Involvement of nitrogen functional groups in high-affinity copper binding in tomato and wheat root apoplasts: spectroscopic and thermodynamic evidence.

Carboxylic groups located in plant cell walls (CW) are generally considered to be the main copper binding sites in plant roots, despite the presence of other functional groups. The aim of this study was to investigate sites responsible for copper binding in root apoplasts, i.e. CW and outer surface of the plasma membrane (PM) continuum. Binding sites in root apoplasts were investigated by comparing isolated CW of a monocotyledon (Triticum aestivum L.) and dicotyledon (Solanum lycopersicum L.) crop with their respective whole roots. Copper speciation was examined by X-ray absorption (XAS) and (13)C-nuclear magnetic resonance spectroscopies while the affinity of ligands involved in copper binding was investigated by modeling copper sorption isotherms. Homogeneous speciation and binding of copper was found in wheat and tomato root apoplasts. Only Cu-N and Cu-O bonds were detected in wheat and tomato root apoplasts. Nitrogen/oxygen ligands were identified in slightly higher proportions (40-70%) than single oxygen ligands. Furthermore, low- and high-affinity binding sites contributed in an almost equivalent proportion to copper binding in root apoplasts. The high-affinity N functional groups embedded in root apoplasts participated in copper binding in the same magnitude than the low-affinity carboxylic groups.

[1]  E. Doelsch,et al.  Isolated cell walls exhibit cation binding properties distinct from those of plant roots , 2014, Plant and Soil.

[2]  J. Hazemann,et al.  Evidence of sulfur-bound reduced copper in bamboo exposed to high silicon and copper concentrations. , 2014, Environmental pollution.

[3]  E. Lombi,et al.  The rhizotoxicity of metal cations is related to their strength of binding to hard ligands , 2014, Environmental toxicology and chemistry.

[4]  A. Simionovici,et al.  Thlaspi arvense binds Cu(II) as a bis-(L-histidinato) complex on root cell walls in an urban ecosystem. , 2013, Metallomics : integrated biometal science.

[5]  T. Eglin,et al.  An inventory of trace elements inputs to French agricultural soils. , 2012, The Science of the total environment.

[6]  F. Zhao,et al.  Identifying the species of copper that are toxic to plant roots in alkaline nutrient solutions , 2012, Plant and Soil.

[7]  Jeffrey T. Rubino,et al.  Coordination chemistry of copper proteins: how nature handles a toxic cargo for essential function. , 2012, Journal of inorganic biochemistry.

[8]  R. Gabbrielli,et al.  On the role of the cell wall in the phenomenon of copper tolerance in Silene paradoxa L. , 2011 .

[9]  Peng Wang,et al.  Toxicity of metals to roots of cowpea in relation to their binding strength , 2011, Environmental toxicology and chemistry.

[10]  Stephen Lofts,et al.  Humic Ion-Binding Model VII: a revised parameterisation of cation-binding by humic substances , 2011 .

[11]  P. Kopittke,et al.  Alleviation of Cu and Pb rhizotoxicities in cowpea (Vigna unguiculata) as related to ion activities at root-cell plasma membrane surface. , 2011, Environmental science & technology.

[12]  Enzo Lombi,et al.  In Situ Distribution and Speciation of Toxic Copper, Nickel, and Zinc in Hydrated Roots of Cowpea1[W][OA] , 2011, Plant Physiology.

[13]  M. Hawkesford,et al.  High-Resolution Secondary Ion Mass Spectrometry Reveals the Contrasting Subcellular Distribution of Arsenic and Silicon in Rice Roots1[C][W][OA] , 2011, Plant Physiology.

[14]  J. Ferrasse,et al.  Investigation of copper speciation in pig slurry by a multitechnique approach. , 2010, Environmental science & technology.

[15]  P. Hinsinger,et al.  Copper uptake kinetics in hydroponically-grown durum wheat (Triticum turgidum durum L.) as compared with soil’s ability to supply copper , 2010, Plant and Soil.

[16]  A. Manceau,et al.  The nature of Cu bonding to natural organic matter , 2010 .

[17]  S. Abdel‐Ghany,et al.  Copper homeostasis. , 2009, The New phytologist.

[18]  A. Shukla,et al.  High-resolution spectroscopy on an X-ray absorption beamline. , 2009, Journal of synchrotron radiation.

[19]  T. Kinraide.  Improved scales for metal ion softness and toxicity , 2009, Environmental toxicology and chemistry.

[20]  Kristin Elgh-Dalgren,et al.  Modeling Copper(II) Complexation in a Peat Soil Based on Spectroscopic Structural Information , 2008 .

[21]  Shekhar C Mande,et al.  Exploiting 3D structural templates for detection of metal‐binding sites in protein structures , 2008, Proteins.

[22]  E. Jamet,et al.  Cell wall proteins: a new insight through proteomics. , 2006, Trends in plant science.

[23]  M. Guerinot,et al.  Metal-binding thermodynamics of the histidine-rich sequence from the metal-transport protein IRT1 of Arabidopsis thaliana. , 2006, Inorganic chemistry.

[24]  S. Nakashima,et al.  Lygodium japonicum fern accumulates copper in the cell wall pectin. , 2005, Journal of experimental botany.

[25]  J. Dumville,et al.  A proposed role for copper ions in cell wall loosening , 2002, Plant and Soil.

[26]  N. Meychik,et al.  Ion exchange properties of plant root cell walls , 2001, Plant and Soil.

[27]  J. Hazemann,et al.  Accumulation forms of Zn and Pb in Phaseolus vulgaris in the presence and absence of EDTA. , 2001, Environmental science & technology.

[28]  L. Schreiber,et al.  Apoplastic barriers in roots: chemical composition of endodermal and hypodermal cell walls , 1999 .

[29]  G. Cassab,et al.  PLANT CELL WALL PROTEINS. , 1998, Annual review of plant physiology and plant molecular biology.

[30]  T. Murakami,et al.  Stabilities of Metal Complexes of Mugineic Acids and Their Specific Affinities for Iron(III) , 1989 .

[31]  S. McLaughlin,et al.  Adsorption of divalent cations to bilayer membranes containing phosphatidylserine , 1981, The Journal of general physiology.

[32]  B. Evertsson.  The crystal structure of bis-l-histidinecopper(II) dinitrate dihydrate , 1969 .

[33]  P. Várnai,et al.  Periplasmic arabinogalactan glycoproteins act as a calcium capacitor that regulates plant growth and development. , 2013, The New phytologist.

[34]  J. Bottero,et al.  Fate and behaviour of Cu and Zn from pig slurry spreading in a tropical water–soil–plant system , 2013 .

[35]  K. D. De Schamphelaere,et al.  Development of an electrostatic model predicting copper toxicity to plants. , 2012, Journal of experimental botany.