Although the pesticide hexachlorocyclohexane (HCH) and its isomers have long been banned, their presence in the environment is still reported worldwide. In this study, we investigated the bioaccumulation potential of α, β, and δ hexachlorocyclohexane (HCH) isomers in black alder saplings (Alnus glutinosa) to assess their environmental impact. Each isomer, at a concentration of 50 mg/kg, was individually mixed with soil, and triplicate setups, including a control without HCH, were monitored for three months with access to water. Gas chromatography-mass spectrometry revealed the highest concentrations of HCH isomers in roots, decreasing towards branches and leaves, with δ-HCH exhibiting the highest uptake (roots-14.7 µg/g, trunk-7.2 µg/g, branches-1.53 µg/g, leaves-1.88 µg/g). Interestingly, α-HCH was detected in high concentrations in β-HCH polluted soil. Phytohormone analysis indicated altered cytokinin, jasmonate, abscisate, and gibberellin levels in A. glutinosa in response to HCH contamination. In addition, amplicon 16S rRNA sequencing was used to study the rhizosphere and soil microbial community. While rhizosphere microbial populations were generally similar in all HCH isomer samples, Pseudomonas spp. decreased across all HCH-amended samples, and Tomentella dominated in β-HCH and control rhizosphere samples but was lowest in δ-HCH samples.

Faculty of Mechatronics Informatics and Interdisciplinary Studies Technical University of Liberec 461 17 Liberec Czech Republic

Faculty of Science Humanities and Education Technical University of Liberec 460 01 Liberec Czech Republic

Institute for Nanomaterials Advanced Technologies and Innovation Technical University of Liberec 460 01 Liberec Czech Republic

Laboratory for Inherited Metabolic Disorders Department of Clinical Biochemistry University Hospital Olomouc and Faculty of Medicine and Dentistry Palacký University Olomouc 775 20 Olomouc Czech Republic

Laboratory of Growth Regulators Institute of Experimental Botany Czech Academy of Sciences and Faculty of Science Palacký University Olomouc 78371 Olomouc Czech Republic

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Bailey RE, van Wijk D, Thomas PC. Sources and prevalence of pentachlorobenzene in the environment. Chemosphere. 2009;75:555–564. doi: 10.1016/j.chemosphere.2009.01.038. PubMed DOI

Barber JL, Sweetman AJ, van Wijk D, Jones KC. Hexachlorobenzene in the global environment: Emissions, levels, distribution, trends and processes. Sci. Total Environ. 2005;349:1–44. doi: 10.1016/j.scitotenv.2005.03.014. PubMed DOI

Vijgen J, et al. Hexachlorocyclohexane (HCH) as new Stockholm Convention POPs—A global perspective on the management of Lindane and its waste isomers. Environ. Sci. Pollut. Res. 2011;18:152–162. doi: 10.1007/s11356-010-0417-9. PubMed DOI

Fernández J, Arjol MA, Cacho C. POP-contaminated sites from HCH production in Sabiñánigo, Spain. Environ. Sci. Pollut. Res. 2013;20:1937–1950. doi: 10.1007/s11356-012-1433-8. PubMed DOI

Vijgen J, International HCH and Pesticides Association . The Legacy of Lindane Hch Isomer Production: A Global Overview of Residue Management, Formulation and Disposal. International HCH and Pesticides Association; 2006.

Vijgen J, de Borst B, Weber R, Stobiecki T, Forter M. HCH and lindane contaminated sites: European and global need for a permanent solution for a long-time neglected issue. Environ. Pollut. 2019;248:696–705. doi: 10.1016/j.envpol.2019.02.029. PubMed DOI

Vijgen J, et al. European cooperation to tackle the legacies of hexachlorocyclohexane (HCH) and lindane. Emerg. Contam. 2022;8:97–112. doi: 10.1016/j.emcon.2022.01.003. DOI

Dominguez CM, et al. Kinetics of lindane dechlorination by zerovalent iron microparticles: Effect of different salts and stability study. Ind. Eng. Chem. Res. 2016;55:12776–12785. doi: 10.1021/acs.iecr.6b03434. DOI

