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Effect of cadmium stress and inoculation with a heavy-metal-resistant bacterium on the growth and enzyme activity of Sorghum bicolor

Environmental Science and Pollution Research volume 22, pages 16098–16109 (2015)Cite this article

Abstract

In this study, the influence of the heavy-metal-resistant rhizobacterial inoculant Rhodococcus ruber N7 on the growth and enzyme activity of Sorghum bicolor (L.) Moench. under cadmium stress was investigated in quartz sand pot experiments. The effect of cadmium and bacterium on the plant biomass accumulation, photosynthetic pigments, protein content, and the activities of plant-tissue enzymes such as peroxidase, laccase, and tyrosinase were estimated. It was shown that the presence of cadmium in the sand influenced the roots to a greater extent than it influenced the aerial parts of sorghum. This is manifested as increased protein content, reduced activity of peroxidase, and increased activity of laccase. Compared with cadmium stress, inoculation of plants with rhizobacterium R. ruber N7 has a stronger (and often opposite) effect on the biochemical parameters of sorghum, including a decrease in the concentration of protein in the plant, but increased the activity of peroxidase, laccase, and tyrosinase. Under cadmium contamination of sand, R. ruber N7 successfully colonizes the roots of Sorghum bicolor, survives in its root zone, and contributes to the accumulation of the metal in the plant roots, thereby reducing the concentration of the pollutant in the environment.

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References

  • Baldrian P, Gabriel J (2002) Copper and cadmium increase laccase activity in Pleurotus ostreatus. FEMS Microbiol Lett 206:69–74

    CAS  Article  Google Scholar 

  • Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, Glick BR (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37:241–250

    CAS  Article  Google Scholar 

  • Berova M, Stoeva N, Zlatev Z, Stoilova T, Chavdarov P (2007) Physiological changes in bean (Phaseolus vulgaris L.) leaves, infected by the most important bean disease. J Cent Eur Agric 8:57–62

    Google Scholar 

  • Bondarenkova A (2009) Rol’ stimuliruyushchih rost rasteniy rizobakteriy v fitoremediacii pochv, zagryaznennyh uglevodorodami (Role of plant growth promoting rhizobacteria I phytoremediation of hydrocarbon-contaminated soil). PhD Thesis. IBPPM RAS, Saratov (in Russian)

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal Biochem 72:248–254

    CAS  Article  Google Scholar 

  • Breckle SW (1991) Growth under stress. Heavy metals. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. Marcel Dekker, New York, pp 351–373

    Google Scholar 

  • Burd GI, Dixon DG, Glick BR (2000) Plant growth-promoting bacteria that decrease heavy metal toxicity in plants. Can J Microbiol 46:237–245

    CAS  Article  Google Scholar 

  • Chernavskaya NM (1988) Fizioloiya rastitel’nyh organizmov i rol’ metallov (Physiology of plant organisms and significance of metals). Moscow State University, Moscow (in Russian)

    Google Scholar 

  • Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182

    CAS  Article  Google Scholar 

  • Criquet S, Joner E, Leglize P, Leyval C (2000) Anthracene and mycorrhiza affect the activity of oxidoreductases in the roots and the rhizosphere of lucerne (Medicago saliva L.). Biotechnol Lett 22:1733–1737

    CAS  Article  Google Scholar 

  • Dell’Amico E, Cavalca L, Andreoni V (2008) Improvement of Brassica napus growth under cadmium stress by cadmium-resistant rhizobacteria. Soil Biol Biochem 40:74–84

    Article  Google Scholar 

  • Dubrovskaya EV, Polikarpova IO, Muratova AY, Pozdnyakova NN, Chernyshova MP, Turkovskaya OV (2014) Changes in physiological, biochemical, and growth parameters of sorghum in the presence of phenanthrene. Russ J Plant Physiol 61:529–536

    CAS  Article  Google Scholar 

  • Epelde L, Mijangos I, Becerril JM, Garbisu C (2009) Soil microbial community as bioindicator of the recovery of soil functioning derived from metal phytoextraction with sorghum. Soil Biol Biochem 41:1788–1794

    CAS  Article  Google Scholar 

  • Glick BR (2003) Phytoremediation: synergistic use of plants and bacteria to clean up the environment. Biotechnol Adv 21:383–393

    CAS  Article  Google Scholar 

  • Golubev SN, Schelud’ko AV, Muratova AY, Makarov OE, Turkovskaya OV (2009) Assessing the potential of rhizobacteria to survive under phenanthrene pollution. Water Air Soil Pollut 198:5–16

    CAS  Article  Google Scholar 

  • Gramene. Sorghum bicolor Enzyme: laccase http://pathway.gramene.org/SORGHUM/NEW-IMAGE?type=ENZYME&object=SB03G038030.1-MONOMER. Accessed 2 June 2015

