Environmental Science and Pollution Research

, Volume 25, Issue 21, pp 21185–21194 | Cite as

Coordinated effects of lead toxicity and nutrient deprivation on growth, oxidative status, and elemental composition of primed and non-primed rice seedlings

  • Fahad Khan
  • Saddam Hussain
  • Mohsin Tanveer
  • Sehrish Khan
  • Hafiz Athar Hussain
  • Biland Iqbal
  • Mingjian Geng
Research Article


Rice crop is highly susceptible to the toxic levels of lead (Pb) during early growth stages. Moreover, a sufficient availability of mineral nutrients is critical for survival of plants particularly under stressful conditions. An experiment was carried out to unravel the coordinated effects of Pb stress (1-mM PbCl2) and different nutrient treatments (sufficient nutrient supply, nitrogen (N) deprivation, phosphorus (P) deprivation, and potassium (K) deprivation) on morphological growth, reactive oxygen species (ROS), antioxidants, and nutrient status in primed and non-primed rice seedlings. Seeding were primed with distilled water, 60-μM selenium, or 100-mg L−1 salicylic acid. Results indicated that Pb toxicity did not affect the root growth, but severely reduced the shoot growth (length and biomass) of rice in N- or P-deprived seedlings. Rice seedlings grown with sufficient supply of nutrients or K-deprivation showed no growth reduction under Pb toxicity. Exposure of Pb stress triggered the production of ROS (H2O2, O2˙, OH) and lipid peroxidation rate particularly under N- or P-deprivation. Moreover, the shoot accumulations of macronutrients (P in particular) were also restricted under Pb toxicity. Seed priming treatments effectively alleviated the undesirable effects of Pb stress on rice growth. The primed rice seedlings showed minimal oxidative damage caused by excessive generation of ROS under Pb stress and/or nutrient deprivation. Seed priming strengthened the antioxidative defense system of rice seedlings by regulating the activities/levels of superoxide dismutase, catalase, peroxidase, and glutathione in rice leaves. Moreover, better accumulation of essential nutrients in primed rice seedlings prevented the excess uptake and translocation of Pb, as evident by the lowered shoot accumulation of Pb.


Antioxidants Lead Nutrient deprivation Reactive oxygen species Rice seedlings Seed priming 


Funding information

We acknowledge the Special Fund for Agro-Scientific Research in the Public Interest of China (Project Nos. 201103005 and 201503122).


