Chromium (Cr) can interfere with plant gene expression, change the content of metabolites and affect plant growth. However, the molecular response mechanism of wetland plants at different time sequences under Cr stress has yet to be fully understood. In this study, Canna indica was exposed to 100 mg/kg Cr-contaminated soil for 0, 7, 14, and 21 days and analyzed using untargeted metabolomics (LC-MS) and transcriptomics. The results showed that Cr stress increased the activities of superoxide dismutase (SOD), ascorbate peroxidase (APX) and peroxidase (POD), the contents of glutathione (GSH), malondialdehyde (MDA), and oxygen free radical (ROS), and inhibited the biosynthesis of photosynthetic pigments, thus leading to changes in plant growth and biomass. Metabonomics analysis showed that Cr stress mainly affected 12 metabolic pathways, involving 38 differentially expressed metabolites, including amino acids, phenylpropane, and flavonoids. By transcriptome analysis, a total of 16,247 differentially expressed genes (DEGs, 7710 up-regulated genes, and 8537 down-regulated genes) were identified, among which, at the early stage of stress (Cr contaminate seven days), C. indica responds to Cr toxicity mainly through galactose, starch and sucrose metabolism. With the extension of stress time, plant hormone signal transduction and MAPK signaling pathway in C. indica in the Cr14 (Cr contaminate 14 days) treatment group were significantly affected. Finally, in the late stage of stress (Cr21), C. indica co-defuses Cr toxicity by activating its Glutathione metabolism and Phenylpropanoid biosynthesis. In conclusion, this study revealed the molecular response mechanism of C. indica to Cr stress at different times through multi-omics methods.

College of Eco Environment Engineering The Karst Environmental Geological Hazard Prevention of Key Laboratory of State Ethnic Affairs Commission Guizhou Minzu University Guiyang 550025 China

Department of Applied Ecology Faculty of Environmental Sciences Czech University of Life Sciences Prague Kamýcka 129 Praha Suchdol 16500 Czech Republic

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Uchimiya M, Bannon D, Nakanishi H, et al. Chemical speciation, plant uptake, and toxicity of heavy metals in agricultural soils. J. Agric. Food Chem. 2020;68:12856–12869. doi: 10.1021/acs.jafc.0c00183. PubMed DOI

Xing SP, Chen BD, Hao ZP, et al. The role of rhizosphere microorganisms in enhancing chromium tolerance of host plants. Asian J. Ecotoxicol. 2021;16:2–14.

Arun KS, Carlos C, Herminia LT, et al. Chromium toxicity in plants. Environ. Int. 2005;31:739–753. doi: 10.1016/j.envint.2005.02.003. PubMed DOI

Ahmad R, Ali S, Rizwan M, et al. Hydrogen sulfide alleviates chromium stress on cauliflower by restricting its uptake and enhancing antioxidative system. Physiologia Plantarum. 2020;168:289–300. doi: 10.1111/ppl.13001. PubMed DOI

Yu XZ, Feng YX, Liang YP. Kinetics of phyto-accumulation of hexavalent and trivalent chromium in rice seedlings. Int. Biodeteriorat. Biodegrad. 2018;128:72–77. doi: 10.1016/j.ibiod.2016.09.003. DOI

Sinha V, Pakshirajan K, Chaturvedi R. Chromium tolerance, bioaccumulation and localization in plants: An overview. Environ. Manag. 2018;206:715–730. PubMed

Kapoor RT, Bani MMF, Alam P, Rinklebe J, Ahmad P. Accumulation of chromium in plants and its repercussion in animals and humans. Environ. Pollut. 2022;301:119044. doi: 10.1016/j.envpol.2022.119044. PubMed DOI

Singh S, Naik TS, Chauhan V, et al. Ecological effects, remediation, distribution, and sensing techniques of chromium. Chemosphere. 2022;307:135804. doi: 10.1016/j.chemosphere.2022.135804. PubMed DOI

Ashraf S, Ali Q, Zahir ZA, et al. Phytoremediation: Environmentally sustainable way for reclamation of heavy metal polluted soils. Ecotoxicol. Environ. Saf. 2019;174:714–727. doi: 10.1016/j.ecoenv.2019.02.068. PubMed DOI

Ao M, Chen XT, Deng THB, et al. Chromium biogeochemical behaviour in soil-plant systems and remediation strategies: A critical review. J. Hazard. Mater. 2022;424:127233. doi: 10.1016/j.jhazmat.2021.127233. PubMed DOI

Anastasis C, Egli CG, Andreas MZ. Uptake of hexavalent chromium by tomato (Solanum lycopersicum L.) plants and mediated effects on their physiology and productivity, along with fruit quality and safety. Environ. Exp. Bot. 2021;189:104564. doi: 10.1016/j.envexpbot.2021.104564. DOI

