Abstract
Microcystins (MCs) are cyclic heptapeptide hepatotoxins that are highly soluble in water and can be transferred to farmland through irrigation with potentially substantial effects on crops, especially rice. In order to investigate the possible negative effects of microcystin-LR (MC-LR) on rice, the oxidative stress induced in rice suspension cells exposed to MC-LR at environmentally relevant concentrations (0.05, 0.5, 5.0, and 50.0 μg·L−1) was investigated. Results showed that the exposure to MC-LR at 0.5–50.0 μg·L−1 resulted in a significant decline in viability of rice suspension cells and an increase in malondialdehyde (MDA) contents. In the 50.0-μg·L−1 MC-LR treatment group, the content of MDA was as much as 5.39 times that of the control group after 6 days of exposure. The excess MDA production indicated that MC-LR exposure has caused lipid peroxidation damage in rice cells, whereas these negative effects could be recovered over time when suspension cells were exposed to low concentration of MC-LR (0.05 μg·L−1). When exposed to MC-LR for 3 days, the O2− content in all treatment groups increased significantly compared with the control group. Additionally, the antioxidant system of rice suspension cells initiated a positive stress response to MC-LR exposure. Indeed, peroxidase (POD) played an active role in the removal of reactive oxygen species (ROS) in rice suspension cells during the early period of exposure, while total superoxide dismutase (T-SOD) was induced after 6 days. Similarly, after 6 days of exposure, the anti-superoxide anion free radical activity (ASAFR), glutathione (GSH), and glutathione-S transferase (GST) in rice suspension cells were higher than that in the control group. These results provided a comprehensive understanding of the exposure time- and dose-dependent oxidative stress induced by the environmentally relevant concentrations of MC-LR in rice suspension cells.
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References
Amado LL, Monserrat JM (2010) Oxidative stress generation by microcystins in aquatic animals: why and how. Environ Int 36(2):226–235. https://doi.org/10.1016/j.envint.2009.10.010
Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(s 1-2):248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Cadenas E (1989) Biochemistry of oxygen toxicity. Annu Rev Biochem 58(1):79–110. https://doi.org/10.1146/annurev.bi.58.070189.000455
Cao Q, **e L (2016) Progress and prospect of eco-toxicity of microcystins in soil-plant system. J Lake Sci 28(05):925–934. https://doi.org/10.18307/2016.0501
Cao Q, Rediske RR, Yao L, **e L (2018) Effect of microcystins on root growth, oxidative response, and exudation of rice (Oryza sativa). Ecotoxicol Environ Saf 149(mar.):143–149. https://doi.org/10.1016/j.ecoenv.2017.11.020
Cao Q, Wan X, Shu X, **e L (2019) Bioaccumulation and detoxication of microcystin-LR in three submerged macrophytes: the important role of glutathione biosynthesis. Chemosphere 225(JUN.):935–942. https://doi.org/10.1016/j.chemosphere.2019.03.055
Castro-Concha LA, Escobedo RM, Miranda-Ham MDL (2006) Measurement of cell viability in in vitro cultures. Methods Mol Biol 318:71. https://doi.org/10.1385/1-59259-959-1:071
Chen J, Song L, Dai J, Gan N, Liu Z (2004) Effects of microcystins on the growth and the activity of superoxide dismutase and peroxidase of rape (Brassica napus L.) and rice (Oryza sativa L.). Toxicon 43(4):393–400. https://doi.org/10.1016/j.toxicon.2004.01.011
Chen J, Han FX, Wang F, Zhang H, Shi Z (2012) Accumulation and phytotoxicity of microcystin-LR in rice (Oryza sativa). Ecotoxicol Environ Saf 76(none):193–199. https://doi.org/10.1016/j.ecoenv.2011.09.022
