Journal of Microbiology and Biotechnology
The Korean Society for Microbiology and Biotechnology publishes the Journal of Microbiology and Biotechnology.

2020 ; Vol.30-1: 118~126

AuthorArjun Adhikari, Ko-Eun Lee, Muhammad Aaqil Khan, Sang-Mo Kang, Bishnu Adhikari, Muhammad Imran, Rahmatullah Jan, Kyung-Min Kim, In-Jung Lee
Place of dutySchool of Applied Biosciences, Kyungpook National University, Daegu 41566, Republic of Korea
TitleEffect of Silicate and Phosphate Solubilizing Rhizobacterium Enterobacter ludwigii GAK2 on Oryza sativa L. under Cadmium Stress
PublicationInfo J. Microbiol. Biotechnol.2020 ; Vol.30-1
AbstractSilicon and phosphorus are elements that are beneficial for plant growth. Despite the abundant availability of silicate and phosphate in the Earth’s crust, crop nutritional requirements for silicon and phosphorus are normally met through the application of fertilizer. However, fertilizers are one of the major causes of heavy metal pollution. In our study, we aimed to assess silicate and phosphate solubilization by the bacteria Enterobacter ludwigii GAK2, in the presence and absence of phosphate [Ca3(PO4)2] or silicate (Mg2O8Si3), to counteract cadmium stress in rice (Oryza sativa L). Our results showed that the GAK2-treated rice plants, grown in soil amended with phosphate [Ca3(PO4)2] or silicate (Mg2O8Si3), had significantly reduced cadmium content, and enhanced plant growth promoting characteristics including fresh shoot and root weight, plant height, and chlorophyll content. These plants showed significant downregulation of the cadmium transporter gene, OsHMA2, and upregulation of the silicon carrier gene, OsLsi1. Moreover, jasmonic acid levels were significantly reduced in the GAK2-inoculated plants, and this was further supported by the downregulation of the jasmonic acid related gene, OsJAZ1. These results indicate that Enterobacter ludwigii GAK2 can be used as a silicon and phosphorus bio-fertilizer, which solubilizes insoluble silicate and phosphate, and mitigates heavy metal toxicity in crops.
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Key_wordCadmium, Enterobacter ludwigii GAK2, phosphorus, rice, silicon
References
  1. Khanna K, Jamwal VL, Gandhi SG, Ohri P, Bhardwaj R. 2019. Metal resistant PGPR lowered Cd uptake and expression of metal transporter genes with improved growth and photosynthetic pigments in Lycopersicon esculentum under metal toxicity. Sci. Rep. 9: 5855.
    Pubmed CrossRef Pubmed Central
  2. Rao K, Mohapatra M, Anand S, Venkateswarlu P. 2010. Review on cadmium removal from aqueous solutions. Int. J. Eng. Sci. Technol. 2.
    CrossRef
  3. Tóth G, Hermann T, Da Silva M, Montanarella L. 2016. Heavy metals in agricultural soils of the European Union with implications for food safety. Environ. Int. 88: 299-309.
    Pubmed CrossRef
  4. Yang X, Long X, Ye H, He Z, Calvert D, Stoffella P. 2004. Cadmium tolerance and hyperaccumulation in a new Znhyperaccumulating plant species (Sedum alfredii Hance). Plant Soil. 259: 181-189.
    CrossRef
  5. Sabiha J, Mehmood T, Chaudhry MM, Tufail M, Irfan N. 2009. Heavy metal pollution from phosphate rock used for the production of fertilizer in Pakistan. Microchem. J. 91: 94-99.
    CrossRef
  6. Su C. 2014. A review on heavy metal contamination in the soil worldwide: situation, impact and remediation techniques. Environmental Skeptics Critics. 3: 24-38.
  7. Clemens S. 2006. Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie. 88: 1707-1719.
    Pubmed CrossRef
  8. Aoshima K. 2012. [Itai-itai disease: cadmium-induced renal tubular osteomalacia]. Nihon Eiseigaku Zasshi. 67: 455-463.
