Skip to main content
SpringerLink
Log in

Low root/shoot (R/S) biomass ratio can be an indicator of low cadmium accumulation in the shoot of Chinese flowering cabbage (Brassica campestris L. ssp. chinensis var. utilis Tsen et Lee) cultivars

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Chinese flowering cabbage is a commonly consumed vegetable that accumulates Cd easily from Cd-contaminated soils. Cultivations of low-Cd cultivars are promising strategies for food safety, but low-Cd-accumulating mechanisms are not fully elucidated. To address this issue, 37 cultivars were screened to identify high- and low-Cd cultivars upon exposure to sewage-irrigated garden soil pretreated with different Cd concentrations (1.81, 2.90, and 3.70 mg kg−1dry soil). The results showed that shoot Cd concentrations differed among the cultivars by maximum degrees of 2.67-, 3.71-, and 3.00-fold under control and treatments, respectively. Soil-pot trial and hydroponic trial found no significant difference in Cd and Ca mobilization, uptake, and transport ability by root per weight between high- and low-Cd cultivars. Interestingly, a stable R/S ratio difference among cultivars (p < 0.01) was observed, and the cultivar variation of Cd accumulation in shoots was mainly dependent on their R/S ratios. R/S ratio was also statistically positively associated with Cd and Ca accumulation in high- and low-Cd cultivars (p < 0.05), both in soil and hydroponics culture. This was mainly due to the lower root biomass of low-Cd cultivars resulted in lower total release of root exudates, lower total Cd and Ca mobilization in rhizosphere soil, and lower total Cd and Ca uptake and transport. The higher shoot biomass of low-Cd cultivars also has dilution effects on Cd concentration in shoot. Overall, low R/S ratio may be regarded as a direct and efficient indicator of low Cd accumulation in the shoot of Chinese flowering cabbage. These findings provided the possibilities to screening low-Cd cultivars using their R/S ratio.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allard V, Martre P, Gouis JL (2013) Genetic variability in biomass allocation to roots in wheat is mainly related to crop tillering dynamics and nitrogen status. Eur J Agron 46:68–76

    Article  CAS  Google Scholar 

  • Bian R, Joseph S, Cui L, Pan G, Li L, Liu X, Zhang A, Rutlidge H, Wong S, Chia C (2014) A three-year experiment confirms continuous immobilization of cadmium and lead in contaminated paddy field with biochar amendment. J Hazard Mater 272:121–128

    Article  CAS  Google Scholar 

  • Cauwet G (1994) HTCO method for dissolved organic carbon analysis in seawater: influence of catalyst on blank estimation. Mar Chem 47:55–64

    Article  CAS  Google Scholar 

  • Chen B, Zhu YG (2006) Humic acids increase the phytoavailability of Cd and Pb to wheat plants cultivated in freshly spiked, contaminated soil (7 pp). J Soils Sediments 6:236–242

    Article  CAS  Google Scholar 

  • Chen Y, Shen Z, Li X (2004) The use of vetiver grass (Vetiveria zizanioides) in the phytoremediation of soils contaminated with heavy metals. Appl Geochem 19:1553–1565

    Article  CAS  Google Scholar 

  • Chen F, Dong J, Wang F, Wu F, Zhang G, Li G, Chen Z, Chen J, Wei K (2007) Identification of barley genotypes with low grain Cd accumulation and its interaction with four microelements. Chemosphere 67:2082–2088

    Article  CAS  Google Scholar 

  • Cheng L, Bucciarelli B, Shen J, Allan D, Vance CP (2011) Update on lupin cluster roots. Update on white lupin cluster root acclimation to phosphorus deficiency. Plant Physiol 156:1025–1032

    Article  CAS  Google Scholar 

  • Chiang PN, Wang MK, Chiu CY, Chou SY (2006) Effects of cadmium amendments on low-molecular-weight organic acid exudates in rhizosphere soils of tobacco and sunflower. Environ Toxicol 21:479–488

    Article  CAS  Google Scholar 

  • Clemens S, Palmgren MG, Krämer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7:309–315

    Article  CAS  Google Scholar 

  • Dahlin AS, Eriksson J, Campbell CD, Öborn I (2016) Soil amendment affects Cd uptake by wheat—are we underestimating the risks from chloride inputs? Sci Total Environ 554-555:349–357

