Effect of Sulfadimethoxine, Oxytetracycline, and Streptomycin Antibiotics in Three Types of Crop Plants—Root, Leafy, and Fruit
"> Figure 1
<p>Uptake of veterinary antibiotics (VAs) by different parts of lettuce, carrot, and pepper grown in soil treated with VAs. Error bars represent standard error. Concentration values followed by different letters are significantly different (<span class="html-italic">p</span> < 0.05) according to Duncan’s multiple range test. SDZ = Sulfadimethoxine; OTC = Oxytetracycline; STR = Streptomycin.</p> "> Figure 1 Cont.
<p>Uptake of veterinary antibiotics (VAs) by different parts of lettuce, carrot, and pepper grown in soil treated with VAs. Error bars represent standard error. Concentration values followed by different letters are significantly different (<span class="html-italic">p</span> < 0.05) according to Duncan’s multiple range test. SDZ = Sulfadimethoxine; OTC = Oxytetracycline; STR = Streptomycin.</p> "> Figure 2
<p>NADPH-cytochrome P450 reductase activity of lettuce, carrot, and pepper grown in soil treated with VAs. Error bars represent standard error. Concentration values followed by different letters are significantly different (<span class="html-italic">p</span> < 0.05) according to Duncan’s multiple range test. SDZ = Sulfadimethoxine; OTC = Oxytetracycline; STR = Streptomycin.</p> "> Figure 3
<p><span class="html-italic">Glutathione-s-transferase</span> (GST) activity of lettuce, carrot and pepper grown in soil treated with VAs. Error bars represent standard error. Concentration values followed by different letters are significantly different (<span class="html-italic">p</span> < 0.05) according to Duncan’s multiple range test. SDZ = Sulfadimethoxine; OTC = Oxytetracycline; STR = Streptomycin.</p> "> Figure 4
<p>Mycorrhizal frequency of lettuce, carrot, and pepper grown in soil treated with VAs. Error bars represent standard error. Concentration values followed by different letters are significantly different (<span class="html-italic">p</span> < 0.05) according to Duncan’s multiple range test. SDZ = Sulfadimethoxine; OTC = Oxytetracycline; STR = Streptomycin.</p> "> Figure 5
<p>Free proline content of lettuce, carrot, and pepper grown in soil treated with VAs. Error bars represent standard error. Concentration values followed by different letters are significantly different (<span class="html-italic">p</span> < 0.05) according to Duncan’s multiple range test. SDZ = Sulfadimethoxine; OTC = Oxytetracycline; STR = Streptomycin.</p> ">
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant
- Leafy: Lettuce, Lactuca sativa, Asteraceae.
- Root: Carrot, Daucus carota, Apiaceae.
- Fruit: Pepper, Capsicum annum, Solanaceae.
2.2. Veterinary Antibiotics
2.3. Phytotoxic Assessment
2.4. Veterinary Antibiotics Accumulation and Bio-Concentration
- Lettuce: Root
- The bottom part of the leaf
- The apical part of the leaf
- Carrot: Leaves
- ∘
- Foot (base): peel, flesh
- ∘
- Brain (upper): peel, flesh
- Pepper: Root
- Stem
- Leaves
- Fruit
2.5. Detoxification of Veterinary Antibiotics
2.6. Secondary Experiments
2.7. Ecological Risk Assessment
3. Results and Discussions
3.1. Phytotoxic Assessment
3.2. VAs Accumulation and Bio-Concentration
3.3. Detoxification of VAs
- Metabolites not formed during the experimental period.
- Metabolites formed are processed by the plant detoxification system and were beyond the detection limit (at the time of analysis).
