The variation of rice cultivars in Cd toxicity and distribution of the seedlings and their root histochemical examination

  • Wan-Ting Chiao
  • Chun-Hui Yu
  • Kai-Wei JuangEmail author


Rice cultivars showing low Cd transportation into the aboveground parts of a plant can be selected to reduce Cd contamination in grains. In this study, eight rice cultivars, TY3, TK9, TNG71, KH145, TKW1, TKW3, TCS10, and TCS17, which are commonly grown in Taiwan, were used. The seedlings of each cultivar were transplanted with 0, 5, 10, 50, 100, and 250 μM CdCl2 solutions, respectively, for a 7-day treatment in hydroponics. The Cd treatment resulted in significant reductions in the root elongation and the shoot extension of rice seedlings for each cultivar. According to the Cd distributions in the root and shoot for the used cultivars, the Cd absorption by rice plants was predominantly accumulated in the root rather than transferred to the shoot. The Cd treatment induced lignification in the sclerenchyma tissue and in the endodermis and metaxylem cell walls of the rice root specimens. The lignification of the cell walls enhancing the Cd sequestration by the root would be related to the tolerance to Cd toxicity and to the Cd transfer into the aboveground parts of a rice plant. Much higher Cd concentrations in the shoot were found for the TY3 and TK9 plants. By contrast, the translocations of Cd in TNG71, KH145, TKW1, and TKW3 plants were relatively low. Thus, TNG71, KH145, TKW1, and TKW3 would be the candidates for cultivation to reduce Cd transported into the aboveground parts of a rice plant. TCS10 and TCS17 cultivars also showed low translocation of Cd from the root to the shoot, but their Cd absorption rates in the plant were much higher than the other cultivars.


Paddy soil Heavy metal Abiotic stress Lignification Pollution-safe cultivar 



This research was sponsored by the Ministry of Science and Technology, Taiwan, under Grant No. MOST 105-2313-B-415-002-MY3. We also thank the anonymous reviewers for providing many constructive comments.