    Pubmed CrossRef
  9. Mulligan CN, Yong RN, Gibbs BF. 2001. An evaluation of technologies for the heavy metal remediation of dredged sediments. J. Hazard. Mater. 85: 145-163.
    CrossRef
  10. Gu H-H, Qiu H, Tian T, Zhan S-S, Chaney RL, Wang S-Z, et al. 2011. Mitigation effects of silicon rich amendments on heavy metal accumulation in rice (Oryza sativa L.) planted on multi-metal contaminated acidic soil. Chemosphere 83: 1234-1240.
    Pubmed CrossRef
  11. Rajkumar M, Freitas H. 2008. Influence of metal resistantplant growth-promoting bacteria on the growth of Ricinus communis in soil contaminated with heavy metals. Chemosphere 71: 834-842.
    Pubmed CrossRef
  12. Rogalla H, Römheld V. 2002. Role of leaf apoplast in siliconmediated manganese tolerance of Cucumis sativus L. Plant Cell Environ. 25: 549-555.
    CrossRef
  13. Liang Y, Yang C, Shi H. 2001. Effects of silicon on growth and mineral composition of barley grown under toxic levels of aluminum. J. Plant Nutr. 24: 229-243.
    CrossRef
  14. Neumann D, Zur Nieden U. 2001. Silicon and heavy metal tolerance of higher plants. Phytochemistry 56: 685-692.
    CrossRef
  15. Nowakowski W, Nowakowska J. 1997. Silicon and copper interaction in the growth of spring wheat seedlings. Biologia Plantarum 39: 463-466.
    CrossRef
  16. Chen H, Zheng C, Tu C, Shen Z. 2000. Chemical methods and phytoremediation of soil contaminated with heavy metals. Chemosphere 41: 229-234.
    CrossRef
  17. Wang L, Wang Y, Chen Q, Cao W, Li M, Zhang F. 2000. Silicon induced cadmium tolerance of rice seedlings. J. Plant Nutr. 23: 1397-1406.
    CrossRef
  18. Shi Q, Bao Z, Zhu Z, He Y, Qian Q, Yu J. 2005. Siliconmediated alleviation of Mn toxicity in Cucumis sativus in relation to activities of superoxide dismutase and ascorbate peroxidase. Phytochemistry 66: 1551-1559.
    Pubmed CrossRef
  19. Shi G, Cai Q, Liu C, Wu L. 2010. Silicon alleviates cadmium toxicity in peanut plants in relation to cadmium distribution and stimulation of antioxidative enzymes. Plant Growth Regul. 61: 45-52.
    CrossRef
  20. Tubana BS, Babu T, Datnoff LE. 2016. A review of silicon in soils and plants and its role in US agriculture: history and future perspectives. Soil Sci. 181: 393-411.
    CrossRef
  21. Kumar A, Bahadur I, Maurya B, Raghuwanshi R, Meena V, Singh D, et al. 2015. Does a plant growth-promoting rhizobacteria enhance agricultural sustainability. J. Pure Appl. Microbiol. 9: 715-724.
  22. Nriagu JO, Moore P. 2012. Phosphate minerals, pp, 134-402. Ed. Springer Science & Business Media.
  23. Villalba G, Liu Y, Schroder H, Ayres RU. 2008. Global phosphorus flows in the industrial economy from a production perspective. J. Ind. Ecology. 12: 557-569.
    CrossRef
  24. Chowdhury RB, Moore GA, Weatherley AJ, Arora M. 2017. Key sustainability challenges for the global phosphorus resource, their implications for global food security, and options for mitigation. J. Clean. Prod. 140: 945-963.
    CrossRef
  25. Etesami H, Maheshwari DK. 2018. Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: Action mechanisms and future prospects. Ecotoxicol. Environ. Saf. 156: 225-246.
    Pubmed CrossRef
  26. Islam F, Yasmeen T, Ali Q, Ali S, Arif MS, Hussain S, et al. 2014. Influence of Pseudomonas aeruginosa as PGPR on oxidative stress tolerance in wheat under Zn stress. Ecotoxicol. Environ. Saf. 104: 285-293.