3.4. Secondary Experiments
3.5. Environmental Risk Assessment
4. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Appendix A
COMPOUND | Sulfadimethoxine | Oxytetracycline | Streptomycin Sulfate |
---|---|---|---|
Structure | |||
Formula | C12H14N4O4S | C22H24N2O9 | C21H39N7O12 ·1.5 H2SO4 |
M.W (g mol-1) | 310.33 | 460.439 | 728.69 |
Family | Sulfonamide | Tetracycline | Aminoglycoside |
CAS no. | 122-11-2 | 79-57-2 | 3810-74-0 |
References
- Göbel, A.; Thomsen, A.; McArdell, C.S.; Alder, A.C.; Giger, W.; Theib, N.; Loffler, D.; Ternes, T.A. Extraction and determination of sulfonamides, macrolides, and trimethoprim in sewage sludge. J. Chromatogr. A 2005, 1085, 179–189. [Google Scholar] [CrossRef]
- Kemper, N. Veterinary antibiotics in the aquatic and terrestrial environment—A review. Ecol. Indic. 2008, 8, 1–13. [Google Scholar] [CrossRef]
- Jjemba, P. The potential impact of veterinary and human therapeutic agents in manure and biosolids on plants grown on arable land: A review. Agric. Ecosyst. Environ. 2002, 93, 267–278. [Google Scholar] [CrossRef]
- Norman, A.G. Terramycin and plant growth. Agron. J. 1955, 47, 585–587. [Google Scholar] [CrossRef]
- Batchelder, A.R. Chlortetracycline and oxytetracycline effects on plant growth and development in soil systems. J. Environ. Qual. 1982, 11, 675–678. [Google Scholar] [CrossRef]
- Kumar, K.; Gupta, S.C.; Baidoo, S.K.; Chander, Y.; Rosen, C.J. Antibiotic uptake by plants from soil fertilized with animal manure. J. Environ. Qual. 2005, 34, 2082–2085. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kummerer, K. Pharmaceuticals in the Environment: Sources, Fate, Effects and Risks; Springer: Berlin, Germany, 2001. [Google Scholar]
- Rooklidge, S.J. Environmental antimicrobial contamination from terraccumulation and diffuse pollution pathways. Sci. Total Environ. 2004, 325, 1–13. [Google Scholar] [CrossRef] [PubMed]
- Migliore, L.; Cozzolino, S.; Fiori, M. Phytotoxicity to and uptake of enrofloxacin in crop plants. Chemosphere 2003, 52, 1233–1244. [Google Scholar] [CrossRef]
- Kong, W.D.; Zhu, Y.G.; Liang, Y.C.; Zhang, J.; Smith, F.A.; Yang, M. Uptake of oxytetracycline and its phytotoxicity to alfalfa (Medicago sativa L.). Environ. Pollut. 2007, 147, 187–193. [Google Scholar] [CrossRef]
- Farkas, M.H.; Berry, J.O.; Aga, D.S. Chlortetracycline detoxification in maize via induction of glutathione S-transferases after antibiotic exposure. Environ. Sci. Technol. 2007, 41, 1450–1456. [Google Scholar] [CrossRef]
- Liu, F.; Ying, G.G.; Ta, R.; Zhao, J.L.; Yang, J.F.; Zhao, L.F. Effects of six selected antibiotics on plant growth and soil microbial and enzymatic activities. Environ. Pollut. 2009, 157, 1636–1642. [Google Scholar] [CrossRef] [PubMed]
- ISTA (International Seed Testing Association). International rules for seed testing. Annexes Seed Sci. Technol. 1985, 13, 356–513. [Google Scholar]
- Zayed, A.; Gowthaman, S.; Terry, N. Phytoaccumulation of trace elements by wetlands plants: I. Duckweed. J. Environ. Qual. 1998, 27, 715–721. [Google Scholar] [CrossRef]
