{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,1]],"date-time":"2026-06-01T14:09:54Z","timestamp":1780322994930,"version":"3.54.1"},"reference-count":97,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2021,1,23]],"date-time":"2021-01-23T00:00:00Z","timestamp":1611360000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001321","name":"National Research Foundation","doi-asserted-by":"publisher","award":["TTK14052968076"],"award-info":[{"award-number":["TTK14052968076"]}],"id":[{"id":"10.13039\/501100001321","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001321","name":"National Research Foundation","doi-asserted-by":"publisher","award":["TTK150713125714"],"award-info":[{"award-number":["TTK150713125714"]}],"id":[{"id":"10.13039\/501100001321","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001321","name":"National Research Foundation","doi-asserted-by":"publisher","award":["SFH13082430507"],"award-info":[{"award-number":["SFH13082430507"]}],"id":[{"id":"10.13039\/501100001321","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>Combretum erythrophyllum is an indigenous southern African tree species, a metal hyperaccumulator that has been used as a phytoextraction option for tailing dams in Johannesburg, South Africa. In hyperaccumulators, metal detoxification has also been linked or attributed to the activities of endophytes, and, in this regard, metal detoxification can be considered a form of endophytic behavior. Therefore, we report herein on the identification of proteins that confer heavy metal resistance, the in vitro characterization of heavy metal resistance, and the production of plant growth-promoting (PGP) volatiles by Methylobacterium radiotolerans MAMP 4754. Multigenome comparative analyses of M. radiotolerans MAMP 4754 against eight other endophytic strains led to the identification of zinc, copper, and nickel resistance proteins in the genome of this endophyte. The maximum tolerance concentration (MTC) of this strain towards these metals was also investigated. The metal-exposed cells were analyzed by transmission electron microscopy (TEM). The ethyl acetate and chloroform extracts (1:1 v\/v) of heavy metal untreated M. radiotolerans MAMP 4754 were also screened for the production of PGP compounds by Gas Chromatography\u2013Mass Spectroscopy (GC\/MS). The MTC was recorded at 15 mM, 4 mM, and 12 mM for zinc, copper, and nickel, respectively. The TEM analysis showed the accumulation of metals in the intracellular environment of M. radiotolerans MAMP 4754, while the GC\/MS analysis revealed several plant growth-promoting compounds, including alcohols, phthalate esters, alkenes, ketones, sulfide derivatives, phenols, and thiazoles. Our findings suggest that the genetic makeup of M. radiotolerans MAMP 4754 encodes heavy metal resistant proteins that indicate hyperaccumulator-specific endophytic behavior and the potential for application in bioremediation. The production of plant growth-promoting volatiles in pure culture by M. raditotolerans MAMP 4754 is a characteristic feature for plant growth-promoting bacteria.<\/jats:p>","DOI":"10.3390\/ijerph18030997","type":"journal-article","created":{"date-parts":[[2021,1,25]],"date-time":"2021-01-25T02:07:00Z","timestamp":1611540420000},"page":"997","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":30,"title":["Genomic and Physiological Investigation of Heavy Metal Resistance from Plant Endophytic Methylobacterium radiotolerans MAMP 4754, Isolated from Combretum erythrophyllum"],"prefix":"10.3390","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6912-8238","authenticated-orcid":false,"given":"Mampolelo M.","family":"Photolo","sequence":"first","affiliation":[{"name":"Department of Biochemistry, Faculty of Science, Auckland Park Campus, University of Johannesburg, Johannesburg 2092, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0739-9504","authenticated-orcid":false,"given":"Lungile","family":"Sitole","sequence":"additional","affiliation":[{"name":"Department of Biochemistry, Faculty of Science, Auckland Park Campus, University