  • Guo J, Chi J (2014) Effect of Cd-tolerant plant growth-promoting rhizobium on plant growth and Cd uptake by Lolium multiflorum Lam. and Glycine max (L.) Merr. in Cd-contaminated soil. Plant Soil 375:205–214

    CAS  Article  Google Scholar 

  • Hernandez LE, Cooke DT (1997) Modifications of root plasma membrane lipid composition of cadmium treated Pisum sativum. J Exp Bot 48:1375–1381

    CAS  Article  Google Scholar 

  • Hygienic standards GN 2.1.7.020-94. Tentative allowable concentrations (TAC) of heavy metals and arsenic in soils with different physical and chemical properties (gross contents, mg/kg). (Addendum N 1 to the list of MAC and TAC N 6229-91). Moscow, 1995. (in Russian)

  • Kuriakose SV, Prasad MNV (2008) Cadmium stress affects seed germination and seedling growth in Sorghum bicolor (L.) Moench by changing the activities of hydrolyzing enzymes. Plant Growth Regul 54:143–156

    CAS  Article  Google Scholar 

  • Lavid N, Schwartz A, Lewinsohn E, Tel-Or E (2001) Phenols and phenol oxidases are involved in cadmium accumulation in the water plants Nymphoides peltata (Menyanthaceae) and Nymphaeae (Nymphaeaceae). Planta 214:189–195

    CAS  Article  Google Scholar 

  • Leonowicz A, Grzywnowicz K (1981) Quantitative estimation of laccase forms in some white-rot fungi using syringaldazine as a substrate. Enzym Microb Technol 3:55–58

    CAS  Article  Google Scholar 

  • Li X, Zhao M, Guo L, Huang L (2012) Effect of cadmium on photosynthetic pigments, lipid peroxidation, antioxidants, and artemisinin in hydroponically grown Artemisia annua. J Environ Sci 24:1511–1518

    CAS  Article  Google Scholar 

  • Lobato AKS, Gonçalves-Vidigal MC, Vidigal Filho PS, Costa RCL, Cruz FJR, Santos DGC, Silva CR, Silva LI, Sousa LL (2009) Changes in photosynthetic pigment and carbohydrate content in common bean cultivars infected by Colletotrichum lindemuthianum. Plant Soil Environ 55:58–61

    CAS  Google Scholar 

  • Lopes DB, Berger RD (2001) The effects of rust and anthracnose on the photosynthetic competence of diseased bean leaves. Phytopathology 91:212–220

    CAS  Article  Google Scholar 

  • Marchiol L, Fellet G, Perosa D, Zerbi G (2007) Removal of trace metals by Sorghum bicolor and Helianthus annuus in a site polluted by industrial wastes: a field experience. Plant Physiol Biochem 45:379–387

    CAS  Article  Google Scholar 

  • McGrath SP, Zhao FJ (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opin Biotechnol 14:277–282

    CAS  Article  Google Scholar 

  • Mergeay M, Nies D, Schlegel H, Gerites I (1985) Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals. J Bacteriol 162:328–334

    CAS  Google Scholar 

  • Mittra B, Sharma S, Das A, Henry S, Das T, Ghosh P, Ghosh S, Mohanty P (2008) A novel cadmium induced protein in wheat: characterization and localization in root tissue. Biol Plant 52:343–346

    CAS  Article  Google Scholar 

  • Mohamed HI, Gomaa EZ (2012) Effect of plant growth promoting Bacillus subtilis and Pseudomonas fluorescens on growth and pigment composition of radish plants (Raphanus sativus) under NaCl stress. Photosynthetica 50:263–272

    CAS  Article  Google Scholar 

  • Muromtsev GS (1957) Some methods for studying the dissolution of calcium phosphates by microorganisms. Microbiologiya 26:172

    CAS  Google Scholar 

  • Niku-Paavola M-L, Karhunen E, Salola P, Raunio J (1988) Ligninolytic enzymes of white-rot fungus Phlebia radiate. Biochem J 254:877–884

    CAS  Article  Google Scholar 

  • Nunes da Silva M, Mucha AP, Rocha AC, Silva C, Carli C, Gomes CR, Almeida CMR (2014) Evaluation of the ability of two plants for the phytoremediation of Cd in salt marshes. Estuar Coast Shelf Sci 141:78–84

    CAS  Article  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556

    CAS  Article  Google Scholar 

  • Prasad MNV (1995) Cadmium toxicity and tolerance in vascular plants. Environ Exp Bot 35:525–545

    CAS  Article  Google Scholar 

  • Prasad DDK, Prasad ARK (1987) Altered 5-aminolevulinic acid metabolism by lead and mercury in germinating seedlings of Bajra (Pennisetum typhoideum). J Plant Physiol 127:241–249

    CAS  Article  Google Scholar 

  • Ruiz E, Rodríguez L, Alonso-Azcárate J, Rincón J (2009) Phytoextraction pf metal polluted soils around a Pb-Zn mine by crop plants. Int J Phytorem 11:360–384