Chen G, Zheng Z, Bai M, Li Q (2020) Chronic effects of microcystin-LR at environmental relevant concentrations on photosynthesis of Typha angustifolia Linn. Ecotoxicology 29(8):514–523. https://doi.org/10.1007/s10646-020-02196-2
Corbel S, Mougin C, Bouaiecha N (2014) Cyanobacterial toxins: modes of actions, fate in aquatic and soil ecosystems, phytotoxicity and bioaccumulation in agricultural crops—a review. Chemosphere 96(feb.):1–15. https://doi.org/10.1016/j.chemosphere.2013.07.056
Cordeiro-Araújo MK, Chia MA, Arruda-Neto JDT, Tornisielo VL, Vilca FZ, Bittencourt-Oliveira MC (2016) Microcystin-LR bioaccumulation and depuration kinetics in lettuce and arugula: human health risk assessment. Sci Total Environ 566-567:1379–1386. https://doi.org/10.1016/j.scitotenv.2016.05.204
Corinne R, Sophie M, Hennion MC (1998) Determination of some physicochemical parameters of microcystins (cyanobacterial toxins) and trace level analysis in environmental samples using liquid chromatography. J Chromatogr A 799(1-2):155–169. https://doi.org/10.1016/S0021-9673(97)01095-9
Crush JR, Briggs LR, Sprosen JM, Nichols SN (2010) Effect of irrigation with lake water containing microcystins on microcystin content and growth of ryegrass, clover, rape, and lettuce. Environ Toxicol 23(2):246–252. https://doi.org/10.1002/tox.20331
Deng T, Yin H, Ye J, Peng H, Liu Z (2016) Response of Pseudomonas putida cells to MC-LR stress. China Environ Sci 36(02):603–609. https://doi.org/10.3969/j.issn.1000-6923.2016.02.041
Enayati AA, Ranson H, Hemingway J (2005) Insect glutathione transferases and insecticide resistance. Insect Mol Biol 14:3–8. https://doi.org/10.1111/j.1365-2583.2004.00529.x
Fan Y, Jiang W, Liu B, Chang W, Wu S (2018) Temporal microcystin dynamics of the source water and finished water in a waterworks of Lake Taihu. J Lake Sci 30(1):25–33. https://doi.org/10.18307/2018.0103
Feng Y, Wang L (2007) Effect of different irrigation modes on rice yield. Heilongjiang Agric Sci 2007(06):23–24+36. https://doi.org/10.3969/j.issn.1002-2767.2007.06.009
Feng K, Zheng Q, Yu J, Cheng Y, Ye Q, Ruan M, Wang R, Li Z, Yao Z, Yang Y, Wei J, Zhou G, Wang H (2017) The characteristics of superoxide dismutase (SOD) in evolutions and its research in plant resistance. Molec Plant Breed 15(11):4498–4505. https://doi.org/10.13271/j.mpb.015.004498
Freitas M, Azevedo J, Pinto E, Neves J, Campos A, Vasconcelos V (2015) Effects of microcystin-LR, cylindrospermopsin and a microcystin-LR/cylindrospermopsin mixture on growth, oxidative stress and mineral content in lettuce plants (Lactuca sativa L.). Ecotoxicol Environ Saf 116:59–67. https://doi.org/10.1016/j.ecoenv.2015.02.002
Gehringer MM, Kewada V, Coates N, Downing TG (2003) The use of Lepidium sativum in a plant bioassay system for the detection of microcystin-LR. Toxicon 41(7). https://doi.org/10.1016/S0041-0101(03)00049-7
Grace MH, Yousef GG, Gustafson SJ, Truong VD, Yencho GC, Lila MA (2014) Phytochemical changes in phenolics, anthocyanins, ascorbic acid, and carotenoids associated with sweet potato storage and impacts on bioactive properties. Food Chem 145(feb.15):717–724. https://doi.org/10.1016/j.foodchem.2013.08.107
Guzmán-Guillén R, Campos A, Machado J, Freitas M, Azevedo J, Pinto E, Almeida A, Cameán AM, Vasconcelos V (2017) Effects of Chrysosporum (Aphanizomenon) ovalisporum extracts containing cylindrospermopsin on growth, photosynthetic capacity, and mineral content of carrots (Daucus carota). Ecotoxicology 26:22–31. https://doi.org/10.1007/s10646-016-1737-4
Hu Z, Liu Y, Li D, Alain D (2005) Growth and antioxidant system of the cyanobacterium Synechococcus elongatus in response to microcystin-RR. Hydrobiologia 534(1-3):23–29. https://doi.org/10.1007/s10750-004-1319-y
