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The role of root anatomy, organic acids and iron plaque on mercury accumulation in rice

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Abstract

Background and aims

Rice contaminated by mercury [Hg, especially methylmercury (MeHg)] has given rise to great concern in recent years. This study investigated variations in ecophysiological features (anatomy, organic acid secretions, Fe plaque formation) of rice roots and their effects on the uptake and accumulation of total mercury (THg) and MeHg by rice plants.

Methods

The development of apoplastic barriers in roots of four rice cultivars was observed by a hydroponic experiment while the concentrations of five organic acids, Fe and THg in Fe plaque were determined using a rhizobag trial with different Hg treatments.

Results

Cultivars with low Hg accumulation tended to develop strong apoplastic barriers in endodermis, secrete less organic acids and form more Fe plaque on root surfaces and in rhizosphere. Fe concentrations were positively correlated with THg concentrations in rhizosphere’s Fe plaque (R2 = 0.60, P < 0.01), whereas the latter was negatively correlated with bioavailable Hg concentrations in rhizosphere (R2 = 0.40, P < 0.01).

Conclusions

Organic acids and Fe plaque formation of rice roots play important roles in Hg uptake and accumulation. The development of apoplastic barriers in root restricts Hg uptake but the significance of suberin deposition on Hg uptake needs further investigations.

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References

  • Aulakh MS, Wassmann R, Bueno C, Kreuzwieser J, Rennenberg H (2001) Characterization of root exudates at different growth stages of ten rice (Oryza sativa L.) cultivars. Plant Biol 3:139–148

    Article  CAS  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    Article  CAS  PubMed  Google Scholar 

  • Bloom NS, Preus E, Katon J, Hiltner M (2003) Selective extractions to assess the biogeochemically relevant fractionation of inorganic mercury in sediments and soils. Anal Chim Acta 479:233–248

    Article  CAS  Google Scholar 

  • Carrasco-Gil S, Alvarez-Fernandez A, Sobrino-Plata J, Millan R, Carpena-Ruiz RO, Leduc DL, Andrews JC, Abadia J, Hernandez LE (2011) Complexation of Hg with phytochelatins is important for plant Hg tolerance. Plant Cell Environ 34:778–791

    Article  CAS  PubMed  Google Scholar 

  • Carrasco-Gil S, Siebner H, LeDuc DL, Webb SM, Millan R, Andrews JC, Hernandez LE (2013) Mercury localization and speciation in plants grown hydroponically or in a natural environment. Environ Sci Technol 47:3082–3090

    CAS  PubMed  Google Scholar 

  • Chen Z, Zhu YG, Liu WJ, Meharg AA (2005) Direct evidence showing the effect of root surface iron plaque on arsenite and arsenate uptake into rice (Oryza sativa) roots. New Phytol 165:91–97

    Article  CAS  PubMed  Google Scholar 

  • Chen XP, Kong WD, He JZ, Liu WJ, Smith SE, Smith FA, Zhu YG (2008) Do water regimes affect iron-plaque formation and microbial communities in the rhizosphere of paddy rice? J Plant Nutr Soil Sci 171:193–199

    Article  CAS  Google Scholar 

  • Cheng H, Liu Y, Tam NFY, Wang X, Li SY, Chen GZ, Ye ZH (2010) The role of radial oxygen loss and root anatomy on zinc uptake and tolerance in mangrove seedlings. Environ Pollut 158:1189–1196

    Article  CAS  PubMed  Google Scholar 

  • Cheng H, Wang MY, Wong MH, Ye ZH (2014) Does radial oxygen loss and iron plaque formation on roots alter Cd and Pb uptake and distribution in rice plant tissues? Plant Soil 375:137–148

    Article  CAS  Google Scholar 

  • Cieslinski G, Van Rees KCJ, Szmigielska AM, Krishnamurti GSR, Huang PM (1998) Low-molecular-weight organic acids in rhizosphere soils of durum wheat and their effect on cadmium bioaccumulation. Plant Soil 203:109–117

    Article  CAS  Google Scholar 

  • DalCorso G, Manara A, Furini A (2013) An overview of heavy metal challenge in plants: from roots to shoots. Metallomics 5:1117–1132