  1. Ahmad I, Basra SMA, Hussain S, Hussain SA, Rehman H, Rehman A, Ali A (2015) Priming with ascorbic acid, salicylic acid and hydrogen peroxide improves seedling growth of spring maize at suboptimal temperature. J Environ Agric Sci 3:14–22Google Scholar
  2. Ashraf MY, Azhar N, Ashraf M, Hussain M, Arshad M (2011) Influence of lead on growth and nutrient accumulation in canola (Brassica napus L.) cultivars. J Environ Biol 32(5):659Google Scholar
  3. Ashraf U, Kanu AS, Mo Z, Hussain S, Anjum SA, Khan I, Abbas RN, Tang X (2015) Lead toxicity in rice: effects, mechanisms, and mitigation strategies—a mini review. Environ Sci Pollut Res 22:18318–18332CrossRefGoogle Scholar
  4. Bailly C, Benamar A, Corbineau F, Dome D (1996) Changes in malondialdehyde contents and in superoxide dismutase, catalase, glutathione reductase activities in sunflower seeds related to accelerated seed aging. Physiol Plant 97:104–110CrossRefGoogle Scholar
  5. Cakmak I (2005) The role of potassium in alleviating detrimental effects of abiotic stresses in plants. J Plant Nutr Soil Sci 168:521–530CrossRefGoogle Scholar
  6. Cao Y, Huang R, Jiang W, Cao Z (2004) Effect of heavy metal lead and cadmium on grain quality of maize. J Shenyang Agric Uni 36(2):218–220Google Scholar
  7. Chen W, Guo C, Hussain S, Zhu B, Deng F, Xue Y (2016) Role of xylo-oligosaccharides in protection against salinity-induced adversities in Chinese cabbage. Environ Sci Pollut Res 23:1254–1264. CrossRefGoogle Scholar
  8. Cui W, Li L, Gao Z, Wu H, Xie Y, Shen W (2012) Haem oxygenase-1 is involved in salicylic acid-induced alleviation of oxidative stress due to cadmium stress in Medicago sativa. J Exp Bot 63:695–709CrossRefGoogle Scholar
  9. De Lespinay A, Lequeux H, Lambillotte B, Lutts S (2010) Protein synthesis is differentially required for germination in Poa pratensis and Trifolium repens in the absence or in the presence of cadmium. Plant Growth Regul 61:205–214CrossRefGoogle Scholar
  10. Foyer CH, Noctor G (2005) Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071CrossRefGoogle Scholar
  11. Galhaut L, Lespinay A, Walker DJ, Bernal MP, Correal E, Lutts S (2014) Seed priming of Trifolium repens. Improved germination and early seedling growth on heavy metal-contaminated soil. Water Air Soil Pollut 225(4–1905):15Google Scholar
  12. Gopal R, Rizvi AH (2008) Excess lead alters growth, metabolism and translocation of certain nutrients in radish. Chemosphere 70(9):1539–1544CrossRefGoogle Scholar
  13. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefGoogle Scholar
  14. Gunes A, Inal A, Alpaslan M, Eraslan F, Bagci EG, Cicek N (2007) Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. J Plant Physiol 164:728–736CrossRefGoogle Scholar
  15. Gussarsson M (1994) Cadmium-induced alterations in nutrient composition and growth of Betula pendula seedlings: the significance of fine roots as a primary target for cadmium toxicity. J Plant Nutr 17:2151–2163CrossRefGoogle Scholar
  16. Guo B, Liang YC, Zhu YG, Zhao FJ (2007) Role of salicylic acid in alleviating oxidative damage in rice roots (Oryza sativa L.) subjected to cadmium stress. Environ Pollut 147:743–749CrossRefGoogle Scholar
  17. He PP, Lv XZ, Wang GY (2004) Effects of Se and Zn supplementation on the antagonism against Pb and Cd in vegetables. Environ Int 30:167–172CrossRefGoogle Scholar
  18. Hussain, S., Zheng, M., Khan, F., Khaliq, A., Fahad, S., Peng, S., Huang, J.L., Cui, K., Nie, L. (2015) Benefits of rice seed priming are offset permanently by prolonged storage and the storage conditions. Sci Rep : 5: DOI: 10.1038/srep08101Google Scholar
  19. Hussain S, Khan F, Cao W, Wu L, Geng M (2016b) Seed priming alters the production and detoxification of reactive oxygen intermediates in rice seedlings grown under sub-optimal temperature and nutrient supply. Front Plant Sci 7:439Google Scholar
  20. Hussain, S., Khan, F., Hussain, H.A., Nie, L. (2016a) Physiological and biochemical mechanisms of seed priming-induced chilling tolerance in rice cultivars. Front Plant Sci 7: DOI:
  21. Jisha KC, Vijayakumari K, Puthur JT (2013) Seed priming for abiotic stress tolerance: an overview. Acta Physiol Plant 35:1381–1396CrossRefGoogle Scholar
  22. Kabata-Pendias A, Pendias H (1992) Trace elements in soils and plants, 2nd edn. CRC Press, Boca Raton, LondonGoogle Scholar
  23. Kabata-Pendias, A., Mukherjee, A.B. (2007) Trace elements from soil to human. Springer Science & Business MediaGoogle Scholar
  24. Kopittke PM, Asher CJ, Blamey FPC, Menzies NW (2007) Toxic effects of Pb+2 on the growth and mineral nutrition of signal grass (Brachiaria decumbens) and Rhodes grass (Chloris gayana). Plant Soil 300:127–136CrossRefGoogle Scholar
  25. Kumar M, Bijo AJ, Baghel RS, Reddy CRK, Jha B (2012) Selenium and spermine alleviate cadmium induced toxicity in the red seaweed Gracilaria dura by regulating antioxidants and DNA methylation. Plant Physiol Biochem 51:129–138Google Scholar
  26. Larbi A, Morales F, Abadía A, Gogorcena Y, Lucena JJ, Abadía J (2002) Effects of Cd and Pb in sugar beet plants grown in nutrient solution: induced Fe deficiency and growth inhibition. Funct Plant Biol 29:1453–1464CrossRefGoogle Scholar
