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Response and recovery of rice (Oryza sativa) seedlings to irrigation with microcystin-contaminated water

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Abstract

Irrigation with microcystin-contaminated water threatens plant growth and human health. We studied the accumulation of microcystins, growth, and photosynthesis in rice exposed to different concentrations microcystins (0, 1, 100, 1,000, and 3,000 μg L−1) for 7 days and then without microcystins for 7 days. After a 7-day exposure, the accumulation of microcystins in roots was the highest. High concentration microcystins (≥100 μg L−1) inhibited growth, and decreased photosynthetic rate and chlorophyll content. The decrease was positively correlated with microcystins concentrations. After a 7-day restoration, the accumulation of microcystins in organs was lower than that during the exposure period. The dry weight of roots and leaves in rice seedlings treated with 100 μg L−1 was not significantly different from those of the control, although photosynthetic rate and chlorophyll content in rice seedlings treated with 100 μg L−1 were still lower than those of the control. However, growth and photosynthesis in rice seedlings treated with 1,000 or 3,000 μg L−1 microcystins were still lower than those of the control, even worse than those during the exposure period, indicating an irreversible inhibition of microcystins to plants at high concentrations of microcystins. Our results imply that irrigation with microcystin-contaminated water must be monitored and controlled to avoid harmful accumulation of microcystins and damage to plant growth.

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References

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1

    Article  Google Scholar 

  • Calabrese EJ (2002) Hormesis: changing view of the dose-response, a personal account of the history and current status. Mutat Res/Rev Mutat Res 511:181–189

    Article  Google Scholar 

  • Cazenave J, Wunderlin DA, Bistoni MdlÁ, Amé MV, Krause E, Pflugmacher S, Wiegand C (2005) Uptake, tissue distribution and accumulation of microcystin-RR in Corydoras paleatus, Jenynsia multidentata and Odontesthes bonariensis: a field and laboratory study. Aquat Toxicol 75:178–190

    Article  Google Scholar 

  • Chen J, Dai J, Zhang H, Wang C, Zhou G, Han Z, Liu Z (2010) Bioaccumulation of microcystin and its oxidative stress in the apple (Malus pumila). Ecotoxicology 19:796–803

    Article  Google Scholar 

  • 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 43:393–400

    Article  Google Scholar 

  • Chen J, Ye J, Zhang H, Jiang X, Zhang Y, Liu Z (2011) Freshwater toxic cyanobacteria induced DNA damage in apple (Malus pumila), rape (Brassica napus) and rice (Oryza sativa). J Hazard Mater 190:240–244

    Article  Google Scholar 

  • Chia TF, He J (1999) Photosynthetic capacity in oncidium (Orchidaceae) plants after virus eradication. Environ Exp Bot 42:11–16

    Article  Google Scholar 

  • Codd GA, Metcalf JS, Beattie KA (1999) Retention of Microcystis aeruginosa and microcystin by salad lettuce (Lactuca sativa) after spray irrigation with water containing cyanobacteria. Toxicon 37:1181–1185

    Article  Google Scholar 

  • Codd GA, Morrison LF, Metcalf JS (2005) Cyanobacterial toxins: risk management for health protection. Toxicol Appl Pharmacol 203:264–272

    Article  Google Scholar 

  • Corbel S, Mougin C, Bouaïcha N (2014) Cyanobacterial toxins: Modes of actions, fate in aquatic and soil ecosystems, phytotoxicity and bioaccumulation in agricultural crops. Chemosphere 96:1–15

    Article  Google Scholar 

  • Crush J, Briggs L, Sprosen J, Nichols S (2008) Effect of irrigation with lake water containing microcystins on microcystin content and growth of ryegrass, clover, rape, and lettuce. Environ Toxicol 23:246–252

    Article  Google Scholar 

  • Duong TT, Jähnichen S, Le TPQ, Ho CT, Hoang TK, Nguyen TK, Vu TN, Dang DK (2014) The occurrence of cyanobacteria and microcystins in the Hoan Kiem Lake and the Nui Coc reservoir (North Vietnam). Environ Earth Sci 71:2419–2427

    Article  Google Scholar 

  • Funari E, Testai E (2008) Human health risk assessment related to cyanotoxins exposure. Crit Rev Toxicol 38:97–125