Homolková M, Hrabák P, Kolář M, Černík M. Degradability of hexachlorocyclohexanes in water using ferrate (VI) Water Sci. Technol. 2015;71:405–411. doi: 10.2166/wst.2014.516. PubMed DOI

Wacławek S, et al. Chemical oxidation and reduction of hexachlorocyclohexanes: A review. Water Res. 2019;162:302–319. doi: 10.1016/j.watres.2019.06.072. PubMed DOI

Wang C-W, Chang S-C, Liang C. Persistent organic pollutant lindane degradation by alkaline cold-brew green tea. Chemosphere. 2019;232:281–286. doi: 10.1016/j.chemosphere.2019.05.187. PubMed DOI

Nagata Y, Miyauchi K, Takagi M. Complete analysis of genes and enzymes for γ-hexachlorocyclohexane degradation in Sphingomonas paucimobilis UT26. J. Ind. Microbiol. Biotechnol. 1999;23:380–390. doi: 10.1038/sj.jim.2900736. PubMed DOI

Lal R, Dogra C, Malhotra S, Sharma P, Pal R. Diversity, distribution and divergence of lin genes in hexachlorocyclohexane-degrading sphingomonads. Trends Biotechnol. 2006;24:121–130. doi: 10.1016/j.tibtech.2006.01.005. PubMed DOI

Amirbekov A, Mamirova A, Sevcu A, Spanek R, Hrabak P. HCH Removal in a Biochar-Amended Biofilter. Water. 2021;13:3396. doi: 10.3390/w13233396. DOI

Becerra-Castro C, et al. Phytoremediation of hexachlorocyclohexane (HCH)-contaminated soils using Cytisus striatus and bacterial inoculants in soils with distinct organic matter content. Environ. Pollut. 2013;178:202–210. doi: 10.1016/j.envpol.2013.03.027. PubMed DOI

Gotelli MJ, Lo Balbo A, Caballero GM, Gotelli CA. Hexachlorocyclohexane phytoremediation using Eucalyptus dunnii of a contaminated site in Argentina. Int. J. Phytoremediat. 2020;22:1129–1136. doi: 10.1080/15226514.2020.1736511. PubMed DOI

Malaiyandi M, Shah SM, Lee P. Fate of α- and γ-hexachlorocyclohexane isomers under simulated environmental conditions. J. Environ. Sci. Health A Environ. Sci. Eng. 1982;17:283–297. doi: 10.1080/10934528209375035. DOI

Lodha B, et al. Bioisomerization kinetics of γ-HCH and biokinetics of Pseudomonas aeruginosa degrading technical HCH. Biochem. Eng. J. 2007;35:12–19. doi: 10.1016/j.bej.2006.12.015. DOI

Vonk JW, Quirijns JK. Anaerobic formation of α-hexachlorocyclohexane from γ-hexachlorocyclohexane in soil and by Escherichia coli. Pestic. Biochem. Physiol. 1979;12:68–74. doi: 10.1016/0048-3575(79)90095-6. DOI

Bromilow RH, Chamberlain K. Principles Governing Uptake and Transport of Chemicals. CRC Press; 1995. pp. 37–68.

Briggs GG, Bromilow RH, Evans AA. Relationships between lipophilicity and root uptake and translocation of non-ionised chemicals by barley. Pestic. Sci. 1982;13:495–504. doi: 10.1002/ps.2780130506. DOI

Dettenmaier EM, Doucette WJ, Bugbee B. Chemical hydrophobicity and uptake by plant roots. Environ. Sci. Technol. 2009;43:324–329. doi: 10.1021/es801751x. PubMed DOI

ATSDR. Hexachlorocyclohexane (HCH) | Toxicological Profile | ATSDR. https://wwwn.cdc.gov/TSP/ToxProfiles/ToxProfiles.aspx?id=754&tid=138. PubMed

Björk Bæringsdóttir, B. Method Development for Sample Preparation of Fish for Non-target Analysis of Hydrophobic Organic Pollutants (2020).