    Pubmed CrossRef
  27. Gupta P, Kumar V, Usmani Z, Rani R, Chandra A. 2018. Phosphate solubilization and chromium (VI) remediation potential of Klebsiella sp. strain CPSB4 isolated from the chromium contaminated agricultural soil. Chemosphere 192: 318-327.
    Pubmed CrossRef
  28. Adesemoye AO, Kloepper JW. 2009. Plant–microbes interactions in enhanced fertilizer-use efficiency. Appl. Microbiol. Biotechnol. 85: 1-12.
    Pubmed CrossRef
  29. Mukamuhirwa A, Persson Hovmalm H, Bolinsson H, Ortiz R, Nyamangyoku O, Johansson E. 2019. Concurrent drought and temperature stress in rice—a possible result of the predicted climate change: effects on yield attributes, eating characteristics, and health promoting compounds. Int. J. Environ. Res. Public Health 16: 1043.
    Pubmed CrossRef Pubmed Central
  30. Sun S, Zhou X, Li Z, Zhuang P. 2019. In vitro and in vivo testing to determine Cd bioaccessibility and bioavailability in contaminated rice in relation to mouse chow. Int. J. Environ. Res. Public Health 16: 871.
    Pubmed CrossRef Pubmed Central
  31. Farooq MA, Ali S, Hameed A, Ishaque W, Mahmood K, Iqbal Z. 2013. Alleviation of cadmium toxicity by silicon is related to elevated photosynthesis, antioxidant enzymes;suppressed cadmium uptake and oxidative stress in cotton. Ecotoxicol. Environ. Saf. 96: 242-249.
    Pubmed CrossRef
  32. Rizvi A, Khan MS. 2017. Biotoxic impact of heavy metals on growth, oxidative stress and morphological changes in root structure of wheat (Triticum aestivum L.) and stress alleviation by Pseudomonas aeruginosa strain CPSB1. Chemosphere 185: 942-952.
    Pubmed CrossRef
  33. Khan AR, Park G-S, Asaf S, Hong S-J, Jung BK, Shin J-H. 2017. Complete genome analysis of Serratia marcescens RSC-14: A plant growth-promoting bacterium that alleviates cadmium stress in host plants. PLoS One 12: e0171534.
    Pubmed CrossRef Pubmed Central
  34. Sharma RK, Archana G. 2016. Cadmium minimization in food crops by cadmium resistant plant growth promoting rhizobacteria. Appl. Soil Ecol. 107: 66-78.
    CrossRef
  35. Lee K-E, Adhikari A, Kang S-M, You Y-H, Joo G-J, Kim J-H, et al. 2019. Isolation and characterization of the high silicate and phosphate solubilizing novel strain enterobacter ludwigii GAK2 that promotes growth in rice plants. Agronomy 9: 144.
    CrossRef
  36. Kalra YP. 1995. Determination of pH of soils by different methods: collaborative study. J. AOAC Int. 78: 310-324.
  37. Kang S-M, Waqas M, Shahzad R, You Y-H, Asaf S, Khan MA, et al. 2017. Isolation and characterization of a novel silicate-solubilizing bacterial strain Burkholderia eburnea CS4-2 that promotes growth of japonica rice (Oryza sativa L. cv. Dongjin). Soil Sci. Plant Nutr. 63: 233-241.
    CrossRef
  38. Chan C-X, Teo S-S, Ho C-L, Othman RY, Phang S-M. 2004. Optimisation of RNA extraction from Gracilaria changii (Gracilariales, Rhodophyta). J. Appl. Phycology 16: 297-301.
    CrossRef
  39. Kim Y-H, Khan AL, Kim D-H, Lee S-Y, Kim K-M, Waqas M, et al. 2014. Silicon mitigates heavy metal stress by regulating P-type heavy metal ATPases, Oryza sativa low silicon genes, and endogenous phytohormones. BMC Plant Biol. 14: 13.
