Abstract
Key message
Alfalfa has the ability to degrade TNT. TNT exposure caused root disruption of mineral nutrient metabolism. The exposure of TNT imbalanced basal cell energy metabolism.
Abstract
The mechanism of 2,4,6-trinitrotoluene (TNT) toxicity effects was analyzed in alfalfa (Medicago sativa L.) seedlings by examining the mineral nutrition and secondary metabolism of the plant roots. Exposure to 25–100 mg·L−1 TNT in a hydroponic solution for 72 h resulted in a TNT absorption rate of 26.8–63.0%. The contents of S, K, and B in root mineral nutrition metabolism increased significantly by 1.70–5.46 times, 1.38–4.01 times, and 1.40–4.03 times, respectively, after TNT exposure. Non-targeted metabolomics analysis of the roots identified 189 significantly upregulated metabolites and 420 significantly downregulated metabolites. The altered metabolites were primarily lipids and lipid-like molecules, and the most significant enrichment pathways were alanine, aspartate, and glutamate metabolism and glycerophospholipid metabolism. TNT itself was transformed in the root system into several intermediate products, including 4-hydroxylamino-2,6-dinitrotoluene, 4-amino-2,6-dinitrotoluene, 2-hydroxylamino-4,6-dinitrotoluene, 2,4',6,6'-tetranitro-2',4-azoxytoluene, 4,4',6,6'-tetranitro-2,2'-azoxytoluene, and 2,4-dinitrotoluene. Overall, TNT exposure disturbed the mineral metabolism balance, and significantly interfered with basic plant metabolism.
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References
Alhaithloul HA, Soliman MH, Ameta KL, El-Esawi MA, Elkelish A (2020) Changes in ecophysiology, osmolytes, and secondary metabolites of the medicinal plants of Mentha piperita and Catharanthus roseus subjected to drought and heat stress. Biomolecules. https://doi.org/10.3390/biom10010043
Alothman ZA, Bahkali AH, Elgorban AM, Al-Otaibi MS, Ghfar AA, Gabr SA, Wabaidur SM, Habila MA, Hadj Ahmed AYB (2020) Bioremediation of explosive TNT by Trichoderma viride. Molecules. https://doi.org/10.3390/molecules25061393
Arora PK (2020) Bacilli-mediated degradation of xenobiotic compounds and heavy metals. Front Bioeng Biotechnol. https://doi.org/10.3389/fbioe.2020.570307
Balciunaite G, Juodsnukyte J, Savickas A, Ragazinskiene O, Siatkute L, Zvirblyte G, Mistiniene E, Savickiene N (2015) Fractionation and evaluation of proteins in roots of Echinacea purpurea (L.) Moench. Acta Pharm. https://doi.org/10.1515/acph-2015-0036
Bhattacherjee A, Mandal RS, Das S, Kundu S (2014) Sequence and 3D structure based analysis of TNT degrading proteins in Arabidopsis thaliana. J Mol Model. https://doi.org/10.1007/s00894-014-2174-z
Boutté Y, Jaillais Y (2020) Metabolic cellular communications: feedback mechanisms between membrane lipid homeostasis and plant development. Dev Cell. https://doi.org/10.1016/j.devcel.2020.05.005
Brdar-Jokanović M (2020) Boron toxicity and deficiency in agricultural plants. Int J Mol Sci. https://doi.org/10.3390/ijms21041424
Chatterjee S, Deb U, Datta S, Walther C, Gupta DK (2017) Common explosives (TNT, RDX, HMX) and their fate in the environment: emphasizing bioremediation. Chemosphere. https://doi.org/10.1016/j.chemosphere.2017.06.008
Claus H (2014) Microbial degradation of 2,4,6-trinitrotoluene in vitro and in natural environments. Environ Sci Eng. https://doi.org/10.1007/978-3-319-01083-0_2