    Article  Google Scholar 

  • 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 41:871–876

    Article  Google Scholar 

  • Gutiérrez-Praena D, Campos A, Azevedo J, Neves J, Freitas M, Guzmán-Guillén R, Cameán AM, Renaut J, Vasconcelos V (2014) Exposure of Lycopersicon Esculentum to microcystin-LR: Effects in the leaf proteome and toxin translocation from water to leaves and fruits. Toxins 6:1837–1854

    Article  Google Scholar 

  • Hallmann C, Wedekind W, Hause-Reitner D, Hoppert M (2013) Cryptogam covers on sepulchral monuments and re-colonization of a marble surface after cleaning. Environ Earth Sci 69:1149–1160

    Article  Google Scholar 

  • Hiscox J, Israelstam G (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334

    Article  Google Scholar 

  • Holst T, Jorgensen NO, Jorgensen C, Johansen A (2003) Degradation of microcystin in sediments at oxic and anoxic, denitrifying conditions. Water Res 37:4748–4760

    Article  Google Scholar 

  • Jarvenpaa S, Lundberg-Niinisto C, Spoof L, Sjovall O, Tyystjarvi E, Meriluoto J (2007) Effects of microcystins on broccoli and mustard, and analysis of accumulated toxin by liquid chromatography-mass spectrometry. Toxicon 49:865–874

    Article  Google Scholar 

  • Jiang J, Gu X, Song R, Wang X, Yang L (2011) Microcystin-LR induced oxidative stress and ultrastructural alterations in mesophyll cells of submerged macrophyte Vallisneria natans (Lour.) Hara. J Hazard Mater 190:188–196

    Article  Google Scholar 

  • Jones GJ, Orr PT (1994) Release and degradation of microcystin following algicide treatment of a Microcystis aeruginosa bloom in a recreational lake, as determined by HPLC and protein phosphatase inhibition assay. Water Res 28:871–876

    Article  Google Scholar 

  • Kummerová M, Krulová J, Zezulka ŠZ, Tříska J (2006) Evaluation of fluoranthene phytotoxicity in pea plants by Hill reaction and chlorophyll fluorescence. Chemosphere 65:489–496

    Article  Google Scholar 

  • Lahrouni M, Oufdou K, Faghire M, Peix A, El Khalloufi F, Vasconcelos V, Oudra B (2012) Cyanobacterial extracts containing microcystins affect the growth, nodulation process and nitrogen uptake of faba bean (Vicia faba L., Fabaceae). Ecotoxicology 21:681–687

    Article  Google Scholar 

  • Lahti K, Rapala J, Färdig M, Niemelä M, Sivonen K (1997) Persistence of cyanobacterial hepatotoxin, microcystin-LR in particulate material and dissolved in lake water. Water Res 31:1005–1012

    Article  Google Scholar 

  • Lawton LA, Edwards C, Codd GA (1994) Extraction and high-performance liquid chromatographic method for the determination of microcystins in raw and treated waters. Analyst 119:1525–1530

    Article  Google Scholar 

  • Li H, Rao B, Wang G, Shen S, Li D, Hu C, Liu Y (2014) Spatial heterogeneity of cyanobacteria-inoculated sand dunes significantly influences artificial biological soil crusts in the Hopq Desert (China). Environ Earth Sci 71:245–253

    Article  Google Scholar 

  • Liang CJ, van Dijk JP, Scholtens IMJ, Staats M, Prins TW, Voorhuijzen MM, da Silva AM, Arisi ACM, den Dunnen JT, Kok EJ (2014) Detecting authorized and unauthorized genetically modified organisms containing vip3A by real-time PCR and next-generation sequencing. Anal Bioanal Chem 406:2603–2611

    Article  Google Scholar 

  • Liang CJ, Wang WM (2013) Antioxidant response of soybean seedlings to joint stress of lanthanum and acid rain. Environ Sci Pollut Res 20:8182–8191

    Article  Google Scholar 

  • Liu B, Gong Y, **ao B, Liu J, Liu Y (2008) A laboratory study on risk assessment of microcystin-RR in cropland. J Environ Manage 86:566–574

    Article  Google Scholar 

  • McElhiney J, Lawton LA, Leifert C (2001) Investigations into the inhibitory effects of microcystins on plant growth, and the toxicity of plant tissues following exposure. Toxicon 39:1411–1420

    Article  Google Scholar 

  • Miller M, Critchley M, Hutson J, Fallowfield H (2001) The adsorption of cyanobacterial hepatotoxins from water onto soil during batch experiments. Water Res 35:1461–1468