Andria V, Reichenauer TG, Sessitsch A. Expression of alkane monooxygenase (alkB) genes by plant-associated bacteria in the rhizosphere and endosphere of Italian ryegrass (Lolium multiflorum L.) grown in diesel contaminated soil. Environ. Pollut. 2009;157:3347–3350. doi: 10.1016/j.envpol.2009.08.023. PubMed DOI

Weyens N, van der Lelie D, Taghavi S, Newman L, Vangronsveld J. Exploiting plant-microbe partnerships to improve biomass production and remediation. Trends Biotechnol. 2009;27:591–598. doi: 10.1016/j.tibtech.2009.07.006. PubMed DOI

Siciliano SD, et al. Selection of specific endophytic bacterial genotypes by plants in response to soil contamination. Appl. Environ. Microbiol. 2001;67:2469–2475. doi: 10.1128/AEM.67.6.2469-2475.2001. PubMed DOI PMC

Schwitzguébel, J.-P., Meyer, J. & Kidd, P. Pesticides Removal Using Plants: Phytodegradation Versus Phytostimulation. in Phytoremediation Rhizoremediation (eds. Mackova, M., Dowling, D. & Macek, T.) 179–198 (Springer Netherlands, 2006). doi:10.1007/978-1-4020-4999-4_13.

Chaudhry Q, Schröder P, Werck-Reichhart D, Grajek W, Marecik R. Prospects and limitations of phytoremediation for the removal of persistent pesticides in the environment. Environ. Sci. Pollut. Res. Int. 2002;9:4–17. doi: 10.1007/BF02987313. PubMed DOI

Böltner D, Moreno-Morillas S, Ramos J-L. 16S rDNA phylogeny and distribution of lin genes in novel hexachlorocyclohexane-degrading Sphingomonas strains. Environ. Microbiol. 2005;7:1329–1338. doi: 10.1111/j.1462-5822.2005.00820.x. PubMed DOI

Imai R, et al. Dehydrochlorination of γ-hexachlorocyclohexane (γ-BHC) by γ-BHC-assimilating Pseudomonas paucimobilis. Agric. Biol. Chem. 1989;53:2015–2017.

Phillips TM, Seech AG, Lee H, Trevors JT. Biodegradation of hexachlorocyclohexane (HCH) by microorganisms. Biodegradation. 2005;16:363–392. doi: 10.1007/s10532-004-2413-6. PubMed DOI

Semerád J, et al. Remedial trial of sequential anoxic/oxic chemico-biological treatment for decontamination of extreme hexachlorocyclohexane concentrations in polluted soil. J. Hazard. Mater. 2023;443:130199. doi: 10.1016/j.jhazmat.2022.130199. PubMed DOI

Trolldenier G, Curl EA. Truelove: The Rhizosphere. (Advanced Series in Agricultural Sciences, Vol. 15) Springer-Verlag, Berlin-Heidelberg-New York-Tokyo, 1986. 288 p, 57 figs., Hardcover DM 228.00. Z. Pflanzenernähr. Bodenkd. 1987;150:124–125. doi: 10.1002/jpln.19871500214. DOI

Watt M. The rhizosphere: biochemistry and organic substances at the soil–plant interface. Ann. Bot. 2009;104:ix–x. doi: 10.1093/aob/mcp166. DOI

Dakora FD, Phillips DA. Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil. 2002;245:201–213. doi: 10.1023/A:1020809400075. DOI

Anderson TA, Coats JR. Screening rhizosphere soil samples for the ability to mineralize elevated concentrations of atrazine and metolachlor. J. Environ. Sci. Health B. 1995;30:473–484. doi: 10.1080/03601239509372948. DOI

Miya RK, Firestone MK. Enhanced phenanthrene biodegradation in soil by slender oat root exudates and root debris. J. Environ. Qual. 2001;30:1911–1918. doi: 10.2134/jeq2001.1911. PubMed DOI

Shaw LJ. Rhizodeposition and the enhanced mineralization of 2,4-dichlorophenoxyacetic acid in soil from the Trifolium pratense rhizosphere. Environ. Microbiol. 2005 doi: 10.1111/j.1462-2920.2004.00688.x. PubMed DOI

