Environmental Science and Pollution Research

, Volume 26, Issue 14, pp 13738–13745 | Cite as

Differences of Cd uptake and expression of MT family genes and NRAMP2 in two varieties of ryegrasses

  • Yanhua Li
  • Yuli Qin
  • Weihong XuEmail author
  • Yourong ChaiEmail author
  • Tao Li
  • Chunlai Zhang
  • Mei Yang
  • Zhangmi He
  • Deyu Feng
Sustainable Environmental Management


In order to understand the mechanism of the difference of Cd absorption and Cd enrichment in different ryegrass varieties, pot experiment was conducted to study on the response of two varieties of ryegrass (Bond and Abbott) to Cd stress as well as the differences of Cd uptake and expression of MT family genes and NRAMP2. Results showed that root dry weights of two varieties and shoot dry weights of Abbott increased first and then decreased with the increase of Cd level in soil. When exposed to 75 mg kg−1 Cd, shoot dry weight and plant dry weight of Abbott both reached maximum values (10.92 and 12.03 g pot−1), which increased by 11.09 and 10.67% compared with the control, respectively. Shoot dry weight and plant dry weight of Bond decreased with the increase of Cd level in soil. When the Cd level in soil was 75 mg kg−1, shoot Cd concentrations of the two varieties were 111.19 mg kg−1 (Bond) and 133.69 mg kg−1 (Abbott), respectively, both of which exceeded the critical value of Cd hyperaccumulator (100 mg kg−1). The expression of MT gene family and NRAMP2 in the leaf of Bond variety significantly increased at the Cd level of 75 mg kg−1 and reached maximum value (except MT2C) at Cd level of 150 mg kg−1. The expression of MT gene family in the stem of Bond variety showed a double-peak pattern, while the expression of NRAMP2 was a single-peak pattern. The expression of MT gene family and NRAMP2 in Abbott variety was consistent with single-peak pattern. The expression of MT gene family and NRAMP2 in leaf both significantly increased at Cd level of 150 mg kg−1, while that in stem and root significantly increased at Cd level of 75 mg kg−1. For both varieties of ryegrass, the expression amount of MT family genes and Nramp2 in leaf was higher than that in root and stem, indicating the Cd tolerance of ryegrass can be improved by increasing the expression levels of MT family genes and Nramp2 in stem and root. There was significant genotypic difference in the expression of MT gene family and NRAMP2 between the two varieties of ryegrass, and the expression of MT gene family and NRAMP2 in leaves and stems of Bond variety was higher than that in Abbott variety, while the expression of MT gene family and NRAMP2 in roots of Abbott variety was higher than that in Bond variety. The two gene families investigated in this study may be closely related to Cd uptake, but not related to Cd transport from root to leaf and Cd enrichment in shoot.


Soli Cd pollution Ryegrass varieties Cd uptake MT NRAMP2 


Funding information

This work was supported by Fund of China Agriculture Research System (CARS-23), and the National Science and Technology Pillar Program of China (No. 2007BAD87B10).