Corteselli EM, Gibbs-Flournoy E, Simmons SO, Bromberg P, Gold A, Samet JM (2019) Long chain lipid hydroperoxides increase the glutathione redox potential through glutathione peroxidase 4. Biochim Biophys Acta Gen Subj. https://doi.org/10.1016/j.bbagen.2019.03.002
Das P, Sarkar D, Datta R (2017) Kinetics of nitroreductase-mediated phytotransformation of TNT in vetiver grass. Int J Environ Sci Technol. https://doi.org/10.1007/s13762-016-1128-7
Duringer JM, Morrie Craig A, Smith DJ, Chaney RL (2010) Uptake and transformation of soil [14C]-trinitrotoluene by cool-season grasses. Environ Sci Technol. https://doi.org/10.1021/es903671n
Fallahi S, Habibi-Rezaei M, Khayami M, Heydari R (2007) Soil decontamination of 2,4,6- trinitrotoluene by alfalfa (Medicago sativa). Pak J Biol Sci. https://doi.org/10.3923/pjbs.2007.4406.4412
Gonulalan EM, Nemutlu E, Bayazeid O, Koçak E, Yalçın FN, Demirezer LO (2020) Metabolomics and proteomics profiles of some medicinal plants and correlation with BDNF activity. Phytomedicine. https://doi.org/10.1016/j.phymed.2019.152920
Guo N, Hu J, Yan M, Qu H, Luo L, Tegeder M, Xu G (2020) Oryza sativa lysine-histidine-type transporter 1 functions in root uptake and root-to-shoot allocation of amino acids in rice. Plant J. https://doi.org/10.1111/tpj.14742
Hoehamer C, Wolfe N, Eriksson K (2006) Differences in the biotransformation of 2,4,6-trinitrotoluene (TNT) between wild and axenically grown isolates of Myriophyllum aquaticum. Int J Phytorem. https://doi.org/10.1080/15226510600678431
Johnston EJ, Rylott EL, Beynon E, Lorenz A, Chechik V, Bruce NC (2015) Monodehydroascorbate reductase mediates TNT toxicity in plants. Science. https://doi.org/10.1126/science.aab3472
Khan MIR, Khan NA, Jahan B, Goyal V, Hamid J, Khan S, Iqbal N, Alamri S, Siddiqui MH (2021) Phosphorus supplementation modulates nitric oxide biosynthesis and stabilizes the defence system to improve arsenic stress tolerance in mustard. Plant Biol. https://doi.org/10.1111/plb.13211
Lai JL, Liu ZW, Luo XG (2020a) A metabolomic, transcriptomic profiling, and mineral nutrient metabolism study of the phytotoxicity mechanism of uranium. J Hazard Mater. https://doi.org/10.1016/j.jhazmat.2019.121437
Lai JL, Zhang-xuan D, Xiao-hui JI, Xue-gang L (2020b) Absorption and interaction mechanisms of uranium & cadmium in purple sweet potato (Ipomoea batatas L.). J Hazard Mater. https://doi.org/10.1016/j.jhazmat.2020.123264
Lai JL, Liu ZW, Li C, Luo XG (2021) Analysis of accumulation and phytotoxicity mechanism of uranium and cadmium in two sweet potato cultivars. J Hazard Mater. https://doi.org/10.1016/j.jhazmat.2020.124997
Li L, Li T, Jiang Y, Yang Y, Zhang L, Jiang Z, Wei C, Wan X, Yang H (2020) Alteration of local and systemic amino acids metabolism for the inducible defense in tea plant (Camellia sinensis) in response to leaf herbivory by Ectropis oblique. Arch Biochem Biophys. https://doi.org/10.1016/j.abb.2020.108301
Li J, Zhou Q, Li M, Liu Y, Song Q (2021) Monodisperse amino-modified nanosized zero-valent iron for selective and recyclable removal of TNT: Synthesis, characterization, and removal mechanism. J Environ Sci (china). https://doi.org/10.1016/j.jes.2020.10.009
Liang C, Tian J, Liao H (2013) Proteomics dissection of plant responses to mineral nutrient deficiency. Proteomics. https://doi.org/10.1002/pmic.201200263