of Johannesburg, Johannesburg 2092, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4672-6176","authenticated-orcid":false,"given":"Vuyo","family":"Mavumengwana","sequence":"additional","affiliation":[{"name":"DST-NRF Centre of Excellence for Biomedical Tuberculosis Research, South African Medical Research Council Centre for Tuberculosis Research, Division of Molecular Biology and Human Genetics, Faculty of Medicine and Health Sciences, Tygerberg Campus, Stellenbosch University, Cape Town 7505, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3757-2630","authenticated-orcid":false,"given":"Matsobane G.","family":"Tlou","sequence":"additional","affiliation":[{"name":"Department of Biochemistry, School of Physical and Chemical Sciences, Faculty of Natural and Agricultural Sciences, Mafikeng Campus, North-West University, Mafikeng 2790, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,1,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1080\/19490976.2018.1526581","article-title":"Immobilization of Cadmium and Lead by Lactobacillus rhamnosus GR-1 Mitigates Apical-to-basolateral Heavy Metal Translocation in a Caco-2 Model of the Intestinal Epithelium","volume":"10","author":"Daisley","year":"2019","journal-title":"Gut Microbes"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"834","DOI":"10.1007\/BF01935534","article-title":"Heavy Metal Accumulation by Bacteria and other Microorganisms","volume":"46","author":"Gadd","year":"1990","journal-title":"Experientia"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1016\/S0005-2736(00)00133-4","article-title":"Emerging Mechanisms for Heavy Metal Transport in Plants","volume":"1465","author":"Williams","year":"2000","journal-title":"Biochim. Biophys. Acta Biomembr."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"655","DOI":"10.1016\/j.jhazmat.2008.03.038","article-title":"Biosorption of Cadmium (II), Zinc (II) and Lead (II) by Penicillium simplicissimum: Isotherms, Kinetics and Thermodynamics","volume":"160","author":"Fan","year":"2008","journal-title":"J. Hazard. Mater."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"998","DOI":"10.1007\/s00244-009-9417-5","article-title":"Heavy Metal Concentrations in Food Chain of Lake Velenjsko Jezero, Slovenia: An Artificial Lake from Mining","volume":"58","author":"Mazej","year":"2010","journal-title":"Arch. Environ. Contam. Toxicol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1021\/es60074a004","article-title":"Contamination of Soil and Vegetation near a Zinc Smelter by Zinc, Cadmium, Copper, and Lead","volume":"7","author":"Buchauer","year":"1973","journal-title":"Environ. Sci. Technol."},{"key":"ref_7","unstructured":"Alloway, B.J. (1990). Heavy Metals in Soils, John Willey and Sons Inc."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1016\/0958-1669(94)90030-2","article-title":"Bioconcentration of Heavy Metals by Plants","volume":"5","author":"Raskin","year":"1994","journal-title":"Curr. Opin. Biotechnol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1893","DOI":"10.2134\/jeq2002.1893","article-title":"Lead Phytoextraction from Contaminated Soil with High-biomass Plant Species","volume":"31","author":"Shen","year":"2002","journal-title":"J. Environ. Qual."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1186\/2052-336X-12-44","article-title":"The Study of Nickel Resistant Bacteria (NiRB) Isolated from Wastewaters Polluted with Different Industrial Sources","volume":"12","author":"Alboghobeish","year":"2014","journal-title":"J. Environ. Health Sci. Eng."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"831","DOI":"10.5897\/AJMR10.860","article-title":"Multi-Metal Resistance Study of Bacteria Highly Resistant to Mercury Isolated from Dental Clinic Effluent","volume":"5","author":"Keramati","year":"2011","journal-title":"Afr. J. Microbiol. Res."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/S0923-2508(02)01303-7","article-title":"Feasibility of Copper Uptake by the Yeast Pichia guilliermondii Isolated from Sewage Sludge","volume":"153","author":"Balsalobre","year":"2002","journal-title":"Res. Microbiol."