  1. Anjum NA, Gill SS, Gill R (2014) Plant adaptation to environmental change: significance of amino acids and their derivatives. CABI, LondonCrossRefGoogle Scholar
  2. Antoniadis V, Shaheen SM, Boersch J, Frohne T, Du Laing G, Rinklebe J (2017) Bioavailability and risk assessment of potentially toxic elements in garden edible vegetables and soils around a highly contaminated former mining area in Germany. J Environ Manag 186:192–200CrossRefGoogle Scholar
  3. Attinti R, Barrett KR, Datta R, Sarkar D (2017) Ethylenediaminedisuccinic acid (EDDS) enhances phytoextraction of lead by vetiver grass from contaminated residential soils in a panel study in the field. Environ Pollut 225:524–533CrossRefGoogle Scholar
  4. Bermanec V, Vidakovic-Cifrek Z, Fiket Z, Tkalec M, Kampic S, Kniewald G (2016) Influence of digested wastewater sludge on early growth of the perennial ryegrass (Lolium perenne L.). Environ Earth Sci 75(1):32CrossRefGoogle Scholar
  5. Cai HL, Li F, Zeng WA, Yang HW, Tang Z (2017) Functional analysis of NtNramp1 pariticipating in Cd accumulation in tobacco of different Cd accumulating genotypes. Acta Tab Sin 23(4):84–91Google Scholar
  6. Chen ZF, Zhao Y, Fan LD, Xing LT, Yang YJ (2015) Cadmium (Cd) localization in tissues of cotton (Gossypium hirsutum L.), and its phytoremediation potential for Cd-contaminated soils. Bull Environ Contam Toxicol 95(6):784–789CrossRefGoogle Scholar
  7. Fang ZG, Hu ZY, Zhao HH, Yang L, Ding CL, Lou LQ, Cai QS (2017) Screening for cadmium tolerance of 21 cultivars from Italian ryegrass (Lolium multiflorum Lam) during germination. Grassl Sci 63(1):36–45CrossRefGoogle Scholar
  8. Han H, Chen XJ, Hou XL, Liu AQ, Cai LP, Zhou CF, Ma XQ (2016) Effects of cadmium stresses on growth and antioxidant activities of Neyraudia reynaudiana. J Agro-Environ Sci 35(4):647–653Google Scholar
  9. Hassinen VH, Tuomainen M, Peräniemi S, Schat H, Kärenlampi SO, Tervahauta AI (2009) Metallothioneins 2 and 3 contribute to the metal-adapted phenotype but are not directly linked to Zn accumulation in the metal hyperaccumulator, Thlaspi caerulescens. J Exp Bot 60(1):187–196CrossRefGoogle Scholar
  10. Huang DF, Xi JB, Zhao YL (2016) The physiological response of two varieties of Lolium perenne under cadmium stress. Nor Horticul (3):66–68Google Scholar
  11. Ishimaru Y, Takahashi R, Bashir K, Shimo H, Senoura T, Sugimoto K, Ono K, Yano M, Ishikawa S, Arao T, Nakanishi H, Nishizawa NK (2012) Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport. Sci Rep 2:286CrossRefGoogle Scholar
  12. Lee J, Shim D, Song WY, Hwang I, Lee Y (2004) Arabidopsis metallothioneins 2a and 3 enhance resistance to cadmium when expressed in Vicia faba guard cells. Plant Mol Biol 54(6):805–815CrossRefGoogle Scholar
  13. Li HF, Wang Y, Yuan QH (2014) Effects of cadmium stress on growth and physiology of perennial ryegrass. Grassl China 36(4):79–84Google Scholar
  14. Li T, Xu WH, Chai YR, Zhou XB, Wang ZY, Xie DT (2017) Differences of Cd uptake and expression of Cd-tolerance related genes in two varieties of ryegrasses. Bulg Chem Commun 49(3):697–705Google Scholar
  15. Liu Y, Zhang CB, Zhao YL, Sun SJ, Liu ZQ (2017) Effects of growing seasons and genotypes on the accumulation of cadmium and mineral nutrients in rice grown in cadmium contaminated soil. Sci Total Environ 579:1282–1288CrossRefGoogle Scholar
  16. Ma M, Lau PS, Jia YT, Tsang WK, Lam SKS, Tam NFY, Wong YS (2003) The isolation and characterization of type 1 metallothionein (MT) cDNA from a heavy-metal-tolerant plant, Festuca rubra, cv. Merlin. Plant Sci 164(1):51–60CrossRefGoogle Scholar
  17. Malekzadeh R, Shahpiri A (2017) Independent metal-thiolate cluster formation in C-terminal Cys-rich region of a rice type 1 metallothionein isoform. Int J Biol Macromol 96:436–441CrossRefGoogle Scholar
  18. Meng JG, Zhang XD, Tan SK, Zhao KX, Yang ZM (2017) Genome-wide identification of Cd-responsive NRAMP transporter genes and analyzing expression of NRAMP 1 mediated by miR167 in Brassica napus. Biometals 30(6):917–931CrossRefGoogle Scholar
  19. Milner MJ, Mitani-Ueno N, Yamaji N, Yokosho K, Craft E, Fei ZJ, Ebbs S, Zambrano MC, Ma JF, Kochian LV (2014) Root and shoot transcriptome analysis of two ecotypes of Noccaea caerulescens uncovers the role of NcNramp1 in Cd hyperaccumulation. Plant J 78(3):398–410CrossRefGoogle Scholar
