Skip to main content

Advertisement

SpringerLink
Log in

Comparative effectiveness of ACC-deaminase and/or nitrogen-fixing rhizobacteria in promotion of maize (Zea mays L.) growth under lead pollution

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Lead (Pb) pollution is appearing as an alarming threat nowadays. Excessive Pb concentrations in agricultural soils result in minimizing the soil fertility and health which affects the plant growth and leads to decrease in crop production. Plant growth promoting rhizobacteria (PGPR) are beneficial bacteria which can protect the plants against many abiotic stresses, and enhance the growth. The study aimed to identify important rhizobacterial strains by using the 1-aminocyclopropane-1-carboxylate (ACC) enrichment technique and examine their inoculation effects in the growth promotion of maize, under Pb pollution. A pot experiment was conducted and six rhizobacterial isolates were used. Pb was added to 2 kg soil in each pot (with 4 seeds/pot) using Pb(NO3)2 at the rate of 0, 100, 200, 300, and 400 mg kg−1 Pb with three replications in completely randomized design. Rhizobacterial isolates performed significantly better under all Pb levels, i.e., 100 to 400 Pb mg kg−1 soil, compared to control. Comparing the efficacy of the rhizobacterial isolates under different Pb levels, rhizobacterial isolates having both ACC-deaminase and nitrogen-fixing activities (AN8 and AN12) showed highest increase in terms of the physical, chemical and enzymatic growth parameters of maize, followed by the rhizobacterial isolates having ACC-deaminase activity only (ACC5 and ACC8), and then the nitrogen-fixing rhizobia (Azotobacter and RN5). However, the AN8 isolate showed maximum efficiency, and highest shoot and root length (14.2 and 6.1 cm), seedling fresh and dry weights (1.91 and 0.14 g), chlorophyll a, b, and carotenoids (24.1, 30.2 and 77.7 μg/l), protein (0.82 mg/g), proline (3.42 μmol/g), glutathione S-transferase, peroxidase and catalase (12.3, 4.2 and 7.2 units/mg protein), while the lowest Pb uptake in the shoot and root (0.83 and 0.48 mg/kg) were observed under this rhizobial isolate at the highest Pb level (i.e., 400 Pb mg kg−1 soil). The results revealed that PGPR significantly decreases the deleterious effects of Pb pollution and increases the maize growth under all Pb concentrations, i.e., 100–400 Pb mg kg−1 soil. PGPR chelate the Pb in the soil, and ultimately influence its bioavailability, release and uptake. The PGPR having both ACC-deaminase and nitrogen-fixing abilities are more effective and resistive against Pb pollution than PGPR having either ACC-deaminase or nitrogen-fixing activity alone. The ACC enrichment technique is an efficient approach to select promising PGPR.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14

Similar content being viewed by others

References

  • Ahemad M (2012) Implications of bacterial resistance against heavy metals in bioremediation: a review. IIOAB J 3:39–46

    CAS  Google Scholar 

  • Ahemad M, Malik A (2011) Bioaccumulation of heavy metals by zinc resistant bacteria isolated from agricultural soils irrigated with wastewater. Bacteriol J 2:12–21

    Article  Google Scholar 

  • Arnon DI (1949) Copper induced enzyme in isolated chloroplasts; polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  Google Scholar 

  • Bates L, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Belimov AA, Safronova VI, Sergeyeva TA, Egorova TN, Matveyeva VA, Tsyganov VE, Borisov AY, Tikhonovich IA, Kluge C, Preisfeld A, Dietz KJ, Stepanok VV (2001) Characterization of plant growth promoting rhizobacteria isolated from polluted soils and containing 1-aminocyclopropane-1-carboxylate deaminase. Can J Microbiol 47:642–652

    Article  CAS  Google Scholar 

  • Bindler R (2011) Contaminated lead environments of man: reviewing the lead isotopic evidence in sediments, peat, and soils for the temporal and spatial patterns of atmospheric lead pollution in Sweden. Environ Geochem Health 33:11–329

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Burd GI, Dixon DG, Glick BR (1998) A plant growth promoting bacterium that decreases nickel toxicity in seedlings. Appl Environ Microbiol 64:3663–3668

    CAS  Google Scholar 

  • Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxidase dismutase, catalase and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468

    Article  CAS  Google Scholar 

  • Davies KG, Whitbread RA (1989) Comparison of method for measuring the colonization of root system by fluorescent pseudomonads. Plant Soil 116:239–246

  • 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 

  • Dworken M, Foster J (1958) Experiment with some microorganisms which utilize ethane and hydrogen. J Bacteriol 75:92–601

    Google Scholar 

  • Filip Z (2002) International approach to assessing soil quality by ecological related biological parameters. Agric Ecosyst Environ 88:169–174

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Hindawi Publishing Corporation, Scientifica