},{"key":"ref_13","unstructured":"Raskin, I., and Ensley, B.D. (2000). Phytoremediation of Toxic Metals, John Wiley and Sons."},{"key":"ref_14","first-page":"921","article-title":"Phytoremediation of Heavy Metals: Recent Techniques","volume":"8","author":"Jadia","year":"2009","journal-title":"Afr. J. Biotechnol."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Prasad, M.N.V. (2004). Phytoremediation of Metals and Radionuclides in the Environment: The Case for Natural Hyperaccumulators, Metal Transporters, Soil-amending Chelators and Transgenic Plants. Heavy Metal Stress in Plants, Springer.","DOI":"10.1007\/978-3-662-07743-6_14"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1080\/15226510802378368","article-title":"Phytoremediation of Inorganics: Realism and Synergies","volume":"11","author":"Dickinson","year":"2009","journal-title":"Int. J. Phytoremediat."},{"key":"ref_17","first-page":"1","article-title":"Perennial Plants in the Phytoremediation of Lead-Contaminated Soils","volume":"5","author":"Kurukote","year":"2006","journal-title":"Biotechnology"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Regnier, T.C., Kouekam, C.R., Leonard, C.M., Mokgalaka, N.S., and Weiersbye, I.M. (2009, January 9\u201311). Chemical Analysis and Potential use of the Tree Combretum erythrophyllum Grown on Gold and Uranium Mine Tailings Seepage. Proceedings of the Fourth International Conference on Mine Closure, Perth, Australia.","DOI":"10.36487\/ACG_repo\/908_42"},{"key":"ref_19","unstructured":"Weiersbye, I.M., and Cukrowska, E.M. (2008). Elemental Concentrations in Wild Plants and Crops on the Witwatersrand Basin Gold Fields: Recommendations for Safe Land-Uses, Witwatersrand University. AngloGold Ashanti Report."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1339","DOI":"10.1007\/s10311-018-0762-3","article-title":"Phytoremediation of Heavy Metals: Mechanisms, Methods and Enhancements","volume":"16","author":"Muthusaravanan","year":"2018","journal-title":"Environ. Chem. Lett."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1029","DOI":"10.1016\/S0160-4120(03)00091-6","article-title":"Phytoaccumulation of Heavy Metals by Aquatic Plants","volume":"29","author":"Kamal","year":"2004","journal-title":"Environ. Int."},{"key":"ref_22","unstructured":"Berti, W.R., and Cunningham, S.D. (2000). Phytostabilization of Metals, John Willey and Sons Inc."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1016\/j.copbio.2004.04.006","article-title":"Phytodegradation of Organic Compounds","volume":"15","author":"Newman","year":"2004","journal-title":"Curr. Opin. Biotechnol."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Zayed, A.M., Pilon-Smits, E., deSouza, E.M., Lin, Z.-Q., and Terry, N. (2000). Remediation of Selenium-Polluted Soils and Waters by Phytovolatilization. Phytoremediation of Contaminated Soil and Water, Lewis Publishers.","DOI":"10.1201\/9781439822654.ch4"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"8599","DOI":"10.1016\/j.biortech.2010.06.085","article-title":"Bioremediation of Heavy Metals by Growing Hyperaccumulaor Endophytic Bacterium Bacillus sp. L14","volume":"101","author":"Guo","year":"2010","journal-title":"Bioresour. Technol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1016","DOI":"10.3389\/fmicb.2016.01016","article-title":"Exploitation of Endophytic Bacteria to Enhance the Phytoremediation Potential of the Wetland Helophyte Juncus acutus","volume":"7","author":"Syranidou","year":"2016","journal-title":"Front. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"9589","DOI":"10.1007\/s00253-013-5235-9","article-title":"Endophytic Microorganisms\u2014Promising Applications in Bioremediation of Greenhouse Gases","volume":"97","year":"2013","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"10050","DOI":"10.1021\/acs.est.7b01504","article-title":"Enhanced Degradation of TCE on a Superfund Site using Endophyte-assisted Poplar Tree Phytoremediation","volume":"51","author":"Doty","year":"2017","journal-title":"Environ. Sci. Technol."