Kidd PS, Prieto-Fernández A, Monterroso C, Acea MJ. Rhizosphere microbial community and hexachlorocyclohexane degradative potential in contrasting plant species. Plant Soil. 2008;302:233–247. doi: 10.1007/s11104-007-9475-2. DOI

Abhilash PC, et al. Influence of rhizospheric microbial inoculation and tolerant plant species on the rhizoremediation of lindane. Environ. Exp. Bot. 2011;74:127–130. doi: 10.1016/j.envexpbot.2011.05.009. DOI

Salam JA, Hatha MAA, Das N. Microbial-enhanced lindane removal by sugarcane (Saccharum officinarum) in doped soil-applications in phytoremediation and bioaugmentation. J. Environ. Manag. 2017;193:394–399. doi: 10.1016/j.jenvman.2017.02.006. PubMed DOI

Kumari R, et al. Cloning and characterization of lin genes responsible for the degradation of hexachlorocyclohexane isomers by Sphingomonas paucimobilis strain B90. Appl. Environ. Microbiol. 2002;68:6021–6028. doi: 10.1128/AEM.68.12.6021-6028.2002. PubMed DOI PMC

Lal R, et al. Biochemistry of microbial degradation of hexachlorocyclohexane and prospects for bioremediation. Microbiol. Mol. Biol. Rev. 2010;74:58–80. doi: 10.1128/MMBR.00029-09. PubMed DOI PMC

Trantirek L, et al. Reaction mechanism and stereochemistry of γ-hexachlorocyclohexane dehydrochlorinase LinA. J. Biol. Chem. 2001;276:7734–7740. doi: 10.1074/jbc.M007452200. PubMed DOI

Nagata Y, et al. Cloning and sequencing of a dehalogenase gene encoding an enzyme with hydrolase activity involved in the degradation of gamma-hexachlorocyclohexane in Pseudomonas paucimobilis. J. Bacteriol. 1993;175:6403–6410. doi: 10.1128/jb.175.20.6403-6410.1993. PubMed DOI PMC

Raina V, et al. New metabolites in the degradation of alpha- and gamma-hexachlorocyclohexane (HCH): Pentachlorocyclohexenes are hydroxylated to cyclohexenols and cyclohexenediols by the haloalkane dehalogenase LinB from Sphingobium indicum B90A. J. Agric. Food Chem. 2008;56:6594–6603. doi: 10.1021/jf800465q. PubMed DOI

Nagata Y, et al. Degradation of β-hexachlorocyclohexane by haloalkane dehalogenase LinB from Sphingomonas paucimobilis UT26. Appl. Environ. Microbiol. 2005;71:2183–2185. doi: 10.1128/AEM.71.4.2183-2185.2005. PubMed DOI PMC

Miyauchi K, Lee H-S, Fukuda M, Takagi M, Nagata Y. Cloning and characterization of linR, involved in regulation of the downstream pathway for γ-hexachlorocyclohexane degradation in Sphingomonas paucimobilis UT26. Appl. Environ. Microbiol. 2002;68:1803–1807. doi: 10.1128/AEM.68.4.1803-1807.2002. PubMed DOI PMC

Suar M, van der Meer JR, Lawlor K, Holliger C, Lal R. Dynamics of multiple lin gene expression in Sphingomonas paucimobilis B90A in response to different hexachlorocyclohexane isomers. Appl. Environ. Microbiol. 2004;70:6650–6656. doi: 10.1128/AEM.70.11.6650-6656.2004. PubMed DOI PMC

Košková S, Štochlová P, Novotná K, Amirbekov A, Hrabák P. Influence of delta-hexachlorocyclohexane (δ-HCH) to Phytophthora ×alni resistant Alnus glutinosa genotypes − Evaluation of physiological parameters and remediation potential. Ecotoxicol. Environ. Saf. 2022;247:114235. doi: 10.1016/j.ecoenv.2022.114235. PubMed DOI

Desai M, Haigh M, Walkington H. Phytoremediation: Metal decontamination of soils after the sequential forestation of former opencast coal land. Sci. Total Environ. 2019;656:670–680. doi: 10.1016/j.scitotenv.2018.11.327. PubMed DOI

