Abstract
Purpose
There is an urgent need to remediate heavy metal–contaminated soils. However, the role of plant growth–promoting rhizobacteria (PGPR) in phytoextraction of heavy metals is far from being well understood. This study aimed to examine the effect of two newly isolated PGPRs on oilseed rape Brassica juncea to extract cadmium (Cd) from contaminated soils and reveal possible underlying mechanisms of PGPR-assisted Cd phytoextraction.
Methods
Two Cd-resistant PGPRs, Bacillus sp. Kz5 and Enterobacter sp. Kz15, were isolated from the rhizosphere of plants grown in copper-mine soils. Seeds of oilseed rape B. juncea were treated with Kz5 and Kz15 suspension, transplanted into soils, and grown in greenhouse pots for 3 weeks. Plant biomass, Cd concentrations, root morphological parameters, photosynthetic parameters, and rhizosphere soil properties were analyzed. Pearson’s correlation coefficient (PCC) analysis and principal component analysis (PCA) were conducted to examine the relationships among plant biomass, Cd concentrations, and the parameters.
Results
The inoculation of the Kz5 and Kz15 significantly increased the plant biomass and Cd concentrations compared to those without PGPR inoculation (p < 0.05). In addition, the root morphology, photosynthetic activity, and rhizosphere soil properties were improved with the inoculation of the PGPRs. There are significant positive correlations between Cd concentrations and plant development indicators.
Conclusion
Significant effects of PGPRs on plant growth promotion and Cd phytoextraction were observed. Such effects were associated with the improvement of plant root morphology, photosynthetic activity, and rhizosphere soil properties. This study provides PGPRs for assisted phytoextraction as a potential strategy to remediate Cd-contaminated soil.
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Data Availability
All data generated or analyzed during this study are included in this article.
References
Abdelkrim S, Jebara SH, Saadani O, Abid G, Taamalli W, Zemni H, Mannai K, Louati F, Jebara M (2020) In situ effects of Lathyrus sativus- PGPR to remediate and restore quality and fertility of Pb and Cd polluted soils. Ecotoxicol Environ Saf 192:110260
Abou-Shanab RA, Angle JS, Delorme TA, Chaney RL, Van Berkum P, Moawad H, Ghanem K, Ghozlan HA (2003) Rhizobacterial effects on nickel extraction from soil and uptake by Alyssum murale. New Phytol 158:219–224
Ali-Zade V, Alirzayeva E, Shirvani T (2010) Plant resistance to anthropogenic toxicants: approaches to phytoremediation. In: Ashraf M, Ozturk M, Ahmad MSA (eds) Plant adaptation and phytoremediation. Springer, Netherlands, Dordrecht, pp 173–192
Amna XY, Farooq MA, Javed MT, Kamran MA, Mukhtar T, Ali J, Tabassum T, Rehman Su, Hussain Munis MF, Sultan T, Chaudhary HJ (2020) Multi-stress tolerant PGPR Bacillus xiamenensis PM14 activating sugarcane (Saccharum officinarum L.) red rot disease resistance. Plant Physiol Biochem 151:640–649
Arif K, Archana G, Desai AJ (2012) Engineering heterologous iron siderophore complex utilization in rhizobia: effect on growth of peanut and pigeon pea plants. Appl Soil Ecol 53:65–73
Arshad M, Silvestre J, Pinelli E, Kallerhoff J, Kaemmerer M, Tarigo A, Shahid M, Guiresse M, Pradere P, Dumat C (2008) A field study of lead phytoextraction by various scented Pelargonium cultivars. Chemosphere 71:2187–2192
Audet P, Charest C (2007) Heavy metal phytoremediation from a meta-analytical perspective. Environ Pollut 147:231–237
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