},{"key":"ref_29","first-page":"575","article-title":"Investigating the Effects of Plant Growth-Promoting Bacteria and Glomus Mosseae on Cadmium Phytoremediation by Eucalyptus camaldulensis L.","volume":"3","author":"Motesharezadeh","year":"2017","journal-title":"Pollution"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"847","DOI":"10.1016\/j.tibtech.2017.05.001","article-title":"Biotechnological Advances for Restoring Degraded Land for Sustainable Development","volume":"35","author":"Tripathi","year":"2017","journal-title":"Trends Biotechnol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"498","DOI":"10.1111\/jam.13505","article-title":"Influence of Endophytic Root Bacteria on the Growth, Cadmium Tolerance and Uptake of Switchgrass (Panicum virgatum L.)","volume":"123","author":"Afzal","year":"2017","journal-title":"J. Appl. Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1016\/j.biotechadv.2009.06.003","article-title":"Genetically Modified Plants in Phytoremediation of Heavy Metal and Metalloid Soil and Sediment Pollution","volume":"27","author":"Kotrba","year":"2009","journal-title":"Biotechnol. Adv."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1106","DOI":"10.1104\/pp.114.242750","article-title":"Metabolism-Based Herbicide Resistance and Cross-resistance in Crop Weeds: A Threat to Herbicide Sustainability and Global Crop Production","volume":"166","author":"Yu","year":"2014","journal-title":"Plant Physiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.micres.2015.11.008","article-title":"Plant Growth-Promoting Bacterial Endophytes","volume":"183","author":"Santoyo","year":"2016","journal-title":"Microbiol. Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1492","DOI":"10.1007\/s11368-015-1253-9","article-title":"Phytoremediation of Soils Contaminated by Organic Compounds: Hype, Hope and Facts","volume":"17","year":"2017","journal-title":"J. Soils Sediments"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.ecoenv.2017.08.032","article-title":"Bacterial Mediated Alleviation of Heavy Metal Stress and Decreased Accumulation of Metals in Plant Tissues: Mechanisms and Future Prospects","volume":"147","author":"Etesami","year":"2018","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1016\/j.jhazmat.2013.02.014","article-title":"Enhancement of Heavy Metal Phytoremediation by Alnus Firma with Endophytic Bacillus thuringiensis GDB-1","volume":"250","author":"Babu","year":"2013","journal-title":"J. Hazard. Mater."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1007\/s10725-018-0391-7","article-title":"Interactions between Plant Hormones and Thiol-related Heavy Metal Chelators","volume":"85","author":"Janda","year":"2018","journal-title":"Plant Growth Regul."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.micres.2006.07.014","article-title":"Bacteria Associated with Orchid Roots and Microbial Production of Auxin","volume":"162","author":"Tsavkelova","year":"2007","journal-title":"Microbiol. Res."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"9483670","DOI":"10.1155\/2020\/9483670","article-title":"Antimicrobial and Antioxidant Properties of a Bacterial Endophyte, Methylobacterium radiotolerans MAMP 4754, Isolated from Combretum erythrophyllum Seeds","volume":"2020","author":"Photolo","year":"2020","journal-title":"Int. J. Microbiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s13205-018-1403-z","article-title":"Complete Genome Sequencing and Analysis of Endophytic Sphingomonas sp. LK11 and its Potential in Plant Growth","volume":"8","author":"Asaf","year":"2018","journal-title":"3 Biotech"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1016\/j.jenvman.2015.03.024","article-title":"The Hyperaccumulator Sedum plumbizincicola Harbors Metal-Resistant Endophytic Bacteria that Improve its Phytoextraction Capacity in Multi-Metal Contaminated Soil","volume":"156","author":"Ma","year":"2015","journal-title":"J. Environ. Manag."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1016\/j.jtbi.2013.10.007","article-title":"A Bioinformatics Approach to the Determination of Genes Involved in Endophytic Behavior in Burkholderia spp.","volume":"343","author":"Ali","year":"2014","journal-title":"J. Theor. Biol."