Journal of Ginseng Research

The Korean Society of Ginseng (고려인삼학회)
권호 표지
DOI QR코드

DOI QR Code

Siderophore-producing rhizobacteria reduce heavy metal-induced oxidative stress in Panax ginseng Meyer

  • Huo, Yue (Department of Oriental Medicinal Biotechnology, College of Life Sciences, Kyung Hee University) ;
  • Kang, Jong Pyo (Graduate School of Biotechnology, College of Life Sciences, Kyung Hee University) ;
  • Ahn, Jong Chan (Graduate School of Biotechnology, College of Life Sciences, Kyung Hee University) ;
  • Kim, Yeon Ju (Department of Oriental Medicinal Biotechnology, College of Life Sciences, Kyung Hee University) ;
  • Piao, Chun Hong (College of Food Science and Engineering, Jilin Agricultural University) ;
  • Yang, Dong Uk (Department of Oriental Medicinal Biotechnology, College of Life Sciences, Kyung Hee University) ;
  • Yang, Deok Chun (Department of Oriental Medicinal Biotechnology, College of Life Sciences, Kyung Hee University)
  • Received : 2019.07.27
  • Accepted : 2019.12.30
  • Published : 2021.03.01
Download PDF
⟨ Previous Next ⟩

Abstract

Background: Panax ginseng is one of the most important medicinal plants and is usually harvested after 5 to 6 years of cultivation in Korea. Heavy metal (HM) exposure is a type of abiotic stress that can induce oxidative stress and decrease the quality of the ginseng crop. Siderophore-producing rhizobacteria (SPR) may be capable of bioremediating HM contamination. Methods: Several isolates from ginseng rhizosphere were evaluated by in vitro screening of their plant growth-promoting traits and HM resistance. Subsequently, in planta (pot tests) and in vitro (medium tests) were designed to investigate the SPR ability to reduce oxidative stress and enhance HM resistance in P. ginseng inoculated with the SPR candidate. Results: In vitro tests revealed that the siderophore-producing Mesorhizobium panacihumi DCY119T had higher HM resistance than the other tested isolates and was selected as the SPR candidate. In the planta experiments, 2-year-old ginseng seedlings exposed to 25 mL (500 mM) Fe solution had lower biomass and higher reactive oxygen species level than control seedlings. In contrast, seedlings treated with 108 CFU/mL DCY119T for 10 minutes had higher biomass and higher levels of antioxidant genes and nonenzymatic antioxidant chemicals than untreated seedlings. When Fe concentration in the medium was increased, DCY119T can produce siderophores and scavenge reactive oxygen species to reduce Fe toxicity in addition to providing indole-3-acetic acid to promote seedling growth, thereby conferring inoculated ginseng with HM resistance. Conclusions: It was confirmed that SPR DCY119T can potentially be used for bioremediation of HM contamination.

Keywords

Acknowledgement

This study was supported by a grant from the Korea Institute of Planning & Evaluation for Technology in Food, Agriculture, Forestry, & Fisheries (KIPET NO: 317007-3), Republic of Korea.