    Article  CAS  Google Scholar 

  • Dai KJ, Shen YX, Zhou WJ, Deng Y, Liu WY (2005) Mechanism of Pinus yunnanensis seedlings root response to phosphorus deficiency under controlled conditions. Acta Ecol Sin 25:2423–2426

    CAS  Google Scholar 

  • Dar MI, Green ID, Naikoo MI, Khan FA, Ansari AA, Lone MI (2017) Assessment of biotransfer and bioaccumulation of cadmium, lead and zinc from fly ash amended soil in mustard-aphid-beetle food chain. Sci Total Environ 584:1221-1229

  • Dessureaultrompré J, Luster J, Schulin R, Tercierwaeber ML, Nowack B (2010) Decrease of labile Zn and Cd in the rhizosphere of hyperaccumulating Thlaspi caerulescens with time. Environ Pollut 158:1955–1962

    Article  Google Scholar 

  • Dunbar KR, Mclaughlin MJ, Reid RJ (2003) The uptake and partitioning of cadmium in two cultivars of potato (Solanum tuberosum L.). J Exp Bot 54:349–354

    Article  CAS  Google Scholar 

  • Greger M, Landberg T (2008) Role of rhizosphere mechanisms in Cd uptake by various wheat cultivars. Plant Soil 312:195–205

    Article  CAS  Google Scholar 

  • Guo SH, Hu N, Li QS, Yang P, Wang LL, Xu ZM, Chen HJ, He BY, Zeng EY (2018) Response of edible amaranth cultivar to salt stress led to Cd mobilization in rhizosphere soil: a metabolomic analysis ☆. Environ Pollut 241:422–431

    Article  CAS  Google Scholar 

  • Harrison HC (1986) Response of lettuce cultivars to sludge-amended soils and bed types. Commun Soil Sci Plant Anal 17:159–172

    Article  Google Scholar 

  • He BY, Ling L, Zhang LY, Li MR, Li QS, Mei XQ, Li H, Tan L (2015) Cultivar-specific differences in heavy metal (Cd, Cr, Cu, Pb, and Zn) concentrations in water spinach ( Ipomoea aquatic ‘Forsk’) grown on metal-contaminated soil. Plant Soil 386:251–262

    Article  CAS  Google Scholar 

  • Hu L, Mcbride MB, Cheng H, Wu J, Shi J, Xu J, Wu L (2011) Root-induced changes to cadmium speciation in the rhizosphere of two rice ( Oryza sativa L.) genotypes. Environ Res 111:356–361

    Article  CAS  Google Scholar 

  • Huang B, Xin J, Dai H, Liu A, Zhou W, Yi Y, Liao K (2015) Root morphological responses of three hot pepper cultivars to Cd exposure and their correlations with Cd accumulation. Environ Sci Pollut Res 22:1151–1159

    Article  CAS  Google Scholar 

  • Irigoyen JJ, Einerich DW, Sánchez-Díaz M (1992) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa ( Medicago sativd ) plants. Physiol Plant 84:55–60

    Article  CAS  Google Scholar 

  • Kramer U, Smith RD, Wenzel WW, Raskin I, Salt DE (1997) The role of metal transport and tolerance in nickel Hyperaccumulation by Thlaspi goesingense Halacsy. Plant Physiol 115:1641–1650

    Article  CAS  Google Scholar 

  • Kubo K, Watanabe Y, Matsunaka H, Seki M, Fujita M, Kawada N, Hatta K, Nakajima T (2011) Differences in cadmium accumulation and root morphology in seedlings of Japanese wheat varieties with distinctive grain cadmium concentration. Plant Prod Sci 14:148–155

    Article  CAS  Google Scholar 

  • Lambers H, Shane M, Cramer M, Pearse S, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713

    Article  Google Scholar 

  • Li LZ, Chen T, Peijnenburg WJGM, Luo YM (2017) Characteristics of cadmium uptake and membrane transport in roots of intact wheat ( Triticum aestivum L.) seedlings. Environ Pollut 221:351–358

    Article  CAS  Google Scholar 

  • Liao M, Xie XM, Ma AL, Peng Y, Xu JM, Tang CX, He JZ (2010) Different influences of cadmium on soil microbial activity and structure with Chinese cabbage cultivated and non-cultivated. J Soils Sediments 10:818–826

    Article  CAS  Google Scholar 

  • Lin X, Mou R, Cao Z, Xu P, Wu X, Zhu Z, Chen M (2016) Characterization of cadmium-resistant bacteria and their potential for reducing accumulation of cadmium in rice grains. Sci Total Environ 569–570:97–104