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Wall, D.P., and DeLuca, T. (2007). Ortholog Detection using the Reciprocal Smallest Distance Algorithm. Comparative Genomics, Humana Press.","DOI":"10.1007\/978-1-59745-515-2_7"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"2269","DOI":"10.1099\/ijs.0.02902-0","article-title":"Methylobacterium nodulans sp. nov., for a Group of Aerobic, Facultatively Methylotrophic, Legume Root-Nodule-Forming and Nitrogen-Fixing Bacteria","volume":"54","author":"Jourand","year":"2004","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"e00356-13","DOI":"10.1128\/genomeA.00356-13","article-title":"Draft Genome Sequence of Methylobacterium Mesophilicum Strain SR1. 6\/6, Isolated from Citrus Sinensis","volume":"1","author":"Almeida","year":"2013","journal-title":"Genome Announc."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e00976-17","DOI":"10.1128\/genomeA.00976-17","article-title":"Draft Genome Sequence of Methylobacterium radiotolerans Strain MAMP 4754, a Bacterial Endophyte Isolated from Combretum erythrophyllum in South Africa","volume":"5","author":"Photolo","year":"2017","journal-title":"Genome Announc."},{"key":"ref_48","unstructured":"Copeland, A., Lucas, S., Lapidus, A., Glavina Del Rio, T., Dalin, E., Tice, H., Bruce, D., Goodwin, L., Pitluck, S., and Chertkov, O. (2008). Complete Sequence of Chromosome of Methylobacterium sp., US DOE Joint Genome Institute."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Wisniewski-Dy\u00e9, F., Borziak, K., Khalsa-Moyers, G., Alexandre, G., Sukharnikov, L.O., Wuichet, K., Hurst, G.B., McDonald, W.H., Robertson, J.S., and Barbe, V. (2011). Azospirillum Genomes Reveal Transition of Bacteria from Aquatic to Terrestrial Environments. PLoS Genet., 7.","DOI":"10.1371\/journal.pgen.1002430"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"3383","DOI":"10.1128\/JB.05055-11","article-title":"Complete Genome Sequence of the Plant Growth-Promoting Endophyte Burkholderia phytofirmans strain PsJN","volume":"193","author":"Weilharter","year":"2011","journal-title":"J. Bacteriol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"5965","DOI":"10.1128\/JB.01394-12","article-title":"Complete Genome Sequence of the Endophytic Enterobacter cloacae subsp. cloacae strain ENHKU01","volume":"194","author":"Liu","year":"2012","journal-title":"J. Bacteriol."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Taghavi, S., van der Lelie, D., Hoffman, A., Zhang, Y.B., Walla, M.D., Vangronsveld, J., Newman, L., and Monchy, S. (2010). Genome Sequence of the Plant Growth-Promoting Endophytic Bacterium Enterobacter sp. 638. PLoS Genet., 6.","DOI":"10.1371\/journal.pgen.1000943"},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Fouts, D.E., Tyler, H.L., DeBoy, R.T., Daugherty, S., Ren, Q., Badger, J.H., Durkin, A.S., Huot, H., Shrivastava, S., and Kothari, S. (2008). Complete Genome Sequence of the N2-fixing Broad Host Range Endophyte Klebsiella pneumoniae 342 and Virulence Predictions Verified in Mice. PLoS Genet., 4.","DOI":"10.1371\/journal.pgen.1000141"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"748","DOI":"10.1128\/AEM.02239-08","article-title":"Genome Survey and Characterization of Endophytic Bacteria Exhibiting a Beneficial Effect on Growth and Development of Poplar Trees","volume":"75","author":"Taghavi","year":"2009","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_55","first-page":"1495","article-title":"An Inducible Activator Produced by a Serratia proteamaculans Strain and Its Soybean Growth-promoting Activity Under Greenhouse Conditions","volume":"53","author":"Bai","year":"2002","journal-title":"J. Exp. Bot."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"2218","DOI":"10.1128\/aem.61.6.2218-2223.1995","article-title":"Genes Essential for Amber Disease in Grass Grubs Are Located on the Large Plasmid Found in Serratia entomophila and Serratia proteamaculans","volume":"61","author":"Grkovic","year":"1995","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_57","first-page":"34","article-title":"Toxic Heavy Metals Tolerance in Bacterial Isolates Based on their Inducible Mechanism","volume":"2","author":"Vashishth","year":"2015","journal-title":"Int. J. Novel Res. Life Sci."