References

  1. Kim JH. Pharmacological and medical applications of Panax ginseng and ginsenosides: a review for use in cardiovascular diseases. J Ginseng Res 2018;42: 264-9. https://doi.org/10.1016/j.jgr.2017.10.004
  2. Lee JI, Park KS, Cho IH. Panax ginseng: a candidate herbal medicine for autoimmune disease. J Ginseng Res 2019;43:342-8. https://doi.org/10.1016/j.jgr.2018.10.002
  3. Kim YJ, Zhang D, Yang DC. Biosynthesis and biotechnological production of ginsenosides. Biotechnol Adv 2015;33:717-35. https://doi.org/10.1016/j.biotechadv.2015.03.001
  4. Nguyen NL, Kim YJ, Hoang VA, Subramaniyam S, Kang JP, Kang CH, Yang DC. Bacterial diversity and community structure in Korean ginseng field soil are shifted by cultivation Time. PloS One 2016;11:e0155055. https://doi.org/10.1371/journal.pone.0155055
  5. Etesami H, Maheshwari DK. Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: action mechanisms and future prospects. Ecotox Environ Safe 2018;156:225-46. https://doi.org/10.1016/j.ecoenv.2018.03.013
  6. Huo Y, Kang JP, Kim YJ, Yang DC. Paraburkholderia panacihumi sp. nov., an isolate from ginseng-cultivated soil, is antagonistic against root rot fungal pathogen. Arch Microbiol 2018;200:1151-8. https://doi.org/10.1007/s00203-018-1530-2
  7. Sukweenadhi J, Kim YJ, Lee KJ, Koh SC, Hoang VA, Nguyen NL, Yang DC. Paenibacillus yonginensis sp. nov., a potential plant growth promoting bacterium isolated from humus soil of Yongin forest. Antonie Van Leeuwenhoek 2014;106:935-45. https://doi.org/10.1007/s10482-014-0263-8
  8. Farh MEA, Kim YJ, Hoang VA, Sukweenadhi J, Singh P, Huq MA, Yang DC. Burkholderia ginsengiterrae sp. nov. and Burkholderia panaciterrae sp. nov., antagonistic bacteria against root rot pathogen Cylindrocarpon destructans, isolated from ginseng soil. Arch Microbiol 2015;197:439-47. https://doi.org/10.1007/s00203-014-1075-y
  9. Ali H, Khan E, Ilahi I. Environmental chemistry and ecotoxicology of hazardous heavy metals: environmental persistence, toxicity, and bioaccumulation. J Chem 2019;2019:1-14.
  10. Gautam PK, Gautam RK, Banerjee S, Chattopadhyaya MC, Pandey JD. Heavy metals in the environment: fate, transport, toxicity and remediation technologies. Nova Sci Publishers 2016;60:101-30.
  11. Mishra J, Singh R, Arora NK. Alleviation of heavy metal stress in plants and remediation of soil by rhizosphere microorganisms. Front Microbiol 2017;8:1706. https://doi.org/10.3389/fmicb.2017.01706
  12. Ojuederie OB, Babalola OO. Microbial and plant-assisted bioremediation of heavy metal polluted environments: a review. Int J Environ Res Public Health 2017;14:1504. https://doi.org/10.3390/ijerph14121504
  13. Huo Y, Kang JP, Park JK, Li J, Chen L, Yang DC. Rhodanobacter ginsengiterrae sp. nov., an antagonistic bacterium against root rot fungal pathogen Fusarium solani, isolated from ginseng rhizospheric soil. Arch Microbiol 2018;200:1457-63. https://doi.org/10.1007/s00203-018-1560-9
  14. Maheshwari R, Bhutani N, Suneja P. Screening and characterization of siderophore producing endophytic bacteria from Cicer arietinum and Pisum sativum plants. J Appl Biol Biotechnol 2019;7:7-14.
  15. Wang Z, Xu G, Ma P, Lin Y, Yang X, Cao C. Isolation and characterization of a phosphorus-solubilizing bacterium from rhizosphere soils and its colonization of Chinese cabbage (Brassica campestris ssp. chinensis). Front Microbiol 2017;8:1270. https://doi.org/10.3389/fmicb.2017.01270
  16. Kang JP, Huo Y, Kim YJ, Ahn JC, Hurh J, Yang DU, Yang DC. Rhizobium panacihumi sp. nov., an isolate from ginseng-cultivated soil, as a potential plant growth promoting bacterium. Arch Microbiol 2019;201:99-105. https://doi.org/10.1007/s00203-018-1578-z
  17. Gupta K, Chatterjee C, Gupta B. Isolation and characterization of heavy metal tolerant Gram-positive bacteria with bioremedial properties from municipal waste rich soil of Kestopur canal (Kolkata), West Bengal, India. Biologia 2012;67:827-36. https://doi.org/10.2478/s11756-012-0099-5