    Article  Google Scholar 

  • Liu J, Qian M, Cai G, Zhu Q, Wong MH (2007) Variations between rice cultivars in root secretion of organic acids and the relationship with plant cadmium uptake. Environ Geochem Health 29:189–195

    Article  CAS  Google Scholar 

  • Liu W, Zhou Q, Jing A, Sun Y, Rui L (2010) Variations in cadmium accumulation among Chinese cabbage cultivars and screening for Cd-safe cultivars. J Hazard Mater 173:737–743

    Article  CAS  Google Scholar 

  • Liu J, Duan CQ, Zhang XH, Zhu YN, Hu C (2011) Characteristics of chromium(III) uptake in hyperaccumulator Leersia hexandra Swartz. Environ Exp Bot 74:122–126

    Article  CAS  Google Scholar 

  • Lu K (1999) Analytical methods of agricultural chemistry in soil. Agricultural science and Technology Press of China. Beijing, China

    Google Scholar 

  • Lu Z, Zhang Z, Su Y, Liu C, Shi G (2013) Cultivar variation in morphological response of peanut roots to cadmium stress and its relation to cadmium accumulation. Ecotoxicol Environ Saf 91:147–155

    Article  CAS  Google Scholar 

  • Mei X, Li S, Li Q, Yang Y, Luo X, He B, Li H, Xu Z (2014) Sodium chloride salinity reduces Cd uptake by edible amaranth (Amaranthus mangostanus L.) via competition for Ca channels. Ecotoxicol Environ Saf 105:59–64

    Article  CAS  Google Scholar 

  • Mendoza-Cózatl DG, Jobe TO, Hauser F, Schroeder JI (2011) Long-distance transport, vacuolar sequestration, tolerance, and transcriptional responses induced by cadmium and arsenic. Curr Opin Plant Biol 14:554–562

    Article  Google Scholar 

  • Qiu Q, Wang Y, Yang Z, Xin J, Yuan J, Wang J, Xin G (2011a) Responses of different Chinese flowering cabbage (Brassica parachinensis L.) cultivars to cadmium and lead stress: screening for Cd + Pb pollution-safe cultivars. CLEAN - Soil Air Water 39:925–932

    Article  CAS  Google Scholar 

  • Qiu Q, Wang Y, Yang Z, Yuan J (2011b) Effects of phosphorus supplied in soil on subcellular distribution and chemical forms of cadmium in two Chinese flowering cabbage (Brassica parachinensis L.) cultivars differing in cadmium accumulation. Food Chem Toxicol 49:2260–2267

    Article  CAS  Google Scholar 

  • Rosen H (1957) A modified ninhydrin colorimetric analysis for amino acids. Arch Biochem Biophys 67:10–15

    Article  CAS  Google Scholar 

  • Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in Rice. Plant Cell 24:2155–2167

    Article  CAS  Google Scholar 

  • Selvam A, Wong WC (2009) Cadmium uptake potential of Brassica napus cocropped with Brassica parachinensis and Zea mays. J Hazard Mater 167:170–178

    Article  CAS  Google Scholar 

  • Sheng RL, Tong HY, Chai C, Huang SZ (2010) Effect of NaCl stress on seedling growth of different cultivars of Stevia rebaudiana. J Plant Resour Environ 19:60–67 (in Chinese)

    Google Scholar 

  • Solti A, Sárvári E, Tóth B, Basa B, Lévai L, Fodor F (2011) Cd affects the translocation of some metals either Fe-like or Ca-like way in poplar. Plant Physiol Biochem 49:494–498

    Article  CAS  Google Scholar 

  • ​Stritsis C, Steingrobe B, Claassen N (2012) Shoot cadmium concentration of soil‐grown plants as related to their root properties.J Plant Nutr Soil Sci 175:456–465

  • Sun Y, Zhou Q, Lin W, Liu W (2009) Cadmium tolerance and accumulation characteristics of Bidens pilosa L. as a potential Cd-hyperaccumulator. J Hazard Mater 161:808–814

    Article  CAS  Google Scholar 

  • Sun J, Ma B, Lu X (2017) Grazing enhances soil nutrient effects: trade-offs between aboveground and belowground biomass in alpine grasslands of the Tibetan plateau. Land Degrad Dev 29:770

    Google Scholar 

  • Ueno D, Milner MJ, Yamaji N, Yokosho K, Koyama E, Clemencia ZM, Kaskie M, Ebbs S, Kochian LV, Ma JF (2011) Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Plant J 66:852–862