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"955","DOI":"10.3389\/fpls.2016.00955","article-title":"\u201cOmics\u201d Tools for Better Understanding the Plant\u2014Endophyte Interactions","volume":"7","author":"Kaul","year":"2016","journal-title":"Front. Plant Sci."},{"key":"ref_59","unstructured":"Mattoo, A.K., and Suttle, J.C. (1991). Ethylene in root growth and development. The Plant Hormone Ethylene, CRC Press."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/S0168-6445(03)00049-4","article-title":"Escherichia Coli Mechanisms of Copper Homeostasis in a Changing Environment","volume":"27","author":"Rensing","year":"2003","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1111\/j.1574-6941.2007.00365.x","article-title":"Genetic Structure and Diversity of Copper Resistant Bacterial Communities According to Soil Types, Organic Status and Copper Contamination","volume":"61","author":"Lejon","year":"2007","journal-title":"FEMS Microbiol. Ecol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1146\/annurev.micro.112408.134247","article-title":"TonB-Dependent Transporters: Regulation, Structure, and Function","volume":"64","author":"Noinaj","year":"2010","journal-title":"Ann. Rev. Microbiol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1038\/hdy.2016.106","article-title":"Evidence of Prokaryote like Protein Associated with Nickel Resistance in Higher Plants: Horizontal Transfer of TonB-Dependent Receptor\/Protein in Betula Genus or de Novo Mechanisms?","volume":"118","author":"Theriault","year":"2017","journal-title":"Heredity"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"19735","DOI":"10.1074\/jbc.M002232200","article-title":"Regulation of High Affinity Nickel Uptake in Bacteria Ni2+-Dependent Interaction of NikR with Wild-type and Mutant Operator Sites","volume":"275","author":"Chivers","year":"2000","journal-title":"J. Biol. Chem."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"887","DOI":"10.1002\/tox.22100","article-title":"Regulations of Essential Amino Acids and Proteomics of Bacterial Endophytes Sphingomonas sp. L k11 During Cadmium Uptake","volume":"31","author":"Khan","year":"2016","journal-title":"Environ. Toxicol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"809","DOI":"10.1016\/j.scitotenv.2015.10.117","article-title":"Screening of Native Plant Species for Phytoremediation Potential at a Hg-contaminated Mining Site","volume":"542","year":"2016","journal-title":"Sci. Total Environ."},{"key":"ref_67","unstructured":"Guerra, F., Gainza, F., P\u00e9rez, R., and Zamudio, F. (2011). Phytoremediation of Heavy Metals Using Poplars (Populus spp.): A Glimpse of the Plant Responses to Copper, Cadmium and Zinc Stress. Handbook of Phytoremediation, Nova Science."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1080\/17429145.2014.894587","article-title":"Plant Growth-Promoting Rhizobacteria Reduce Adverse Effects of Salinity and Osmotic Stress by Regulating Phytohormones and Antioxidants in Cucumis sativus","volume":"9","author":"Kang","year":"2014","journal-title":"J. Plant Interact."},{"key":"ref_69","doi-asserted-by":"crossref","unstructured":"Dourado, M.N., Ferreira, A., Ara\u00fajo, W.L., Azevedo, J.L., and Lacava, P.T. (2012). The Diversity of Endophytic Methylotrophic Bacteria in an Oil-contaminated and an Oil-free Mangrove Ecosystem and their Tolerance to Heavy Metals. Biotechnol. Res. Int., 2012.","DOI":"10.1155\/2012\/759865"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1111\/nph.16022","article-title":"On the Evolutionary Significance of Horizontal Gene Transfers in Plants","volume":"225","author":"Wickell","year":"2019","journal-title":"N. Phytol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1016\/j.tree.2010.06.001","article-title":"Promiscuous DNA: Horizontal Transfer of Transposable Elements and Why It Matters for Eukaryotic Evolution","volume":"25","author":"Schaack","year":"2010","journal-title":"Trends Ecol. Evol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1146\/annurev.phyto.38.1.325","article-title":"Role of Horizontal Gene Transfer in the Evolution of Fungi","volume":"38","author":"Rosewich","year":"2000","journal-title":"Ann. Rev. Phytopathol."