Abstract
Soil contamination by heavy metals is one of the major abiotic stresses that cause retarded plant growth and low productivity. Among the heavy metals, excessive accumulations of zinc (Zn) cause toxicity to plants. The toxicity caused by Zn could be managed by application of Zn-tolerant plant growth-promoting (PGP) bacteria. In this study, five Zn-tolerant bacteria (100–400 mg−1 Zn resistant) were selected and identified as Lysinibacillus spp. based on 16S rRNA gene sequencing. The PGP properties of the Lysinibacillus spp. showed the production of indole acetic acid (60.0–84.0 μg/ml) and siderophore, as well as solubilization of potassium. Furthermore, the isolates were evaluated under greenhouse condition with 2 g kg−1 Zn stress and without Zn stress along with control on Zea mays. The results showed that Lysinibacillus spp. coated seeds enhanced plant growth attributes and biomass yield in both conditions compared with control plants. The enhancement of root growth ranged from 49.2 to 148.6% and shoot length from 83.3 to 111.7% under Zn-stressed soils. Also, the inoculated seedlings substantially enhanced chlorophyll a and b, proline, total phenol, and ascorbic acid. The uptake of Zn by maize root ranged from 31.5 to 210.0% compared with control plants. Therefore, this study suggested that the tested Zn-tolerant Lysinibacillus spp. may be used for cultivation of Z. mays in Zn-contaminated agricultural lands.
Similar content being viewed by others
Data Availability
All data generated or analyzed during this study are included in this published article
References
Aguirre-Monroy AM, Santana-Martínez JC, Dussán J (2019) Lysinibacillus sphaericus as a nutrient enhancer during fire-impacted soil replantation. Appl Environ Soil Sci 2019:1–8
Aleksandrov VG, Blagodyr RN, Iiiev IP (1967) Liberation of phosphoric acid from apatite by silicate bacteria. Mikrobiol Zh 29:111–114
Arora A, Byrem TM, Nari MG, Strasburg GM (2000) Modulation of liposomal membranes fluidity by flavonoids and isoflavonoids. Arch Biochem Biophys 373:102–109
Bates L, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Brick JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indole acetic acid production by bacteria immobilized on nitrocellulose membrane. Appl Environ Microbiol 57:535–538
Cambrollé J, Mancilla-Leytón J, Muñoz-Vallés S, Luque T, Figueroa M (2012) Zinc tolerance and accumulation in the salt-marsh shrub Halimione portulacoides. Chemosphere 86:867–874
Chauhan JS, Rai JPN (2009) Phytoextraction of soil cadmium and zinc by microbes-inoculated Indian mustard (Brassica juncea). J Plant Interact 4:279–287
Cheng M, Zhang H, Zhang J, Hu G, Zhang J, He J, Huang X (2015) Lysinibacillus fluoroglycofenilyticus sp. nov., a bacterium isolated from fluoroglycofen contaminated soil. Antonie van Leeuwenhoek 107:157–164
Cherif J, Derbel N, Nakkach M, von Bergmann H, Jemal F, Lakhdar ZB (2010) Analysis of in vivo chlorophyll fluorescence spectra to monitor physiological state of tomato plants growing under zinc stress. J Photochem Photobiol B: Biol 101:332–339
de Souza R, Meyer J, Schoenfeld R, da Costa PB, Passaglia LMP (2015) Characterization of plant growth-promoting bacteria associated with rice cropped in iron-stressed soils. Ann Microbiol 65:951–964
Dinesh R, Srinivasan V, Hamza S, Sarathambal C, Anke Gowda SJ, Ganeshamurthy AN, Gupta SB, Aparna Nair V, Subila KP, Lijina A, Divya VC (2018) Isolation and characterization of potential Zn solubilizing bacteria from soil and its effects on soil Zn release rates, soil available Zn and plant Zn content. Geoderma 321:173–186
dos Santos JO, Andrade CA, de Souza KRD, de Oliveira SM, Brandão IR, Alves JD, Santos IS (2019) Impact of zinc stress on biochemical and biophysical parameters in Coffea arabica seedlings. J Crop Sci Biotech 22:253–264
Du Laing G, Vanthuyne D, Vandecasteele B, Tack F, Verloo M (2007) Influence of hydrological regime on pore water metal concentrations in a contaminated sediment derived soil. Environ Pollut 147:615–625
Emenike CU, Agamuthu P, Fauziah SH (2016) Blending Bacillus sp., Lysinibacillus sp. and Rhodococcus sp. for optimal reduction of heavy metals in leachate contaminated soil. Environ Earth Sci 75:26
Freitas MA, Medeiros FHV, Carvalho SP, Guilherme LRG, Teixeira WD, Zhang H, Paré PW (2015) Augmenting iron accumulation in cassava by the beneficial soil bacterium Bacillus subtilis (GBO3). Front Plant Sci 6:596