    Article  CAS  Google Scholar 

  • 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 60:2677–2688

    Article  CAS  Google Scholar 

  • Veresoglou SD, Menexes G, Rillig MC (2012) Do arbuscular mycorrhizal fungi affect the allometric partition of host plant biomass to shoots and roots? A meta-analysis of studies from 1990 to 2010. Mycorrhiza 22:227–235

    Article  Google Scholar 

  • Vymazal J (2016) Concentration is not enough to evaluate accumulation of heavy metals and nutrients in plants. Sci Total Environ 544:495–498

    Article  CAS  Google Scholar 

  • Walk TC, Jaramillo R, Lynch JP (2006) Architectural tradeoffs between adventitious and basal roots for phosphorus acquisition. Plant Soil 279:347–366

    Article  CAS  Google Scholar 

  • Wang J, Fang W, Yang Z, Yuan J, Zhu Y, Yu H (2007) Inter- and intraspecific variations of cadmium accumulation of 13 leafy vegetable species in a greenhouse experiment. J Agric Food Chem 55:9118–9123

    Article  CAS  Google Scholar 

  • Wang J, Yuan J, Yang Z, Huang B, Zhou Y, Xin J, Gong Y, Yu H (2009) Variation in cadmium accumulation among 30 cultivars and cadmium subcellular distribution in 2 selected cultivars of water spinach (Ipomoea aquatica Forsk.). J Agric Food Chem 57:8942–8949

    Article  CAS  Google Scholar 

  • Wang MY, Chen AK, Wong MH, Qiu RL, Cheng H, Ye ZH (2011) Cadmium accumulation in and tolerance of rice ( Oryza sativa L.) varieties with different rates of radial oxygen loss. Environ Pollut 159:1730–1736

    Article  CAS  Google Scholar 

  • Wei S, Zhou Q (2008) Screen of Chinese weed species for cadmium tolerance and accumulation characteristics. Int J Phytoremediation 10:584–597

    Article  CAS  Google Scholar 

  • Wei S, Zhou Q, Wang X (2005) Identification of weed plants excluding the uptake of heavy metals. Environ Int 31:829–834

    Article  Google Scholar 

  • Welch RM, Hart JJ, Norvell WA, Sullivan LA, Kochian LV (1999) Effects of nutrient solution zinc activity on net uptake, translocation, and root export of cadmium and zinc by separated sections of intact durum wheat (Triticum turgidum L. var durum) seedling roots. Plant Soil 208:243–250

    Article  CAS  Google Scholar 

  • Werner T, Nehnevajova E, Köllmer I, Novák O, Strnad M, Krämer U, Schmülling T (2010) Root-specific reduction of cytokinin causes enhanced root growth, drought tolerance, and leaf mineral enrichment in Arabidopsis and tobacco. Plant Cell 22:3905–3920

    Article  Google Scholar 

  • Wu J, Yuan YX, Zhang XW, Zhao J, Song X, Li Y, Li X, Sun R, Koornneef M, Aarts MGM (2008) Mapping QTLs for mineral accumulation and shoot dry biomass under different Zn nutritional conditions in Chinese cabbage ( Brassica rapa L. ssp. pekinensis). Plant Soil 310:25–40

    Article  CAS  Google Scholar 

  • Xia S, Deng R, Zheng Z, Liu C, Shi G (2016) Variations in the accumulation and translocation of cadmium among pak choi cultivars as related to root morphology. Environ Sci Pollut Res 23:9832–9842

    Article  CAS  Google Scholar 

  • Xin J, Huang B, Liu A, Zhou W, Liao K (2013) Identification of hot pepper cultivars containing low Cd levels after growing on contaminated soil: uptake and redistribution to the edible plant parts. Plant Soil 373:415–425

    Article  CAS  Google Scholar 

  • Xin J, Huang B, Dai H (2015a) Difference in root-to-shoot Cd translocation and characterization of Cd accumulation during fruit development in two Capsicum annuum cultivars. Plant Soil 394:287–300

    Article  CAS  Google Scholar 

  • Xin J, Huang B, Dai H, Zhou W, Yi Y, Peng L (2015b) Roles of rhizosphere and root-derived organic acids in Cd accumulation by two hot pepper cultivars. Environ Sci Pollut Res 22:6254–6261