Lima DRS, Bezerra MLS, Neves EB, Moreira FR (2011) Impact of ammunition and military explosives on human health and the environment. Rev Environ Health. https://doi.org/10.1515/REVEH.2011.014
Liu Y, Qu J, Zhang L, Xu X, Wei G, Zhao Z, Ren M, Cao M (2019) Identification and characterization of the TCA cycle genes in maize. BMC Plant Biol. https://doi.org/10.1186/s12870-019-2213-0
Liu X, Tan C, Cheng X, Zhao X, Li T, Jiang J (2020) miR168 targets Argonaute1A mediated miRNAs regulation pathways in response to potassium deficiency stress in tomato. BMC Plant Biol. https://doi.org/10.1186/s12870-020-02660-5
Michaud M, Jouhet J (2019) Lipid trafficking at membrane contact sites during plant development and stress response. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00002
Panz K, Miksch K (2012) Phytoremediation of explosives (TNT, RDX, HMX) by wild-type and transgenic plants. J Environ Manage. https://doi.org/10.1016/j.jenvman.2012.08.016
Serrano-González MY, Chandra R, Castillo-Zacarias C, Robledo-Padilla F, de Rostro-Alanis MJ, Parra-Saldivar R (2018) Biotransformation and degradation of 2,4,6-trinitrotoluene by microbial metabolism and their interaction. Defence Technol 14(2):151–164. https://doi.org/10.1016/j.dt.2018.01.004
Seymour RS, Maass E, Bolin JF (2009) Floral thermogenesis of three species of Hydnora (Hydnoraceae) in Africa. Ann Bot. https://doi.org/10.1093/aob/mcp168
Skubij N, Dzida K, Jarosz Z, Pitura K, Jaroszuk-sierocińska M (2020) Nutritional value of savory herb (Satureja hortensis L.) and plant response to variable mineral nutrition conditions in various phases of development. Plants. https://doi.org/10.3390/plants9060706
Subki A, Ho CL, Nabihan Ismail NF, Zainal Abidin AA, Balia Yusof ZN (2020) Identification and characterisation of thiamine pyrophosphate (TPP) riboswitch in Elaeis guineensis. PLoS ONE. https://doi.org/10.1371/journal.pone.0235431
Thijs S, Sillen W, Truyens S, Beckers B, van Hamme J, van Dillewijn P, Samyn P, Carleer R, Weyens N, Vangronsveld J (2018) The sycamore maple bacterial culture collection from a TNT polluted site shows novel plant-growth promoting and explosives degrading bacteria. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01134
Tisarum R, Theerawitaya C, Samphumphuang T, Singh HP, Cha-um S (2020) Foliar application of glycinebetaine regulates soluble sugars and modulates physiological adaptations in sweet potato (Ipomoea batatas) under water deficit. Protoplasma. https://doi.org/10.1007/s00709-019-01429-4
Tzafestas K, Razalan MM, Gyulev I, Mazari AMA, Mannervik B, Rylott EL, Bruce NC (2017) Expression of a Drosophila glutathione transferase in Arabidopsis confers the ability to detoxify the environmental pollutant, and explosive, 2,4,6-trinitrotoluene. New Phytol. https://doi.org/10.1111/nph.14326
Tzafestas K, Ahmad L, Dani MP, Grogan G, Rylott EL, Bruce NC (2018) Structure-guided mechanisms behind the metabolism of 2,4,6-trinitrotoluene by glutathione transferases U25 and U24 that lead to alternate product distribution. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01846
Via SM, Zinnert JC, Young DR (2017) Multiple metrics quantify and differentiate responses of vegetation to composition B. Int J Phytorem. https://doi.org/10.1080/15226514.2016.1216080
Wang C, Lyon DY, Hughes JB, Bennett GN (2003) Role of hydroxylamine intermediates in the phytotransformation of 2,4,6-trinitrotoluene by Myriophyllum aquaticum. Environ Sci Technol. https://doi.org/10.1021/es030010a