  • Grichko VP, Glick BR (2001) Amelioration of flooding stress by ACC deaminase-containing plant growth-promoting bacteria. Plant Physiol Biochem 39:11–17

    Article  CAS  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathion S-transferases, the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    CAS  Google Scholar 

  • Hammerschmidt R, Nucckles F, Kuc I (1982) Association of enhance peroxidase activity with induced systemic resistance of cucumber to Colletotrichum largenarium. Physiol Plant Pathol 20:73–82

    Article  CAS  Google Scholar 

  • Hassan W (2013) C and N mineralization and dissolved organic matter potentials of two contrasting plant residues: effects of residue type, moisture and temperature. Acta Agric Scand B Soil Plant Sci 63:642–652

    CAS  Google Scholar 

  • Hassan W, David J (2013) Effect of lead pollution on soil microbiological index under spinach (Spinacia oleracea L.) cultivation. J Soils Sediments 14:44–59

    Article  Google Scholar 

  • Hassan W, Akmal M, Muhammad I, Younas M, Zahaid KR, Ali F (2013a) Response of soil microbial biomass and enzymes activity to cadmium (Cd) toxicity under different soil textures and incubation times. Aust J Crop Sci 7:674–680

    CAS  Google Scholar 

  • Hassan W, David J, Abbas F (2013b) Effect of type and quality of two contrasting plant residues on CO2 emission potential of Ultisol soil: implications for indirect influence of temperature and moisture. Catena 114:90–96

    Article  Google Scholar 

  • Hassan W, Chen W, Huang Q, Mohamed I (2013c) Microcalorimetric evaluation of soil microbiological properties under plant residues and dogmatic water gradients in Red soil. Soil Sci Plant Nutr 59:858–870

    Article  Google Scholar 

  • Hassan W, Chen W, Cai P, Huang Q (2013d) Oxidative enzymes, the ultimate regulator: implications for factors affecting their efficiency. J Environ Qual 42:1779–1790

    Article  CAS  Google Scholar 

  • Hassan W, Chen W, Cai P, Huang Q (2014a) Estimation of enzymatic, microbial and chemical properties in Brown soil by microcalorimetry. J Therm Anal Cal 116:969–988

    Article  CAS  Google Scholar 

  • Hassan W, Bano R, Khatak BU, Hussain I, Yousaf M, David J (2014b) Temperature sensitivity and soil organic carbon pools decomposition under different moisture regimes: effect on total microbial and enzymatic activity. CLEAN — Soil Air Water. doi:10.1002/clen.201300727

    Google Scholar 

  • Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598

    Article  Google Scholar 

  • Honma M, Shimomura T (1978) Metabolism of 1-aminocyclopropane-1-carboxylic acid. Agric Biol Chem 42:1825–1831

    Article  CAS  Google Scholar 

  • Komarek M, Ettler V, Chrastny V, Mihaljevic M (2008) Lead isotopes in environmental sciences: a review. Environ Int 34:562–577

    Article  CAS  Google Scholar 

  • Kuffner M, Puschenreiter M, Wieshammer G, Gorfer M, Sessitsch A (2008) Rhizosphere bacteria affect growth and metal uptake of heavy metal accumulating willows. Plant Soil 304:35–44

    Article  CAS  Google Scholar 

  • Li J, Ovakim DH, Charles TC, Glick BR (2000) An ACC-deaminase minus mutant of Enterobacter cloacae UW4 no longer promotes root elongation. Curr Microbiol 41:101–105

    Article  CAS  Google Scholar 

  • Majid NM, Islam MM, Rauf RA (2012) Evaluation of Jelutong (Dyera cotulata) as a phytoremediator to uptake copper (Cu) from contaminated soils. Aust J Crop Sci 6:369–374

    CAS  Google Scholar 

  • Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572

    Article  CAS  Google Scholar 

  • Mia MAB, Shamsuddin ZH, Wahab Z, Marziah M (2010) Effect of plant growth promoting rhizobacterial (PGPR) inoculation on growth and nitrogen incorporation of tissue-cultured Musa plantlets under nitrogen-free hydroponics condition. Aust J Crop Sci 4:85–90

    Google Scholar 

  • Nadeem SM, Zahir ZA, Naveed M, Arshad M, Shahzad SM (2006) Variation in growth and ion uptake of maize due to inoculation with plant growth promoting rhizobacteria under salt stress. Soil Environ 25:78–84

    Google Scholar 

  • Nakano Y, Azada K (1987) Purification of ascorbate peroxidase in spinach chloroplasts: its inactivation in ascorbate depleted medium and reactivation by monodehydroascorbate radical. Plant Cell Physiol 28:131–140

    CAS  Google Scholar 

  • Page AL, Miller RH, Keeney DR (1982) Methods of soil analysis—chemical and microbiological properties: Part 2, 2nd edn. Amer Soc Agron (ASA) No. 9, Madison

