The Influence of pH on Cadmium Accumulation in Seedlings of Rice (Oryza sativa L.)

  • Umed Ali
  • Min Zhong
  • Tahmina Shar
  • Sajid Fiaz
  • Lihong Xie
  • Guiai Jiao
  • Shakeel Ahmad
  • Zhonghua Sheng
  • Shaoqing Tang
  • Xiangjin WeiEmail author
  • Peisong HuEmail author


The growth, development, and quality of rice are inhibited by the presence of cadmium (Cd) in the soil, the uptake of which depends strongly on the pH of the growth medium. Here, a hydroponics-based experiment was conducted to characterize the relationship between Cd accumulation and the pH of the medium in seedlings of the two cultivars, Zhonjiazao17 (ZJZ17) and Xiangzhengyu (XZY). The uptakes of Cd by the roots of both cultivars and its translocation to the shoots were the highest from a medium of pH 6.0. XZY plants accumulated more Cd than ZJZ17 ones. Transcription profiling indicated that the genes, OsNRAMP1 and OsHMA2, were actively involved in Cd uptake and transport, as they were both strongly upregulated at pH 6.0. Both the Cd concentration of the medium and its pH exerted significant effects on the seedling growth. At pH 6.0, zinc was efficiently transported, but the translocation of iron was suppressed in shoot. The genes, OsZIP5 and OsYSL15, are the most likely responsible for the uptake and translocation of both these elements in rice seedlings.


Cd accumulation pH levels Gene transcription Seedlings Rice (Oryza sativa L.) 



This work was supported by the National Key Research and Development Program of China (2017YFD0100300; 2016YFD0101801), Agricultural Sciences and Technologies Innovation Program of the Chinese Academy of Agricultural Sciences (CAAS), and by the Central Level, Non-Profit, Scientific Research Institutes Basic R & D Operations Special Fund (Y2017PT46; 2017RG002-1).

Author Contributions

PH, XW, and ST conceived and designed experiment. UA performed the experiment. MZ, TS, and LX helped in hydroponics-based solution preparation and metal determination. MZ, TS, and SF helped RNA extraction. SA made the graphs and figures. UA, ZS, XW, and GJ analyzed the data and drafted the manuscript which was critically revised by PH and XW, All the authors read and approved the final manuscript.

Compliance with Ethical Standards

Conflicts of interest

The authors have no conflicts of interest to disclose.

Supplementary material

344_2019_10034_MOESM1_ESM.pdf (718 kb)
Electronic supplementary material 1 (PDF 718 kb)