    Article  Google Scholar 

  • Mohamed ZA, Al Shehri AM (2009) Microcystins in groundwater wells and their accumulation in vegetable plants irrigated with contaminated waters in Saudi Arabia. J Hazard Mater 172:310–315

    Article  Google Scholar 

  • Nimptsch J, Wiegand C, Pflugmacher S (2008) Cyanobacterial toxin elimination via bioaccumulation of MC-LR in aquatic macrophytes: an application of the “Green Liver Concept”. Environ Sci Technol 42:8552–8557

    Article  Google Scholar 

  • Ou H, Gao N, Wei C, Deng Y, Qiao J (2012) Immediate and long-term impacts of potassium permanganate on photosynthetic activity, survival and microcystin-LR release risk of Microcystis aeruginosa. J Hazard Mater 219:267–275

    Article  Google Scholar 

  • Pflugmacher S (2004) Promotion of oxidative stress in the aquatic macrophyte Ceratophyllum demersum during biotransformation of the cyanobacterial toxin microcystin-LR. Aquat Toxicol 70:169–178

    Article  Google Scholar 

  • Pflugmacher S, Hofmann J, Huebner B (2007) Effects on growth and physiological parameters in wheat (Triticum aestivum L.) grown in soil and irrigated with cyanobacterial toxin contaminated water. Environ Toxico Chem 26:2710–2716

    Article  Google Scholar 

  • Pires L, Karlsson K, Meriluoto J, Kardinaal E, Visser P, Siewertsen K, Donk EV, Ibelings B (2004) Assimilation and depuration of microcystin-LR by the zebra mussel, Dreissena polymorpha. Aquat Toxicol 69:385–396

    Article  Google Scholar 

  • Qiu Z, Wang L, Zhou Q (2013) Effects of bisphenol A on growth, photosynthesis and chlorophyll fluorescence in above-ground organs of soybean seedlings. Chemosphere 90(3):1274–1280

    Article  Google Scholar 

  • Saqrane S, El Ghazali I, Oudra B, Bouarab L, Vasconcelos V (2008) Effects of cyanobacteria producing microcystins on seed germination and seedling growth of several agricultural plants. J Environ Sci Health, Part B 43(5):443–451

    Article  Google Scholar 

  • Saqrane S, Ouahid Y, Ghazali EI, Oudra B, Bouarab L, del Campo FF (2009) Physiological changes in Triticum durum, Zea mays, Pisum sativum and Lens esculenta cultivars, caused by irrigation with water contaminated with microcystins: a laboratory experimental approach. Toxicon 53(7):786–796

    Article  Google Scholar 

  • Svrcek C, Smith DW (2004) Cyanobacteria toxins and the current state of knowledge on water treatment options: a review. J Environ Eng Sci 3:155–185

    Article  Google Scholar 

  • Vassilakaki M, Pflugmacher S (2008) Oxidative stress response of Synechocystis sp (PCC 6803) due to exposure to microcystin-LR and cell-free cyanobacterial crude extract containing microcystin-LR. J Appl Phycol 20:219–225

    Article  Google Scholar 

  • Wang Z, **ao B, Song L, Wang C, Zhang J (2012) Responses and toxin bioaccumulation in duckweed (Lemna minor) under microcystin-LR, linear alkybenzene sulfonate and their joint stress. J Hazard Mater 229:137–144

    Article  Google Scholar 

  • WHO (1998) Guidelines for drinking-water quality: health criteria and other supporting information. World Health Organanisation

  • Zhu Y, Di T, Xu G, Chen X, Zeng H, Yan F, Shen Q (2009) Adaptation of plasma membrane H+-ATPase of rice roots to low pH as related to ammonium nutrition. Plant Cell Environ 32:1428–1440

    Article  Google Scholar 

Download references

Acknowledgments

The authors are grateful for the financial support from the National Natural Science Foundation of China (31000245, 31370517), and the assistance of Dr. Hua Zou for collecting fresh cyanobacteria in Taihu Lake.

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Correspondence to Chanjuan Liang.

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Liang, C., Wang, W. Response and recovery of rice (Oryza sativa) seedlings to irrigation with microcystin-contaminated water. Environ Earth Sci 73, 4573–4580 (2015). https://doi.org/10.1007/s12665-014-3746-z

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