Tischer S, Hübner T. Model trials for phytoremediation of hydrocarbon-contaminated sites by the use of different plant species. Int. J. Phytoremediat. 2002;4:187–203. doi: 10.1080/15226510208500082. DOI

Šimura J, et al. Plant hormonomics: Multiple phytohormone profiling by targeted metabolomics. Plant Physiol. 2018;177:476–489. doi: 10.1104/pp.18.00293. PubMed DOI PMC

Bala K, Sharma P, Lal R. Sphingobium quisquiliarum sp. Nov., a hexachlorocyclohexane (HCH)-degrading bacterium isolated from an HCH-contaminated soil. Int. J. Syst. Evolut. Microbiol. 2010;60:429–433. doi: 10.1099/ijs.0.010868-0. PubMed DOI

Gupta SK, et al. Changes in the bacterial community and lin genes diversity during biostimulation of indigenous bacterial community of hexachlorocyclohexane (HCH) dumpsite soil. Microbiology. 2013;82:234–240. doi: 10.1134/S0026261713020185. DOI

Clifford RJ, et al. Detection of bacterial 16S rRNA and identification of four clinically important bacteria by real-time PCR. PLoS One. 2012;7:e48558. doi: 10.1371/journal.pone.0048558. PubMed DOI PMC

Nechanická MDL, Dolinová I. Use of nanofiber carriers for monitoring of microbial biomass. In: Nechanická MDL, Dolinová I, editors. Topical Issues of Rational Use of Natural Resources: Proceedings of the 361. CRC Press; 2018.

Claesson MJ, et al. Comparison of two next-generation sequencing technologies for resolving highly complex microbiota composition using tandem variable 16S rRNA gene regions. Nucleic Acids Res. 2010;38:e200–e200. doi: 10.1093/nar/gkq873. PubMed DOI PMC

White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR Protocols. Academic Press; 1990. pp. 315–322.

Bolyen E, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 2019;37:852–857. doi: 10.1038/s41587-019-0209-9. PubMed DOI PMC

Callahan BJ, et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods. 2016;13:581–583. doi: 10.1038/nmeth.3869. PubMed DOI PMC

Bokulich NA, et al. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome. 2018;6:90. doi: 10.1186/s40168-018-0470-z. PubMed DOI PMC

Quast C, et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–D596. doi: 10.1093/nar/gks1219. PubMed DOI PMC

McMurdie PJ, Holmes S. phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One. 2013;8:e61217. doi: 10.1371/journal.pone.0061217. PubMed DOI PMC

Liu X, Wu L, Kümmel S, Richnow HH. Characterizing the biotransformation of hexachlorocyclohexanes in wheat using compound-specific stable isotope analysis and enantiomer fraction analysis. J. Hazard. Mater. 2021;406:124301. doi: 10.1016/j.jhazmat.2020.124301. PubMed DOI

Chen Q, et al. Purification effects on β-HCH removal and bacterial community differences of vertical-flow constructed wetlands with different vegetation plantations. Sustainability. 2021;13:13244. doi: 10.3390/su132313244. DOI

Amirbekov A, et al. Biodiversity in wetland+ system: A passive solution for HCH dump effluents. Water Sci. Technol. 2023 doi: 10.2166/wst.2023.395. PubMed DOI

Bianconi, D. et al. Field-Scale rhyzoremediation of a contaminated soil with hexachlorocyclohexane (HCH) isomers: The potential of poplars for environmental restoration and economical sustainability. In Handbook of Phytoremediation (2011).

Liu X, et al. Soil from a hexachlorocyclohexane contaminated field site inoculates wheat in a pot experiment to facilitate the microbial transformation of β-hexachlorocyclohexane examined by compound-specific isotope analysis. Environ. Sci. Technol. 2021;55:13812–13821. doi: 10.1021/acs.est.1c03322. PubMed DOI

Huntjens, J. L. M. et al. Biodegradation of Alpha-Hexachlorocyclohexane by a Bacterium Isolated from Polluted Soil. In Contaminated Soil ’88: Second International TNO/BMFT Conference on Contaminated Soil, 11–15 April 1988, Hamburg, Federal Republic of Germany (eds Wolf, K., Van Den Brink, W. J. & Colon, F. J.), 733–737 (Springer Netherlands, 1988). doi:10.1007/978-94-009-2807-7_118.