  1. Ahsan N, Nakamura T, Komatsu S (2012) Differential responses of microsomal proteins and metabolites in two contrasting cadmium (Cd)-accumulating soybean cultivars under Cd stress. Amino Acids 42:317–327CrossRefGoogle Scholar
  2. Alvarez I, Sam O, Reynaldo I, Testillano P, del Carmen Risueño M, Arias M (2012) Morphological and cellular changes in rice roots (Oryza sativa L.) caused by Al stress. Bot Stud 53:67–73Google Scholar
  3. Arao T, Ae N (2003) Genotypic variations in cadmium levels of rice grain. Soil Sci Plant Nutr 49:473–479CrossRefGoogle Scholar
  4. Arao T, Ishikawa S (2006) Genotypic differences in Cd concentration and distribution of soybean and rice. Jpn Agric Res Q 40:21–30CrossRefGoogle Scholar
  5. Ashraf U, Hussain S, Anjum SA, Abbas F, Tanveer M, Noor MA, Tang X (2017) Alterations in growth, oxidative damage, and metal uptake of five aromatic rice cultivars under lead toxicity. Plant Physiol Biochem 115:461–471CrossRefGoogle Scholar
  6. Begović L, Ravlić J, Lepeduš H, Leljak-Levanić D, Cesar V (2015) The pattern of lignin deposition in the cell walls of internodes during barley (Hordeum vulgare L.) development. Acta Biol Crac Ser Bot 57:55–66Google Scholar
  7. Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Ann Rev Plant Physiol 54:519–546Google Scholar
  8. Chaffey N, Cholewa E, Regan S, Sundberg B (2002) Secondary xylem development in Arabidopsis: a model for wood formation. Physiol Plant 114:594–600CrossRefGoogle Scholar
  9. Chen BC, Lai HY, Lee DY, Juang KW (2011) Using chemical fractionation to evaluate the phytoextraction of cadmium by switchgrass from Cd-contaminated soils. Ecotoxicology 20:409–418CrossRefGoogle Scholar
  10. Chiao W-T, Syu C-H, Chen B-C, Juang K-W (2019) Cadmium in rice grains from a field trial in relation to model parameters of Cd-toxicity and -absorption in rice seedlings. Ecotoxicol Environ Saf 169:837–847CrossRefGoogle Scholar
  11. Choppala G, Saifullah Bolan N, Bibi S, Iqbal M, Rengel Z, Kunhikrishnan A, Ashwath N, Ok YS (2014) Cellular mechanisms in higher plants governing tolerance to cadmium toxicity. Crit Rev Plant Sci 33:374–391CrossRefGoogle Scholar
  12. CODEX (2006) Report of the 38th session of the CODEX committee on food additives and contaminants. Joint FAO/WHO Food Standards Programme, Codex Alimentarius Commission, ALINORM 06/29/12Google Scholar
  13. Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380CrossRefGoogle Scholar
  14. Douchiche O, Driouich A, Morvan C (2010a) Spatial regulation of cell-wall structure in response to heavy metal stress: cadmium-induced alteration of the methyl-esterification pattern of homogalacturonans. Ann Bot 105:481–491CrossRefGoogle Scholar
  15. Douchiche O, Soret-Morvan O, Chaibi W, Morvan C, Paynel F (2010b) Characteristics of cadmium tolerance in ‘Hermes’ flax seedlings: contribution of cell walls. Chemosphere 81:1430–1436CrossRefGoogle Scholar
  16. Fan J-L, Hu Z-Y, Ziadi N, Xia X (2010) Excessive sulfur supply reduces cadmium accumulation in brown rice (Oryza sativa L.). Environ Pollut 158:409–415CrossRefGoogle Scholar
  17. Fleck AT, Nye T, Repenning C, Stahl F, Zahn M, Schenk MK (2011) Silicon enhances suberization and lignification in roots of rice (Oryza sativa). J Exp Bot 62:2001–2011CrossRefGoogle Scholar
  18. Grant CA, Clarke JM, Duguid S, Chaney RL (2008) Selection and breeding of plant cultivars to minimize cadmium accumulation. Sci Total Environ 390:301–310CrossRefGoogle Scholar
  19. He JY, Zhu C, Ren FY, Yan PY, Cheng C, Jiang DA, Sun ZX (2008) Uptake, subcellular distribution, and chemical forms of cadmium in wild-type and mutant rice. Pedosphere 18:371–377CrossRefGoogle Scholar