  1. Alam SM (1981) Effects of solution pH on the growth and chemical composition of rice plants. J Plant Nutr 4:247–260CrossRefGoogle Scholar
  2. Chaney RL, Green CE, Ajwa HA, Smith RF (2009) Zinc fertilization plus liming to reduce cadmium uptake by Romaine lettuce on Cd-mineralized Lockwood soil. In: Paper presented at the Proceedings of the International Plant Nutrition Colloquium XVI, California, USAGoogle Scholar
  3. Chen YX, He YF, Luo YM, Yu YL, Lin Q, Wong MH (2003) Physiological mechanism of plant roots exposed to cadmium. Chemosphere 50:789–793CrossRefGoogle Scholar
  4. Chen A, Wang M, Liu X (2013) Research progress on the effect of cadmium on rice and its absorption and tolerance mechanisms. Ecol Sci 32:514–522Google Scholar
  5. Chen D, Chen D, Xue R, Long J, Lin X, Lin Y, Jia L, Zeng R, Song Y (2019) Effects of boron, silicon and their interactions on cadmium accumulation and toxicity in rice plants. J Hazard Mater 367:447–455CrossRefGoogle Scholar
  6. Christensen TH (1984) Cadmium soil sorption at low concentrations: I. Effect of time, cadmium load, pH, and calcium. Water Air Soil Poll 21:105–114CrossRefGoogle Scholar
  7. Cikili Y, Samet H, Dursun S (2016) Cadmium toxicity and its effects on growth and metal nutrient ion accumulation in Solanaceae plants. J Agr Sci 22:576–587Google Scholar
  8. Cunha KP, do Nascimento CW, Pimentel RM, Ferreira CP (2008) Cellular localization of cadmium and structural changes in maize plants grown on a cadmium contaminated soil with and without liming. J Hazard Mater 160:228–234CrossRefGoogle Scholar
  9. Francois L, Fortin C, Campbell PG (2007) pH modulates transport rates of manganese and cadmium in the green alga chlamydomonas reinhardtii through non-competitive interactions: implications for an algal BLM. Aquat Toxicol 84:123–132CrossRefGoogle Scholar
  10. Gao L, Chang J, Chen R, Li H, Lu H, Tao L, Xiong J (2016) Comparison on cellular mechanisms of iron and cadmium accumulation in rice: prospects for cultivating Fe-rich but Cd-free rice. Rice 9:39CrossRefGoogle Scholar
  11. Godt J, Scheidig F, Grosse-Siestrup C, Esche V, Brandenburg P, Reich A, Groneberg DA (2006) The toxicity of cadmium and resulting hazards for human health. J Occup Me Toxicol 1:22CrossRefGoogle Scholar
  12. Goel S, Malik JA, Awasthi R, Sandhir R, Nayyar H (2012) Growth and metabolic responses of maize (C4 species) and rice (C3 species) genotypes to cadmium toxicity. Cereal Res Commun 40:225–234CrossRefGoogle Scholar
  13. Grant C, Bailey L, Mclaughlin M, Singh B (1999) Management Factors which influence cadmium concentrations in crops. Springer, Netherlands, pp 151–198Google Scholar
  14. Hatch D, Jones L, Burau R (1988) The effect of pH on the uptake of cadmium by four plant species grown in flowing solution culture. Plant Soil 105:121–126CrossRefGoogle Scholar
  15. He J, Li H, Ma C, Zhang Y, Polle A, Rennenberg H, Cheng X, Luo Z (2015) Overexpression of bacterial gamma-glutamylcysteine synthetase mediates changes in cadmium influx, allocation and detoxification in poplar. New Phytol 205:240–254CrossRefGoogle Scholar
  16. Jain M, Pal M, Gupta P, Gadre R (2007) Effect of cadmium on chlorophyll biosynthesis and enzymes of nitrogen assimilation in greening maize leaf segments: role of 2-oxoglutarate. Indian J Exp Biol 45:385–389PubMedGoogle Scholar
  17. Javed MT, Greger M (2011) Cadmium triggers elodea canadensis to change the surrounding water pH and thereby Cd uptake. Int J Phytoremediat 13:95–106CrossRefGoogle Scholar
  18. Juo A, Uzu F (1977) Liming and nutrient interactions in two ultisols from southern Nigeria. Plant Soil 47:419–430CrossRefGoogle Scholar
  19. Larsson JEH, Asp H (2013) Effects of pH and nitrogen on cadmium uptake in potato. Biol Plantarum 57:788–792CrossRefGoogle Scholar
  20. Lee S, Chiecko JC, Kim SA, Walker EL, Lee Y, Guerinot ML, An G (2009) Disruption of OsYSL15 leads to iron inefficiency in rice plants. Plant physiol 150:786–800CrossRefGoogle Scholar
  21. Liu D, Zhang C, Chen X, Yang Y, Wang S, Li Y, Hu H, Ge Y, Cheng W (2013) Effects of pH, Fe, and Cd on the uptake of Fe2+ and Cd2+ by rice. Environ Sci and Pollut Res Int 20:8947–8954CrossRefGoogle Scholar
  22. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408CrossRefGoogle Scholar
  23. Nakanishi H, Ogawa I, Ishimaru Y, Mori S, Nishizawa NK (2006) Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice. Soil Sci Plant Nutr 52:464–469CrossRefGoogle Scholar
  24. Nocito FF, Lancilli C, Dendena B, Lucchini G, Sacchi GA (2011) Cadmium retention in rice roots is influenced by cadmium availability, chelation and translocation. Plant Cell Environ 34:994–1008CrossRefGoogle Scholar
