Abstract
There has been little agreement regarding the mechanism by which proline reduces heavy metal stress. The present work examines the relationship between Hg2+-induced oxidative stress and proline accumulation in rice and explores the possible mechanisms through which proline protects against Hg2+ stress. The effect of proline on alleviation of Hg2+ toxicity was studied by spectrophotography and enzymatic methods. Hg2+ induced oxidative stress in rice by increasing lipid peroxidation. Pretreatment of the rice with 2 mM proline for 12 h profoundly alleviated Hg2+-induced lipid peroxidation and minimized H2O2 accumulation. Proline pretreatment significantly reduced (p < 0.01) the Hg2+ content in rice leaves. A comparison of the effects of proline pretreatment on H2O2 accumulation by Hg2+ and aminotrazole suggested that proline protected cells from Hg2+-induced oxidative stress by scavenging reactive oxygen species. The present work demonstrates a protective effect of proline on Hg2+ toxicity through detoxifying reactive oxygen species, rather than chelating metal ions or maintaining the water balance under Hg2+ stress.
Similar content being viewed by others
Abbreviations
- AT:
-
Aminotriazole
- GSH:
-
Glutathione
- GSSG:
-
Oxidative glutathione
- MDA:
-
Malonaldehyde
- ROS:
-
Reactive oxygen species
- TBA:
-
2-Thiobarbituric acid
References
Alia MP, Matysik J (2001) Effect of proline on the production of singlet oxygen. Amino Acids 21:195–200. doi:10.1007/s007260170026
Arnon DI (1949) Copper enzymes in isolated chloroplast: polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15
Backor M, Fahselt D, Wu CT (2004) Free proline content is positively correlated with copper tolerance of the lichen photobiont Trebouxia erici (Chlorophyta). Plant Sci 167:151–157. doi:10.1016/j.plantsci.2004.03.012
Bates LS, Waldren RP, Tear ID (1975) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207. doi:10.1007/BF00018060
Briat JF (2002) Metal ion-activated oxidative stress and its control. Taylor and Francis, New York, pp 171–179
Cabrera F, Clemente L, Diaz BE, Lopez R, Murillo JM (1999) Heavy metal pollution of soils affected by the Guadiamar toxic flood. Sci Total Environ 242:117–129. doi:10.1016/S0048-9697(99)00379-4
Carrier P, Baryla A, Havaux M (2003) Cadmium distribution and microlocalization in oilseed rape (Brassica napus) after long-term growth on cadmium-contaminated soil. Planta 216:939–950
Chai T, Didierjean L, Burkard G, Genot G (1998) Expression of a green tissue-specific 11 kDa proline-rich protein gene in bean in response to heavy metals. Plant Sci 133:47–56. doi:10.1016/S0168-9452(98)00028-4
Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719. doi:10.1016/j.biochi.2006.07.003
Cobbett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123:825–832. doi:10.1104/pp.123.3.825
Colmer TD, Fan TWM, Läuchli A, Higashi RM (1996) Interactive effects of salinity, nitrogen and sulphur on the organic solutes in Spartina alterniflora leaf blades. J Exp Bot 47:369–375. doi:10.1093/jxb/47.3.369
Dietz KJ, Baier M, Kramer U (1999) Free radicals and reactive oxygen species as mediators of heavy metal toxicity in plants. In: Hagemeyer J (ed) Prasad MNY. Springer-Verlag, Berlin, pp 73–97
Farago ME, Mullen WA (1979) Plants which accumulate metals. Part IV. A possible copper-proline complex from the roots of Armeria maritime. Inorg Chim Acta 32:93–94. doi:10.1016/S0020-1693(00)91627-X
Girousse C, Bournoville R, Bonnemain JL (1996) Water deficit-induced changes in concentrations in proline and some other amino acids in the phloem sap of alfalfa. Plant Physiol 111:109–113
Grill E, Loffler S, Winnacker EL, Zenk MH (1989) Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific γ-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc Natl Acad Sci 86:6838–6842. doi:10.1073/pnas.86.18.6838
Halliwell B, Gutteridge JMC (1989) Protection against oxdiants in biological systems: the super oxide theory of oxygen toxicity. In: Halliwell B, Gutteridge JMC (eds) Free Radicals in Biology and Medicine. Clarendon Press, Oxford, pp 86–123
Jana S, Choudhuri MA (1981) Glycolate metabolism of three submerged aquatic angiosperms during aging. Aquat Bot 12:345–354. doi:10.1016/0304-3770(82)90026-2
Lin YH, Guo MX, Gan WM (2006) Mercury pollution from small gold mines in China. Water, Air Soil Poll 9:233–239. doi:10.1023/A:1018384822608
Li ZG, Du CK, Gong M (2003) Simultaneous measurement of ASA/DHA and GSH/GSSG using a single extraction system. J Yunnan Normal Univ (Natural Sci) 23:67–70
Lutts S, Kinet JM, Bouharmont J (1996) Effects of various salts and of mannitol on ion and proline accumulation in relation to osmotic adjustment in rice (Oryza sativa L.) callus cultures. J Plant Physiol 149:186–195