    Article  CAS  PubMed  Google Scholar 

  • Feng XB, Li P, Qiu GL, Wang S, Li GH, Shang LH, Meng B, Jiang HM, Bai WY, Li ZG, Fu XW (2008) Human exposure to methylmercury through rice intake in mercury mining areas, Guizhou Province, China. Environ Sci Technol 42:326–332

    Article  CAS  PubMed  Google Scholar 

  • Fleming EJ, Mack EE, Green PG, Nelson DC (2006) Mercury methylation from unexpected sources: molybdate-inhibited freshwater sediments and an iron-reducing bacterium. Appl Environ Microbiol 72:457–464

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Guo TR, Zhang GP, Zhou MX, Wu FB, Chen JX (2007) Influence of aluminum and cadmium stresses on mineral nutrition and root exudates in two barley cultivars. Pedosphere 17:505–512

    Article  CAS  Google Scholar 

  • Hansel CM, Fendorf S, Sutton S, Newville M (2001) Characterization of Fe plaque and associated metals on the roots of mine-waste impacted aquatic plants. Environ Sci Technol 35:3863–3868

    Article  CAS  PubMed  Google Scholar 

  • Hartmann A, Schmid M, van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257

    Article  CAS  Google Scholar 

  • Heikens A, Panaullah GM, Meharg AA (2007) Arsenic behaviour from groundwater and soil to crops: impacts on agriculture and food safety. Rev Environ Contam Toxicol 189:43–87

    CAS  PubMed  Google Scholar 

  • ISO (2005) 10390 Soil quality, determination of pH. International Organization for Standardization, Geneve

  • Jiang GB, Shi JB, Feng XB (2006) Mercury pollution in China. Environ Sci Technol 40:3672–3678

    Article  CAS  Google Scholar 

  • Kerin EJ, Gilmour CC, Roden E, Suzuki MT, Coates JD, Mason RP (2006) Mercury methylation by dissimilatory iron-reducing bacteria. Appl Environ Microbiol 72:7919–7921

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kotula L, Ranathunge K, Schreiber L, Steudle E (2009) Functional and chemical comparison of apoplastic barriers to radial oxygen loss in roots of rice (Oryza sativa L.) grown in aerated or deoxygenated solution. J Exp Bot 60:2155–2167

    Article  CAS  PubMed  Google Scholar 

  • Li B, Shi JB, Wang X, Meng M, Huang L, Qi XL, He B, Ye ZH (2013) Variations and constancy of mercury and methylmercury accumulation in rice grown at contaminated paddy field sites in three provinces of China. Environ Pollut 181:91–97

    Article  CAS  PubMed  Google Scholar 

  • Liang L, Horvat M, Cernichiari E, Gelein B, Balogh S (1996) Simple solvent extraction technique for elimination of matrix interferences in the determination of methylmercury in environmental and biological samples by ethylation-gas chromatography-cold vapor atomic fluorescence spectrometry. Talanta 43:1883–1888

    Article  CAS  PubMed  Google Scholar 

  • Liu JG, Qian M, Cai GL, Zhu QS, 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  PubMed  Google Scholar 

  • Lux A, Sottnikova A, Opatrna J, Greger M (2004) Differences in structure of adventitious roots in Salix clones with contrasting characteristics of cadmium accumulation and sensitivity. Physiol Plant 120:537–545

    Article  CAS  PubMed  Google Scholar 

  • Lux A, Martinka M, Vaculik M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37

    Article  CAS  PubMed  Google Scholar 

  • Ma JF, Zheng SJ, Matsumoto H (1997) Specific secretion of citric acid induced by Al stress in Cassia tora L. Plant Cell Physiol 38:1019–1025

    Article  CAS  Google Scholar 

  • Martinka M, Lux A (2004) Response of roots of three populations of Silene dioica to cadmium treatment. Biologia 59:185–189

    CAS  Google Scholar 

  • Mendoza-Cozatl 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  PubMed Central  CAS  PubMed  Google Scholar 

  • Mergler D, Anderson HA, Chan LHM, Mahaffey KR, Murray M, Sakamoto M, Stern AH (2007) Methylmercury exposure and health effects in humans: a worldwide concern. Ambio 36:3–11