- Tiquia, S.M.; Tam, N.F.Y.; Hodgkiss, I.J. Effects of composting on Phytotoxicity of spent pig-manure sawdust litter. Environ. Pollut. 1996, 93, 249–256. [Google Scholar] [CrossRef]
- Sandermann, H., Jr. Higher plant metabolism of xenobiotics: The “green liver” concept. Pharmacogenetics 1994, 4, 225–241. [Google Scholar] [CrossRef]
- Sánchez-Gómez, F.J.; Díez-Dacal, B.; García-Martín, E.; Agúndez, J.A.; Pajares, M.A.; Pérez-Sala, D. Detoxifying Enzymes at the Cross-Roads of Inflammation, Oxidative Stress, and Drug Hypersensitivity: Role of Glutathione Transferase P1-1 and Aldose Reductase. Front. Pharmacol. 2016, 7, 237. [Google Scholar] [CrossRef] [Green Version]
- Habig, W.H.; Pabst, M.J.; Jakoby, W.B. Glutathione s-transferases: The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 1974, 249, 7130–7139. [Google Scholar]
- Trouvelot, A.; Kough, L.; Gianinazzi-Pearson, V. Evaluation of va infection levels in root systems. In Research for Estimation Methods Having a Functional Significance, Physiological and Genetical Aspects of Mycorrhizae; Gianinazzi-Pearson, V., Gianinazzi, S., Eds.; INRA Press: Paris, France, 1986; pp. 217–221. [Google Scholar]
- Phillips, J.M.; Haymann, D.S. Improved procedure for clearing and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 1970, 55, 158–161. [Google Scholar] [CrossRef]
- Bates, L.S. Rapid determination of free proline for water stress studies. Plant Soil 1973, 39, 205–207. [Google Scholar] [CrossRef]
- EMA. European Medicine Agency Guideline on the Environmental Risk Assessment of Medicinal Products for Human Use (EMEA/CHMP/SWP/4447/00); EMA: Amsterdam, The Netherlands, 2006. [Google Scholar]
- Marti, E.; Sierra, J.; Sanchez, M.; Cruanas, R.; Garau, M.A. Ecotoxicological tests assessment of soils polluted by chromium (VI) or pentachlorophenol. Sci. Total Environ. 2007, 378, 53–57. [Google Scholar] [CrossRef]
- Migliore, L.; Civitareale, C.; Cozzolino, S.; Casoria, P.; Gambilla, F.; Gaudio, L. Laboratory models to evaluate phytotoxicity of sulphadimethoxine on terrestrial plants. Chemosphere 1998, 37, 2957–2961. [Google Scholar] [CrossRef]
- NAAS (National Academy of Agricultural Sciences). Antibiotics in manure and soil—A grave threat to human and animal health. Policy Pap. 2010, 43, 1–20. [Google Scholar]
- Dolliver, H.; Kumar, K.; Gupta, S.C. Sulfamethazine uptake by plants from manure-amended soil. J. Environ. Qual. 2007, 36, 1224–1230. [Google Scholar] [CrossRef] [PubMed]
- Tan, L.R.; Lu, Y.C.; Zhang, J.J.; Luo, F.; Yang, H. A collection of cytochrome P450 monooxygenase genes involved in modification and detoxification of herbicide atrazine in rice (Oryza sativa) plants. Ecotoxicol. Environ. Saf. 2015, 119, 25–34. [Google Scholar]
- Bolwell, G.P.; Bozak, K.; Zimmerlin, A. Plant cytochrome P450. Phytochemistry 1994, 37, 1491–1506. [Google Scholar] [CrossRef]
- Deavall, D.G.; Martin, E.A.; Horner, J.M.; Roberts, R. Drug-induced oxidative stress and toxicity. J. Toxicol. 2012, 2012, 645460. [Google Scholar] [CrossRef] [Green Version]
- Chronopoulou, E.; Georgakis, N.; Nianiou-Obeidat, I.; Madesis, P.; Perperopoulou, F.; Vasilopoulou, E. Glutathione in Plant Growth, Development, and Stress Tolerance; Springer International Publishing: Berlin, Germany, 2017; pp. 215–233. [Google Scholar]
