Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

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)
  • Received : 2011.01.20
  • Accepted : 2011.05.12
  • Published : 2011.08.28
Download PDF
⟨ Previous Next ⟩

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

References

  1. Adesemoye, A. O. and J. W. Kloepper. 2009. Plant-microbes interactions in enhanced fertilizer-use efficiency. Appl. Microbiol. Biotechnol. 85: 1-12. https://doi.org/10.1007/s00253-009-2196-0
  2. 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. https://doi.org/10.1093/jxb/eri197
  3. 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. https://doi.org/10.1111/j.1469-8137.2008.02657.x
  4. 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. https://doi.org/10.1093/jxb/erm010
  5. 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. https://doi.org/10.1016/S1369-5266(00)00183-7
  6. 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. https://doi.org/10.1128/AEM.00324-07
  7. 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. https://doi.org/10.1080/15324989609381416
  8. 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. https://doi.org/10.5423/PPJ.2004.20.2.097
  9. 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. https://doi.org/10.1128/AEM.71.4.1685-1693.2005
  10. Dobereiner, J., S. Urquiaga, and R. M. Boddey. 1995. Alternatives for nitrogen nutrition of crops in tropical agriculture. Fertilizer Res. 42: 339-346. https://doi.org/10.1007/BF00750526
  11. Dworkin, M. and J. Roster. 1958. Experiments with some microorganisms which utilize ethane and hydrogen. J. Bacteriol. 75: 592-601.
  12. Gordon, S. A. and R. P. Weber. 1951. Colorimetric estimation of indole acetic acid. Plant Physiol. 26: 192-195. https://doi.org/10.1104/pp.26.1.192
  13. 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. https://doi.org/10.1007/s00284-008-9339-x
  14. 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. https://doi.org/10.1016/j.colsurfb.2007.05.012
  15. 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.
  16. 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. https://doi.org/10.1016/j.scienta.2007.04.013
  17. 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. https://doi.org/10.1046/j.1365-2672.2003.02161.x
  18. 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.
  19. 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.
  20. 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. https://doi.org/10.1111/j.1462-2920.2004.00658.x
  21. 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. https://doi.org/10.1016/j.envpol.2007.09.015
  22. 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. https://doi.org/10.1016/j.syapm.2009.04.003
  23. 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. https://doi.org/10.1139/W08-144
  24. Lucy, M., E. Reed, and B. R. Glick. 2004. Applications of free living plant growth-promoting rhizobacteria. Antonie Van Leeuwenhoek 86: 1-25. https://doi.org/10.1023/B:ANTO.0000024903.10757.6e
  25. Lugtenberg, B. and F. Kamilova. 2009. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63: 541-556. https://doi.org/10.1146/annurev.micro.62.081307.162918
  26. 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. https://doi.org/10.1016/j.chemosphere.2007.04.017
  27. 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. https://doi.org/10.1074/jbc.M212364200
  28. 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. https://doi.org/10.1007/s10123-002-0085-9
  29. 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. https://doi.org/10.1094/PHYTO.2003.93.10.1301
  30. 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. https://doi.org/10.3923/pjbs.2009.26.32
  31. 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. https://doi.org/10.1002/jobm.200700365
  32. Pikovskaya, R. I. 1948. Mobilization of phosphorous in soil in connection with the vital activity of some microbial species. Mikrobiologiya 17: 362-370.
  33. Polz, M. F. and C. M. Cavanaugh. 1998. Bias in template-toproduct ratios in multitemplate PCR. Appl. Environ. Microbiol. 64: 3724-3730.
  34. 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. https://doi.org/10.1007/s002480000081
  35. 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. https://doi.org/10.1139/w06-059
  36. 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. https://doi.org/10.1139/w06-059
  37. Rodriguez, H. and R. Fraga. 1999. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Adv. 17: 319-339. https://doi.org/10.1016/S0734-9750(99)00014-2
  38. 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. https://doi.org/10.1038/nrmicro2163
  39. 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. https://doi.org/10.1111/j.1574-6968.2007.00918.x
  40. 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. https://doi.org/10.1111/j.1365-313X.2004.02142.x
  41. 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. https://doi.org/10.1016/j.biocontrol.2006.04.014
  42. 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. https://doi.org/10.1016/j.micres.2009.12.002
  43. 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. https://doi.org/10.1007/s00203-010-0613-5
  44. 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.
  45. Schwyn, B. and J. B. Neilands. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160: 47-56. https://doi.org/10.1016/0003-2697(87)90612-9
  46. 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.
  47. 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. https://doi.org/10.1128/AEM.71.11.6501-6507.2005
  48. 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.
  49. 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. https://doi.org/10.5423/PPJ.2005.21.1.068
  50. 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. https://doi.org/10.1016/j.envpol.2008.04.007
  51. 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. https://doi.org/10.1016/j.soilbio.2007.12.031
  52. 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. https://doi.org/10.1186/gb-2009-10-5-r51
  53. 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. https://doi.org/10.1093/molbev/msm092
  54. 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. https://doi.org/10.1111/j.1365-2672.2009.04265.x
  55. 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. https://doi.org/10.1002/jobm.200700224
  56. 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. https://doi.org/10.1016/j.pbi.2008.05.005
  57. 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. https://doi.org/10.1139/w03-073
  58. 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. https://doi.org/10.1099/00207713-50-6-2083
  59. 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. https://doi.org/10.3923/pjbs.2008.1935.1939
  60. 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. https://doi.org/10.1139/w03-051
  61. Yang, J., J. W. Kloepper, and C. M. Ryu. 2009. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 14: 1-4. https://doi.org/10.1016/j.tplants.2008.10.004
  62. 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.
  63. 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. https://doi.org/10.1556/AMicr.56.2009.3.6
  64. 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. https://doi.org/10.1016/j.biortech.2010.07.092