    Pubmed CrossRef Pubmed Central
  40. McCloud ES, Baldwin IT. 1997. Herbivory and caterpillar regurgitants amplify the wound-induced increases in jasmonic acid but not nicotine in Nicotiana sylvestris. Planta 203: 430-435.
    CrossRef
  41. Shahzad R, Waqas M, Khan AL, Asaf S, Khan MA, Kang S-M, et al. 2016. Seed-borne endophytic Bacillus amyloliquefaciens RWL-1 produces gibberellins and regulates endogenous phytohormones of Oryza sativa. Plant Physiol. Biochem. 106: 236-243.
    Pubmed CrossRef
  42. Ma JF, Yamaji N, Mitani N, Tamai K, Konishi S, Fujiwara T, et al. 2007. An efflux transporter of silicon in rice. Nature 448: 209-212.
    Pubmed CrossRef
  43. Tirado R, Allsopp M. 2012. Phosphorus in agriculture:problems and solutions. Greenpeace Research Laboratories Technical Report (Review). 2.
  44. Walpola BC, & Yoon MH. 2012. Prospectus of phosphate solubilizing microorganisms and phosphorus availability in agricultural soils: A review. Afr. J. Microbiol. Res. 37: 6600-6605.
  45. Naureen Z, Aqeel M, Hassan MN, Gilani SA, Bouqellah N, Mabood F, et al. 2015. Isolation and Screening of Silicate Bacteria from Various Habitats for Biological Control of Phytopathogenic Fungi. American J. Plant Sci. 6: 2850-2859.
    CrossRef
  46. Das P, Samantaray S, Rout G. 1997. Studies on cadmium toxicity in plants: a review. Environ. Pollut. 98: 29-36.
    CrossRef
  47. Metwally A, Safronova VI, Belimov AA, Dietz K-J. 2004. Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J. Exp. Bot. 56: 167-178.
    Pubmed CrossRef
  48. Rajkumar M, Sandhya S, Prasad MNV, Freitas H. 2012. Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol. Adv. 30: 1562-1574.
    Pubmed CrossRef
  49. Lee KE. 2015. Silicon absorption promoting effect of rice by Enterobacter ludwigii GAK2. Master’s Thesis. Kyungpook National University.
  50. Meharg A, Cairney JW. 1999. Co-evolution of mycorrhizal symbionts and their hosts to metal-contaminated environments. Adv. Ecol. Res. 30: 69-112.
    CrossRef
  51. Zaidi S, Usmani S, Singh BR, Musarrat J. 2006. Significance of Bacillus subtilis strain SJ-101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64: 991-997.
    Pubmed CrossRef
  52. Madhaiyan M, Poonguzhali S, Sa T. 2007. Metal tolerating methylotrophic bacteria reduces nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon esculentum L.). Chemosphere 69: 220-228.
    Pubmed CrossRef
  53. Kang SM, Khan AL, Waqas M, You YH, Hamayun M, Joo GJ, et al. 2015. Gibberellin-producing Serratia nematodiphila PEJ1011 ameliorates low temperature stress in Capsicum annuum L. Eur.J. Soil Biol. 68: 85-93.
    CrossRef
  54. TRAN TA, Popova LP. 2013. Functions and toxicity of cadmium in plants: recent advances and future prospects. Turkish J. Botany 37: 1-13.
  55. Govarthanan M, Mythili R, Selvankumar T, Kamala-Kannan S, Rajasekar A, Chang Y-C. 2016. Bioremediation of heavy metals using an endophytic bacterium Paenibacillus sp. RM isolated from the roots of Tridax procumbens. 3 Biotech. 6: 242.
    Pubmed CrossRef Pubmed Central
  56. Naidu R, Bolan N, Kookana RS, Tiller K. 1994. Ionicstrength and pH effects on the sorption of cadmium and the surface charge of soils. Eur. J. Soil Sci. 45: 419-429.
    CrossRef
  57. Li Z , L i L , C hen GPJ. 2005. B ioavailability o f C d i n a soil rice system in China: soil type versus genotype effects. Plant Soil 271: 165-173.
    CrossRef



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