Okeke BC, Siddique T, Arbestain MC, Frankenberger WT. Biodegradation of gamma-hexachlorocyclohexane (lindane) and alpha-hexachlorocyclohexane in water and a soil slurry by a Pandoraea species. J. Agric. Food Chem. 2002;50:2548–2555. doi: 10.1021/jf011422a. PubMed DOI

Sineli PE, Tortella G, Dávila Costa JS, Benimeli CS, Cuozzo SA. Evidence of α-, β- and γ-HCH mixture aerobic degradation by the native actinobacteria Streptomyces sp. M7. World J. Microbiol. Biotechnol. 2016;32:81. doi: 10.1007/s11274-016-2037-0. PubMed DOI

Trapp S, Miglioranza KSB. Sorption of lipophilic organic compounds to wood and implications for their environmental fate. Environ. Sci. Technol. 2001;35:1561–1566. doi: 10.1021/es000204f. PubMed DOI

Middeldorp PJM, Jaspers M, Zehnder AJB, Schraa G. Biotransformation of α-, β-, γ-, and δ-hexachlorocyclohexane under Methanogenic Conditions. Environ. Sci. Technol. 1996;30:2345–2349. doi: 10.1021/es950782+. DOI

Kurt Z, Spain JC. Biodegradation of chlorobenzene, 1,2-dichlorobenzene, and 1,4-dichlorobenzene in the Vadose zone. Environ. Sci. Technol. 2013;47:6846–6854. doi: 10.1021/es3049465. PubMed DOI

Wang C, et al. PAHs biodegradation potential of indigenous consortia from agricultural soil and contaminated soil in two-liquid-phase bioreactor (TLPB) J. Hazard. Mater. 2010;176:41–47. doi: 10.1016/j.jhazmat.2009.10.123. PubMed DOI

Langenhoff AAM, Staps SJM, Pijls C, Rijnaarts HHM. Stimulation of hexachlorocyclohexane (HCH) biodegradation in a full scale in situ bioscreen. Environ. Sci. Technol. 2013;47:11182–11188. doi: 10.1021/es4024833. PubMed DOI

Ramanand K, Balba MT, Duffy J. Reductive dehalogenation of chlorinated benzenes and toluenes under methanogenic conditions. Appl. Environ. Microbiol. 1993;59:3266–3272. doi: 10.1128/aem.59.10.3266-3272.1993. PubMed DOI PMC

Nishino SF, Spain JC, Belcher LA, Litchfield CD. Chlorobenzene degradation by bacteria isolated from contaminated groundwater. Appl. Environ. Microbiol. 1992;58:1719–1726. doi: 10.1128/aem.58.5.1719-1726.1992. PubMed DOI PMC

Burken JG, Schnoor JL. Predictive relationships for uptake of organic contaminants by hybrid poplar trees. Environ. Sci. Technol. 1998;32:3379–3385. doi: 10.1021/es9706817. DOI

Calvelo Pereira R, Camps-Arbestain M, Rodríguez Garrido B, Macías F, Monterroso C. Behaviour of α-, β-, γ-, and δ-hexachlorocyclohexane in the soil–plant system of a contaminated site. Environ. Pollut. 2006;144:210–217. doi: 10.1016/j.envpol.2005.12.030. PubMed DOI

Mano Y, Nemoto K. The pathway of auxin biosynthesis in plants. J Exp Bot. 2012;63:2853–2872. doi: 10.1093/jxb/ers091. PubMed DOI

Podlešáková K, et al. Rhizobial synthesized cytokinins contribute to but are not essential for the symbiotic interaction between photosynthetic Bradyrhizobia and Aeschynomene legumes. Mol. Plant Microbe Interact. 2013;26:1232–1238. doi: 10.1094/MPMI-03-13-0076-R. PubMed DOI