Mansour MMF (1998) Protection of plasma membrane of onion epidermal cells by glycinebetaine and proline against NaCl stress. Plant physiol Biochem 36:767–772. doi:10.1016/S0981-9428(98)80028-4
Matysik JA, Bhalu B, Mohanty P (2002) Molecular mechanism of quenching of reactive oxygen species by proline under stress in plants. Curr Sci 82:525–532
May MJ, Vernoux T, Leaver C, Montagu MV, Inzé D (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49:649–667. doi:10.1093/jexbot/49.321.649
Mehta SK, Gaur JP (1999) Heavy metal-induced proline accumulation and its role in ameliorating metal toxicity in Chlorella vulgaris. New Phytol 143:253–259. doi:10.1046/j.1469-8137.1999.00447.x
Michaeli A, Feitelson J (1994) Reactivity of singlet oxygen toward amino acids and peptides. Photochem Photobiol 59:284–289. doi:10.1111/j.1751-1097.1994.tb05035.x
Molinari HBC, Marur CJ, Daros E, Campos MKF, Carvalho JFRP, Filh JCB, Pereira LFP, Vieira LGE (2007) Evaluation of the stress-inducible production of proline in transgenic sugarcane (Saccharum spp.): osmotic adjustment chlorophyll fluorescence and oxidative stress. Physiol Planta 130:218–229. doi:10.1111/j.1399-3054.2007.00909.x
Patra M, Sharma A (2000) Mercury toxicity in plants. Bot Rev 66:379–422. doi:10.1007/BF02868923
Rubén RÁ, Cristina OV, Ana ÁF, Francisca FC, Luis EH (2006) Stress responses of zea mays to cadmium and mercury. Plant Soil 279:41–50. doi:10.1007/s11104-005-3900-1
Sandalio LM, Dalurzo HC, Gomez M, Romero-Puertas MC, Ril LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126
Sanita TL, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130. doi:10.1016/S0098-8472(98)00058-6
Schat H, Sharma SS, Vooijs R (1997) Heavy metal-induced accumulation of free proline in a metal-tolerant and a nontolerant ecotype of Silene vulgaris. Plant Physiol 101:477–482. doi:10.1111/j.1399-3054.1997.tb01026.x
Shah K, Dubey RS (1998) Effect of cadmium on proline accumulation and ribonuclease activity in rice seedlings: role of proline as a possible enzyme protectant. Biol Plantarum 40:121–130. doi:10.1023/A:100095680391
Shakya K, Chettri MK, Sawidis T (2008) Impact of heavy metals (Copper, Zinc, and Lead) on the chlorophyll content of some Mosses. Arch Environ Contam Toxicol 54:412–421. doi:10.1007/s00244-007-9060-y
Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726. doi:10.1093/jxb/erj073
Sharma SS, Schat H, Vooijs R (1998) In vitro alleviation of heavy metal-induced enzyme inhibition by praline. Phytochem 49:1531–1535. doi:10.1016/S0031-9422(98)00282-9
Siripornadulsil S, Train S, Verma DPS, Sayre RT (2002) Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14:2837–2847. doi:10.1105/tpc.004853
Tang QY, Feng MG (2002) DPS data processing system for practical statistics. Science Press, Beijing
Tatar O, Gevrek MN (2008) Influence of water stress on proline accumulation, lipid peroxidation and water content of wheat. Asian J Plant Sci 1682–3974
Tripathi BN, Gaur JP (2004) Relationship between copper- and zinc-induced oxidative stress and proline accumulation in Scenedesmus sp. Planta 219:397–404. doi:10.1007/s00425-004-1237-2
Van AF, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Physiol 34:165–168
Vangronsveld J, Clijsters H (1994) Toxic effects of metals. VCH Verlagsgesellschaft, Weinheim, pp 50–177
Wang AG, Luo GH (1990) Quantitative relation between the reaction of hydroxylamine and superoxide anion radicals in plants. Plant Physiol Commu 6:55–57 (in Chinese with English abstract)
Wu JT, Hsieh MT, Kow LC (1998) Role of proline accumulation in response to toxic copper in Chlorella sp., (Chlorophyceae) cells. J Phycol 34:113–117. doi:10.1046/j.1529-8817.1998.340113.x
Xu QS, Shi GX, Gu GP (2000) Study of toxic effect of Hg2+ on Nymphaea tetragona Georgi. Acta Bot Boreal Occident Sin 20:784–789 (in Chinese with English abstract)
Zeng B, Wang FJ, Zhu C, Sun ZX (2008) Effect of AsA-GSH cycle on Hg2+-Tolerance in rice mutant. Acta Agron Sin 34:823–830
Zengin FK, Munzuroglu O (2005) Effect of some heavy metals on content of chlorophyll, proline and some antioxidant chemicals in bean seedling. Acta Biol Cracov 47:157–164
Zhao SJ, Xu CC, Zhou Q, Meng QW (1994) Improvements of method for measurement of malondialdehyde in plant tissues. Plant Physiol Commun 30:207–210
Acknowledgments
This work was supported by the National Key Technologies R&D Program of China during the 11th Five-Year Plan Period (NO. 2006BAK02A18), the Natural Science Foundation of Zhejiang Province (NO. Z306300), and the National Key Basic Research and Development Program (NO. 2002CB410804).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wang, F., Zeng, B., Sun, Z. et al. Relationship Between Proline and Hg2+-Induced Oxidative Stress in a Tolerant Rice Mutant. Arch Environ Contam Toxicol 56, 723–731 (2009). https://doi.org/10.1007/s00244-008-9226-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00244-008-9226-2