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Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Root uptake and xylem transport of cadmium in wheat and triticale as affected by exogenous amino acids

K. Khodamoradi A , A. H. Khoshgoftarmanesh A C and S. A. M. Mirmohammady Maibody B
+ Author Affiliations
- Author Affiliations

A Department of Soil Science, College of Agriculture, Isfahan University of Technology, Isfahan 84156-83111, Iran.

B Department of Agronomy and Plant Breeding, College of Agriculture, Isfahan University of Technology, Isfahan 84156-83111, Iran.

C Corresponding author. Email: amirhkhosh@cc.iut.ac.ir

Crop and Pasture Science 68(5) 415-420 https://doi.org/10.1071/CP17061
Submitted: 12 February 2017  Accepted: 28 May 2017   Published: 14 June 2017

Abstract

Organic acids exuded from plant roots significantly modify uptake and long-distance translocation of metals. Little is known about the effect of amino acids on metal ion uptake by plant roots. The present study investigated the effects of exogenous amino acids (histidine and glycine) in a nutrient solution on root uptake and xylem sap transport of cadmium (Cd) in triticale (× Triticosecale cv. Elinor) and bread wheat (Triticum aestivum L. cv. Back Cross Rushan). Plant seedlings were grown in a Cd-free modified Hoagland nutrient solution to which 1 µm Cd was added with either 50 µm histidine or 50 µm glycine or without amino acids at 4 weeks after germination. A control treatment consisted of a nutrient solution free of Cd and amino acids. In bread wheat, addition of histidine to the Cd-containing nutrient solution resulted in a higher operationally defined symplastic Cd fraction but a lower apoplastic one in the roots. In triticale, addition of either amino acid decreased the symplastic Cd fraction but increased the apoplastic one. Addition of histidine to the nutrient solution increased Cd concentration in wheat xylem sap but had no significant effect on Cd concentration in triticale xylem sap. Compared with the Cd-only treatment, the glycine-containing treatment led to significantly reduced Cd concentrations in xylem sap of both plant species. Wheat plants supplied with histidine and Cd accumulated greater amounts of Cd in their shoots than those supplied with Cd alone. Glycine had no significant effects on the Cd content of wheat shoots but decreased it in triticale shoots. Results indicate that the effects of amino acids on plant root uptake and xylem sap translocation of Cd depend on the type of amino acid supplemented. This finding is of great importance for selecting and/or breeding cultivars with Cd-toxicity tolerance.

Additional keywords: heavy metals, long-distance transport, organic acids, symplastic uptake.


References

Alloway BJ (1995) ‘Heavy metals in soils.’ (Blackie Academic and Professional: London)

Bharat Kumar Naik K, Ananda Kumar B, Raju S, Rao GN (2012) Speciation studies of l-histidine complexes of Pb(II), Cd(II), and Hg(II) in DMSO-water mixtures. International Journal of Inorganic Chemistry 2012, 265–249.

Boominathan R, Doran PM (2003) Organic acid complexation, heavy metal distribution and the effect of ATPase inhibition in hairy roots of hyperaccumulator plant species. Journal of Biotechnology 101, 131–146.
Organic acid complexation, heavy metal distribution and the effect of ATPase inhibition in hairy roots of hyperaccumulator plant species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpsV2rtA%3D%3D&md5=bd0b5cbb317e71d0fc68bdddd69e621aCAS |

Chen B, Zhang Y, Rafiq M, Yasmin Khan K, Pan F, Yang X, Feng Y (2014) Improvement of cadmium uptake and accumulation in Sedum alfredii by endophytic bacteria Sphingomonas SaMR12: Effects on plant growth and root exudates. Chemosphere 117, 367–373.
Improvement of cadmium uptake and accumulation in Sedum alfredii by endophytic bacteria Sphingomonas SaMR12: Effects on plant growth and root exudates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht12ntb7L&md5=c50891207a9f1c78addf6d30ede367b9CAS |

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. Environmental Toxicology 21, 479–488.
Effects of cadmium amendments on low-molecular-weight organic acid exudates in rhizosphere soils of tobacco and sunflower.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVCjsbnI&md5=da645de58e95d2daed38495273de8518CAS |

Deschamps P, Kulkarni P, Gautam-Basak M, Sarkar B (2005) The saga of copper(II)-L-histidine. Coordination Chemistry Reviews 249, 895–909.

Dong J, Mao W, Zhang G, Wu F, Cai Y (2007) Root excretion and plant tolerance to cadmium toxicity—a review. Plant, Soil and Environment 53, 190–193.