Jiang J (2015) Rice plant response to longterm microcystinLR exposure: gene expression profiling. Toxicol Lett 238(2):S83. https://doi.org/10.1016/j.toxlet.2015.08.280
Jiang J, Gu X, Song R, Wang X, Yang L (2011a) Microcystin-LR induced oxidative stress and ultrastructural alterations in mesophyll cells of submerged macrophyte Vallisneria natans (Lour.) Hara. J Hazard Mater 190(1):188–196. https://doi.org/10.1016/j.jhazmat.2011.03.023
Jiang J, Song R, Ren J, Wang X, Yang L (2011b) Advances in pollution of cyanobacterial blooms-producing microcystins and their ecotoxicological effects on aquatic organisms. Progr Chem 23(1):246–253. https://doi.org/10.1691/ph.2011.0254
Jiang J, Shan Z, Xu W, Wang X, Zhou J, Kong D, Xu J (2013) Microcystin-LR induced reactive oxygen species mediate cytoskeletal disruption and apoptosis of hepatocytes in Cyprinus carpio L. PLoS One 8(12):e84768. https://doi.org/10.1371/journal.pone.0084768
** H, Chang Z (2013) The pollution way of microcystins and their bioaccumulation in terrestrial plants: a review. Acta Ecol Sin 33(11):3298–3310. https://doi.org/10.5846/stxb201203160356
Kondo F, Matsumoto H, Yamada S, Ishikawa N, Harada KI (1996) Detection and identification of metabolites of microcystins formed in vivo in mouse and rat livers. Chem Res Toxicol 9(8):1355–1359. https://doi.org/10.1021/tx960085a
Lahti K, Rapala J, Färdig M, Niemelä M, Sivonen K, Fardig M, Niemela M (1997) Persistence of cyanobacterial hepatotoxin, microcystin-LR in particulate material and dissolved in lake water. Water Res 31(5):1005–1012. https://doi.org/10.1016/S0043-1354(96)00353-3
Li X, Song L, Liu Y (1999) The production, detection and toxicology of microcystins. Acta Hydrobiol Sin 05:123–129
Li J, Ding Y, **ang R, Song L (2010) Programmed cell death in phytoplankton. Ecol Environ Sci 19(11):2743–2748. https://doi.org/10.16258/j.cnki.1674-5906.2010.11.016
Li W, Chen J, **e P, He J, Guo X, Tuo X, Zhang W, Wu L (2014) Rapid conversion and reversible conjugation of glutathione detoxification of microcystins in bighead carp (Aristichthys nobilis). Aquat Toxicol 147:18–25. https://doi.org/10.1016/j.aquatox.2013.12.001
Li Y, Zhang JW, Wei J, Zhao W (2015) Advances in mechanism of the occurrence, hazard, and prevention/control utilization of cyanophytic blooms in China. J Microbiol 35(04):93–97. https://doi.org/10.3969/j.issn.1005-7021.2015.04.016
Li L, Cai J, Zhao Z, Sun X (2017) Study on the extraction and purification of 3 isomers of microcystins. J Anhui Agric Sci 45(15):51–53. https://doi.org/10.13989/j.cnki.0517-6611.2017.15.018
Li Q, Gu P, Zhang C, Luo X, Zhang H, Zheng Z (2020) Combined toxic effects of anatoxin-A and microcystin-LR on submerged macrophytes and biofilms. J Hazard Mater 389:122053. https://doi.org/10.1016/j.jhazmat.2020.122053
Lins RPM, Barbosa LG, Minillo A, De Ceballos BSO (2016) Cyanobacteria in a eutrophicated reservoir in a semi-arid region in Brazil: dominance and microcystin events of blooms. Braz J Bot 39(2):583–591. https://doi.org/10.1007/s40415-016-0267-x
Maadane A, Merghoub N, Ainane T, El Arroussi H, Benhima R, Amzazi S, Bakri Y, Wahby I (2015) Antioxidant activity of some moroccan marine microalgae: pufa profiles, carotenoids and phenolic content. J Biotechnol 215:13–19. https://doi.org/10.1016/j.jbiotec.2015.06.400
Machado J, Azevedo J, Freitas M, Pinto E, Almeida A, Vasconcelos V, Campos A (2016) Analysis of the use of microcystin-contaminated water in the growth and nutritional quality of the root-vegetable, Daucus carota. Environ Sci Pollut Res 24(1):752–764. https://doi.org/10.1007/s11356-016-7822-7
MacKintosh C, Beattie KA, Klumpp S, Cohen P, Codd GA (1990) Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants. FEBS Lett 264(2):187–192. https://doi.org/10.1016/0014-5793(90)80245-E
Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, nadph turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52(4):561–591. https://doi.org/10.1134/S1028334X0901036X
Mumby MC, Walter G (1993) Protein serine/threonine phosphatases: structure, regulation, and functions in cell growth. Physiol Rev 73(4):673–699. https://doi.org/10.1152/physrev.1993.73.4.673
Pflugmacher S (2004) Promotion of oxidative stress in the aquatic macrophyte Ceratophyllum demersum during biotransformation of the cyanobacterial toxin microcystin-LR. Aquat Toxicol 70(3):178. https://doi.org/10.1016/j.aquatox.2004.06.010
Pinho GLL, Rosa CMD, Maciel FE, Bianchini A, Yunes JS, Proenca LAO, Monserrat JM (2005) Antioxidant responses and oxidative stress after microcystin exposure in the hepatopancreas of an estuarine crab species. Ecotoxicol Environ Saf 61(3):353–360. https://doi.org/10.1016/j.ecoenv.2004.11.014
Prieto A, Campos A, Cameán A, Vasconcelos V (2011) Effects on growth and oxidative stress status of rice plants (Oryza sativa) exposed to two extracts of toxin producing cyanobacteria (Aphanizomenon ovalisporum and Microcystis aeruginosa). Ecotoxicol Environ Saf 74(7). https://doi.org/10.1016/j.ecoenv.2011.06.009
Qin B, Yang G, Ma J, Deng J, Li M (2016) Dynamics of variability and mechanism of harmful cyanobacteria bloom in Lake Taihu, China. Chin Sci Bull 61(7):759–770. https://doi.org/10.1360/N972015-00400
Romero-Oliva CS, Contardo-Jara V, Pflugmacher S (2015) Antioxidative response of the three macrophytes Ceratophyllum demersum, Egeria densa, and Hydrilla verticillata to a time dependent exposure of cell-free crude extracts containing three microcystins from cyanobacterial blooms of Lake Amatitlán, Guatemala. Aquat Toxicol 163:130–139. https://doi.org/10.1016/j.aquatox.2015.04.001
Shu X, **e L, Wan X, Yao L, Xue Q, Li J (2019) Vertical distribution characteristics of microcystin concentration in water and sediment of Meiliang Bay, Lake Taihu. J Lake Sci 31(4):976–987. https://doi.org/10.18307/2019.0426
Takenaka S (2001) Covalent glutathione conjugation to cyanobacterial hepatotoxin microcystin-LR by f344 rat cytosolic and microsomal glutathione S-transferases. Environ Toxicol Pharmacol 9(4):139. https://doi.org/10.1016/S1382-6689(00)00049-1
Wan X, Tai Y, Wang R, Man Y, Yang Y, He W, Yang Y, Wang J (2017) Distribution patterns of microcystins-producing Microcystis and microcystin-LR during blooms in drinking water source areas of Lake Erhai. Acta Sci Circumst 37(6):2040–2047. https://doi.org/10.13671/j.hjkxxb.2017.0037
Wang M, Li X (2009) Advances in cell suspension culture of rice. Molec Plant Breed 7(06):1200–1206. https://doi.org/10.3969/mpb.007.001200
Wang N, Wang C (2018) Effects of microcystin-LR on the tissue growth and physiological responses of the aquatic plant Iris pseudacorus L. Aquat Toxicol:197–205. https://doi.org/10.1016/j.aquatox.2018.04.019
Wang X, Huang D, Wu Q, Cheng G, Yuan Z (2015a) Oxidative stress induced by mycotoxins and its toxicological significance. Asian J Ecotoxicol 10(06):62–70. https://doi.org/10.7524/AJE.1673-5897.20141126001
Wang Y, Zhu W, Wang W, Liang C (2015b) Effects of microcystins on growth and chlorophyll fluorescence in rice seedlings. Acta Sci Circumst 35(02):602–607. https://doi.org/10.13671/j.hjkxxb.2014.0749
Wang Y, Li Y, Feng Y, Zhang E, **a X, Liu L (2017) Research progress on cyanobacterial toxins and the cyanotoxin synthetase gene. Chin J Ecol 36(2):517–523. https://doi.org/10.13292/j.1000-4890.201702.008