Berkelaar E, Hale B (2000) The relationship between root morphology and cadmium accumulation in seedlings of two durum wheat cultivars. Can J Bot 78:381–387
Chen J, Huang H, Zhang C, Huang D, Zhu Y, Chai X (2022) The mechanism of Cd sorption by silkworm excrement organic fertilizer and its effect on Cd accumulation in rice. J Soils Sediments 22:2184–2195
Chen L, Luo S, Li X, Wan Y, Chen J, Liu C (2014) Interaction of Cd-hyperaccumulator Solanum nigrum L. and functional endophyte Pseudomonas sp. Lk9 on soil heavy metals uptake. Soil Biol Biochem 68:300–308
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
Deng Z, Cao L (2017) Fungal endophytes and their interactions with plants in phytoremediation: a review. Chemosphere 168:1100–1106
Eissa MA, Roshdy NMK (2018) Nitrogen fertilization: effect on Cd-phytoextraction by the halophytic plant quail bush [Atriplex lentiformis (Torr.) S. Wats]. S Afr J Bot 115:126–131
Elinder C (1992) Cadmium as an environmental hazard. IARC Sci Publ 118:123–132
Ge L, Cang L, Yang J, Zhou D (2016) Effects of root morphology and leaf transpiration on Cd uptake and translocation in rice under different growth temperature. Environ Sci Pollut Res 23:24205–24214
Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7
Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theor Biol 190:63–68
He X, Xu M, Wei Q, Tang M, Guan L, Lou L, Xu X, Hu Z, Chen Y, Shen Z, Xia Y (2020) Promotion of growth and phytoextraction of cadmium and lead in Solanum nigrum L. mediated by plant-growth-promoting rhizobacteria. Ecotoxicol Environ Saf 205:111333
Huang B, Xin J, Dai H, Liu A, Zhou W, Yi Y, Liao K (2015) Root morphological responses of three hot pepper cultivars to Cd exposure and their correlations with Cd accumulation. Environ Sci Pollut Res 22:1151–1159
Huang X, Liu Y, Li Y, Guo P, Fang X, Yi Z (2019) Foliage application of nitrogen has less influence on soil microbial biomass and community composition than soil application of nitrogen. J Soils Sediments 19:221–231
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
Jiang C, Sheng X, Qian M, Wang Q (2008) Isolation and characterization of a heavy metal-resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal-polluted soil. Chemosphere 72:157–164
Ke T, Zhang J, Tao Y, Zhang C, Chen L (2020) Individual and combined application of Cu-tolerant Bacillus spp. enhance the Cu phytoextraction efficiency of perennial ryegrass. Chemosphere 127952
Khan KY, Ali B, Cui X, Feng Y, Stoffella PJ, Tang L, Yang X (2017) Effect of humic acid amendment on cadmium bioavailability and accumulation by pak choi (Brassica rapa ssp. chinensis L.) to alleviate dietary toxicity risk. Arch Agron Soil Sci 63:1431–1442
Khan MIR, Jahan B, AlAjmi MF, Rehman MT, Iqbal N, Irfan M, Sehar Z, Khan NA (2021) Crosstalk of plant growth regulators protects photosynthetic performance from arsenic damage by modulating defense systems in rice. Ecotoxicol Environ Saf 222:112535
Khan MS, Zaidi A, Wani PA, Oves M (2009) Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ Chem Lett 7:1–19
Kızılkaya R (2008) Yield response and nitrogen concentrations of spring wheat (Triticum aestivum) inoculated with Azotobacter chroococcum strains. Ecol Eng 33:150–156
Kong Z, Glick BR (2017) Chapter Two - The role of plant growth-promoting bacteria in metal phytoremediation. In: Poole RK (ed) Advances in microbial physiology. Academic Press, pp 97–132
Kumar PBAN, Dushenkov V, Motto H, Raskin I (1995) Phytoextraction: the use of plants to remove heavy metals from soils. Environ Sci Technol 29:1232–1238
