Korean Journal of Environmental Biology (환경생물)

Korean Society of Environmental Biology (한국환경생물학회)
권호 표지
DOI QR코드

DOI QR Code

Molecular physiological inhibitory effects of chloroacetanilide herbicide pretilachlor on marine dinoflagellate Prorocentrum minimum

해양 와편모조류 Prorocentrum minimum에 대한 아세트아닐라이드계 제초제 프레틸라클로르의 분자 생물학적 저해 효과

  • Hansol Kim (Department of Biotechnology, Sangmyung University) ;
  • Jang-Seu Ki (Department of Biotechnology, Sangmyung University)
  • 김한솔 (상명대학교 생명공학과) ;
  • 기장서 (상명대학교 생명공학과)
  • Received : 2021.11.05
  • Accepted : 2021.11.16
  • Published : 2021.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Pretilachlor (PRE) is a common acetanilide herbicide used worldwide. However, its effects on aquatic organisms, particularly marine photosynthetic life, are not sufficiently known. Herein, we evaluated the toxic effects of PRE by physiological and molecular parameters in the photosynthetic dinoflagellate Prorocentrum minimum. The cell density, pigment content, and photosynthetic parameters (Fv/Fm and PIABS) were considerably decreased with increased PRE exposure time and doses. In addition, photosynthesis-related genes, PmpsbA, PmpsaA, and PmatpB, were significantly upregulated when exposed to 1.0 mg L-1 of PRE for 24 h (p<0.001). In 72 h treatment, the relative gene expression was significantly increased (0.1 and 0.5 mg L-1; p<0.01). In contrast, PmrbcL was decreased or little changed compared to the controls. Reactive oxygen species (ROS) increased after 24 h exposure (p<0.001). However, the transcriptional fold-changes in glutathione S-transferase (GST) were significantly increased (0.5 and 1.0 mg L-1; p<0.001) at 72 h. These findings suggested that the PmGST might be involved in PRE detoxification in P. minimum. In addition, PRE may affect the photosystem function in phytoplankton similar to other acetanilides, causing severe damage or cell death.

Pretilachlor (PRE)는 전 세계적으로 사용되는 아세트아닐리드계 제초제이며 수생 광영양생물에 미치는 영향에 대해서는 알려진 바가 거의 없다. 본 연구에서 해양 와편모조류 P. minimum를 대상으로 PRE의 생리적, 분자적 독성 영향을 평가하였다. 그 결과, PRE는 P. minimum의 성장률, 색소, 광합성 지표를 유의하게 감소시켰다. 또한, 광합성 관련 유전자 PmpsbA, PmpsaA 및 항산화 단백질 PmGST의 상대적 유전자 발현율과 세포 내 ROS 증가가 유의하였다. 이는 PRE가 P. minimum의 광합성 효율 저하 및 광계 손상을 야기하며, GST가 세포 내 산화 스트레스 및 PRE의 무독화에 관여함을 보여준다. 본 연구 결과는 PRE를 비롯한 아세트아닐라이드계 제초제가 해양 와편모조류의 세포 독성을 야기하며, 광합성 저해가 스트레스의 주요 원인임을 제시한다. 다른 아세트아닐라이드계 제초제가 비표적 광영양 생물에게 미치는 독성 영향은 아직 연구가 부족하므로, 향후 연구에서 다양한 생물종을 대상으로 추가 연구가 필요하다.

Keywords

Acknowledgement

이 논문은 2020년도 정부(미래창조과학부)의 재원으로 한국연구재단의 지원을 받아 수행된 기초연구사업임(No.2020R1A2C2013373).

