Abstract
Maize is a plant known for food, feed, and energy value, but being a greater biomass, it may also be utilized to extract pollutants from soil. Plant growth-promoting rhizobacteria (PGPR) may act as biofertilizer to improve plant health and indirectly may enhance metal extraction. This study focuses on five bacterial strains isolated from the vegetable (Bitter gourd) rhizosphere irrigated with industrial effluent and characterized for various plant growth-promoting activities. Based on 16S rRNA gene sequencing, bacterial strains belonging to the genera, Bacillus (CIK-517, CIK-519), Klebsiella (CIK-518), Leifsonia (CIK-521), and Enterobacter (CIK-521R), were tested for their ability to promote maize growth in axenic conditions. Results showed negative and positive regulation of maize growth by the exogenous application of Cd and PGPR, respectively. Seed germination assays revealed significant reduction in relative seedling growth of maize cultivars upon Cd exposure (0–80 mg Cd L−1). The tested strains showed tolerance to Cd (1.78–4.45 mmol L−1) and were positive for catalase, oxidase, phosphate solubilization, exopolysaccharide (EPS), and auxin production, whereas CIK-518, CIK-519, and CIK-521R were negative for EPS, phosphate solubilization, and oxidase activities, respectively. Bacterial strains significantly increased shoot/root growth and their dry biomass in normal and Cd-contaminated soil as compared to their respective controls. None of the strains showed significant effects on relative water content or membrane permeability; however, Cd uptake significantly increased in plant tissues upon bacterial inoculation. Bacterial strains CIK-518 and CIK-521R are effective colonizers and thus can be potential inoculants to promote maize growth and Cd extraction/stabilization in Cd-contaminated soil.
Similar content being viewed by others
References
Ahmad I, Akhtar MJ, Zahir ZA, Jamil A (2012) Effect of cadmium on seed germination and seedling growth of four wheat (Triticum aestivum L.) cultivars. Pak J Bot 44:1569–1574
Ahmad I, Akhtar MJ, Asghar HN, Zahir ZA (2013) Comparative efficacy of growth media in causing cadmium toxicity to wheat at seed germination stage. Int J Agric Biol 15:517–522
Ahmad I, Akhtar MJ, Zahir ZA, Naveed M, Mitter B, Sessitsch A (2014) Cadmium-tolerant bacteria induce metal stress tolerance in cereals. Environ Sci Pollut Res 21:11054–11065
Alami Y, Achouk W, Marol C, Heulin T (2000) Rhizosphere soil aggregation and plant growth promotion of sunflowers by an exopolysaccharide-producing Rhizobium sp. strain isolated from sunflower roots. Appl Environ Microbiol 66:3393–3398
Alloway BJ (1995) Heavy metals in soil. Blackie Academic and Professional, London
An YJ (2004) Soil ecotoxicity assessment using cadmium sensitive plants. Environ Pollut 127:21–26
Dimkpa CO, Merten D, Svatos A, Büchel G, Kothe E (2009) Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus), respectively. J Appl Microbiol 107:1687–1696
Dodd IC, Belimov AA, Sobeih WY, Safronova VI, Grierson D, Davies WJ (2010) Will modifying plant ethylene status improve plant productivity in water limited environments? In: New directions for a diverse planet: Proc. Int. Crop Sci. Congr., 4th, Brisbane, Australia, 26 September–1 October 2004. www.cropscience.org.au/icsc2004/poster/1/3/4/510_doddicref.htm (verified 10 January 2010). Regional Inst., Gosford, NSW, Australia
Dourado MN, Martins PF, Quecine MC, Piotto FA, Souza LA, Franco MR, Tezotto T, Azevedo RA (2013) Burkholderia sp. SCMS54 reduces cadmium toxicity and promotes growth in tomato. Ann Appl Biol 163:494–507
Edwards U, Rogall T, Blocker H, Emde M, Bottger EC (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17:7843–7853
Foucault Y, Lévêque T, Xiong T, Schreck E, Austruy A, Shahid M, Dumat C (2013) Green manure plants for remediation of soils polluted by metals and metalloids: ecotoxicity and human bioavailability assessment. Chemosphere 93:1430–1435
Gadd GM (2004) Microbial influence on metal mobility and application for bioremediation. Geoderma 122:109–119
Garg N, Aggarwal N (2011) Effects of interactions between cadmium and lead on growth, nitrogen fixation, phytochelatin, and glutathione production in mycorrhizal Cajanus cajan L. Mill sp. J Plant Growth Regul 30:286–300
Grandlic CJ, Mendez MO, Chorover J, Machado B, Maier RM (2008) Plant growth-promoting bacteria for phytostabilization of mine tailings. Environ Sci Technol 42:2079–2084
Groppa MD, Ianuzzo MP, Tomaro ML, Benavides MP (2007) Polyamine metabolism in sunflower plants under long-term cadmium or copper stress. Amino Acids 32:265–275
Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11
Hussain MB, Zahir ZA, Asghar HN, Asghar M (2014) Can catalase and exopolysaccharides producing rhizobia ameliorate drought stress in wheat? Int J Agric Biol 16:3–13
Iram S, Ahmad I, Akhtar S (2012) Distribution of heavy metals in peri-urban agricultural areas soils. J Chem Soc Pak 34:861–869
Jeong S, Moon HS, Nam K, Kim JY, Kim TS (2012) Application of phosphate-solubilizing bacteria for enhancing bioavailability and phytoextraction of cadmium (Cd) from polluted soil. Chemosphere 88:204–210