    Google Scholar 

  • Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 118:10–15

    Article  CAS  Google Scholar 

  • Pishchik VN, Vorobyev NI, Chernyaeva II, Timofeeva SV, Kozhemyakov AP, Alexeev YV, Lukinm SM (2002) Experimental and mathematical simulation of plant growth promoting rhizobacteria and plant interaction under cadmium stress. Plant Soil 243:173–186

    Article  CAS  Google Scholar 

  • Premono HME, Moawad AM, Vlek PLG (1996) Effect of phosphate-solubilizing Pseudomonas putida on the growth of maize and its survival in the rhizosphere. Indonesian J Crop Sci 11:13–23

    Google Scholar 

  • Rajkumar M, Nagendran R, Lee KJ, Lee WH, Kim SZ (2006) Influence of plant growth promoting bacteria and Cr6+ on the growth of Indian mustard. Chemosphere 62:741–748

  • Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol Biol Evol 21:541–554

  • Regan DL (1988) Other micro-algae. In: Borowitzka MA and Borowitzka LJ edn, Microalgal Biotechnology, Cambridge University Press, Cambridge, pp. 135–150

  • Ribaudo CM, Krumpholz EM, Cassan FD, Bottini R, Cantore ML, Cura JA (2006) Azospirillum sp. Promotes root hair development into tomato plants through a mechanism that involves ethylene. J. Plant Growth Regul 25:175–185

    Article  CAS  Google Scholar 

  • Sahran BS, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res 2011: LSMR-21

  • Saikia R, Kumar R, Arora DR, Gogoi DK, Azad P (2006) Pseudomonas aeruginosa inducing rice resistance against Rhizoctonia solani: production of salicylic acid and peroxidases. Folia Microbiol 51:375–380

    Article  CAS  Google Scholar 

  • Saleem M, Arshad M, Hussain S, Bhatti AS (2007) Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J Indian Microbiol Biotechnol 34:635–648

    Article  CAS  Google Scholar 

  • US Salinity Lab Staff (1954) Diagnosis and improvement of saline and alkali soils. USDA Hand Book No 60. Washington DC, USA, pp 160

  • Sarwar M, Arshad M, Martins DA, Frankenberger WT Jr (1992) Tryptophan-dependent biosynthesis of auxins in soil. Plant Soil 147:207–215

    Article  CAS  Google Scholar 

  • Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52

    Article  CAS  Google Scholar 

  • Singh S, Sinha S (2005) Accumulation of metals and its effects in Brassica juncea (L.) Czern (cv. Rohini) grown on various amendments of tannery waste. Ecotoxicol Environ Saf 62:118–127

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic Press, London, p 605

    Google Scholar 

  • Spaepen S, Vanderleyden J (2011) Auxin and plant–microbe interactions. Cold Spring Harb Perspect Biol 3(4). doi: 10.1101/cshperspect.a001438

  • Stefan M, Munteanu N, Stoleru V, Mihasan M (2013) Effects of inoculation with plant growth promoting rhizobacteria on photosynthesis, antioxidant status and yield of runner bean. Rom Biotechnol Lett 18(2)

  • Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wollum AG II (1982) Cultural methods for soil microorganisms. In: Page AL (ed) Methods of soil analysis: Part 2. Chemical and microbiological properties. Agronomy No 9, ASA, Madison, pp 781–802

    Google Scholar 

  • Young SA, Guo A, Guikema JA, White F, Leach IE (1995) Rice cationic peroxidase accumulation in xylem vessels during incompatible interaction with Xanthomonas oryzae. Plant Physiol 107:1333–1341

    Article  CAS  Google Scholar 

  • Zahir ZA, Munir A, Asghar HN, Shaharoona B, Arshad M (2008) Effectiveness of rhizobacteria containing ACC-deaminase for growth promotion of pea (Pisum sativum) under drought conditions. J Microbiol Biotechnol 18:958–963

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Huazhong Agricultural University, Wuhan, 430070, China

    Waseem Hassan

  2. University of Agriculture Faisalabad, Faisalabad, 38040, Pakistan

    Waseem Hassan

  3. On Farm Water Management, Multan, Pakistan

    Rizwana Bano

  4. Soil and Water Testing Laboratory, Dera Ghazi Khan, Pakistan

    Farhat Bashir

  5. Freie Universität, Berlin, 14195, Germany

    Julie David

Authors
  1. Waseem Hassan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rizwana Bano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Farhat Bashir
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Julie David
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Waseem Hassan.

Additional information

Responsible editor: Elena Maestri

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hassan, W., Bano, R., Bashir, F. et al. Comparative effectiveness of ACC-deaminase and/or nitrogen-fixing rhizobacteria in promotion of maize (Zea mays L.) growth under lead pollution. Environ Sci Pollut Res 21, 10983–10996 (2014). https://doi.org/10.1007/s11356-014-3083-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3083-5

Keywords

Search

Navigation