References

  1. Abassi S and JS Ki. 2021. Increased nitrate concentration differentially affects cell growth and expression of nitrate transporter and other nitrogen-related genes in the harmful dinoflagellate Prorocentrum minimum. Chemosphere 288:132526.
  2. Almeida C, P Serodio, MH Florencio and JMF Nogueira. 2007. New strategies to screen for endocrine-disrupting chemicals in the Portuguese marine environment utilizing large volume injection-capillary gas chromatography-mass spectrometry combined with retention time locking libraries (LVI-GC-MSRTL). Anal. Bioanal. Chem. 387:2569-2583. https://doi.org/10.1007/s00216-006-1101-2
  3. Ashton FM, OT de Villiers, RK Glenn and WB Duke. 1977. Localization of metabolic sites of action of herbicides. Pestic. Biochem. Physol. 7:122-141. https://doi.org/10.1016/0048-3575(77)90024-4
  4. Benekos K, C Kissoudis, I Nianiou-Obeidat, N Labrou, P Madesis, M Kalamaki, A Makris and A Tsaftaris. 2010. Overexpression of a specific soybean GmGSTU4 isoenzyme improves diphenyl ether and chloroacetanilide herbicide tolerance of transgenic tobacco plants. J. Biotechnol. 150:195-201.
  5. Campbell SJ, LJ McKenzie and SP Kerville. 2006. Photosynthetic responses of seven tropical seagrasses to elevated seawater temperature. J. Exp. Mar. Biol. Ecol. 330:455-468. https://doi.org/10.1016/j.jembe.2005.09.017
  6. Cummins I, DJ Wortley, F Sabbadin, Z He, CR Coxon, HE Straker, JD Sellars, K Knight, L Edwards, D Hughes, SS Kaundun, SJ Hutchings, PG Steel and R Edwards. 2013. Key role for a glutathione transferase in multiple-herbicide resistance in grass weeds. Proc. Natl. Acad. Sci. U.S.A. 110:5812-5817. https://doi.org/10.1073/pnas.1221179110
  7. De Kuhn RM, C Streb, R Breiter, P Richter, T Neesse and DP Hader. 2006. Screening for unicellular algae as possible bioassay organisms for monitoring marine water samples. Water Res. 40:2695-2703. https://doi.org/10.1016/j.watres.2006.04.045
  8. Ebenezer V and JS Ki. 2013a. Physiological and biochemical responses of the marine dinoflagellate Prorocentrum minimum exposed to the oxidizing biocide chlorine. Ecotox. Environ. Safe. 92:129-134. https://doi.org/10.1016/j.ecoenv.2013.03.014
  9. Ebenezer V and JS Ki. 2013b. Quantification of toxic effects of the herbicide metolachlor on marine microalgae Ditylum brightwellii (Bacillariophyceae), Prorocentrum minimum (Dinophyceae), and Tetraselmis suecica (Chlorophyceae). J. Microbiol. 51:136-139. https://doi.org/10.1007/s12275-013-2114-0
  10. Ebenezer V and JS Ki. 2014. Quantification of toxic effects of the organochlorine insecticide endosulfan on marine green algae, diatom and dinoflagellate. Indian J. Mar. Sci. 43:393-399.
  11. Ebenezer V and JS Ki. 2016. Toxic effects of Aroclor 1016 and bisphenol A on marine green algae Tetraselmis suecica, diatom Ditylum brightwellii and dinoflagellate Prorocentrum minimum. Korean J. Microbiol. 52:306-312. https://doi.org/10.7845/kjm.2016.6050
  12. EFSA. 2008. Opinion on a request from EFSA related to the default Q10 value used to describe the temperature effect on transformation rates of pesticides in soil - Scientific: Opinion of the Panel on Plant Protection Products and their Residues. EFSA J. 622:1-32.
  13. EU. 2007. European Communities (Drinking Water) No. 2 Regulations. No. 278. European Union. pp. 22-23.