Wong MH, Giraldo JP, Kwak SY, Koman VB, Sinclair R, Lew TTS, Bisker G, Liu P, Strano MS (2017) Nitroaromatic detection and infrared communication from wild-type plants using plant nanobionics. Nat Mater. https://doi.org/10.1038/nmat4771
Xu CY, Schuster WSF, Griffin KL (2007) Seasonal variation of temperature response of respiration in invasive Berberis thunbergii (Japanese barberry) and two co-occurring native understory shrubs in a northeastern US deciduous forest. Oecologia. https://doi.org/10.1007/s00442-007-0790-3
Yang Z, Chen J, Zhou Y, Huang H, Xu D, Zhang C (2018) Understanding the hydrogen transfer mechanism for the biodegradation of 2,4,6-trinitrotoluene catalyzed by pentaerythritol tetranitrate reductase: molecular dynamics simulations. Phys Chem Chem Phys. https://doi.org/10.1039/c8cp00345a
Yang X, Lai JL, Zhang Y, Luo XG, Han MW, Zhao SP (2021a) Microbial community structure and metabolome profiling characteristics of soil contaminated by TNT, RDX, and HMX. Environ Pollut. https://doi.org/10.1016/j.envpol.2021.117478
Yang X, Zhang Y, Lai JL, Luo XG, Han MW, Zhao SP, Zhu YB (2021b) Analysis of the biodegradation and phytotoxicity mechanism of TNT, RDX, HMX in alfalfa (Medicago sativa). Chemosphere
Yasin NA, Zaheer MM, Khan WU, Ahmad SR, Ahmad A, Ali A, Akram W (2018) The beneficial role of potassium in Cd-induced stress alleviation and growth improvement in Gladiolus grandiflora L. Int J Phytorem. https://doi.org/10.1080/15226514.2017.1374337
Yu LX (2017) Identification of single-nucleotide polymorphic loci associated with biomass yield under water deficit in alfalfa (Medicago sativa L.) using genome-wide sequencing and association mapping. Front Plant Sci. https://doi.org/10.3389/fpls.2017.01152
Zhang Y, Lai JL, Ji XH, Luo XG (2020) Unraveling response mechanism of photosynthetic metabolism and respiratory metabolism to uranium-exposure in Vicia faba. J Hazard Mater. https://doi.org/10.1016/j.jhazmat.2020.122997
Ziganshin AM, Ziganshina EE, Byrne J, Gerlach R, Struve E, Biktagirov T, Rodionov A, Kappler A (2015) Fe(III) mineral reduction followed by partial dissolution and reactive oxygen species generation during 2,4,6-trinitrotoluene transformation by the aerobic yeast Yarrowia lipolytica. AMB Express. https://doi.org/10.1186/s13568-014-0094-z
Acknowledgements
This study was financially supported by National Key Laboratory of National Nuclear and Biochemical Disaster Protection Open Fund Project (No. JK20182A060328). In addition, we thank Shanghai luming biology Co., Ltd. for their assistance in the analysis of metabolome data.
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This study was funded by a grant (No. JK20182A060328) of the National Key Laboratory of National Nuclear and Biochemical Disaster Protection Open Fund Project.
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X-gL conceived and designed the experiments. YZ performed the experiments. J-lL analyzed the data. XY wrote the manuscript.
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Yang, X., Lai, Jl., Zhang, Y. et al. Toxicity analysis of TNT to alfalfa's mineral nutrition and secondary metabolism. Plant Cell Rep 41, 1273–1284 (2022). https://doi.org/10.1007/s00299-022-02856-z
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DOI: https://doi.org/10.1007/s00299-022-02856-z