Vibha S, Kannan P, Rakhi C. Chromium tolerance, bioaccumulation and localization in plants: An overview. J. Environ. Manag. 2018;206:715–730. doi: 10.1016/j.jenvman.2017.10.033. PubMed DOI

Zhang F, Lu F, Wang Y, Zhang Z, Wang J, Zhang K, Wu H, Zou J, Duan Y, Ke F, Zhu K. Combined transcriptomic and physiological metabolomic analyses elucidate key biological pathways in the response of two sorghum genotypes to salinity stress. Front. Plant Sci. 2022;13:880373. doi: 10.3389/fpls.2022.880373. PubMed DOI PMC

Zhao B, Zhu SX, Xu C. Response of physiological and ecological characteristics of Canna indica under Cr(VI) stress. Sci. Technol. Eng. 2017;2017(17):44–49.

Wang BC, Zhu SX, Li WJ, et al. Effects of chromium stress on the rhizosphere microbial community composition of Cyperus alternifolius. Ecotoxicol. Environ. Saf. 2021;218:112253. doi: 10.1016/j.ecoenv.2021.112253. PubMed DOI

Wang AY, Huang SS, Zhong GF, et al. Effect of Cr (VI) stress on growth of three herbaceous plant and their Cruptake. Environ. Sci. 2012;33:2018–2037. PubMed

Wang J, Chen X, Chu S, Hayat K, Chi Y, Zhi Y, Zhang D, Zhou P. Influence of Cd toxicity on subcellular distribution, chemical forms, and physiological responses of cell wall components towards short-term Cd stress in Solanum nigrum. Environ. Sci. Pollut. Res. 2021;28:13955–13969. doi: 10.1007/s11356-020-11505-5. PubMed DOI

Yuan Y, Imtiaz M, Rizwan M, Dai Z, Hossain MM, Zhang Y, Huang H, Tu S. The role and its transcriptome mechanisms of cell wall polysaccharides in vanadium detoxication of rice. J. Hazard. Mater. 2022;425:127966. doi: 10.1016/j.jhazmat.2021.127966. PubMed DOI

Zhong MY, Zhang XQ, Yang XY, et al. Recent advances in plant response to chromium stress. Pratacult. Sci. 2019;36:1962–1975.

Wei TL, Wang Y, Xie ZZ, Guo DY, Chen CW, Fan QJ, Deng XD, Liu JH. Enhanced ROS scavenging and sugar accumulation contribute to drought tolerance of naturally occurring autotetraploids in Poncirus trifoliata. Plant Biotechnol. J. 2019;17:1394–1407. doi: 10.1111/pbi.13064. PubMed DOI PMC

Zhang XM, Wang TT, Xu ZJ, et al. Effect of heavy metals in mixed domestic-industrial wastewater onperformance of recirculating standing hybrid constructed wetlands (RSHCWs) and their removal. Chem. Eng. J. 2020;379:122363. doi: 10.1016/j.cej.2019.122363. DOI

Liu Y, Guo PY, Liao JH. Resistant reaction of Canna indica and Scindapsus aureum to Cr(VI) stress in purifying eutrophication water. J. Zhejiang Univ. (Sci. Edn.) 2011;38:78–84.

Dong XX, Yang F, Yang SP, et al. Subcellular distribution and tolerance of cadmium in Canna indica L. Ecotoxicol Environ. Saf. 2019;185:109692. doi: 10.1016/j.ecoenv.2019.109692. PubMed DOI

Xiang, H.M., Lan, N., Wang, F.G., Zhao, B.L., Wei, H., Zhang, J.E., An effective planting model to decrease cadmium accumulation in rice grain and plant: Intercropping rice with wetlandplants. Pedosphere 32 (2022).

Ibarra AAG, Wrobel K, Barrientos EY, et al. Impact of Cr(VI) on the oxidation of polyunsaturated fatty acids in Helianthus annuus roots studied by metabolomic tools. Chemosphere. 2019;220:442–451. doi: 10.1016/j.chemosphere.2018.12.145. PubMed DOI

Jia H, Wang X, Dou Y, et al. Hydrogen sulfide-cysteine cycle system enhances cadmium tolerance through alleviating cadmium-induced oxidative stress and ion toxicity in Arabidopsis roots. Sci. Rep. 2016;6:39702. doi: 10.1038/srep39702. PubMed DOI PMC

Roy SK, Cho SW, Kwon SJ, et al. Morpho-physiological and proteome level responses to cadmium stress in sorghum. PLoS One. 2016;11:1–27. doi: 10.1371/journal.pone.0150431. PubMed DOI PMC

Wei FS, Yang GZ, Jiang DZ, Liu ZH, Sun BM. Basic statistics and characteristics of background values of soil elements in China. China Natl. Environ. Monit. Centre. 1991;01:1–6.