  14. Gotz T and P Boger. 2004. The very-long-chain fatty acid synthase is inhibited by chloroacetamides. Z. Naturforsch. C 59:549-553. https://doi.org/10.1515/znc-2004-7-818
  15. Guillard RR. 1975. Culture of phytoplankton for feeding marine invertebrates. pp. 29-60. In: Culture of Marine Invertebrate Animals. Springer, Boston, MA.
  16. Guo R, V Ebenezer and JS Ki. 2012. Transcriptional responses of heat shock protein 70 (Hsp70) to thermal, bisphenol A, and copper stresses in the dinoflagellate Prorocentrum minimum. Chemosphere 89:512-520. https://doi.org/10.1016/j.chemosphere.2012.05.014
  17. Guo R, V Ebenezer, H Wang and JS Ki. 2017. Chlorine affects photosystem II and modulates the transcriptional levels of photosynthesis-related genes in the dinoflagellate Prorocentrum minimum. J. Appl. Phycol. 29:153-163. https://doi.org/10.1007/s10811-016-0955-8
  18. Guo R and JS Ki. 2012. Evaluation and validation of internal control genes for studying gene expression in the dinoflagellate Prorocentrum minimum using real-time PCR. Eur. J. Protistol. 48:199-206. https://doi.org/10.1016/j.ejop.2011.11.001
  19. Guo R and JS Ki. 2013. Characterization of a novel catalase-peroxidase (KATG) gene from the dinoflagellate Prorocentrum minimum. J. Phycol. 49:1011-1016. https://doi.org/10.1111/jpy.12094
  20. Guo R, V Ebenezer and JS Ki. 2014. PmMGST3, a novel microsomal glutathione S-transferase gene in the dinoflagellate Prorocentrum minimum, is a potential biomarker of oxidative stress. Gene 546:378-385. https://doi.org/10.1016/j.gene.2014.05.046
  21. Guo R, V Ebenezer, H Wang and JS Ki. 2017. Chlorine affects photosystem II and modulates the transcriptional levels of photosynthesis-related genes in the dinoflagellate Prorocentrum minimum. J. Appl. Phycol. 29:153-163. https://doi.org/10.1007/s10811-016-0955-8
  22. Hayes JD and DJ Pulford. 1995. The glutathione S-transferase supergene family: regulation of GST and the contribution of the lsoenzymes to cancer chemoprotection and drug resistance part I. Crit. Rev. Biochem. Mol. Biol. 30:445-520. https://doi.org/10.3109/10409239509083491
  23. Heil CA, PM Glibert and C Fan. 2005. Prorocentrum minimum (Pavillard) Schiller: a review of a harmful algal bloom species of growing worldwide importance. Harmful Algae 4:449-470. https://doi.org/10.1016/j.hal.2004.08.003
  24. Junghans M, T Backhaus, M Faust, M Scholze and LH Grimme. 2003. Predictability of combined effects of eight chloroacetanilide herbicides on algal reproduction. Pest Manag. Sci. 59:1101-1110. https://doi.org/10.1002/ps.735
  25. Jursik M, J Soukup, J Holec and J Andr. 2011. Herbicide mode of actions and symptoms of plant injury by herbicides: Inhibitors of very long chain fatty acid biosynthesis. Listy Cukrov. Repar. 127:15.
  26. Kasai F and S Hatakeyama. 1993. Herbicide susceptibility in two green algae, Chlorella vulgaris and Selenastrum capricornutum. Chemosphere 27:899-904. https://doi.org/10.1016/0045-6535(93)90019-2
  27. Kasai F, N Takamura and S Hatakeyama. 1993. Effects of simetryne on growth of various freshwater algal taxa. Environ. Pollut. 79:77-83. https://doi.org/10.1016/0269-7491(93)90180-V
  28. Kaushik S. 2010. Effect of herbicides with different modes of action on physiological and cellular traits of Anabaena fertilissima. Paddy Water Environ. 8:277-282. https://doi.org/10.1007/s10333-010-0208-4