  20. He J, Ren Y, Chen X, Chen H (2014) Protective roles of nitric oxide on seed germination and seedling growth of rice (Oryza sativa L.) under cadmium stress. Ecotoxicol Environ Saf 108:114–119CrossRefGoogle Scholar
  21. Hsu YT, Kao CH (2003) Role of abscisic acid in cadmium tolerance of rice (Oryza sativa L.) seedlings. Plant Cell Environ 20:867–874CrossRefGoogle Scholar
  22. Ishikawa S, Ae N, Sugiyama M, Murakami M, Arao T (2005) Genotypic variation in shoot cadmium concentration in rice and soybean in soils with different levels of cadmium contamination. Soil Sci Plant Nutr 51:101–108CrossRefGoogle Scholar
  23. Ishikawa S, Ae N, Murakami M, Wagatsuma T (2006) Is Brassica juncea a suitable plant for phytoremediation of cadmium in soils with moderately low cadmium contamination? Possibility of using other plant species for Cd-phytoextraction. Soil Sci Plant Nutr 52:32–42CrossRefGoogle Scholar
  24. Ishikawa S, Ishimaru Y, Igura M, Kuranata M, Abe T, Senoura T, Hase Y, Arao T, Nishizawa NK, Nakanishi H (2012) Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. Proc Natl Acad Sci USA 109:19166–19171CrossRefGoogle Scholar
  25. Juang KW, Ho PC, Yu CH (2012) Short-term effects of compost amendment on the fractionation of cadmium in soil and cadmium accumulation in rice plants. Environ Sci Pollut Res 19:1696–1708CrossRefGoogle Scholar
  26. Kikuchi Y, Okazaki M, Toyota K, Motobayashi T, Kato M (2007) The input–output balance of cadmium in a paddy field of Tokyo. Chemosphere 67:920–927CrossRefGoogle Scholar
  27. Krzesłowska M (2011) The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiol Plant 33:35–51CrossRefGoogle Scholar
  28. Krzesłowska M, Lenartowska M, Mellerowicz EJ, Samardakiewicz S, Woźny A (2009) Pectinous cell wall thickenings formation: a response of moss protonemata cells to Pb. Environ Exp Bot 65:119–131CrossRefGoogle Scholar
  29. Lee CH, Hsieh YC, Lin TH, Lee DY (2013) Iron plaque formation and its effect on arsenic uptake by different genotypes of paddy rice. Plant Soil 363:231–241CrossRefGoogle Scholar
  30. Leita L, De Nobili M, Cesco S, Mondini C (1996) Analysis of intercellular cadmium forms in roots and leaves of bush bean. J Plant Nutr 19:527–533CrossRefGoogle Scholar
  31. Liu J, Qian M, Cai G, Yang J, Zhu Q (2007a) Uptake and translocation of Cd in different rice cultivars and the relation with Cd accumulation in rice grain. J Hazard Mater 143:443–447CrossRefGoogle Scholar
  32. Liu WX, Shen LF, Liu JW, Wang YW, Li SR (2007b) Uptake of toxic heavy metals by rice (Oryza sativa L.) cultivated in the agricultural soil near Zhengzhou City, People’s Republic of China. Bull Environ Contam Toxicol 79:209–213CrossRefGoogle Scholar
  33. Liu Q, Zheng L, He F, Zhao FJ, Shen Z, Zheng L (2015) Transcriptional and physiological analyses identify a regulatory role for hydrogen peroxide in the lignin biosynthesis of copper-stressed rice roots. Plant Soil 387:323–336CrossRefGoogle Scholar
  34. Liu Q, Luo L, Zheng L (2018) Lignins: biosynthesis and biological functions in plants. Int J Mol Sci 19:335CrossRefGoogle Scholar
  35. Loix C, Huybrechts M, Vangronsveld J, Gielen M, Keunen E, Cuypers A (2017) Reciprocal interactions between cadmium-induced cell wall responses and oxidative stress in plants. Front Plant Sci 8:1867CrossRefGoogle Scholar
  36. Lur HS, Wu YC, Chang SJ, Lao CL, Hsu CL, Kondo M (2009) Effects of high temperature on yield and grain quality of rice in Taiwan. In: Hasegawa T, Sakai H (eds) Proceeding of the MARCO symposium. National Institute for Agro-Environmental Sciences, Tsukuba, pp 38–43Google Scholar