Wei Z, Sixi Z, Xiuqin Y, Guodong X, Baichun W, Baojing G. Arbuscular mycorrhizal fungi alter rhizosphere bacterial community characteristics to improve Cr tolerance of Acorus calamus. Ecotoxicol. Environ. Saf. 2023;253:114652. doi: 10.1016/j.ecoenv.2023.114652. PubMed DOI

Wei Z, Sixi Z, Baojing G, Xiuqin Y, Guodong X, Baichun W. Effects of Cr stress on bacterial community structure and composition in rhizosphere soil of iris tectorum under different cultivation modes. Microbiol. Res. 2023;14:243–261. doi: 10.3390/microbiolres14010020. DOI

Bao SD. Analytical Methods of Soil Agro-chemistry. China Agriculture Press; 2000.

Zhao W, Chen Z, Yang X, Sheng L, Mao H, Zhu S. Metagenomics reveal arbuscular mycorrhizal fungi altering functional gene expression of rhizosphere microbial community to enhance Iris tectorum's resistance to Cr stress. Sci. Total Environ. 2023;895:164970. doi: 10.1016/j.scitotenv.2023.164970. PubMed DOI

Kanehisa M, Furumichi M, Sato Y, Kawashima M, Ishiguro-Watanabe M. KEGG for taxonomy-based analysis of pathways and genomes. Nucleic Acids Res. 2023;51:D587–D592. doi: 10.1093/nar/gkac963. PubMed DOI PMC

Wei Z, Zhongbing C, Xiuqin Y, Luying S, Huan M, Sixi Z. Integrated transcriptomics and metabolomics reveal key metabolic pathway responses in Pistia stratiotes under Cd stress. J. Hazard. Mater. 2023;452:131214. doi: 10.1016/j.jhazmat.2023.131214. PubMed DOI

Su Z, Xiao Q, Shen J, et al. Metabolomics analysis of litchi leaves during floral induction reveals metabolic improvement by stem girdling. Molecules (Basel, Switzerland) 2021;26:4048. doi: 10.3390/molecules26134048. PubMed DOI PMC

Mumtaz MA, Hao Y, Mehmood S, Shu H, Zhou Y, Jin W, Chen C, Li L, Altaf MA, Wang Z. Physiological and transcriptomic analysis provide molecular insight into 24-Epibrassinolide mediated Cr(VI)-toxicity tolerance in Pepper plants. Environ. Pollut. 2022;306:119375. doi: 10.1016/j.envpol.2022.119375. PubMed DOI

Xu CC, Li ZY, Wang JB. Temporal and tissue-specific transcriptome analyses reveal mechanistic insights into the Solidago canadensis response to cadmium contamination. Chemosphere. 2022;292:133501. doi: 10.1016/j.chemosphere.2021.133501. PubMed DOI

Pan CL, Lu HL, Yang CY, Wang L, Chen JM, Yan CL. Comparative transcriptome analysis reveals different functions of Kandelia obovata superoxide dismutases in regulation of cadmium translocation. Sci. Total Environ. 2021;771:144922. doi: 10.1016/j.scitotenv.2020.144922. PubMed DOI

Chen H, Jin J, Hu S, Shen L, Zhang P, Li Z, Fang Z, Liu H. Metabolomics and proteomics reveal the toxicological mechanisms of florfenicol stress on wheat (Triticum aestivum L.) seedlings. J. Hazard. Mater. 2022;443:130264. doi: 10.1016/j.jhazmat.2022.130264. PubMed DOI

El Rasafi T, Oukarroum A, Haddioui A, et al. Cadmium stress in plants: A critical review of the effects, mechanisms, and tolerance strategies. Crit. Rev. Environ. Sci. Technol. 2020;52:675–726. doi: 10.1080/10643389.2020.1835435. DOI

Meng L, Yang Y, Ma Z, Jiang J, Zhang X, Chen Z, Cui G, Yin X. Integrated physiological, transcriptomic and metabolomic analysis of the response of Trifolium pratense L. to Pb toxicity. J. Hazard. Mater. 2022;436:129128. doi: 10.1016/j.jhazmat.2022.129128. PubMed DOI

Verma D, Jalmi SK, Bhagat PK, Verma N, Sinha AK. A bHLH transcription factor, MYC2, imparts salt intolerance by regulating proline biosynthesis in Arabidopsis. Eur. J. Biochem. 2020;287:2560–2576. PubMed

Wang J, Chen X, Chu S, You Y, Chi Y, Wang R, Yang X, Hayat K, Zhang D, Zhou P. Comparative cytology combined with transcriptomic and metabolomic analyses of Solanum nigrum L. in response to Cd toxicity. J. Hazard. Mater. 2022;423:127168. doi: 10.1016/j.jhazmat.2021.127168. PubMed DOI