  29. Kim H, H Wang, S Abassi and JS Ki. 2020. The herbicide alachlor severely affects photosystem function and photosynthetic gene expression in the marine dinoflagellate Prorocentrum minimum. J. Environ. Sci. Health Part B 55:620-629. https://doi.org/10.1080/03601234.2020.1755198
  30. Kim H, H Wang and JS Ki. 2021. Chloroacetanilides inhibit photosynthesis and disrupt the thylakoid membranes of the dinoflagellate Prorocentrum minimum as revealed with metazachlor treatment. Ecotox. Environ. Safe. 211:111928.
  31. Lee JK, KS Kyung, IS Jung, KC Ahn and JW Gwon. 1988. Elution of permeable insecticide carbofuran and herbicide pretilachlor in the soil column. Korean J. Pest. Sci. 2:59-67.
  32. Levitan O, SA Kranz, D Spungin, O Prasil, B Rost, I Berman-Frank. 2010. Combined effects of CO2 and light on the N2 -fixing cyanobacterium Trichodesmium IMS101: a mechanistic view. Plant Physiol. 154:346-356. https://doi.org/10.1104/pp.110.159285
  33. Moon YH, SY Ma and HS Yang. 1987. Movement characteristics of herbicide pretilachlor in plants and soil. Korean J. Pest. Sci. 30:351-356.
  34. Ma J, L Xu, S Wang, R Zheng, S Jin, S Huang and Y Huang. 2002. Toxicity of 40 herbicides to the green alga Chlorella vulgaris. Ecotox. Environ. Safe. 51:128-132. https://doi.org/10.1006/eesa.2001.2113
  35. Ma J, S Wang, P Wang, L Ma, X Chen and R Xu. 2006. Toxicity assessment of 40 herbicides to the green alga Raphidocelis subcapitata. Ecotox. Environ. Safe. 63:456-462. https://doi.org/10.1016/j.ecoenv.2004.12.001
  36. Machado MD and EV Soares. 2021. Exposure of the alga Pseudokirchneriella subcapitata to environmentally relevant concentrations of the herbicide metolachlor: Impact on the redox homeostasis. Ecotox. Environ. Safe. 207:111264.
  37. Martin H and CR Worthing. 1974. Pesticide Manual, Fourth ed. British Crop Protection Council. Cambridge, UK.
  38. Mezzari MP, K Walters, M Jelinkova, MC Shih, CL Just and JL Schnoor. 2005. Gene expression and microscopic analysis of Arabidopsis exposed to chloroacetanilide herbicides and explosive compounds. A phytoremediation approach. Plant Physiol. 138:858-869.
  39. Milligan AS, A Daly, MAJ Parry, PA Lazzeri and I Jepson. 2001. The expression of a maize glutathione S-transferase gene in transgenic wheat confers herbicide tolerance, both in planta and in vitro. Mol. Breed. 7:301-315. https://doi.org/10.1023/A:1011652821765
  40. MFDS. 2018. Enforcement of PLS from 1 January 2019. Ministry of Food and Drug Safety. Cheongju, Korea. Retrieved from Retrieved from https://www.mfds.go.kr/eng/index.do on Dec. 27
  41. Mohr S, R Berghahn, M Feibicke, S Meinecke, T Ottenstroer, I Schmiedling, R Schmiedling and R Schmidt. 2007. Effects of the herbicide metazachlor on macrophytes and ecosystem function in freshwater pond and stream mesocosms. Aquat. Toxicol. 82:73-84. https://doi.org/10.1016/j.aquatox.2007.02.001
  42. Mohr S, M Feibicke, R Berghahn, R Schmiediche and R Schmidt. 2008. Response of plankton communities in freshwater pond and stream mesocosms to the herbicide metazachlor. Environ. Pollut. 152:530-542. https://doi.org/10.1016/j.envpol.2007.07.010
  43. Nagai T, K Taya and I Yoda. 2016. Comparative toxicity of 20 herbicides to 5 periphytic algae and the relationship with mode of action. Environ. Toxicol. Chem. 35:368-375. https://doi.org/10.1002/etc.3150