- Boyer, L.R.; Brain, P.; Xu, X.M.; Jeffries, P. Inoculation of drought-stressed strawberry with a mixed inoculum of two arbuscular mycorrhizal fungi: Effects on population dynamics of fungal species in roots and consequential plant tolerance to water. Mycorrhiza 2014, 25, 215–227. [Google Scholar] [CrossRef]
- Moradtalab, N.; Hajiboland, R.; Aliasgharzad, N.; Hartmann, T.E.; Neumann, G. Silicon and the association with an arbuscular-mycorrhizal fungus (Rhizophagus clarus) mitigate the adverse effects of drought stress on strawberry. Agronomy 2019, 9, 41. [Google Scholar] [CrossRef] [Green Version]
- Sharma, N.; Yadav, K.; Cheema, J.; Badda, N.; Aggarwal, A. Arbuscular mycorrhizal symbiosis and water stress: A critical review. Pertanika J. Trop. Agric. Sci. 2015, 38, 427–453. [Google Scholar]
- Khalil, F.; Rauf, S.; Monneveux, P.; Anwar, S.; Iqbal, Z. Genetic analysis of proline concentration under osmotic stress in sunflower (Helianthus annuus L.). Breed Sci. 2016, 66, 463–470. [Google Scholar] [CrossRef] [Green Version]
- Molinari, H.B.C.; Marur, C.J.; Daros, E.; De Campos, M.K.F.; De Carvalho, J.F.R.P.; Pereira, L.F.P.; Vieira, L.G.E. Evaluation of the stress-inducible production of proline in transgenic sugarcane (Saccharum spp.): Osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiol. Plant. 2007, 130, 218–229. [Google Scholar] [CrossRef]
- Liu, D.; Ford, K.L.; Roessner, U.; Natera, S.; Cassin, A.M.; Patterson, J.H.; Bacic, A. Rice suspension cultured cells are evaluated as a model system to study salt responsive networks in plants using a combined proteomic and metabolomic profiling approach. Proteomics 2013, 13, 2046–2062. [Google Scholar] [CrossRef] [PubMed]
- Hoson, T.; Wada, S. Role of hydroxyprolinerich cell wall protein in growth regulation of rice coleoptiles grown on or under water. Plant Cell Physiol. 1980, 21, 511–524. [Google Scholar] [CrossRef]
- Hayat, S.; Hayat, Q.; Alyemeni, M.N.; Wani, A.S.; Pichtel, J.; Ahmad, A. Role of proline under changing environments: A review. Plant Signal Behav. 2012, 7, 1456–1466. [Google Scholar] [CrossRef] [Green Version]
- Yaish, M.W. Proline accumulation is a general response to abiotic stress in the date palm tree (Phoenix dactylifera L.). Genet. Mol. Res. 2015, 14, 9943–9950. [Google Scholar] [CrossRef]
Soil Type | Sand (%) | Silt (%) | Clay (%) | OM (%) | pH (DW) | EC (μS/cm) | N (mg kg−1) | P (mg kg−1) | K (mg kg−1) |
---|---|---|---|---|---|---|---|---|---|
Sandy clay loam | 59.47 | 9.8 | 30.73 | 1.23 | 5.23 | 72.85 | 518 | 379.1 | 3400 |
Veterinary Antibiotics | EC50 (mg kg−1) | ||
---|---|---|---|
Lettuce | Carrot | Pepper | |
Sulfadimethoxine | 10.89 | 7.49 | 11.76 |
Oxytetracycline | 13.15 | 9.11 | 28.06 |
Streptomycin | 60.24 | 36.89 | 306.84 |
Veterinary Antibiotics | Endpoint | EC50 (mg kg−1) | ||
---|---|---|---|---|
Lettuce | Carrot | Pepper | ||
Oxytetracycline | Plant height | 167.103 | 155.608 | 325.307 |
Root length | 97.825 | 61.662 | 113.06 | |
Sulfadimethoxine | Plant height | 55.201 | 40.835 | 152.142 |
Root length | 14.983 | 16.919 | 47.7 | |