  37. Makino T, Takano H, Kamiya T, Itou T, Sekiya N, Inahara M, Sakurai Y (2008) Restoration of cadmium-contaminated paddy soils by washing with ferric chloride: Cd extraction mechanism and bench-scale verification. Chemosphere 70:1035–1043CrossRefGoogle Scholar
  38. Máthé C, Vasas G, Borbely G, Erdodi F, Beyer DE, Kiss A, Suranyi G, Gonda S, Jámbrik K, M-Hamvas M (2013) Histological, cytological and biochemical alterations induced by microcystin-LR and cylindrospermopsin in white mustard (Sinapis alba L.) seedlings. Acta Biol Hung 64:71–85CrossRefGoogle Scholar
  39. McGrath SP, Zhao FJ, Lombi E (2001) Plant and rhizosphere processes involved in phytoremediation of metal-contaminated soils. Plant Soil 232:207–214CrossRefGoogle Scholar
  40. Mohamed AA, Castagna A, Ranieri A, Sanità di Toppi L (2012) Cadmium tolerance in Brassica juncea roots and shoots is affected by antioxidant status and phytochelatin biosynthesis. Plant Physiol Biochem 57:15–22CrossRefGoogle Scholar
  41. Muñoz N, Gonzalez C, Molina A, Zirulnik F, Luna CM (2008) Cadmium-induced early changes in O2–, H2O2 and antioxidative enzymes in soybean (Glycine max L.) leaves. Plant Growth Regul 56:159–166CrossRefGoogle Scholar
  42. Nishizono H, Ichikawa H, Suzuki S, Ishii F (1987) The role of the root cell wall in heavy metal tolerance of Athyrium yokosense. Plant Soil 101:15–20CrossRefGoogle Scholar
  43. Obata H, Umebayashi M (1993) Production of SH compounds in higher plants of different tolerance to Cd. Plant Soil 155:533–536CrossRefGoogle Scholar
  44. Pan CX, Nakao Y, Nii N (2006) Anatomical development of phi thickening and the Casparian strip in loquat root. J Jpn Soc Hort Sci 75:445–449CrossRefGoogle Scholar
  45. Pomar F, Merino F, Barceló AR (2002) O-4-Linked coniferyl and sinapyl aldehydes in lignifying cell walls are the main targets of the Wiesner (phloroglucinol-HCl) reaction. Protoplasma 220:17–28CrossRefGoogle Scholar
  46. Poschenrieder C, Gunsé B, Corrales I, Barceló J (2008) A glance into aluminium toxicity and resistance in plants. Sci Total Environ 400:356–368CrossRefGoogle Scholar
  47. Probst A, Liu H, Fanjul M, Liao B, Hollande E (2009) Response of Vicia faba L. to metal toxicity on mine tailing substrate: geochemical and morphological changes in leaf and root. Environ Exp Bot 66:297–308CrossRefGoogle Scholar
  48. Römkens PFAM, Guo HY, Chu CL, Liu TS, Chiang CF, Koopmans GF (2009) Prediction of cadmium uptake by brown rice and derivation of soil-plant transfer models to improve soil protection guidelines. Environ Pollut 157:2435–2444CrossRefGoogle Scholar
  49. Sarwar N, Malhi SS, Zia MH, Naeem A, Bibi S, Farid G (2010) Role of mineral nutrition in minimizing cadmium accumulation by plants. J Sci Food Agric 90:925–937Google Scholar
  50. Singh RP, Agrawal M (2010) Variations in heavy metal accumulation, growth and yield of rice plants grown at different sewage sludge amendment rates. Ecotoxiol Environ Saf 73:632–641CrossRefGoogle Scholar
  51. Song Y, Ye L, Nii N (2011) Effects of soil water availability on development of suberin lamellae in the endodermis and exodermis and on cortical cell wall thickening in red bayberry (Myrica rubra Sieb. et Zucc.) tree roots. Sci Hort 129:554–560CrossRefGoogle Scholar
  52. Song X-Q, Liu L-F, Jiang Y-J, Zhang B-C, Gao Y-P, Liu X-L, Lin Q-S, Ling H-Q, Zhou Y-H (2013) Disruption of secondary wall cellulose biosynthesis alters cadmium translocation and tolerance in rice plants. Mol Plant 6:768–780CrossRefGoogle Scholar