  25. Olsen LI, Palmgren MG (2014) Many rivers to cross: the journey of zinc from soil to seed. Front Plant Sci 5:30PubMedPubMedCentralGoogle Scholar
  26. Onwu F, Ogah S (2010) Studies on the effect of pH on the sorption of cadmium (ll), nickel (II), lead (III) and chromium (VI) from aqueous solutions by African white star apple (Chrysophyllum albidium) shell. Afr J Biotechnol 9:7086–7093Google Scholar
  27. Rafiq MT, Aziz R, Yang X, Xiao W, Rafiq MK, Ali B, Li T (2014) Cadmium phytoavailability to rice (Oryza sativa L.) grown in representative Chinese soils. A model to improve soil environmental quality guidelines for food safety. Ecotox Environ Saf 103:101–107CrossRefGoogle Scholar
  28. Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24:2155–2167CrossRefGoogle Scholar
  29. Song W, Chen S, Liu J, Chen L, Song N, Li N, Liu B (2015) Variation of Cd concentration in various rice cultivars and derivation of cadmium toxicity thresholds for paddy soil by species-sensitivity distribution. J Integr Agr 14:1845–1854CrossRefGoogle Scholar
  30. Spain JM, Francis CA, Howeler RH, Calvo F (1975) Differential species and varietal tolerance to soil acidity in tropical crops and pastures. North Carolina State Univiversity Raleigh, NC, USA, pp 308–329Google Scholar
  31. Sui FQ, Chang JD, Tang Z, Liu WJ, Huang XY, Zhao FJ (2018) Nramp5 expression and functionality likely explain higher cadmium uptake in rice than in wheat and maize. Plant Soil 433:377–389CrossRefGoogle Scholar
  32. Takahashi R, Ishimaru Y, Nakanishi H, Nishizawa NK (2011a) Role of the iron transporter OsNRAMP1 in cadmium uptake and accumulation in rice. Plant Signal Behav 6:1813–1816CrossRefGoogle Scholar
  33. Takahashi R et al (2011b) The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. J Exp Bot 62:4843–4850CrossRefGoogle Scholar
  34. Takahashi R, Ishimaru Y, Shimo H, Ogo Y, Senoura T, Nishizawa NK, Nakanishi H (2012) The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice. Plant Cell Environ 35:1948–1957CrossRefGoogle Scholar
  35. Tiong J, McDonald G, Genc Y, Shirley N, Langridge P, Huang CY (2015) Increased expression of six ZIP family genes by zinc (Zn) deficiency is associated with enhanced uptake and root-to-shoot translocation of Zn in barley (Hordeum vulgare). New Phytol 207:1097–1109CrossRefGoogle Scholar
  36. Uraguchi S, Fujiwara T (2012) Cadmium transport and tolerance in rice: perspectives for reducing grain cadmium accumulation. Rice 5:5CrossRefGoogle Scholar
  37. Vassilev A, Lidon F (2011) Cd-induced membrane damages and changes in soluble protein and free amino acid contents in young barley plants. Emir J Food Agr 23:130–136CrossRefGoogle Scholar
  38. Wallace A, Romney E, Alexander G, Soufi S, Patel P (1977) Some interactions in plants among cadmium, other heavy metals, and chelating agents. Agron J 69:18–20CrossRefGoogle Scholar
  39. Wang AS, Angle JS, Chaney RL, Delorme TA, Reeves RD (2006) Soil pH effects on uptake of Cd and Zn by Thlaspi caerulescens. Plant Soil 281:325–337CrossRefGoogle Scholar
  40. Wang J, Fang Y, Tian B, Zhang X, Zeng D, Guo L, Hu J, Xue D (2018) New QTLs identified for leaf correlative traits in rice seedlings under cadmium stress. Plant Grow Reg 85:329–335CrossRefGoogle Scholar
  41. Xue D, Jiang H, Deng X, Zhang X, Wang H, Xu X, Hu J, Zeng D, Guo L, Qian Q (2014) Comparative proteomic analysis provides new insights into cadmium accumulation in rice grain under cadmium stress. J Hazard Mater 280:269–278CrossRefGoogle Scholar
  42. Yamaji N, Xia J, Mitani-Ueno N, Yokosho K, Feng Ma J (2013) Preferential delivery of zinc to developing tissues in rice is mediated by P-type heavy metal ATPase OsHMA2. Plant Physiol 162:927–939CrossRefGoogle Scholar
  43. Yang Y, Chen J, Huang Q, Tang S, Wang J, Hu P, Shao G (2018) Can liming reduce cadmium (Cd) accumulation in rice (Oryza sativa) in slightly acidic soils? A contradictory dynamic equilibrium between Cd uptake capacity of roots and Cd immobilisation in soils. Chemosphere 193:547–556CrossRefGoogle Scholar
  44. Yoshida S, Forno DA, Cook JH, Gomez KA (1976) Laboratory manual for physiological studies of rice. International Rice Research Institute, Los Baños, Philippines, pp 61–66Google Scholar
  45. Zhang X, Chen H, Jiang H, Lu W, Pan J, Qian Q, Xue D (2015) Measuring the damage of heavy metal cadmium in rice seedlings by SRAP analysis combined with physiological and biochemical parameters. J Sci Food Agric 95:2292–2298CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.State Key Laboratory of Rice BiologyChina National Rice Research InstituteHangzhouChina

Personalised recommendations