Wang Y, Meng Y, Mu S, Yan D, Xu X, Zhang L, Xu B. Changes in phenotype and gene expression under lead stress revealed key genetic responses to lead tolerance in Medicago sativa L. Gene. 2021;791:145714. doi: 10.1016/j.gene.2021.145714. PubMed DOI

Yu G, Ullah H, Wang X, Liu J, Chen B, Jiang P, Lin H, Sunahara GI, You S, Zhang X, Shahab A. Integrated transcriptome and metabolome analysis reveals the mechanism of tolerance to manganese and cadmium toxicity in the Mn/Cd hyperaccumulator Celosia argentea Linn. J. Hazard. Mater. 2023;443:130206. doi: 10.1016/j.jhazmat.2022.130206. PubMed DOI

Mittler R, Zandalinas SI, Fichman Y, Van BF. Reactive oxygen species signalling in plant stress responses. Nat. Rev. Mol. Cell Biol. 2022;23:663–679. doi: 10.1038/s41580-022-00499-2. PubMed DOI

Kumar K, Raina SK, Sultan SM. Arabidopsis MAPK signaling pathways and their cross talks in abiotic stress response. J. Plant Biochem. Biotechnol. 2020;29:700–714. doi: 10.1007/s13562-020-00596-3. DOI

Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR. Abscisic acid: Emergence of a core signaling network. Annu. Rev. Plant Biol. 2010;61:651–679. doi: 10.1146/annurev-arplant-042809-112122. PubMed DOI

Sharma A, Kapoor D, Wang J, Shahzad B, Kumar V, Bali AS, Jasrotia S, Zheng B, Yuan H, Yan D. Chromium bioaccumulation and its impacts on plants: An overview. Plants. 2020;9:100. doi: 10.3390/plants9010100. PubMed DOI PMC

Xian JP, Wang Y, Niu KJ, Ma HL, Ma X. Transcriptional regulation and expression network responding to cadmium stress in a Cd-tolerant perennial grass Poa Pratensis. Chemosphere. 2020;250:126158. doi: 10.1016/j.chemosphere.2020.126158. PubMed DOI

Guo X, Luo J, Du Y, Li J, Liu Y, Liang Y, Li T. Coordination between root cell wall thickening and pectin modification is involved in cadmium accumulation in Sedum alfredii. Environ. Pollut. 2021;268:115665. doi: 10.1016/j.envpol.2020.115665. PubMed DOI

Adams ZP, Ehlting J, Edwards R. The regulatory role of shikimate in plant phenylalanine metabolism. J. Theor. Biol. 2019;462:158–170. doi: 10.1016/j.jtbi.2018.11.005. PubMed DOI

Li CH, Zheng C, Fu HX, Zhai SH, Hu F, Naveed S, Zhang CH, Ge Y. Contrasting detoxification mechanisms of Chlamydomonas reinhardtii under Cd and Pb stress. Chemosphere. 2021;274:129771. doi: 10.1016/j.chemosphere.2021.129771. PubMed DOI

Hasanuzzaman M, Bhuyan MHMB, Zulfiqar F, Raza A, Mohsin SM, Al Mahmud J, Fujita M, Fotopoulos V. Reactive oxygen species and antioxidant defense in plants under abiotic stress: Revisiting the crucial role of a universal defense regulator. Antioxidants. 2020;9:681. doi: 10.3390/antiox9080681. PubMed DOI PMC

Guo ZH, Zeng P, Xiao XY, Peng C. Physiological, anatomical, and transcriptional responses of mulberry (Morus alba L.) to Cd stress in contaminated soil. Environ. Pollut. 2021;284:117387. doi: 10.1016/j.envpol.2021.117387. PubMed DOI

Singh S, Parihar P, Singh R, Singh VP, Prasad SM. Heavy metal tolerance in plants: Role of transcriptomics, proteomics, metabolomics, and ionomics. Front. Plant Sci. 2016 doi: 10.3389/fpls.2015.01143. PubMed DOI PMC

Yuan J, Liu R, Sheng S, Fu H, Wang X. Untargeted LC-MS/MS-based metabolomic profiling for the edible and medicinal plant Salvia miltiorrhiza under different levels of cadmium stress. Front. Plant Sci. 2022;28:889370. doi: 10.3389/fpls.2022.889370. PubMed DOI PMC

Feng Z, Ji SY, Ping JF, Cui D. Recent advances in metabolomics for studying heavy metal stress in plants. TrAC. Trends Anal. Chem. 2021;143:116402. doi: 10.1016/j.trac.2021.116402. DOI