Lebeau T, Braud A, Jézéquel K (2008) Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: a review. Environ Pollut 153:497–522
Li T, Di Z, Han X, Yang X (2012) Elevated CO2 improves root growth and cadmium accumulation in the hyperaccumulator Sedum alfredii. Plant Soil 354:325–334
Li T, Yang X, Lu L, Islam E, He Z (2009) Effects of zinc and cadmium interactions on root morphology and metal translocation in a hyperaccumulating species under hydroponic conditions. J Hazard Mater 169:734–741
Li T, Yang X, Jin X, He Z, Stoffella PJ, Hu Q (2005) Root responses and metal accumulation in two contrasting ecotypes of Sedum Alfredii hance under lead and zinc toxic stress. J Environ Sci Health, Part A 40:1081–1096
Li Y, Mo L, Zhou X, Yao Y, Ma J, Liu K, Yu F (2022) Characterization of plant growth-promoting traits of Enterobacter sp. and its ability to promote cadmium/lead accumulation in Centella asiatica L. Environ Sci Pollut Res 29:4101–4115
Ma Y, Rajkumar M, Zhang C, Freitas H (2016) Inoculation of Brassica oxyrrhina with plant growth promoting bacteria for the improvement of heavy metal phytoremediation under drought conditions. J Hazard Mater 320:36–44
Madline A, Benidire L, Boularbah A (2021) Alleviation of salinity and metal stress using plant growth-promoting rhizobacteria isolated from semiarid Moroccan copper-mine soils. Environ Sci Pollut Res 28:67185–67202
Manjanatha MG, Loynachan TE, Atherly AG (1992) Tn5 mutagenesis of chinese Rhizobium fredii for siderophore overproduction. Soil Biol Biochem 24:151–155
Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166:525–530
Mitra S, Pramanik K, Sarkar A, Ghosh PK, Soren T, Maiti TK (2018) Bioaccumulation of cadmium by Enterobacter sp. and enhancement of rice seedling growth under cadmium stress. Ecotoxicol Environ Saf 156:183–196
Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170:265–270
Nelson DW (1983) Determination of ammonium in KCl extracts of soils by the salicylate method. Commun Soil Sci Plant Anal 14:1051–1062
Ou Z, Chen Y, Niu X, He W, Song B, Fan D, Sun X (2017) High-mobility group box 1 regulates cytoprotective autophagy in a mouse spermatocyte cell line (GC-2spd) exposed to cadmium. Ir J Med Sci 186:1041–1050
Pan F, Meng Q, Luo S, Shen J, Chen B, Khan KY, Japenga J, Ma X, Yang X, Feng Y (2017) Enhanced Cd extraction of oilseed rape (Brassica napus) by plant growth-promoting bacteria isolated from Cd hyperaccumulator Sedum alfredii Hance. Int J Phytoremediat 19:281–289
Peng J, Zhang S, Han Y, Bate B, Ke H, Chen Y (2022) Soil heavy metal pollution of industrial legacies in China and health risk assessment. Sci Total Environ 816:151632
Piñeros MA, Shaff JE, Kochian LV (1998) Development, characterization, and application of a cadmium-selective microelectrode for the measurement of cadmium fluxes in roots of Thlaspi species and wheat1. Plant Physiol 116:1393–1401
Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149
Rezapour S, Atashpaz B, Moghaddam SS, Damalas CA (2019) Heavy metal bioavailability and accumulation in winter wheat (Triticum aestivum L.) irrigated with treated wastewater in calcareous soils. Sci Total Environ 656:261–269
Rodrı́guez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339
RoyChowdhury A, Datta R, Sarkar D (2018) Chapter 3.10 - Heavy metal pollution and remediation. In: Török B, Dransfield T (eds) Green chemistry. Elsevier, pp 359–373
Saleh SS, Glick BR (2001) Involvement of gacS and rpoS in enhancement of the plant growth-promoting capabilities of Enterobacter cloacae CAL2 and UW4. Can J Microbiol 47:698–705