  27. Liu D, Jiang W, Gao X (2003) Effect of cadmium on root growth, cell division and nucleoli in root tip cells of garlic. Biol Plant 47:79–83CrossRefGoogle Scholar
  28. Liu H, Hussain S, Zheng M, Peng S, Huang J, Cui K, Nie L (2015) Dry direct-seeded rice as an alternative to transplanted-flooded rice in central China. Agron Sustain Dev 35:285–294CrossRefGoogle Scholar
  29. Marschner H (1995) Mineral nutrition of high plants, 2nd edn. London Acad. Press, London, p 889Google Scholar
  30. Martin, S.A., Emilio, R., Mahara, V. (2011) Role of oxidative stress in transformation induced by metal mixture. Oxidative Med Cell Longev 935–160Google Scholar
  31. Haussling M, Jorns CA, Lehmbecker G, Hecht-Bucholz, Marschner H (1998) Ion and water uptake in relation to root development of Norway spruce (Picea abies (L.) Karst). J Plant Physiol 133:486–491CrossRefGoogle Scholar
  32. Mengel K, Kirkby EA (2001) Principles of plant nutrition, 5th edn. Kluwer Academic Publishers, DordrechtCrossRefGoogle Scholar
  33. Noriega G, Caggiano E, Lecube ML, Cruz DS, Batlle A, Tomaro M, Balestrasse KB (2012) The role of salicylic acid in the prevention of oxidative stress elicited by cadmium in soybean plants. Biometals 25:1155–1165CrossRefGoogle Scholar
  34. Panda SK, Choudhary S (2005) Chromium stress in plants. Braz J Plant Physiol 17:19–102Google Scholar
  35. Patterson BD, MacRae EA, Ferguson IB (1984) Estimation of hydrogen peroxide in plant extracts using titanium (IV). Anal Biochem 139:487–492Google Scholar
  36. Schmelz EA, Alborn HT, Engelberth J, Tumlinson JH (2003) Nitrogen deficiency increases volicitin-induced volatile emission, jasmonic acid accumulation, and ethylene sensitivity in maize. Plant Physiol 133:295–306CrossRefGoogle Scholar
  37. Shah Z, Haq IU, Rehman A, Khan A, Afzal M (2013) Soil amendments and seed priming influence nutrients uptake, soil properties, yield and yield components of wheat (Triticum aestivum L.) in alkali soils. Soil Sci Plant Nutr 59:262–270CrossRefGoogle Scholar
  38. Shah H, Jalwat T, Arif M, Miraj G (2012) Seed priming improves early seedling growth and nutrient uptake in mungbean. J Plant Nutr 35:805–816CrossRefGoogle Scholar
  39. Sharma P, Dubey RS (2005) Pb toxicity in plants. Braz J Plant Physiol 17(1):35–52CrossRefGoogle Scholar
  40. Shin R, Berg RH, Schachtman DP (2005) Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant Cell Physiol 46:1350–1357CrossRefGoogle Scholar
  41. Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655CrossRefGoogle Scholar
  42. Walch P, Neumann G, Bangerth F, Engels C (2000) Rapid effects of nitrogen form on leaf morphogenesis in tobacco. J Exp Bot 51(343):227–237CrossRefGoogle Scholar
  43. Williamson LC, Ribrioux SPCP, Fitter AH, Leyser HMO (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–890CrossRefGoogle Scholar
  44. Xin P, Donghong W, An P (2001) Effect of lead stress on the activity of antioxidant enzymes in wheat seedling. Ch J Environ Sci 5:025Google Scholar
  45. Xiong Z, Zhao F, Li M (2006) Lead toxicity in Brassica pekinensis Rupr.: effect on nitrate assimilation and growth. Environ Toxicol 21(2):147–153CrossRefGoogle Scholar
  46. Xiong F, Yu X, Zhou L, Wang Z (2013) Effect of nitrogen application at the booting stage on wheat progeny seed germination and seedling growth. J Plant Stud 2(2):158CrossRefGoogle Scholar
  47. Yang QW, Shu WS, Qiu JW, Wang HB, Lan CY (2004) Lead in paddy soils and rice plants and its potential health risk around Lechang lead/zinc mine, Guangdong, China. Environ Int 30:883–889CrossRefGoogle Scholar
  48. Yang Y, Wei X, Lu J, You J, Wang W, Shi R (2010) Lead-induced phytotoxicity mechanism involved in seed germination and seedling growth of wheat (Triticum aestivum L.). Ecotoxicol Environ Saf 73:1982–1987CrossRefGoogle Scholar
  49. Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of rice. IRRI, Los Banos, Laguna, p 83Google Scholar
  50. Zacchini M, Rea E, Tullio M, de Agazio M (2003) Increased antioxidative capacity in maize calli during and after oxidative stress induced by a long lead treatment. Plant Physiol Biochem 41(1):49–54CrossRefGoogle Scholar
  51. Zembala M, Filek M, Walas S, Mrowiec H, Kornas A, Miszalski Z, Hartikainen H (2010) Effect of selenium on macro- and microelement distribution and physiological parameters of rape and wheat seedlings exposed to cadmium stress. Plant Soil 329(1–2):457–468CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Fahad Khan
    • 1
  • Saddam Hussain
    • 1
    • 2
  • Mohsin Tanveer
    • 3
  • Sehrish Khan
    • 4
  • Hafiz Athar Hussain
    • 5
  • Biland Iqbal
    • 6
  • Mingjian Geng
    • 1
  1. 1.College of Resources and EnvironmentHuazhong Agricultural UniversityWuhanChina
  2. 2.Department of AgronomyUniversity of AgricultureFaisalabadPakistan
  3. 3.Tasmania Institute of AgricultureUniversity of TasmaniaHobartAustralia
  4. 4.Department of Environmental SciencesUniversity of PeshawarKhyber PakhtunkhwaPakistan
  5. 5.College of Agronomy and BiotechnologySouthwest UniversityChongqingChina
  6. 6.Department of Agriculture ResearchKhyber PakhtunkhwaPakistan

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