  18. Paudyal S, Aryal RR, Chauhan S, Maheshwari D. Effect of heavy metals on growth of Rhizobium strains and symbiotic efficiency of two species of tropical legumes. Sci World 2007;5:27-32.
  19. Oaikhena EE, Makaije DB, Denwe SD, Namadi MM, Haroun AA. Bioremediation potentials of heavy metal tolerant bacteria isolated from petroleum refinery effluent. Am J Environ Protect 2016;5:29-34. https://doi.org/10.11648/j.ajep.20160502.12
  20. Egler M, Grosse C, Grass G, Nies DH. Role of the extracytoplasmic function protein family sigma factor RpoE in metal resistance of Escherichia coli. J Bacteriol 2005;187:2297-307. https://doi.org/10.1128/JB.187.7.2297-2307.2005
  21. Fones HN, McCurrach H, Mithani A, Smith JAC, Preston GM. Local adaptation is associated with zinc tolerance in Pseudomonas endophytes of the metal-hyperaccumulator plant Noccaea caerulescens. Proc R Soc B-Biol Sci 2016;283:20160648. https://doi.org/10.1098/rspb.2016.0648
  22. Jeon YH, Kim YH. Differential structural responses of ginseng root tissues to different initial inoculum levels of Paenibacillus polymyxa GBR-1. Plant Pathol J 2008;24:352-6. https://doi.org/10.5423/PPJ.2008.24.3.352
  23. Wang QX, Xu CL, Sun H, Ma L, Li L, Zhang DD, Zhang YY. Analysis of the relationship between rusty root incidences and soil properties in Panax ginseng. In: IOP conference series: earth and environmental science, vol. 41. IOP Publishing; 2016, 012001.
  24. Nxele X, Klein A, Ndimba BK. Drought and salinity stress alters ROS accumulation, water retention, and osmolyte content in sorghum plants. S Afr J Bot 2017;108:261-6. https://doi.org/10.1016/j.sajb.2016.11.003
  25. Wang CJ, Yang W, Wang C, Gu C, Niu DD, Liu HX, Wang YP, Guo JH. Induction of drought tolerance in cucumber plants by a consortium of three plant growth-promoting rhizobacterium strains. PLoS One 2012;7:e52565. https://doi.org/10.1371/journal.pone.0052565
  26. Rejeb KB, Benzarti M, Debez A, Bailly C, Savoure A, Abdelly C. NADPH oxidasedependent H2O2 production is required for salt-induced antioxidant defense in Arabidopsis thaliana. J Plant Physiol 2015;174:5-15. https://doi.org/10.1016/j.jplph.2014.08.022
  27. Ali MB, Hahn EJ, Paek KY. CO2-induced total phenolics in suspension cultures of Panax ginseng CA Mayer roots: role of antioxidants and enzymes. Plant Physiol Biochem 2005;43:449-57. https://doi.org/10.1016/j.plaphy.2005.03.005
  28. Farokhzad A, Nobakht S, Alahveran A, Sarkhosh A, Mohseniazar M. Biochemical changes in terminal buds of three different walnut (Juglans regia L.) genotypes during dormancy break. Biochem Syst Ecol 2018;76:52-7. https://doi.org/10.1016/j.bse.2017.12.002
  29. Jin Y, Kim YJ, Jeon JN, Wang C, Min JW, Noh HY, Yang DC. Effect of white, red and black ginseng on physicochemical properties and ginsenosides. Plant Food Hum Nutr 2015;70:141-5. https://doi.org/10.1007/s11130-015-0470-0
  30. Liu J, Wang Q, Sun M, Zhu L, Yang M, Zhao Y. Selection of reference genes for quantitative real-time PCR normalization in Panax ginseng at different stages of growth and in different organs. PLoS One 2014;9:e112177. https://doi.org/10.1371/journal.pone.0112177
  31. Liu C, Pan TM. In vitro effects of lactic acid bacteria on cancer cell viability and antioxidant activity. J Food Drug Anal 2010;18:77-86.
  32. Hansda A, Kumar V, Anshumali A, Usmani Z. Phytoremediation of heavy metals contaminated soil using plant growth promoting rhizobacteria (PGPR): a current perspective. Recent Res Sci Technol 2014;6:131-4.
  33. Tirry N, Joutey NT, Sayel H, Kouchou A, Bahafid W, Asri M, El Ghachtouli N. Screening of plant growth promoting traits in heavy metals resistant bacteria: prospects in phytoremediation. J Genet Eng Biotechnol 2018;16:613-9. https://doi.org/10.1016/j.jgeb.2018.06.004