Dresler S, Hanaka A, Bednarek W, Maksymiec W (2014) Accumulation of low molecular-weight organic acids in roots and leaf segments of Zea mays plants treated with cadmium and copper. Acta Physiologiae Plantarum 36, 1565–1575.
Accumulation of low molecular-weight organic acids in roots and leaf segments of Zea mays plants treated with cadmium and copper.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVCgsLs%3D&md5=c99e1620ddd0bda3fd40bc27d570ce5aCAS |

Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiology 144, 197–205.
The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXls1Kjt7k%3D&md5=45bda651a926ecc7ad496add7dda16c1CAS |

Gramlich A, Tandy S, Frossard E, Eikenberg J, Schulin R (2013) Availability of zinc and the ligands citrate and histidine to wheat: Does uptake of entire complexes play a role? Journal of Agricultural and Food Chemistry 61, 10409–10417.
Availability of zinc and the ligands citrate and histidine to wheat: Does uptake of entire complexes play a role?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFGhu7%2FI&md5=9b98176763f9728b155d7e53d105565eCAS |

Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. Journal of Experimental Botany 53, 1–11.
Cellular mechanisms for heavy metal detoxification and tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptlKgtLw%3D&md5=2b9c5eaac9ae55c473a314fe71f2277eCAS |

Harrison SJ, Lepp NW, Phipps DA (1979) Uptake of copper by excised roots. II. Copper desorption from the free space. Zeitschrift für Pflanzenphysiologie 94, 27–34.
Uptake of copper by excised roots. II. Copper desorption from the free space.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXktlGrsrw%3D&md5=138026858a79eedd11008626fa4c5599CAS |

Hawrylak-Nowak B, Dresler S, Matraszek R (2015) Exogenous malic and acetic acids reduce cadmium phytotoxicity and enhance cadmium accumulation in roots of sunflower plants. Plant Physiology and Biochemistry 94, 225–234.
Exogenous malic and acetic acids reduce cadmium phytotoxicity and enhance cadmium accumulation in roots of sunflower plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXht1KgtbrP&md5=496a00e3dfada75e526b5a5466a5cc2aCAS |

Janicka-Russak M, Kabała K, Burzyński M, Kłobus G (2008) Response of plasma membrane H+-ATPase to heavy metal stress in Cucumis sativus roots. Journal of Experimental Botany 59, 3721–3728.
Response of plasma membrane H+-ATPase to heavy metal stress in Cucumis sativus roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1SisLbP&md5=e6000ee77c4b4eb80cfc3e5350411f1bCAS |

Kerkeb L, Kramer U (2003) The role of free histidine in xylem loading of nickel in Lyssum lesbiacum and Brassica juncea. Plant Physiology 131, 716–724.
The role of free histidine in xylem loading of nickel in Lyssum lesbiacum and Brassica juncea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtlyjs7k%3D&md5=d4f17166240c26751508a70c1243f5a5CAS |

Khodamoradi K, Khoshgoftarmanesh AH, Dalir N, Afyuni M, Schulin R (2015) How do glycine and histidine in nutrient solution affect zinc uptake and root-to-shoot translocation by wheat and triticale? Crop & Pasture Science 66, 1105–1110.
How do glycine and histidine in nutrient solution affect zinc uptake and root-to-shoot translocation by wheat and triticale?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhslylu7nF&md5=5b316c1f6fc07d669e27367adbd25926CAS |

Kozhevnikova AD, Seregin IV, Verweij R, Schat H (2014) Histidine promotes the loading of nickel and zinc, but not of cadmium, into the xylem in Noccaea caerulescens. Plant Signaling & Behavior 9, e29580-1-9

Krämer U, Cotter-Howells JD, Charnock JM, Baker AJM, Smith JAC (1996) Free histidine as a metal chelator in plants that accumulate nickel. Nature 379, 635–638.
Free histidine as a metal chelator in plants that accumulate nickel.Crossref | GoogleScholarGoogle Scholar |

Laurie SH, Tancock NP, McGrath SP, Sanders JR (1991) Influence of complexation on metal nutrient uptake of plants. I. EDTA in a multi-metal and computer simulation study. Journal of Experimental Botany 42, 509–513.
Influence of complexation on metal nutrient uptake of plants. I. EDTA in a multi-metal and computer simulation study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXkt1yhs7s%3D&md5=32dc39d975f04817ece8faa45803de05CAS |

Li T, Tao Q, Liang C, Shohag MJI, Yang X, Sparks DL (2013) Complexation with dissolved organic matter and mobility control of heavy metals in the rhizosphere of hyperaccumulator Sedum alfredii. Environmental Pollution 182, 248–255.