Glick BR (2003) Phytoremediation: synergistic use of plants and bacteria to clean up the environment. Biotechnol Adv 21:383–393
Gopi K, Jinal HN, Prittesh P, Kartik VP, Amaresan N (2020) Effect of copper-resistant Stenotrophomonas maltophilia on maize (Zea mays) growth, physiological properties, and copper accumulation: potential for phytoremediation into biofortification. Int J Phytoremediat 22:662–668
Hattab S, Hattab S, Flores-Casseres ML, Boussetta H, Doumas P, Hernandez LE, Banni M (2016) Characterisation of lead-induced stress molecular biomarkers in Medicago sativa plants. Environ Exp Bot 123:1–12
He CQ, Tan GE, Liang X, Du W, Chen YL, Zhi GY, Zhu Y (2010) Effect of Zn-tolerant bacterial strains on growth and Zn accumulation in Orychophragmus violaceus. Appl Soil Ecol 44:1–5
Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334
Ibrahim MH, Chee Kong Y, Mohd Zain NA (2017) Effect of cadmium and copper exposure on growth, secondary metabolites and antioxidant activity in the medicinal plant sambung nyawa (Gynura procumbens (Lour.) Merr). Molecules 22:E1623
Irtelli B, Navari-Izzo F (2006) Influence of sodium nitrilotriacetate (NTA) and citric acid on phenolic and organic acids in Brassica juncea grown in excess of cadmium. Chemosphere 65:1348–1354
Islam F, Yasmeen T, Ali Q, Ali S, Arif MS, Hussain S, Rizvi H (2014a) Influence of Pseudomonas aeruginosa as PGPR on oxidative stress tolerance in wheat under Zn stress. Ecotoxicol Environ Saf 104:285–293
Islam F, Yasmeen T, Riaz M, Arif MS, Ali S, Raza SH (2014b) Proteus mirabilis alleviates zinc toxicity by preventing oxidative stress in maize (Zea mays) plants. Ecotoxicol Environ Saf 110:143–152
Jain D, Kour R, Bhojiya AA, Meena RH, Singh A, Mohanty SR, Rajpurohit D, Ameta KD (2020) Zinc tolerant plant growth promoting bacteria alleviates phytotoxic effects of zinc on maize through zinc immobilization. Sci Rep 10:13865
Jiang K, Wu B, Wang C, Ran Q (2019) Ecotoxicological effects of metals with different concentrations and types on the morphological and physiological performance of wheat. Ecotoxicol Environ Saf 167:345–353
Jinal HN, Gopi K, Prittesh P, Kartik VP, Amaresan N (2019) Phytoextraction of iron from contaminated soils by inoculation of iron-tolerant plant growth-promoting bacteria in Brassica juncea L. Czern. Environ Sci Pollut Res 26:32815–32823
Kabata-Pendias A, Pendias H (2001) Trace Elements in Soils and Plants. CRC Press Inc, Boca Raton, FL, USA
Kartik VP, Jinal HN, Amaresan N (2016) Characterization of cadmium resistant bacteria for its potential in promoting plant growth and cadmium accumulation in Sesbania bispinosa root. Int J Phytoremediat 18:1061–1066
Kumar K, Manigundan K, Amaresan N (2017) Influence of salt tolerant Trichoderma spp on growth of maize (Zea mays) under different salinity conditions. J Basic Microbiol 57:141–150
Kumazawa S, Hamasaka T, Nakayama T (2004) Antioxidant activity of propolis of various geographic origins. Food Chem 84:329–339
Li K, Ramakrishna W (2011) Effect of multiple metal resistant bacteria from contaminated lake sediments on metal accumulation and plant growth. J Hazard Mater 189:531–539
Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol J Environ Stud 15:523–530
Mukherjee SP, Choudhuri MA (1983) Implications of water stress-induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiol Plant 58:166–170
Mumtaz MZ, Ahmad M, Jamil M, Hussain T (2017) Zinc solubilizing Bacillus spp. potential candidates for biofortification in maize. Microbiol Res 202:51–60
Oves M, Khan M, Zaidi A (2013) Chromium reducing and plant growth promoting novel strain Pseudomonas aeruginosa OSG41 enhance chickpea growth in chromium amended soils. Eur J Soil Biol 56:72–83
Parlak UK, Yilmaz DD (2012) Response of antioxidant defences to Zn stress in three duckweed species. Ecotoxicol Environ Saf 85:52–58
Płociniczak CT, Sinkkonen A, Romantschuk M, Sułowicz S, Zofia Piotrowska-Seget Z (2016) Rhizospheric bacterial strain Brevibacterium casei MH8a colonizes plant tissues and enhances Cd, Zn, Cu phytoextraction by white mustard. Front Plant Sci 7:101
Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives of plant associated microbes in heavy metal phytoremediation. Biotechnol Adv 30:1562–1574
Rajkumar M, Prasad MNV, Sandhya S, Freitas H (2013) Climate change driven plant-metal-microbe interactions. Environ Int 53:74–86