},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Wang, X., Chen, M., Xiao, J., Hao, L., Crowley, D.E., Zhang, Z., Yu, J., Huang, N., Huo, M., and Wu, J. (2015). Genome Sequence Analysis of the Naphthenic Acid Degrading and Metal Resistant Bacterium Cupriavidus gilardii CR3. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0132881"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"e0170080","DOI":"10.1590\/18069657rbcs20170080","article-title":"Tolerance to and Accumulation of Cadmium, Copper, and Zinc by Cupriavidus necator","volume":"42","author":"Vicentin","year":"2018","journal-title":"Revista Brasileira de Ci\u00eancia do Solo"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2018\/2568038","article-title":"Toxicity and Bioremediation of Heavy Metals Contaminated Ecosystem from Tannery Wastewater: A Review","volume":"2018","author":"Igiri","year":"2018","journal-title":"J. Toxicol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1080\/07929978.1996.10676631","article-title":"Root Elongation in Various Agronomic Crops by the Plant Growth-Promoting Rhizobacterium Pseudomonas putida GR12\u20132","volume":"44","author":"Hall","year":"1996","journal-title":"Isr. J. Plant Sci."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1006\/jtbi.1997.0532","article-title":"A Model for the Lowering of Plant Ethylene Concentrations by Plant Growth-Promoting Bacteria","volume":"190","author":"Glick","year":"1998","journal-title":"J. Theor. Biol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.1007\/s00253-008-1760-3","article-title":"Bacterial Volatiles and Their Action Potential","volume":"81","author":"Kai","year":"2009","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_79","doi-asserted-by":"crossref","unstructured":"Vaishnav, A., Varma, A., Tuteja, N., and Choudhary, D.K. (2017). PGPR-Mediated Amelioration of Crops Under Salt Stress. Plant-Microbe Interaction: An Approach to Sustainable Agriculture, Springer.","DOI":"10.1007\/978-981-10-2854-0_10"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"2209","DOI":"10.1111\/mpp.12691","article-title":"Heat Shock Transcription Factor 3 Regulates Plant Immune Response Through Modulation of Salicylic Acid Accumulation and Signalling in Cassava","volume":"19","author":"Wei","year":"2018","journal-title":"Mol. Plant Pathol."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"196","DOI":"10.3389\/fmicb.2016.00196","article-title":"Are bacterial volatile compounds poisonous odors to a fungal pathogen Botrytis cinerea, alarm signals to Arabidopsis seedlings for eliciting induced resistance, or both?","volume":"7","author":"Sharifi","year":"2016","journal-title":"Front. Microbiol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1007\/s13199-010-0066-2","article-title":"Plant Growth-Promoting Rhizobacteria Modulate Root-system Architecture in Arabidopsis thaliana through Volatile Organic Compound Emission","volume":"51","year":"2010","journal-title":"Symbiosis"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"892","DOI":"10.1007\/s10886-013-0315-y","article-title":"Production of Bioactive Volatiles by Different Burkholderia ambifaria strains","volume":"39","author":"Groenhagen","year":"2013","journal-title":"J. Chem. Ecol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"729","DOI":"10.1007\/s00248-011-9818-7","article-title":"An Endophytic Phomopsis sp. Possessing Bioactivity and Fuel Potential with its Volatile Organic Compounds","volume":"61","author":"Singh","year":"2011","journal-title":"Microb. Ecol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"96","DOI":"10.5943\/ppq\/7\/2\/2","article-title":"Potential Effect of Piriformospora indica on Plant Growth and Essential Oil Yield in Mentha piperita","volume":"7","author":"Dolatabad","year":"2017","journal-title":"Plant. Pathol. Quar."