Kotov AA, Kotova LM, Romanov GA. Signaling network regulating plant branching: Recent advances and new challenges. Plant Sci. 2021;307:110880. doi: 10.1016/j.plantsci.2021.110880. PubMed DOI

Planas-Riverola A, et al. Brassinosteroid signaling in plant development and adaptation to stress. Development. 2019;146:dev151894. doi: 10.1242/dev.151894. PubMed DOI PMC

Waadt R, et al. Plant hormone regulation of abiotic stress responses. Nat. Rev. Mol. Cell Biol. 2022;23:680–694. doi: 10.1038/s41580-022-00479-6. PubMed DOI PMC

Ha S, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Tran L-SP. Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci. 2012;17:172–179. doi: 10.1016/j.tplants.2011.12.005. PubMed DOI

Osugi A, Sakakibara H. Q&A: How do plants respond to cytokinins and what is their importance? BMC Biol. 2015;13:102. doi: 10.1186/s12915-015-0214-5. PubMed DOI PMC

Zürcher E, Liu J, di Donato M, Geisler M, Müller B. Plant development regulated by cytokinin sinks. Science. 2016;353:1027–1030. doi: 10.1126/science.aaf7254. PubMed DOI

Hedden P. The current status of research on gibberellin biosynthesis. Plant Cell Physiol. 2020;61:1832–1849. doi: 10.1093/pcp/pcaa092. PubMed DOI PMC

Zanewich KP, Rood SB. Endogenous gibberellins in flushing buds of three deciduous trees: Alder, aspen, and birch. J. Plant Growth Regul. (USA) 1994;13:159–162. doi: 10.1007/BF00196381. DOI

Anderson JP, et al. Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell. 2004;16:3460–3479. doi: 10.1105/tpc.104.025833. PubMed DOI PMC

Proietti S, et al. Genome-wide association study reveals novel players in defense hormone crosstalk in Arabidopsis. Plant Cell Environ. 2018;41:2342–2356. doi: 10.1111/pce.13357. PubMed DOI PMC

Yuan K, Rashotte AM, Wysocka-Diller JW. ABA and GA signaling pathways interact and regulate seed germination and seedling development under salt stress. Acta Physiol. Plant. 2011;33:261–271. doi: 10.1007/s11738-010-0542-6. DOI

Zheng X, et al. Organochlorine contamination enriches virus-encoded metabolism and pesticide degradation associated auxiliary genes in soil microbiomes. ISME J. 2022;16:1397–1408. doi: 10.1038/s41396-022-01188-w. PubMed DOI PMC

Gołębiewski M, Deja-Sikora E, Cichosz M, Tretyn A, Wróbel B. 16S rDNA pyrosequencing analysis of bacterial community in heavy metals polluted soils. Microb. Ecol. 2014;67:635–647. doi: 10.1007/s00248-013-0344-7. PubMed DOI PMC

Wegner C-E, Liesack W. Unexpected dominance of elusive acidobacteria in early industrial soft coal slags. Front. Microbiol. 2017 doi: 10.3389/fmicb.2017.01023. PubMed DOI PMC

Albuquerque L, da Costa MS. The Family Gaiellaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F, editors. The Prokaryotes: Actinobacteria. Springer; 2014. pp. 357–360.

Tedersoo L, Suvi T, Jairus T, Ostonen I, Põlme S. Revisiting ectomycorrhizal fungi of the genus Alnus: Differential host specificity, diversity and determinants of the fungal community. New Phytol. 2009;182:727–735. doi: 10.1111/j.1469-8137.2009.02792.x. PubMed DOI

Vrålstad T, Schumacher T, Taylor AFS. Mycorrhizal synthesis between fungal strains of the Hymenoscyphus ericae aggregate and potential ectomycorrhizal and ericoid hosts. New Phytol. 2002;153:143–152. doi: 10.1046/j.0028-646X.2001.00290.x. DOI

Sharma P, et al. Haloalkane dehalogenase LinB is responsible for β- and δ-hexachlorocyclohexane transformation in Sphingobium indicum B90A. Appl. Environ. Microbiol. 2006;72:5720–5727. doi: 10.1128/AEM.00192-06. PubMed DOI PMC