. Ryan, and D. N. Dowling. 2008. Bacterial endophytes: Recent developments and applications. FEMS Microbiol. Lett. 278: 1-9.   DOI   ScienceOn
37 Ryu, C. M., J. Kim, O. Choi, S. H. Kim, and C. S. Park. 2006. Improvement of biological control capacity of Paenibacillus polymyxa E681 by seed pelleting on sesame. Biol. Control 39: 282-289.   DOI   ScienceOn
38 Sachdev, D., P. Nema, P. Dhakephalkar, S. Zinjarde, and B. Chopade. 2010. Assessment of 16S rRNA gene-based phylogenetic diversity and promising plant growth-promoting traits of Acinetobacter community from the rhizosphere of wheat. Microbiol. Res. 165: 627-638.   DOI   ScienceOn
39 Sandhya, V., S. Z. Ali, B. Venkateswarlu, G. Reddy, and M. Grover. 2010. Effect of osmotic stress on plant growth promoting Pseudomonas spp. Arch. Microbiol. 192: 867-876.   DOI   ScienceOn
40 Saravanan, V. S., J. Osborne, M. Madhaiyan, L. Mathew, J. Chung, K. Ahn, and T. Sa. 2007. Zinc metal solubilization by Gluconacetobacter diazotrophicus and induction of pleomorphic cells. J. Microbiol. Biotechnol. 17: 1477-1482.
41 Schwyn, B. and J. B. Neilands. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160: 47-56.   DOI   ScienceOn
42 Seldin, L., A. S. Rosado, D. W. da Cruz, A. Nobrega, J. D. van Elsas, and E. Paiva. 1998. Comparison of Paenibacillus azotofixans strains isolated from rhizoplane, rhizosphere, and non-root-associated soil from maize planted in two different Brazilian soils. Appl. Environ. Microbiol. 64: 3860-3868.
43 Pikovskaya, R. I. 1948. Mobilization of phosphorous in soil in connection with the vital activity of some microbial species. Mikrobiologiya 17: 362-370.
44 Selim, S., J. Negrel, C. Govaerts, S. Gianinazzi, and D. van Tuinen. 2005. Isolation and partial characterization of antagonistic peptides produced by Paenibacillus sp. strain B2 isolated from the sorghum mycorrhizosphere. Appl. Environ. Microbiol. 71: 6501-6507.   DOI   ScienceOn
45 Nezarat, S. and A. Gholami. 2009. Screening plant growth promoting rhizobacteria for improving seed germination, seedling growth and yield of maize. Pak. J. Biol. Sci. 12: 26-32.   DOI   ScienceOn
46 Paul, D. and S. Nair. 2008. Stress adaptations in a plant growth promoting rhizobacterium (PGPR) with increasing salinity in the coastal agricultural soils. J. Basic Microbiol. 48: 378-384.   DOI   ScienceOn
47 Polz, M. F. and C. M. Cavanaugh. 1998. Bias in template-toproduct ratios in multitemplate PCR. Appl. Environ. Microbiol. 64: 3724-3730.
48 Probanza, A., J. L. Mateos, J. A. Lucas Garcia, B. Ramos, M. R. De Felipe, and F. J. Gutierrez Manero. 2001. Effects of inoculation with PGPR Bacillus and Pisolithus tinctorius on Pinus pinea L. growth, bacterial rhizosphere colonization, and mycorrhizal infection. Microb. Ecol. 41: 140-148.   DOI
49 Rasche, F., R. Trondl, C. Naglreiter, T. G. Reichenauer, and A. Sessitsch. 2006. Chilling and cultivar type affect the diversity of bacterial endophytes colonizing sweet pepper (Capsicum anuum L.). Can. J. Microbiol. 52: 1036-1045.   DOI   ScienceOn
50 Rasche, F., R. Trondl, C. Naglreiter, T. G. Reichenauer, and A. Sessitsch. 2006. Chilling and cultivar type affect the diversity of bacterial endophytes colonizing sweet pepper (Capsicum anuum L.). Can. J. Microbiol. 52: 1036-1045.   DOI   ScienceOn
51 Rodriguez, H. and R. Fraga. 1999. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Adv. 17: 319-339.   DOI
52 Liddycoat, S. M., B. M. Greenberg, and D. J. Wolyn. 2009. The effect of plant growth-promoting rhizobacteria on asparagus seedlings and germinating seeds subjected to water stress under greenhouse conditions. Can. J. Microbiol. 55: 388-394.   DOI   ScienceOn
53 Lucy, M., E. Reed, and B. R. Glick. 2004. Applications of free living plant growth-promoting rhizobacteria. Antonie Van Leeuwenhoek 86: 1-25.   DOI
54 Lugtenberg, B. and F. Kamilova. 2009. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63: 541-556.   DOI   ScienceOn
55 Madhaiyan, M., S. Poonguzhali, and T. Sa. 2007. Metal tolerating methylotrophic bacteria reduces nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon esculentum L.). Chemosphere 69: 220-228.   DOI   ScienceOn
56 Martin, N. I., H. Hu, M. M. Moake, J. J. Churey, R. Whittal, R. W. Worobo, and J. C. Vederas. 2003. Isolation, structural characterization, and properties of mattacin (polymyxin M), a cyclic peptide antibiotic produced by Paenibacillus kobensis M. J. Biol. Chem. 278: 13124-13132.   DOI
57 Karlidag, H., A. Esitken, M. Turan, and F. Sahin. 2007. Effects of root inoculation of plant growth promoting rhizobacteria (PGPR) on yield, growth and nutrient element contents of leaves of apple. Sci. Hortic. 114: 16-20.   DOI   ScienceOn
58 Montesinos, E., A. Bonaterra, E. Badosa, J. Frances, J. Alemany, I. Llorente, and C. Moragrega. 2002. Plant-microbe interactions and the new biotechnological methods of plant disease control. Int. Microbiol. 5: 169-175.   DOI   ScienceOn
59 Murphy, J. F., M. S. Reddy, C. M. Ryu, J. W. Kloepper, and R. Li. 2003. Rhizobacteria-mediated growth promotion of tomato leads to protection against Cucumber Mosaic Virus. Phytopathology 93: 1301-1307.   DOI   ScienceOn
60 Kang, S. H., H. S. Cho, H. Cheong, C. M. Ryu, J. F. Kim, and S. H. Park. 2007. Two bacterial entophytes eliciting both plant growth promotion and plant defense on pepper (Capsicum annuum L.). J. Microbiol. Biotechnol. 17: 96-103.
61 Khalid, A., M. Arshad, and Z. A. Zahir. 2004. Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J. Appl. Microbiol. 96: 473-480.   DOI   ScienceOn
62 Kloepper, J. W., R. M. Zablotowicz, E. M. Tipping, and R. Lifshitz. 1991. Plant growth promotion mediated by bacterial rhizosphere colonizers, pp. 315-326. In D. L. Keister and P. B. Cregan (eds.). The Rhizosphere and Plant Growth. Kluwer Academic Publishers, Dordrecht, The Netherlands.
63 Koo, S. Y. and K. S. Cho. 2009. Isolation and characterization of a plant growth-promoting rhizobacterium, Serratia sp. SY5. J. Microbiol. Biotechnol. 19: 1431-1438.
64 Kuklinsky-Sobral, J., W. L. Araujo, R. Mendes, I. O. Geraldi, A. A. Pizzirani-Kleiner, and J. L. Azevedo. 2004. Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ. Microbiol. 6: 1244-1251.   DOI   ScienceOn