Wang L, Wen M, Chen F, Luo Z, Yin J, Chen Y, Huang H (2020) High oxygen atmospheric packaging (HOAP) reduces H2O2 production by regulating the accumulation of oxidative stress-related proteins in Chinese flowering cabbage. Postharvest Biol Technol 165:111183. https://doi.org/10.1016/j.postharvbio.2020.111183
Wei D, Su J, Chen X, Ji D, Wang J, Huo S, Wu C (2014) Distribution of microcystins and its relationship with eutrophication factors in Yangcheng Lake and Gehu Lake. Chin J Environ Eng 8(6):2322–2328
Wiegand C, Pflugmacher S (2005) Ecotoxicological effects of selected cyanobacterial secondary metabolites a short review. Toxicol Appl Pharmacol 203(3):201–218. https://doi.org/10.1016/j.taap.2004.11.002
Wu T, Qin B, Ma J, Yang Z, Yang G (2019) Movement of cyanobacterial colonies in a large, shallow and eutrophic lake: a review. Chin Sci Bull 64(36):3833–3843. https://doi.org/10.1360/TB-2019-0033
Yin D, Hu B (2006) Establishment and cryopreservation of rice suspension cells line. J Northeast Agric Univ 06:750–754. https://doi.org/10.1016/S1872-2040(06)60047-9
Yin L, Huang J, Shen Q, Li Q, Liu Y, Liu Y (2005a) Responses of antioxidant systems in tobacco BY-2 suspension cells to the toxicity of microcystin-RR. China Environ Sci 25(5):576–580. https://doi.org/10.3321/j.issn:1000-6923.2005.05.016
Yin L, Huang J, Huang W, Li D, Liu Y (2005b) Responses of antioxidant system in Arabidopsis thaliana suspension cells to the toxicity of microcystin-RR. Toxicon 46(8):859–864. https://doi.org/10.1016/j.toxicon.2004.12.025
Yu L, Zhu G, Kong F, Li S, Shi X, Zhang M, Yang Z, Xu H, Zhu M (2019) Spatiotemporal characteristics of microcystin variants composition and associations with environmental parameters in Lake Chaohu, China. J Lake Sci 31(3):700–713. https://doi.org/10.18307/2019.0309
Zhang M, Jiang J, Zhou J, Shan Z, Bu Y, Xu W (2014) Effects of microcystin-LR at environmental relevant concentrations on growth and antioxidant enzymes of Oryza sativa L. at vegetative stage. J Agro-Environ Sci 33(12):2296–2302. https://doi.org/10.11654/jaes.2014.12.003
Zhang H, Jiang J, Zhang Y, Shan Z (2017) Physiological and bio-chemical effects of pure MC-LR and Microcystis aeruginosa crude extracts on Oryza sativa L. at vegetative stage. China Environ Sci 37(8):3134–3141. https://doi.org/10.3969/j.issn.1000-6923.2017.08.039
Zhou Q, He A, Yang W, Zhang J, Wang Z, Chen J (2018) Determination of microcystins in water by ultra-high-performance liquid chromatography quadrupole-Orbitrap mass spectrometry. J Environ Health 35(6):524–527. https://doi.org/10.16241/j.cnki.1001-5914.2018.06.014
Zhu G, Ma Y, Huo Z, Guo X, Deng R, Wang H, Wei X (2014) The activities of protective enzymes and product of membrane lipid peroxidation of Ziziphus jujuba Mill. responsed to drought stress. Chin Wild Plant Resour 33(03):5–10. https://doi.org/10.3969/j.issn.1006-9690.2014.03.002
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This work was financially supported by the National Key Research and Development Program of China (2017YFD0801500) and the National Natural Science Foundation of China (21407056).
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**lin Jiang contributed to the study conception and design. Material preparation and data collection were performed by **ngcheng Zhu and Renbin Liu. Analysis was performed by Tao Long, Huanchao Zhang, and Shaopo Deng. Shihui Chen and **lin Jiang wrote the manuscript. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Chen, S., Jiang, J., Long, T. et al. Oxidative stress induced in rice suspension cells exposed to microcystin-LR at environmentally relevant concentrations. Environ Sci Pollut Res 28, 38393–38405 (2021). https://doi.org/10.1007/s11356-021-13353-3
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DOI: https://doi.org/10.1007/s11356-021-13353-3