    Article  CAS  PubMed  Google Scholar 

  • Otte M, Rozema J, Koster L, Haarsma M, Broekman R (1989) Iron plaque on roots of Aster tripolium L.: interaction with zinc uptake. New Phytol 111:309–317

  • Peng XY, Liu FJ, Wang WX, Ye ZH (2012) Reducing total mercury and methylmercury accumulation in rice grains through water management and deliberate selection of rice cultivars. Environ Pollut 162:202–208

    Article  CAS  PubMed  Google Scholar 

  • Rothenberg SE, Feng XB, Zhou WJ, Tu M, Jin BW, You JM (2012) Environment and genotype controls on mercury accumulation in rice (Oryza sativa L.) cultivated along a contamination gradient in Guizhou, China. Sci Total Environ 426:272–280

    Article  CAS  PubMed  Google Scholar 

  • Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoto H (2004) A wheat gene encoding an aluminum-activated malate transporter. Plant J 37:645–653

    Article  CAS  PubMed  Google Scholar 

  • Schreiber L, Hartmann K, Skrabs M, Zeier J (1999) Apoplastic barriers in roots: chemical composition of endodermal and hypodermal cell walls. J Exp Bot 50:1267–1280

    CAS  Google Scholar 

  • Schreiber L, Franke R, Hartmann KD, Ranathunge K, Steudle E (2005) The chemical composition of suberin in apoplastic barriers affects radial hydraulic conductivity differently in the roots of rice (Oryza sativa L. cv. IR64) and corn (Zea mays L. cv. Helix). J Exp Bot 56:1427–1436

    Article  CAS  PubMed  Google Scholar 

  • Shen H, He LF, Sasaki T, Yamamoto Y, Zheng SJ, Ligaba A, Yan XL, Ahn SJ, Yamaguchi M, Sasakawa H, Matsumoto H (2005) Citrate secretion coupled with the modulation of soybean root tip under aluminum stress. Up-regulation of transcription, translation, and threonine-oriented phosphorylation of plasma membrane H+-ATPase. Plant Physiol 138:287–296

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Somenahally AC, Hollister EB, Loeppert RH, Yan WG, Gentry TJ (2011a) Microbial communities in rice rhizosphere altered by intermittent and continuous flooding in fields with long-term arsenic application. Soil Biol Biochem 43:1220–1228

    Article  CAS  Google Scholar 

  • Somenahally AC, Hollister EB, Yan W, Gentry TJ, Loeppert RH (2011b) Water management impacts on arsenic speciation and iron-reducing bacteria in contrasting rice-rhizosphere compartments. Environ Sci Technol 45:8328–8335

    Article  CAS  PubMed  Google Scholar 

  • Taylor GJ, Crowder AA, Rodden R (1984) Formation and morphology of an iron plaque on the roots of Typha latifolia L. grown in solution culture. Am J Bot 71:666–675

    Article  CAS  Google Scholar 

  • Ullrich SM, Tanton TW, Abdrashitova SA (2001) Mercury in the aquatic environment: a review of factors affecting methylation. Crit Rev Environ Sci Technol 31:241–293

    Article  CAS  Google Scholar 

  • Vaculik M, Lux A, Luxova M, Tanimoto E, Lichtscheidl I (2009) Silicon mitigates cadmium inhibitory effects in young maize plants. Environ Exp Bot 67:52–58

    Article  CAS  Google Scholar 

  • Wang JX, Feng XB, Anderson CWN, Wang H, Zheng LR, Hu TD (2012) Implications of mercury speciation in thiosulfate treated plants. Environ Sci Technol 46:5361–5368

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Li B, Tam NFY, Huang L, Qi XL, Wang HB, Ye ZH, Meng M, Shi JB (2014a) Radial oxygen loss has different effects on the accumulation of total mercury and methylmercury in rice. Plant Soil 385:343–355

    Article  CAS  Google Scholar 

  • Wang X, Tam NFY, Fu S, Ametkhan A, Ouyang Y, Ye ZH (2014b) Selenium addition alters mercury uptake, bioavailability in the rhizosphere and root anatomy of rice (Oryza sativa). Ann Bot-London 114:271–278