  20. Moreno-Jiménez E, Sepúlveda R, Esteban E, Beesley L (2017) Efficiency of organic and mineral based amendments to reduce metal [loid] mobility and uptake (Lolium perenne) from a pyrite-waste contaminated soil. J Geochem Explor 174:46–52CrossRefGoogle Scholar
  21. Nezhad RM, Shahpiri A, Mirlohi A (2013) Discrimination between two rice metallothionein isoforms belonging to type 1 and type 4 in metal-binding ability. Biotechnol Appl Biochem 60(3):275–282CrossRefGoogle Scholar
  22. Pirzadeh S, Shahpiri A (2016) Functional characterization of a type 2 metallothionein isoform (OsMTI-2b) from rice. Int J Biol Macromol 88:491–496CrossRefGoogle Scholar
  23. Sanz-Fernández M, Rodríguez-Serrano M, Sevilla-Perea A, Pena L, Mingorance MD, Sandalio LM, Romero-Puertas MC (2017) Screening Arabidopsis mutants in genes useful for phytoremediation. J Hazard Mater 335:143–151CrossRefGoogle Scholar
  24. 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(5):2155–2167CrossRefGoogle Scholar
  25. Shahpiri A, Soleimanifard I, Asadollahi MA (2015) Functional characterization of a type 3 metallolthionein isoform (OsMTI-3a) from rice. Int J Biol Macromol 73(10):154–159CrossRefGoogle Scholar
  26. Shi C, Wang CL, Huang CF, An SZ (2015) Effects of Cd stress on the growth and physiological characteristics of Avena fatua seedlings. Acta Agrestia Sin 23(3):526–532Google Scholar
  27. Shim D, Hwang JU, Lee J, Lee S, Choi Y, An G, Martinoia E, Lee Y (2009) Orthologs of the class A4 heat shock transcription factor HsfA4a confer cadmium tolerance in wheat and rice. Plant Cell 21(12):4031–4043CrossRefGoogle Scholar
  28. Tang L, Luo WJ, Tian SK, He ZL, Stoffella PJ, Yang XE (2016) Genotypic differences in cadmium and nitrate co-accumulation among the Chinese cabbage genotypes under field conditions. Sci Hortic 201:92–100CrossRefGoogle Scholar
  29. Takahashi R, Ishimaru Y, Shimo H, Bashir K, Senoura T, Sugimoto K, Ono K, Suzui N, Kawachi N, Ishii S, Yin YG, Fujimaki S, Yano M, Nishizawa NK, Nakanishi H (2014) From laboratory to field: OsNRAMP5-knockdown rice is a promising candidate for Cd phytoremediation in paddy fields. PLoS One 9(6):e98816CrossRefGoogle Scholar
  30. Tejada-Jiménez M, Castro-Rodríguez R, Kryvoruchko I, Lucas MM, Udvardi M, Imperial J, González-Guerrero M (2015) Medicago truncatula natural resistance-associated macrophage protein1 is required for iron uptake by rhizobia-infected nodule cells. Plant Physiol 168(1):258–272CrossRefGoogle Scholar
  31. Thomine S, Lelièvre F, Debarbieux E, Schroeder JI, Barbier-Brygoo H (2003) AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J 34(5):685–695CrossRefGoogle Scholar
  32. Tiwari M, Sharma D, Dwivedi S, Singh M, Tripathi RD, Trivedi PK (2014) Expression in Arabidopsis and cellular localization reveal involvement of rice NRAMP, OsNRAMP1, in arsenic transport and tolerance. Plant Cell Environ 37(1):140–152CrossRefGoogle Scholar
  33. Van-Hoof NALM, Hassinen VH, Hakvoort HWJ, Ballintijn KF, Schat H, Verkleij JAC, Ernst WHO, Karenlampi SO, Tervahauta AI (2001) Enhanced copper tolerance in Silene vulgaris (Moench) Garcke populations from copper mines is associated with increased transcript levels of a 2b-type metallothionein gene. Plant Physiol 126(4):1519–1526CrossRefGoogle Scholar
  34. Wei SH, Zhou QX (2004) Discussion on basic principles and strengthening measures for phytoremediation of soils contaminated by heavy metals. Chin J Ecol 23(1):65–72Google Scholar
  35. Xu WH, Li YR, He JP, Ma QF, Zhang XJ, Chen GQ, Wang HX, Zhang HB (2010) Cd uptake in rice cultivars treated with organic acids and EDTA. J Environ Sci 22(3):441–447CrossRefGoogle Scholar
  36. Zhao YP, Cui JL, Chan TS, Dong JC, Chen DL, Li XD (2018) Role of chelant on Cu distribution and speciation in Lolium multiflorum by synchrotron techniques. Sci Total Environ 621:772–781CrossRefGoogle Scholar
  37. Zhou F, Wang J, Yang N (2015) Growth responses, antioxidant enzyme activities and lead accumulation of Sophora japonica, and Platycladus orientalis, seedlings under Pb and water stress. Plant Growth Regul 75(1):383–389CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Yanhua Li
    • 1
  • Yuli Qin
    • 1
  • Weihong Xu
    • 1
    Email author
  • Yourong Chai
    • 2
    Email author
  • Tao Li
    • 1
  • Chunlai Zhang
    • 1
  • Mei Yang
    • 1
  • Zhangmi He
    • 1
  • Deyu Feng
    • 1
  1. 1.College of Resources and Environmental SciencesSouthwest UniversityChongqingPeople’s Republic of China
  2. 2.College of Agronomy and BiotechnologySouthwest UniversityChongqingPeople’s Republic of China

Personalised recommendations