  44. Nykiel-Szymanska J, P Bernat and M Slaba. 2020. Biotransformation and detoxification of chloroacetanilide herbicides by Trichoderma spp. with plant growth-promoting activities. Pest. Biochem. Physiol. 163:216-226. https://doi.org/10.1016/j.pestbp.2019.11.018
  45. Okumura Y, J Iro Koayama and S Unol. 2003. The relationship between logPow and molecular weight of polycyclic aromatic hydrocarbons and EC50 values. La mer 41:182-191.
  46. Oukarroum A, S El Madidi, G Schansker and RJ Strasser. 2007. Probing the responses of barley cultivars (Hordeum vulgare L.) by chlorophyll a fluorescence OLKJIP under drought stress and re-watering. Environ. Exp. Bot. 60:438-446. https://doi.org/10.1016/j.envexpbot.2007.01.002
  47. Parsons TR, Y Maita and CMI Lalli. 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press. Oxford, UK.
  48. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:45-45. https://doi.org/10.1093/nar/29.9.e45
  49. Ponmani T, R Guo and JS Ki. 2015. A novel cyclophilin gene from the dinoflagellate Prorocentrum minimum and its possible role in the environmental stress response. Chemosphere 139:260-267. https://doi.org/10.1016/j.chemosphere.2015.06.036
  50. Posecion N, E Ostrea, D Bielawski, M Corrion, J Seagraves and Y Jin. 2006. Detection of exposure to environmental pesticides during pregnancy by the analysis of maternal hair using GC-MS. Chromatographia 64:681-687. https://doi.org/10.1365/s10337-006-0092-7
  51. Qian H, X Pan, S Shi, S Yu, H Jiang, Z Lin and Z Fu. 2011. Effect of nonylphenol on response of physiology and photosynthesis-related gene transcription of Chlorella vulgaris. Environ. Monit. Assess. 182:61-69. https://doi.org/10.1007/s10661-010-1858-9
  52. Qin Y, M Lu and X Gong. 2008. Dihydrorhodamine 123 is superior to 2,7-dichlorodihydrofluorescein diacetate and dihydrorhodamine 6G in detecting intracellular hydrogen peroxide in tumor cells. Cell Biol. Int. 32:224-228. https://doi.org/10.1016/j.cellbi.2007.08.028
  53. Rial D, VM Leon and J Bellas. 2017. Integrative assessment of coastal marine pollution in the Bay of Santander and the Upper Galician Rias. J. Sea Res. 130:239-247. https://doi.org/10.1016/j.seares.2017.03.006
  54. Sakurai I, D Stazic, M Eisenhut, E Vuorio, C Steglich, WR Hess and EM Aro. 2012. Positive regulation of psbA gene expression by cis-encoded antisense RNAs in Synechocystis sp. PCC 6803. Plant Physiol. 160:1000-1010. https://doi.org/10.1104/pp.112.202127
  55. Shapira M, A Lers, PB Heifetz, V Irihimovitz, CB Osmond, NW Gillham and JE Boynton. 1997. Differential regulation of chloroplast gene expression in Chlamydomonas reinhardtii during photoacclimation: light stress transiently suppresses synthesis of the Rubisco LSU protein while enhancing synthesis of the PS II D1 protein. Plant Mol. Biol. 33:1001-1001. https://doi.org/10.1023/A:1005814800641
  56. Skaggs RW, JW Gilliam, TJ Sheets and JS Barnes. 1980. Effect of Agricultural Land Development on Drainage Waters in the NC Tidewater Region. Water Resources Research Institute of the University of North Carolina. Raleigh, NC.
  57. Sloan ME and ND Camper. 1986. Effects of alachlor and metolachlor on cucumber seedlings. Environ. Exp. Bot. 26:1-7. https://doi.org/10.1016/0098-8472(86)90046-8