    Article  CAS  Google Scholar 

  • Xu ZM, Li QS, Yang P, Ye HJ, Chen ZS, Guo SH, Wang LL, He BY, Zeng EY (2017) Impact of osmoregulation on the differences in Cd accumulation between two contrasting edible amaranth cultivars grown on Cd-polluted saline soils. Environ Pollut 224:89–97

    Article  CAS  Google Scholar 

  • Xu ZM, Tan XQ, Mei XQ, Li QS, Zhou C, Wang LL, Ye HJ, Yang P (2018) Low-cd tomato cultivars ( Solanum lycopersicum L.) screened in non-saline soils also accumulated low Cd, Zn, and Cu in heavy metal-polluted saline soils. Environ Sci Pollut Res 25:27439–27450

  • Yanai J, Zhao FJ, Mcgrath SP, Kosaki T (2006) Effect of soil characteristics on Cd uptake by the hyperaccumulator Thlaspi caerulescens. Environ Pollut 139:167–175

    Article  CAS  Google Scholar 

  • Yang Y, Dou Y, An S, Zhu Z (2018) Abiotic and biotic factors modulate plant biomass and root/shoot (R/S) ratios in grassland on the Loess plateau, China. Sci Total Environ 636:621–631

    Article  CAS  Google Scholar 

  • Ye J, Yan C, Liu J, Lu H, Liu T, Song Z (2012) Effects of silicon on the distribution of cadmium compartmentation in root tips of Kandelia obovata (S., L.) Yong. J Food Agric Environ 162:369–373

    CAS  Google Scholar 

  • Yoon J, Cao X, Zhou Q, Ma LQ (2006) Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci Total Environ 368:456–464

    Article  CAS  Google Scholar 

  • Zeng F, Mao Y, Cheng W, Wu F, Zhang G (2008) Genotypic and environmental variation in chromium, cadmium and lead concentrations in rice. Environ Pollut 153:309–314

    Article  CAS  Google Scholar 

  • Zhou Q, Guo JJ, He CT, Shen C, Huang YY, Chen JX, Guo JH, Yuan J, Yang Z (2016) Comparative transcriptome analysis between low- and high-cadmium-accumulating genotypes of pakchoi (Brassica chinensis L.) in response to cadmium stress. Environ Sci Technol 50:6485–6494

    Article  CAS  Google Scholar 

  • Zhu Y, Yu H, Wang J, Fang W, Jiangang Yuan A, Yang Z (2007) Heavy metal accumulations of 24 asparagus bean cultivars grown in soil contaminated with Cd alone and with multiple metals (Cd, Pb, and Zn). J Agric Food Chem 55:1045–1052

    Article  CAS  Google Scholar 

  • Zong LG, Sun JK, Shen QY, Zhang XP (2007) Impacts of cadmium and lead pollution in soil on leaf vegetables growth and toxic-symptoms. Asian J Ecotoxicol 2:63-68 (in Chinese)

Download references

Acknowledgments

The authors are grateful to the National Key Research Project of China (No.2017YFD0801305), the National Natural Science Foundation of China (No. 41371321), and the Department of Science and Technology of Guangdong Province, China (No. 2017A010105005) for their financial support.

Author information

Authors and Affiliations

  1. School of Environment, Key Laboratory of Environmental Pollution and Health of Guangdong Province, Jinan University, Guangzhou, 510632, China

    Zhi-Min Xu, Xiu-Qin Mei, Ling Tan, Qu-Sheng Li, Li-Li Wang, Bao-Yan He, Shi-Hong Guo, Chu Zhou & Han-Jie Ye

  2. Department of Ecology, Jinan University, Guangzhou, 510632, China

    Zhi-Min Xu

Authors
  1. Zhi-Min Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiu-Qin Mei
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ling Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qu-Sheng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Li-Li Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bao-Yan He
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shi-Hong Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Chu Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Han-Jie Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Qu-Sheng Li.

Additional information

Responsible editor: Yi-ping Chen

Electronic supplementary material

ESM 1

(DOC 4463 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, ZM., Mei, XQ., Tan, L. et al. Low root/shoot (R/S) biomass ratio can be an indicator of low cadmium accumulation in the shoot of Chinese flowering cabbage (Brassica campestris L. ssp. chinensis var. utilis Tsen et Lee) cultivars. Environ Sci Pollut Res 25, 36328–36340 (2018). https://doi.org/10.1007/s11356-018-3566-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-018-3566-x

Keywords

Search

Navigation