Cited by

  1. Draft Genome Sequence of Pantoea ananatis B1-9, a Nonpathogenic Plant Growth-Promoting Bacterium vol.194, pp.3, 2011, https://doi.org/10.1128/jb.06484-11
  2. Growth Promotion of Pepper Plants by Pantoea ananatis B1-9 and its Efficient Endophytic Colonization Capacity in Plant Tissues vol.28, pp.3, 2011, https://doi.org/10.5423/ppj.oa.02.2012.0026
  3. Draft Genome Sequence of Plant Growth-Promoting Rhizobacterium Pantoea sp. Strain AS-PWVM4 vol.1, pp.6, 2011, https://doi.org/10.1128/genomea.00947-13
  4. Analysis of the Pantoea ananatis pan-genome reveals factors underlying its ability to colonize and interact with plant, insect and vertebrate hosts vol.15, pp.1, 2014, https://doi.org/10.1186/1471-2164-15-404
  5. Antifungal Activity of Paenibacillus kribbensis Strain T-9 Isolated from Soils against Several Plant Pathogenic Fungi vol.30, pp.1, 2014, https://doi.org/10.5423/ppj.oa.05.2013.0052
  6. Culturable diversity and functional annotation of psychrotrophic bacteria from cold desert of Leh Ladakh (India) vol.31, pp.1, 2011, https://doi.org/10.1007/s11274-014-1768-z
  7. Rizospheric Microbiota of Espeletia spp. from Santa Inés and Frontino-Urrao Paramos in Antioquia, Colombia vol.20, pp.1, 2011, https://doi.org/10.15446/abc.v20n1.42827
  8. Plant Growth Promoting Rhizobacteria and Silicon Synergistically Enhance Salinity Tolerance of Mung Bean vol.7, pp.None, 2011, https://doi.org/10.3389/fpls.2016.00876
  9. Plant growth-promoting potential of endophytic bacteria isolated from roots of wild Dodonaea viscosa L. vol.81, pp.3, 2017, https://doi.org/10.1007/s10725-016-0216-5
  10. Desert plant bacteria reveal host influence and beneficial plant growth properties vol.13, pp.12, 2011, https://doi.org/10.1371/journal.pone.0208223
  11. Genome analysis of Paenibacillus polymyxa A18 gives insights into the features associated with its adaptation to the termite gut environment vol.9, pp.None, 2011, https://doi.org/10.1038/s41598-019-42572-5
  12. Development and Application of Low-Cost and Eco-Sustainable Bio-Stimulant Containing a New Plant Growth-Promoting Strain Kosakonia pseudosacchari TL13 vol.11, pp.None, 2011, https://doi.org/10.3389/fmicb.2020.02044
  13. Plant growth‐promoting endophytic bacteria augment growth and salinity tolerance in rice plants vol.22, pp.5, 2011, https://doi.org/10.1111/plb.13124
  14. Thermotolerance effect of plant growth-promoting Bacillus cereus SA1 on soybean during heat stress vol.20, pp.None, 2020, https://doi.org/10.1186/s12866-020-01822-7
  15. The Diversity of Culture-Dependent Gram-Negative Rhizobacteria Associated with Manihot esculenta Crantz Plants Subjected to Water-Deficit Stress vol.13, pp.8, 2011, https://doi.org/10.3390/d13080366