  34. Chatterjee C, Gopal R, Dube BK. Impact of iron stress on biomass, yield, metabolism and quality of potato (Solanum tuberosum L.). Sci Hortic 2006;108:1-6. https://doi.org/10.1016/j.scienta.2006.01.004
  35. Rahman M, Punja ZK. Biochemistry of ginseng root tissues affected by rusty root symptoms. Plant Physiol Biochem 2005;43:1103-14. https://doi.org/10.1016/j.plaphy.2005.09.004
  36. Ghani A. Toxic effects of heavy metals on plant growth and metal accumulation in maize (Zea maysL.). Iranian J Toxi 2010;4:325-34.
  37. Sayyed RZ, Gangurde NS, Patel PR, Josh SA, Chincholkar SB. Siderophore production by Alcaligenes faecalis and its application for growth promotion in Arachis hypogaea. Indian J Microbiol 2010;9:302-7.
  38. Saha M, Sarkar S, Sarkar B, Sharma BK, Bhattacharjee S, Tribedi P. Microbial siderophores and their potential applications: a review. Environ Sci Pollut Res 2016;23:3984-99. https://doi.org/10.1007/s11356-015-4294-0
  39. Farh MEA, Kim YJ, Sukweenadhi J, Singh P, Yang DC. Aluminium resistant, plant growth promoting bacteria induce overexpression of Aluminium stress related genes in Arabidopsis thaliana and increase the ginseng tolerance against Aluminium stress. Microbiol Res 2017;200:45-52. https://doi.org/10.1016/j.micres.2017.04.004
  40. Sukweenadhi J, Balusamy SR, Kim YJ, Lee CH, Kim YJ, Koh SC, Yang DC. A growth promoting bacteria, Paenibacillus yonginensis DCY84T enhanced salt stress tolerance by activating defense-related systems in Panax ginseng. Front Plant Sci 2018;9:813. https://doi.org/10.3389/fpls.2018.00813
  41. Nadeem SM, Ahmad M, Zahir ZA, Javaid A, Ashraf M. The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol Adv 2014;32:429-48. https://doi.org/10.1016/j.biotechadv.2013.12.005
  42. Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 2010;48:909-30. https://doi.org/10.1016/j.plaphy.2010.08.016
  43. You J, Chan Z. ROS regulation during abiotic stress responses in crop plants. Front Plant Sci 2015;6:1092.
  44. Hu T, Chen K, Hu L, Amombo E, Fu J. H2O2 and Ca2+-based signaling and associated ion accumulation, antioxidant systems and secondary metabolism orchestrate the response to NaCl stress in perennial ryegrass. Sci Rep 2016;6:36396. https://doi.org/10.1038/srep36396
  45. de Oliveira JG, Cambraia J, Ribeiro C, de Oliveira JA, de Paula SO, Olivan MA. Impact of iron toxicity on oxidative metabolism in young Eugenia uniflora L. plants. Acta Physiol Plant 2013;35:1645-57. https://doi.org/10.1007/s11738-012-1207-4
  46. GU Chibuike, Obiora SC. Heavy metal polluted soils: effect on plants and bioremediation methods. Appl Environ Soil Sci 2014;2014:1-12.
  47. Vardharajula S, Zulfikar Ali S, Grover M, Reddy G, Bandi V. Drought-tolerant plant growth promoting Bacillus spp.: effect on growth, osmolytes, and antioxidant status of maize under drought stress. J Plant Interact 2011;6:1-14. https://doi.org/10.1080/17429145.2010.535178
  48. Etesami H. Bacterial mediated alleviation of heavy metal stress and decreased accumulation of metals in plant tissues: mechanisms and future prospects. Ecotox Environ Safe 2018;147:175-91. https://doi.org/10.1016/j.ecoenv.2017.08.032
  49. Dimkpa C, Weinand T, Asch F. Planterhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 2009;32:1682-94. https://doi.org/10.1111/j.1365-3040.2009.02028.x
  50. Sessitsch A, Kuffner M, Kidd P, Vangronsveld J, Wenzel WW, Fallmann K, Puschenreiter M. The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol Biochem 2013;60:182-94. https://doi.org/10.1016/j.soilbio.2013.01.012

Cited by

  1. Comprehensive Genome Analysis on the Novel Species Sphingomonas panacis DCY99 T Reveals Insights into Iron Tolerance of Ginseng vol.21, pp.6, 2021, https://doi.org/10.3390/ijms21062019
  2. Alleviation of salinity and metal stress using plant growth-promoting rhizobacteria isolated from semiarid Moroccan copper-mine soils vol.28, pp.47, 2021, https://doi.org/10.1007/s11356-021-15168-8