Sanità di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130
Sheng X, Xia J, Jiang C, He L, Qian M (2008) Characterization of heavy metal-resistant endophytic bacteria from rape (Brassica napus) roots and their potential in promoting the growth and lead accumulation of rape. Environ Pollut 156:1164–1170
Singh S, Singh A, Srivastava PK, Prasad SM (2018) Cadmium toxicity and its amelioration by kinetin in tomato seedlings vis-à-vis ascorbate-glutathione cycle. J Photochem Photobiol B 178:76–84
Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Springer Netherlands, Dordrecht, pp 321–362
Vara Prasad MN, de Oliveira Freitas HM (2003) Metal hyperaccumulation in plants: biodiversity prospecting for phytoremediation technology. Electron J Biotechnol 6:285–321
Wang R, Tian H, Shi Y, Li X (2020) Experimental study on introduction and planting of spring rape varieties in northern Shanxi. Agric Technol Equip 366:3
Weng B, Xie X, Weiss DJ, Liu J, Lu H, Yan C (2012) Kandelia obovata (S., L.) Yong tolerance mechanisms to cadmium: subcellular distribution, chemical forms and thiol pools. Mar Pollut Bull 64:2453–2460
Wu B, He T, Wang Z, Qiao S, Wang Y, Xu F, Xu H (2020) Insight into the mechanisms of plant growth promoting strain SNB6 on enhancing the phytoextraction in cadmium contaminated soil. J Hazard Mater 385:121587
Yang Y, Xiong J, Tao L, Cao Z, Tang W, Zhang J, Yu X, Fu G, Zhang X, Lu Y (2020) Regulatory mechanisms of nitrogen (N) on cadmium (Cd) uptake and accumulation in plants: a review. Sci Total Environ 708:135186
Yahaghi Z, Shirvani M, Nourbakhsh F, De La Pena TC, Pueyo JJ, Talebi M (2018) Isolation and characterization of Pb-solubilizing bacteria and their effects on Pb uptake by Brassica juncea: implications for microbe-assisted phytoremediation. J Microbiol Biotechnol 28:1156–1167
Zhang F, Zhang J, Chen L, Shi X, Lui Z, Li C (2015) Heterologous expression of ACC deaminase from Trichoderma asperellum improves the growth performance of Arabidopsis thaliana under normal and salt stress conditions. Plant Physiol Biochem 94:41–47
Zhang H, Xu Z, Guo K, Huo Y, He G, Sun H, Guan Y, Xu N, Yang W, Sun G (2020a) Toxic effects of heavy metal Cd and Zn on chlorophyll, carotenoid metabolism and photosynthetic function in tobacco leaves revealed by physiological and proteomics analysis. Ecotoxicol Environ Saf 202:110856
Zhao T, Deng X, Xiao Q, Han Y, Zhu S, Chen J (2020) IAA priming improves the germination and seedling growth in cotton (Gossypium hirsutum L.) via regulating the endogenous phytohormones and enhancing the sucrose metabolism. Ind Crops Prod 155:112788
Zhang Y, Ouyang S, Nie L, Chen X (2020b) Soil diatom communities and their relation to environmental factors in three types of soil from four cities in central-west China. Eur J Soil Biol 98:103175
Zhuang X, Chen J, Shim H, Bai Z (2007) New advances in plant growth-promoting rhizobacteria for bioremediation. Environ Int 33:406–413
Funding
This study was supported by the National Key Research and Development Program of China (2018YFC1801703) and the Open Project of Key Laboratory for Green Chemical Process of Ministry of Education (GCP202110).
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Zhang, Y., Wu, X., Tao, Y. et al. Effect of plant growth–promoting rhizobacteria on oilseed rape Brassica juncea and phytoextraction of cadmium. J Soils Sediments 23, 3472–3484 (2023). https://doi.org/10.1007/s11368-023-03559-y
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DOI: https://doi.org/10.1007/s11368-023-03559-y