  53. Srivastava RK, Pandey P, Rajpoot R, Rani A, Gautam A, Dubey RS (2015) Exogenous application of calcium and silica alleviates cadmium toxicity by suppressing oxidative damage in rice seedlings. Protoplasma 252:959–975CrossRefGoogle Scholar
  54. Sun HY, Chen ZH, Chen F, Xie LP, Zhang GP, Vincze E, Wu EB (2015) DNA microarray revealed and RNAi plants confirmed key genes conferring low Cd accumulation in barley grains. BMC Plant Biol 15:1–17CrossRefGoogle Scholar
  55. Syu CH, Lee CH, Jiang PY, Chen MK, Lee DY (2014) Comparison of As sequestration in iron plaque and uptake by different genotypes of rice plants grown in As-contaminated paddy soils. Plant Soil 374:411–422CrossRefGoogle Scholar
  56. Thounaojam TC, Panda P, Mazumdar P, Kumar D, Sharma GD, Sahoo L, Sanjib P (2012) Excess copper induced oxidative stress and response of antioxidants in rice. Plant Physiol Biochem 53:33–39CrossRefGoogle Scholar
  57. Tian BH, Liu LY, Zhang LX, Song SX, Wang JG, Wu LF, Li HJ (2015) Characterization of culm morphology, anatomy and chemical composition of foxtail millet cultivars differing in lodging resistance. J Agric Sci 153:1437–1448CrossRefGoogle Scholar
  58. Tuladhar A, Ohtsuka S, Nii N (2014) Formation of exclusive pattern during accumulation of ligno-suberic material in cell wall of Myrtaceae root tissues including epidermis, exodermis, endodermis and polyderm. Plant Root 8:24–32CrossRefGoogle Scholar
  59. Ueno D, Iwashita T, Zhao FJ, Ma JF (2008) Characterization of Cd translocation and identification of Cd form in xylem sap of the Cd-hyperaccumulator Arabidopsis halleri. Plant Cell Physiol 49:540–548CrossRefGoogle Scholar
  60. Uraguchi S, Mori S, Kuramata M, Kawasaki A, Arao T, Ishikawa S (2009) Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J Exp Bot 60:2677–2688CrossRefGoogle Scholar
  61. Vogel J (2008) Unique aspects of the grass cell wall. Curr Opin Plant Biol 11:301–307CrossRefGoogle Scholar
  62. Wang GQ, Koopmans GF, Song J, Temminghoff EJM, Luo YM, Zhao QG, Japenga J (2007) Mobilization of heavy metals from contaminated paddy soil by EDDS, EDTA, and elemental sulfur. Environ Geochem Heal 29:221–235CrossRefGoogle Scholar
  63. Wang F, Wang M, Liu Z, Han T, Ye Y, Gong N, Sun J, Zhu C (2015) Different responses of low grain-Cd-accumulating and high grain-Cd-accumulating rice cultivars to Cd stress. Plant Physiol Biochem 96:261–269CrossRefGoogle Scholar
  64. Xiong J, An L, Lu H, Zhu C (2009) Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta 230:755–765CrossRefGoogle Scholar
  65. Xu D, Chen Z, Sun K, Yan D, Kang M, Zhao Y (2013) Effect of cadmium on the physiological parameters and the subcellular cadmium localization in the potato (Solanum tuberosum L.). Ecotox Environ Safe 97:147–153CrossRefGoogle Scholar
  66. Yang CM, Juang KW (2015) Alleviation effects of calcium and potassium on cadmium rhizotoxicity and absorption by soybean and wheat roots. J Plant Nutr Soil Sci 178:748–754CrossRefGoogle Scholar
  67. Yu H, Wang J, Fang W, Yuan J, Yang Z (2006) Cadmium accumulation in different rice cultivars and screening for pollution-safe cultivars of rice. Sci Total Environ 370:302–309CrossRefGoogle Scholar
  68. Zhang J, Sun W, Li Z, Liang Y, Song A (2009) Cadmium fate and tolerance in rice cultivars. Agron Sustain Dev 29:483–490CrossRefGoogle Scholar

Copyright information

© The International Society of Paddy and Water Environment Engineering 2019

Authors and Affiliations

  1. 1.Ph.D. Program of Agriculture ScienceNational Chiayi UniversityChiayi CityTaiwan
  2. 2.Department of AgronomyNational Chiayi UniversityChiayi CityTaiwan

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