Liang YC, Wong JWC, Wei L (2005) Silicon-mediated enhancement of cadmium tolerance in maize (Zea mays L.) grown in cadmium contaminated soil. Chemosphere 58, 475–483.
Silicon-mediated enhancement of cadmium tolerance in maize (Zea mays L.) grown in cadmium contaminated soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFGiurnF&md5=5294d2e4c844999466b46fe67b97a55bCAS |

Lu LL, Tian SK, Yang XE, Wang XC, Li TQ, He ZL (2009) Cadmium uptake and xylem loading are active processes in the hyperaccumulator Sedum alfredii. Journal of Plant Physiology 166, 579–587.
Cadmium uptake and xylem loading are active processes in the hyperaccumulator Sedum alfredii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktlSgu70%3D&md5=621de24db50c60b00936de258ae36679CAS |

Ma JF, Hiradate S (2000) Form of aluminum for uptake and translocation in buckwheat (Fagopyrum esculentum Moench). Planta 211, 355–360.
Form of aluminum for uptake and translocation in buckwheat (Fagopyrum esculentum Moench).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsVWqs7Y%3D&md5=01d9c76962aaec446a4717eb502b2617CAS |

Mullins GL, Sommers LE, Housley TL (1986) Metal speciation in xylem and phloem exudates. Plant and Soil 96, 377–391.
Metal speciation in xylem and phloem exudates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhtFKks78%3D&md5=51e7f48ce641a654e71263c954b90f5fCAS |

Nowack B, Schulin R, Robinson BH (2006) A critical assessment of chelant-enhanced metal phytoextraction. Environmental Science & Technology 40, 5225–5232.
A critical assessment of chelant-enhanced metal phytoextraction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xnslyns74%3D&md5=615f89ec404f7ec119894823694c6cdcCAS |

Oburger E, Kirk GJD, Wenzel WW, Puschenreiter M, Jones DL (2009) Interactive effects of organic acids in the rhizosphere. Soil Biology & Biochemistry 41, 449–457.
Interactive effects of organic acids in the rhizosphere.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXit1Omtr8%3D&md5=197229901f4cba4f43a6e929fbcc137cCAS |

Pich A, Scholz G (1996) Translocation of copper and other micronutrients in tomato plants (Lycopersicon esculentum Mill.): nicotianamine-stimulated copper transport in the xylem. Journal of Experimental Botany 47, 41–47.
Translocation of copper and other micronutrients in tomato plants (Lycopersicon esculentum Mill.): nicotianamine-stimulated copper transport in the xylem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhtlajtLo%3D&md5=4e0a3bd159caf3510942e91990174a78CAS |

Rajkumar M, Sandhya S, Prasad M, Freitas H (2012) Perspectives of plant associated microbes in heavy metal phytoremediation. Biotechnology Advances 30, 1562–1574.
Perspectives of plant associated microbes in heavy metal phytoremediation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnslaks7k%3D&md5=ce71f65415d720ac96c0f70cfecd43f1CAS |

Rauser WE (1999) Structure and function of metal chelators produced by plants—the case for organic acids, amino acids, phytin and metallothioneins. Cell Biochemistry and Biophysics 31, 19–48.
Structure and function of metal chelators produced by plants—the case for organic acids, amino acids, phytin and metallothioneins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmt1yjsr8%3D&md5=c18a6c27b1bd829bd6a01a797fc23ceeCAS |

Richau KH, Kozhevnikova AD, Seregin IV, Vooijs R, Paul L, Koevoets M, Andrew J, Smith C, Ivanov VRB, Schat H (2009) Chelation by histidine inhibits the vacuolar sequestration of nickel in roots of the hyperaccumulator Thlaspi caerulescens. New Phytologist 183, 106–116.
Chelation by histidine inhibits the vacuolar sequestration of nickel in roots of the hyperaccumulator Thlaspi caerulescens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosFCku7k%3D&md5=56601e5dceca1f6a90cc095b5d8aae71CAS |

Saber NE, Abdel-Moneim AM, Barakat SY (1999) Role of organic acids in sunflower tolerance to heavy metals. Biologia Plantarum 42, 65–73.
Role of organic acids in sunflower tolerance to heavy metals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjs1SlsLY%3D&md5=11f9381e7279962225256835742e4b47CAS |

Salt DE, Prince RC, Baker AJM, Raskin I, Pickering IJ (1999) Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectroscopy. Environmental Science & Technology 33, 713–717.
Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectroscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksVajsw%3D%3D&md5=ace3cea3c9d29f8618899a3beebb2df0CAS |