  58. Souissi Y, S Bouchonnet, S Bourcier, KO Kusk, M Sablier and HR Andersen. 2013. Identification and ecotoxicity of degradation products of chloroacetamide herbicides from UV-treatment of water. Sci. Total Environ. 458:527-534.
  59. Strasser RJ, A Srivastava and M Tsimilli-Michael. 2000. The fluorescence transient as a tool to characterize and screen photosynthetic samples. pp. 445-483. In: Probing Photosynthesis: Mechanisms, Regulation and Adaptation. CRC Press. Boca Raton, FL.
  60. Sulmon C, G Gouesbet, I Couee and A El Amrani. 2004. Sugar-induced tolerance to atrazine in Arabidopsis seedlings: interacting effects of atrazine and soluble sugars on psbA mRNA and D1 protein levels. Plant Sci. 167:913-923. https://doi.org/10.1016/j.plantsci.2004.05.036
  61. Sverdrup LE, T Kallqvist, AE Kelley, CS Furst and SB Hagen. 2001. Comparative toxicity of acrylic acid to marine and freshwater microalgae and the significance for environmental effects assessments. Chemosphere 45:653-658. https://doi.org/10.1016/S0045-6535(01)00044-3
  62. Trenkamp S, W Martin and K Tietjen. 2004. Specific and differential inhibition of very-long-chain fatty Acid Elongases from Arabidopsis thaliana by different herbicides. Proc. Natl. Acad. Sci. 101:11903-11908. https://doi.org/10.1073/pnas.0404600101
  63. Tsuda T, T Nakamura, A Inoue and K Tanaka. 2009. Pesticides in water, fish and shellfish from littoral area of Lake Biwa. Bull. Environ. Contam. Toxicol. 82:716-721. https://doi.org/10.1007/s00128-009-9681-0
  64. Tyohemba RL, L Pillay and MS Humphries. 2020. Herbicide residues in sediments from Lake St Lucia (iSimangaliso World Heritage Site, South Africa) and its catchment areas: Occurrence and ecological risk assessment. Environ. Pollut. 267:115566.
  65. Ueda K and T Nagai. 2021. Relative sensitivity of duckweed Lemna minor and six algae to seven herbicides. J. Pest. Sci. 46:267-273. https://doi.org/10.1584/jpestics.D21-018
  66. Urso ML and PM Clarkson. 2003. Oxidative stress, exercise, and antioxidant supplementation. Toxicology 189:41-54. https://doi.org/10.1016/S0300-483X(03)00151-3
  67. Van Toan P, Z Sebesvari, M Blasing, I Rosendahl and FG Renaud. 2013. Pesticide management and their residues in sediments and surface and drinking water in the Mekong Delta, Vietnam. Sci. Total Environ. 452:28-39.
  68. Wang H, S Abassi and JS Ki. 2019. Origin and roles of a novel copper-zinc superoxide dismutase (CuZnSOD) gene from the harmful dinoflagellate Prorocentrum minimum. Gene 683:113-122. https://doi.org/10.1016/j.gene.2018.10.013
  69. Wauchope RD. 1978. The pesticide content of surface water draining from agricultural fields - a review. J. Environ. Qual. 7:459-472. https://doi.org/10.2134/jeq1978.00472425000700040001x
  70. Wei J, Y Feng, X Sun, J Liu and L Zhu. 2011. Effectiveness and pathways of electrochemical degradation of pretilachlor herbicides. J. Hazard. Mater. 189:84-91. https://doi.org/10.1016/j.jhazmat.2011.02.002
  71. Wilkinson RE. 1981. Metolachlor [2-chloro-N-(2-ethyl-6-methylphenyl)-N-(2-methoxy-1-methylethyl) acetamide] inhibition of gibberellin precursor biosynthesis. Pestic. Biochem. Physiol. 16:199-205. https://doi.org/10.1016/0048-3575(81)90053-5
  72. Wilkinson RE. 1982. Alachlor influence on sorghum growth and gibberellin precursor synthesis. Pestic. Biochem. Physiol. 17:177-184.  https://doi.org/10.1016/0048-3575(82)90023-2