    CAS  Article  Google Scholar 

  • Saidi I, Chtourou Y, Djebali W (2014) Selenium alleviates cadmium toxicity by preventing oxidative stress in sunflower (Helianthus annuus) seedlings. J Plant Physiol 171:85–91

    CAS  Article  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    CAS  Article  Google Scholar 

  • Seregin IV, Ivanov VB (2001) Physiological aspects of cadmium and lead toxic effects on higher plants. Russ J Plant Physiol 48:523–544

    CAS  Article  Google Scholar 

  • Siciliano SD, Goldie H, Germida JJ (1998) Enzymatic activity in root exudates of Dahurian wild rye (Elymus dauricus) that degrades 2-chlorbenzoic acid. J Agric Food Chem 46:5–7

    CAS  Article  Google Scholar 

  • Siddiqui Y, Meon S (2009) Effect of seed bacterization on plant growth response and induction of disease resistance in chilli. Agric Sci China 8:963–971

    Article  Google Scholar 

  • Smith GS, Johnston CM, Cornforth IS (1983) Comparison of nutrient solutions for growth of plants in sand culture. New Phytol 94:537–548

    CAS  Article  Google Scholar 

  • Soudek P, Petrová Š, Vaňková R, Song J, Vaněk T (2014) Accumulation of heavy metals using Sorghum sp. Chemosphere 104:15–24

    CAS  Article  Google Scholar 

  • Tran TA, Popova LP (2013) Functions and toxicity of cadmium in plants: recent advances and future prospects. Turk J Bot 37:1–13

    CAS  Google Scholar 

  • Trivedi P, Pandey A, Sa T (2007) Chromate reducing and plant growth promoting activities of psychrotrophic Rhodococcus erythropolis MtCC 7905. J Basic Microbiol 47:513–517

    CAS  Article  Google Scholar 

  • von Wettstein D (1957) Chlorophyll-letale und der submicroskoposche Formwechsel der Plastiden. Exp Cell Res 12:427–506

    Article  Google Scholar 

  • Wan Y, Luo S, Chen J, Xiao X, Chen L, Zeng G, Liu C, He Y (2012) Effect of endophyte-infection on growth parameters and Cd-induced phytotoxicity of Cd-hyperaccumulator Solanum nigrum L. Chemosphere 89:743–750

  • Wang C, Knill E, Glick BR, Défago G (2000) Effect of transferring 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase genes into Pseudomonas fluorescens strain CHA0 and its gacA derivative CHA96 on their growth promoting and disease-suppressive capacities. Can J Microbiol 46:898–907

    CAS  Article  Google Scholar 

  • Wani PA, Khan MS (2013) Nickel detoxification and plant growth promotion by multi metal resistant plant growth promoting Rhizobium species RL9. Bull Environ Contam Toxicol 91:117–124

    CAS  Article  Google Scholar 

  • Yang Y-J, Cheng L-M, Liu Z-H (2007) Rapid effect of cadmium on lignin biosynthesis in soybean roots. Plant Sci 172:632–639

    CAS  Article  Google Scholar 

  • Zengin FK, Munzuroglu O (2005) Effects of some heavy metals on content of chlorophyll, proline and some antioxidant chemicals in bean (Phaseolus vulgaris L.) seedlings. Acta Biol Cracov Ser Bot 47:157–164

    Google Scholar 

  • Zhuang P, Shu W, Li Z, Liao B, Li J, Shao J (2009) Removal of metals by sorghum plants from contaminated land. J Environ Sci 21:1432–1437

    CAS  Article  Google Scholar 

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Acknowledgments

We thank Anastasia Bondarenkova, Ph.D. (IBPPM RAS), for the supporting information on R. ruber N7.

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Affiliations

  1. Institute of Biochemistry and Physiology of Plants and Microorganisms, Russian Academy of Sciences, 13 Prospekt Entuziastov, Saratov, Russia, 410049

    Anna Muratova, Yelena Lyubun, Kristina German & Olga Turkovskaya

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  1. Anna Muratova
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  2. Yelena Lyubun
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  3. Kristina German
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  4. Olga Turkovskaya
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Correspondence to Anna Muratova.

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Responsible editor: Philippe Garrigues

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Muratova, A., Lyubun, Y., German, K. et al. Effect of cadmium stress and inoculation with a heavy-metal-resistant bacterium on the growth and enzyme activity of Sorghum bicolor . Environ Sci Pollut Res 22, 16098–16109 (2015). https://doi.org/10.1007/s11356-015-4798-7

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  • DOI: https://doi.org/10.1007/s11356-015-4798-7

Keywords

  • Cadmium
  • Sorghum bicolor
  • Rhodococcus ruber
  • Peroxidase
  • Laccase