Senden MHMN, Wolterbeek HTh (1990) Effect of citric acid on the transport of cadmium through xylem vessels of excised tomato stem-leaf systems. Acta Botanica Neerlandica 39, 297–303.
Effect of citric acid on the transport of cadmium through xylem vessels of excised tomato stem-leaf systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhtFymtbo%3D&md5=b6e3e219c61189e0841f035e4d14d02dCAS |

Senden MHMN, Vander Meer AJGM, Verburg TG, Wolterbeek HT (1994) Effects of cadmium on the behaviour of citric acid in isolated tomato xylem cell walls. Journal of Experimental Botany 45, 597–606.
Effects of cadmium on the behaviour of citric acid in isolated tomato xylem cell walls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXltVWmsLc%3D&md5=c843f6892baad3dc4557f4ec977c1dd9CAS |

Senden MHMN, Van der Meer AJGM, Verburg TG, Wolterbeek HTh (1995) Citric acid in tomato plant roots and its effect on cadmium uptake and distribution. Plant and Soil 171, 333–339.
Citric acid in tomato plant roots and its effect on cadmium uptake and distribution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmsVamtLY%3D&md5=1eca821e7a84e0b053d4cb4f7b582518CAS |

Sinclair S, Thomine B, Kraemer U (2012) The zinc homeostasis network of land plants. Biochimica et Biophysica Acta 1823, 1553–1567.
The zinc homeostasis network of land plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XovVGqt7c%3D&md5=bb9964ca69b8f50976158d07de6778f4CAS |

Sovago I, Varnagy K (2013) Cadmim (Cd) complexes of amino acids and peptides. In ‘Cadmium from toxicity to essentiality, metal ions in life sciences’. (Eds A Sigel, H Sigel, RKO Sigel) pp. 303–335. (Springer Science, Business Media: Dordrecht, London)

Sun Q, Wang XR, Ding SM, Yuan XF (2005) Effects of exogenous organic chelators on phytochelatins production and its relationship with cadmium toxicity in wheat (Triticum aestivum L.) under cadmium stress. Chemosphere 60, 22–31.
Effects of exogenous organic chelators on phytochelatins production and its relationship with cadmium toxicity in wheat (Triticum aestivum L.) under cadmium stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1Cqsrs%3D&md5=35d3d9d3d7d4f3bde3a39a9d187226f9CAS |

Svennerstam EH, Jamtgard S, Ahmad I, Huss-Danell K, Nasholm T, Ganeteg U (2011) Transporters in Arabidopsis roots mediating uptake of amino acids at naturally occurring concentrations. New Phytologist 191, 459–467.
Transporters in Arabidopsis roots mediating uptake of amino acids at naturally occurring concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFSqtr%2FF&md5=222bf35ba89112e2d5fb6703cca5dba2CAS |

Uraguchi SI, Watanabe A, Yoshitomi M, Kiyono K, Kuno L (2009) Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. Journal of Experimental Botany 60, 2677–2688.
Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntlGisb8%3D&md5=1ecb4f9395e80c663688c7eec2751263CAS |

Valenta P, Simoes Goncalves MLS, Sugavara M (1984) Voltammetric studies on the speciation of cadmium and zinc by amino acids in seawater. In ‘Complexation of trace metals in natural waters. Proceedings International Symposium’. 2–4 May 1983, Texel. (Eds CJM Kramer, JC Duinker) pp. 357–366. (Martinus Nijhoff Publishers: Leiden, The Netherlands)

Xing JP, Jiang RF, Ueno D, Ma JF, Schat H, McGrath SP, Zhao FJ (2008) Variation in root-to-shoot translocation of cadmium and zinc among different accessions of the hyperaccumulators Thlaspi caerulescens and Thlaspi praecox. New Phytologist 178, 315–325.
Variation in root-to-shoot translocation of cadmium and zinc among different accessions of the hyperaccumulators Thlaspi caerulescens and Thlaspi praecox.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXls1Gqt78%3D&md5=08b218d610f87a5bc903d5b34bfa71c9CAS |

Zhang J, Shi Q (2006) Determination of stability constants of cadmium-glycine complexes by a unified treatment for potentiometric and polarographic data. Chinese Journal of Chemical Physics 19, 164–168.

Zhou F, Zhou J, Li R, Wang H, Wang J (2007) Effect of exogenous amino acids on Cu uptake and translocation in maize seedlings. Plant and Soil 292, 105–117.
Effect of exogenous amino acids on Cu uptake and translocation in maize seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtlCjur4%3D&md5=36fa8aaf9333136a03302b74ef621bcfCAS |