    Article  CAS  Google Scholar 

  • Weber KA, Achenbach LA, Coates JD (2006) Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol 4:752–764

    Article  CAS  PubMed  Google Scholar 

  • Weiss JV, Emerson D, Backer SM, Megonigal JP (2003) Enumeration of Fe(II)-oxidizing and Fe(III)-reducing bacteria in the root zone of wetland plants: Implications for a rhizosphere iron cycle. Biogeochemistry 64:77–96

    Article  CAS  Google Scholar 

  • Xu WH, Liu H, Ma QF, Xiong ZT (2007) Root exudates, rhizosphere Zn fractions, and Zn accumulation of ryegrass at different soil Zn levels. Pedosphere 17:389–396

    Article  CAS  Google Scholar 

  • Yang YY, Jung JY, Song WY, Suh HS, Lee Y (2000) Identification of rice varieties with high tolerance or sensitivity to lead and characterization of the mechanism of tolerance. Plant Physiol 124:1019–1026

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang JL, Zhang L, Li YY, You JF, Wu P, Zheng SJ (2006) Citrate transporters play a critical role in aluminium-stimulated citrate efflux in rice bean (Vigna umbellata) roots. Ann Bot-London 97:579–584

    Article  CAS  Google Scholar 

  • Yang JX, Liu Y, Ye ZH (2012) Root-induced changes of pH, Eh, Fe(II) and fractions of Pb and Zn in rhizosphere soils of four wetland plants with different radial oxygen losses. Pedosphere 22:518–527

    Article  CAS  Google Scholar 

  • Yang JX, Tam NFY, Ye ZH (2014) Root porosity, radial oxygen loss and iron plaque on roots of wetland plants in relation to zinc tolerance and accumulation. Plant Soil 374:815–828

    Article  CAS  Google Scholar 

  • Ye ZH, Baker AJM, Wong MH, Willis AJ (1997) Copper and nickel uptake, accumulation and tolerance in Typha latifolia with and without iron plaque on the root surface. New Phytol 136:481–488

    Article  CAS  Google Scholar 

  • Zeng FR, Chen S, Miao Y, Wu FB, Zhang GP (2008) Changes of organic acid exudation and rhizosphere pH in rice plants under chromium stress. Environ Pollut 155:284–289

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Feng XB, Larssen T, Qiu GL, Vogt RD (2010) In inland China, rice, rather than fish, is the major pathway for methylmercury exposure. Environ Health Perspect 118:1183–1188

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhu XF, Zheng C, Hu YT, Jiang T, Liu Y, Dong NY, Yang JL, Zheng SJ (2011) Cadmium-induced oxalate secretion from root apex is associated with cadmium exclusion and resistance in Lycopersicon esulentum. Plant Cell Environ 34:1055–1064

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was funded by the National Natural Science Foundation of China (30770417), the National ‘863’ project of China (2012AA061510, 2013AA062609), Guangdong Provincial Key Laboratory of Plant Resources, and the Strategic Research Grant of the City University of Hong Kong (Project No.: 7004206). We thank Prof. A.J.M. Baker (The Universities of Melbourne and Queensland, Australia) for help in the initial preparation and improvement of this paper.

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Authors and Affiliations

  1. State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, 510006, People’s Republic of China

    Xun Wang, Huaidong He & Zhihong Ye

  2. Department of Biology and Chemistry, City University of Hong Kong, Kowloon, Hong Kong, SAR, People’s Republic of China

    Nora Fung-Yee Tam

  3. State Key Laboratory in Marine Pollution, City University of Hong Kong, Kowloon, Hong Kong, SAR, People’s Republic of China

    Nora Fung-Yee Tam

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  1. Xun Wang
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  2. Nora Fung-Yee Tam
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  3. Huaidong He
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  4. Zhihong Ye
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Correspondence to Zhihong Ye.

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Responsible Editor: Henk Schat.

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Wang, X., Tam, N.FY., He, H. et al. The role of root anatomy, organic acids and iron plaque on mercury accumulation in rice. Plant Soil 394, 301–313 (2015). https://doi.org/10.1007/s11104-015-2537-y

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