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"1629","DOI":"10.1016\/j.soilbio.2008.01.018","article-title":"Volatile Organic Compound (VOC) Emissions from Soil and Litter Samples","volume":"40","author":"Leff","year":"2008","journal-title":"Soil Biol. Biochem."},{"key":"ref_87","doi-asserted-by":"crossref","unstructured":"Shah, S., Shrestha, R., Maharjan, S., Selosse, M.A., and Pant, B. (2019). Isolation and Characterization of Plant Growth-promoting Endophytic Fungi from the Roots of Dendrobium moniliforme. Plants, 8.","DOI":"10.3390\/plants8010005"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"955","DOI":"10.1016\/j.soilbio.2004.10.021","article-title":"Identification and Use of Potential Bacterial Organic Antifungal Volatiles in Biocontrol","volume":"37","author":"Fernando","year":"2005","journal-title":"Soil Biol. Biochem."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"1274","DOI":"10.1002\/jobm.201600188","article-title":"PGPR-Mediated Expression of Salt Tolerance Gene in Soybean Through Volatiles Under Sodium Nitroprusside","volume":"56","author":"Vaishnav","year":"2016","journal-title":"J. Basic Microbiol."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"2731","DOI":"10.1105\/tpc.113.114744","article-title":"Dimethyl Disulfide Produced by the Naturally Associated Bacterium Bacillus sp. B55 Promotes Nicotiana attenuata Growth by Enhancing Sulfur Nutrition","volume":"25","author":"Meldau","year":"2013","journal-title":"Plant Cell"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1093\/chromsci\/bms012","article-title":"Separation and Identification of Volatile Compounds from Liquid Cultures of Trichoderma harzianum by GC-MS Using Three Different Capillary Columns","volume":"50","author":"Siddiquee","year":"2012","journal-title":"J. Chromatogr. Sci."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1016\/j.jhazmat.2009.10.066","article-title":"Effects of Cadmium Stress on Growth and Anti-Oxidative Systems in Achnatherum inebrians Symbiotic with Neotyphodium gansuense","volume":"175","author":"Zhang","year":"2010","journal-title":"J. Hazard. Mater."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1016\/j.plaphy.2008.11.007","article-title":"Exogenous Treatment with Salicylic Acid Attenuates Cadmium Toxicity in Pea Seedlings","volume":"47","author":"Popova","year":"2009","journal-title":"Plant Physiol. Biochem."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1016\/j.cj.2016.01.010","article-title":"Phytohormones and Their Metabolic Engineering for Abiotic Stress Tolerance in Crop Plants","volume":"4","author":"Wani","year":"2016","journal-title":"Crop J."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1094\/MPMI-3-004","article-title":"Phenolic Compounds as Regulators of Gene Expression in Plant-Microbe Interactions","volume":"3","author":"Peters","year":"1990","journal-title":"Mol. Plant Microbe Interact."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1111\/j.1469-8137.2008.02583.x","article-title":"Salt Tolerance of Barley Induced by the Root Endophyte Piriformospora indica is Associated with a Strong Increase in Antioxidants","volume":"180","author":"Baltruschat","year":"2008","journal-title":"N. Phytol."},{"key":"ref_97","first-page":"59","article-title":"In Vitro Biocontrol Activity of Methylobacterium extorquens against Fungal Pathogens","volume":"2","author":"Poorniammal","year":"2009","journal-title":"Int. J. Plant Prot."}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/18\/3\/997\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:14:25Z","timestamp":1760159665000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/18\/3\/997"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,1,23]]},"references-count":97,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2021,2]]}},"alternative-id":["ijerph18030997"],"URL":"https:\/\/doi.org\/10.3390\/ijerph18030997","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,1,23]]}}}