Streptomycin | Plant height | 484.38 | 306.995 | 893.606 |
Root length | 197.44 | 153.72 | 377.77p |
VAs (mg kg−1) | Lettuce (mg kg−1) | Carrot (mg kg−1) | Pepper (mg kg−1) |
---|---|---|---|
Control | 0.00 ± 0.00 | 0.00 ± 0.00 | 0.00 ± 0.00 |
SDZ 10 | 1.19 ± 0.829 d | 1.41 ± 0.069 cd | 1.97 ± 0.001 d |
SDZ 50 | 3.31 ± 1.797 c | 3.84 ± 2.214 b | 4.41 ± 0.057 b |
SDZ 100 | 12.47 ± 3.173 a | 14.34 ± 1.681 a | 16.88 ± 0.047 a |
OTC 10 | 0.43 ± 0.649 e | 0.39 ± 0.049 e | 0.23 ± 0.058 e |
OTC 50 | 1.19 ± 0.741 d | 2.03 ± 0.237 c | 1.72 ± 0.784 d |
OTC 100 | 4.95 ± 0.794 b | 3.84 ± 0.343 b | 3.51 ± 0.402 c |
STR 10 | 0.07 ± 0.049 f | 0.08 ± 0.784 f | 0.09 ± 0.851 f |
STR 50 | 0.41 ± 0.649 e | 0.33 ± 0.049 e | 0.41 ± 0.058 e |
STR 100 | 1.29 ± 2.262 d | 1.17 ± 4.275 d | 1.57 ± 3.627 d |
Veterinary Antibiotics (mg kg−1) | Bio-Concentration Factor (μg kg−1) | ||||
---|---|---|---|---|---|
Lettuce | Carrot | Pepper | |||
SHOOT | OTC | 10 | 0.069 ± 0.003 | 0.010 ± 0.054 | 0.033 ± 0.010 |
50 | 0.240 ± 0.008 | 0.043 ± 0.013 | 0.109 ± 0.003 | ||
100 | 2.307 ± 0.008 | 0.610 ± 0.009 | 0.102 ± 0.003 | ||
SDZ | 10 | 0.286 ± 0.002 | 0.018 ± 0.023 | 0.066 ± 0.005 | |
50 | 2.373 ± 0.006 | 1.069 ± 0.006 | 0.727 ± 0.002 | ||
100 | 6.103 ± 0.005 | 3.088 ± 0.004 | 1.227 ± 0.001 | ||
STR | 10 | - | - | - | |
50 | - | - | - | ||
100 | - | - | - | ||
ROOT | OTC | 10 | 0.065 ± 0.013 | 0.515 ± 0.009 | 0.134 ± 0.091 |
50 | 0.177 ± 0.004 | 1.517 ± 0.005 | 0.374 ± 0.094 | ||
100 | 0.243 ± 0.003 | 2.132 ± 0.003 | 0.474 ± 0.118 | ||
SDZ | 10 | 0.227 ± 0.004 | 1.250 ± 0.003 | 0.513 ± 0.016 | |
50 | 1.485 ± 0.021 | 5.003 ± 0.003 | 1.016 ± 0.057 | ||
100 | 4.671 ± 0.041 | 8.859 ± 0.002 | 3.361 ± 0.099 | ||
STR | 10 | - | - | - | |
50 | - | - | - | ||
100 | - | - | - |
VA’s | Plant | PNEC | PEC (mg kg−1) | RQ | ERA |
---|---|---|---|---|---|
SDZ | Lettuce | 2.107 × 10−3 | 3.684 × 10−3 | 1.785 | High |
Carrot | 1.175 × 10−3 | 3.684 × 10−3 | 3.135 | High | |
Pepper | 3.395 × 10−3 | 3.684 × 10−3 | 1.085 | High | |
OTC | Lettuce | 1.166 × 10−3 | 1.052 × 10−3 | 0.902 | Medium |
Carrot | 1.411 × 10−3 | 1.052 × 10−3 | 0.745 | Medium | |
Pepper | 2.511 × 10−3 | 1.052 × 10−3 | 0.419 | Medium | |
STR | Lettuce | 6.09 × 10−3 | 1.05 × 10−1 | 0.017 | Low |
Carrot | 3.365 × 10−3 | 1.05 × 10−1 | 0.031 | Low | |
Pepper | 1.048 × 10−2 | 1.05 × 10−1 | 0.1001 | Low |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Tasho, R.P.; Ryu, S.-H.; Cho, J.-Y. Effect of Sulfadimethoxine, Oxytetracycline, and Streptomycin Antibiotics in Three Types of Crop Plants—Root, Leafy, and Fruit. Appl. Sci. 2020, 10, 1111. https://doi.org/10.3390/app10031111
Tasho RP, Ryu S-H, Cho J-Y. Effect of Sulfadimethoxine, Oxytetracycline, and Streptomycin Antibiotics in Three Types of Crop Plants—Root, Leafy, and Fruit. Applied Sciences. 2020; 10(3):1111. https://doi.org/10.3390/app10031111
Chicago/Turabian StyleTasho, Reep Pandi, Song-Hee Ryu, and Jae-Young Cho. 2020. "Effect of Sulfadimethoxine, Oxytetracycline, and Streptomycin Antibiotics in Three Types of Crop Plants—Root, Leafy, and Fruit" Applied Sciences 10, no. 3: 1111. https://doi.org/10.3390/app10031111