Kabata-Pendias A, Pendias H (2001) Trace elements in soils and plants, 3rd edn. CRC Press, Boca Raton
Khan AL, Lee IJ (2013) Endophytic Penicillium funiculosum LHL06 secretes gibberellin that reprograms Glycine max L. growth during copper stress. BMC Plant Biol 13:86–100
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
Kuffner M, De Maria S, Puschenreiter M, Fallmann K, Wieshammer G, Gorfer M, Strauss J, Rivelli AR, Sessitsch A (2010) Culturable bacteria from Zn- and Cd-accumulating Salix caprea with differential effects on plant growth and heavy metal availability. J Appl Microbiol 108:1471–1484
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
Malik RN, Jadoon WA, Husain SZ (2010) Metal contamination of surface soils of industrial city Sialkot, Pakistan: a multivariate and GIS approach. Environ Geochem Health 32:179–191
Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance in tomato and pepper plants to salt stress. Plant Sci 166:525–530
Mehta S, Nautiyal CS (2001) An efficient method for qualitative screening of phosphate-solubilizing bacteria. Curr Microbiol 43:51–56
Mengoni A, Schat H, Vangronsveld J (2010) Plants as extreme environments? Ni resistant bacteria and Ni-hyperaccumulators of serpentine flora. Plant Soil 331:5–16
Metwally A, Safronova VI, Belimov AA, Dietz KJ (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J Exp Bot 409:167–178
Mobin M, Khan NA (2007) Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. J Plant Physiol 164:601–610
Morel JL, Mench M, Guckert A (1986) Measurement of Pb, Cu and Cd binding with mucilage exudates from maize (Zea mays L.) roots. Biol Fertil Soils 2:29–34
Nadeem SM, Zahir ZA, Naveed M, Asghar HN, Arshad M (2010) Rhizobacteria capable of producing ACC-deaminase may mitigate salt stress in wheat. Soil Sci Soc Am J 74:533–542
Naveed M, Mitter B, Reichenauer TG, Wieczorek K, Sessitsch A (2014) Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ Exp Bot 97:30–39
Naz N, Young HK, Ahmed N, Gadd GM (2005) Cadmium accumulation and DNA homology with metal resistance genes in sulfate-reducing bacteria. Appl Environ Microbiol 71:4610–4618
Rajkumar M, Prasad MNV, Freitas H, Ae N (2009) Biotechnological applications of serpentine soil bacteria for phytoremediation of trace elements. Crit Rev Biotechnol 29:120–130
Roane TM, Pepper IL (2000) Microbial responses to environmentally toxic cadmium. Microb Ecol 38:358–364
Sathyapriya H, Sariah M, Akmar ASN, Wong M (2012) Root colonisation of Pseudomonas aeruginosa strain UPMP3 and induction of defence-related genes in oil palm (Elaeis guineensis). Ann Appl Biol 160:137–144
Sessitsch A, Kuffner M, Kidd P, Vangronsveld J, Wenzel WW, Fallmann K, Puschenreiter M (2013) The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol Biochem 60:182–194
Simons M, van der Bij A, Brand I, de Weger LA, Wijffelman CA, Laugtenberg BJJ (1996) Gnotobiotic system for studying rhizosphere colonoization by plant growth-promoting Pseudomonas bacteria. Mol Plant Microbe Interact 9:600–607
Smyth EM, McCarthy J, Nevin R, Khan MR, Dow JM, O’Gara F, Doohan FM (2011) In vitro analyses are not reliable predictors of the plant growth promotion capability of bacteria; a Pseudomonas fluorescens strain that promotes the growth and yield of wheat. J Appl Microbiol 111:683–692
Talboys PJ, Owen DW, Healey JR, Withers PJA, Jones DL (2014) Auxin secretion by Bacillus amyloliquefaciens FZB42 both stimulates root exudation and limits phosphorus uptake in Triticum aestivium. BMC Plant Biol 14:51–58
Vangronsveld J, Herzig R, Weyens N, Boulet J, Adriaensen K, Ruttens A, Thewys T, Vassilev A, Meers E, Nehnelajova E, van der Lelie D, Mench M (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut Res 16:765–794
Vardharajula S, Ali SZ, Grover M, Reddy G, Bandi V (2011) Drought-tolerant plant growth promoting Bacillus spp.: effect on growth, osmolytes and antioxidant status of maize under drought stress. J Plant Interact 6:1–14
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 43:1691–1705
Weyens N, van der Lelie D, Taghavi S, Newman L, Vangronsveld J (2009) Exploiting plant microbe partnerships for improving biomass production and remediation. Trends Biotechnol 27:591–598
Xiong T, Leveque T, Shahid M, Foucault Y, Mombo S, Dumat C (2014) Lead and cadmium phytoavailability and human bioaccessibility for vegetables exposed to soil or atmospheric pollution by process ultrafine particles. J Environ Qual 43:1593–1600
Yang Y, Zhang F, Li H, Jiang R (2009) Accumulation of cadmium in the edible parts of six vegetable species grown in Cd-contaminated soils. J Environ Manage 90:1117–1122
Acknowledgments
This work was financially supported by the “Higher Education Commission” of Pakistan under the Indigenous 5000 Fellowship Scheme, Batch IV.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ahmad, I., Akhtar, M.J., Asghar, H.N. et al. Differential Effects of Plant Growth-Promoting Rhizobacteria on Maize Growth and Cadmium Uptake. J Plant Growth Regul 35, 303–315 (2016). https://doi.org/10.1007/s00344-015-9534-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-015-9534-5