Rice-Evans CA, Miller NJ, Paganga G (1996) Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic Biol Med 20:933–956
Rizvi A, Khan MS (2018) Heavy metal induced oxidative damage and root morphology alterations of maize (Zea mays L.) plants and stress mitigation by metal tolerant nitrogen fixing Azotobacter chroococcum. Ecotoxicol Environ Saf 157:9–20
Rodríguez MP, Melo C, Jiménez E, Dussán J (2019) Glyphosate bioremediation through the sarcosine oxidase pathway mediated by Lysinibacillus sphaericus in soils cultivated with potatoes. Agriculture 2019:1–16
Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56
Sedlakova-Kadukova J, Kopcakova A, Gresakova L, Godany A, Pristas P (2019) Bioaccumulation and biosorption of zinc by a novel Streptomyces K11 strain isolated from highly alkaline aluminium brown mud disposal site. Ecotoxicol Environ Saf 167:204–211
Shaikh S, Saraf M (2017) Biofortification of Triticum aestivum through the inoculation of zinc solubilizing plant growth promoting rhizobacteria in field experiment. Biocatal Agric Biotechnol 9:120–126
Shreya D, Jinal HN, Kartik VP, Amaresan N (2020) Amelioration effect of chromium-tolerant bacteria on growth, physiological properties and chromium mobilization in chickpea (Cicer arietinum) under chromium stress. Arch Microbiol 202:887–894
Singh RP, Mishra S, Jha P, Raghuvanshi S, Jha PN (2018) Effect of inoculation of zinc-resistant bacterium Enterobacter ludwigii CDP-14 on growth, biochemical parameters and zinc uptake in wheat (Triticum aestivum L.) plant. Ecol Eng 116:163–173
Turan V (2019) Confident performance of chitosan and pistachio shell biochar on reducing Ni bioavailability in soil and plant plus improved the soil enzymatic activities, antioxidant defense system and nutritional quality of lettuce. Ecotoxicol Environ Saf 183:109594
Turan V (2020) Potential of pistachio shell biochar and dicalcium phosphate combination to reduce Pb speciation in spinach, improved soil enzymatic activities, plant nutritional quality, and antioxidant defense system. Chemosphere 245:125611
Turan V, Schröder P, Bilen S, Insam H, Juárez MFD (2019) Co-inoculation effect of Rhizobium and Achillea millefolium L. oil extracts on growth of common bean (Phaseolus vulgaris L.) and soil microbial-chemical properties. Sci Rep 9:15178
Uadhyaya CP, Akula N, Kim HS, Jeon JH, Ho OM, Chun SC, Kim DH, Park SW (2011) Biochemical analysis of enhanced tolerance in transgenic potato plants over expressing D-galacturonic acid reductase gene in response to various abiotic stresses. Mol Breed 28:105–115
Vamerali T, Bandiera M, Mosca G (2010) Field crops for phytoremediation of metal-contaminated land. A review. Environ Chem Lett 8:1–17
Verma SC, Ladha JK, Tripathi AK (2001) Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. J Biotechnol 91:127–141
Xie H, Pasternak JJ, Glick BR (1996) Isolation and characterization of mutants of the plant growth-promoting rhizobacterium Pseudomonas putida GR-122 that overproduce indole acetic acid. Curr Microbiol 32:67–71
Yahaghi Z, Shirvani M, Nourbakhsh F, Pueyo JJ (2019) Uptake and effects of lead and zinc on alfalfa (Medicago sativa L.) seed germination and seedling growth: Role of plant growth promoting bacteria. S Afr J Bot 124:573–582
Acknowledgments
The authors acknowledge the constant support provided by UTU management and Director, CGBIBT, and access to necessary facilities to carry out the work. The authors also thank GSBTM for 16S rRNA gene sequencing and Mahuva Sugar Factory, Mahuva for physicochemical studies.
Author information
Authors and Affiliations
Contributions
NA and KK, designed the study and wrote the manuscript; HJN and KG, performed the experiments; HJN, analyzed the data.
Corresponding authors
Ethics declarations
Conflicts of interests
The authors declare that they have no conflict of interest.
Ethical approval
Not applicable.
Consent to participate
Not applicable.
Consent to publish
Not applicable.
Additional information
Responsible Editor: Gangrong Shi
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Jinal, H.N., Gopi, K., Kumar, K. et al. Effect of zinc-resistant Lysinibacillus species inoculation on growth, physiological properties, and zinc uptake in maize (Zea mays L.). Environ Sci Pollut Res 28, 6540–6548 (2021). https://doi.org/10.1007/s11356-020-10998-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-10998-4