Contribution of apoplast to short-term copper uptake by wheat and mung bean roots
Nataly Meychik A B , Yuliya Nikolaeva A , Maria Kushunina A and Igor Yermakov A
+ Author Affiliations
- Author Affiliations
A Department of Plant Physiology, Faculty of Biology, Moscow State University, Moscow, 119234, Russia.
B Corresponding author. Email: meychik@mail.ru
Functional Plant Biology 43(5) 403-412 https://doi.org/10.1071/FP15356
Submitted: 30 July 2015 Accepted: 22 December 2015 Published: 16 February 2016
Abstract
In this study we addressed the controversial issue of contribution of cell walls (CWs) to Cu binding in plant roots. We compared short-term Cu uptake at different solution Cu levels by mung bean (Vigna radiata (L.) R. Wilczek) and wheat (Triticum aestivum L., cv. Inna) and by root CWs isolated from either Cu-treated or non-treated plants. Twenty four hours of plant exposure to Cu affected Cu-binding capacity of mung bean root CWs but not wheat CWs. Amounts of Cu associated with CWs and roots increased with Cu concentration. The Cu accumulated in CWs could account for total Cu content of roots (except for wheat in highest Cu treatment). Pectin content of the CWs and their Cu-sorption capacity were positively correlated. The accumulation of Cu in root CWs is a principal response of wheat and mung bean plants to excess Cu, limiting symplastic Cu uptake in roots in short-term treatment. The contribution of CWs to Cu absorption by plant roots depends on Cu level in the medium and plant species.
Additional keywords: cell walls, copper stress, heavy metal stress, metal uptake.
References
Bravin M, Le Merrer B, Denaix L, Schneider A, Hinsinger P (2010) Copper uptake kinetics in hydroponically–grown durum wheat (Triticum turgidum durum L.) as compared with soil’s ability to supply copper. Plant and Soil 331, 91–104.| Copper uptake kinetics in hydroponically–grown durum wheat (Triticum turgidum durum L.) as compared with soil’s ability to supply copper.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvVOhsbk%3D&md5=99ddec9dcb796c683b9ed678b4c01043CAS |
Colzi I, Doumett S, Del Bubba N, Fornaini J, Arnetoli M, Gabbrielli R, Gonnelli C (2011) On the role of the cell wall in the phenomenon of copper tolerance in Silene paradoxa L. Environmental and Experimental Botany 72, 77–83.
| On the role of the cell wall in the phenomenon of copper tolerance in Silene paradoxa L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltFykurg%3D&md5=3f28a7a7d8f1fccf0ea2fd80c9f36567CAS |
Colzi I, Arnetoli M, Gallo A, Doumett S, Del Bubba M, Pignattelli S, Gabbrielli R, Gonnelli C (2012) Copper tolerance strategies involving the root cell wall pectins in Silene paradoxa L. Environmental and Experimental Botany 78, 91–98.
| Copper tolerance strategies involving the root cell wall pectins in Silene paradoxa L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XisFGit7k%3D&md5=0a4cc1f3e47a371239fb04302e91548fCAS |
Douchiche O, Rihouey C, Schaumann A, Driouich A, Morvan C (2007) Cadmium-induced alterations of the structural features of pectins in flax hypocotyl. Planta 225, 1301–1312.
| Cadmium-induced alterations of the structural features of pectins in flax hypocotyl.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtVWjsL8%3D&md5=7a7b0f843682274c222c91c632fc78ffCAS | 17086399PubMed |
Eticha D, Stass A, Horst WJ (2005) Cell–wall pectin and its degree of methylation in the maize root–apex: significance for genotypic differences in aluminium resistance. Plant, Cell & Environment 28, 1410–1420.
| Cell–wall pectin and its degree of methylation in the maize root–apex: significance for genotypic differences in aluminium resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Olu7rM&md5=1c5a2c3b5283bc1145b2290ed6664363CAS |
Felle HH (1998) The apoplastic pH of the Zea mays root cortex as measured with pH-sensitive microelectrodes: aspects of regulation. Journal of Experimental Botany 49, 987–995.
| The apoplastic pH of the Zea mays root cortex as measured with pH-sensitive microelectrodes: aspects of regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjvFeitrw%3D&md5=a09d75c968693d7c8b7e0058f7d70b60CAS |
Grignon C, Sentenac H (1991) pH and ionic conditions in the apoplast. Annual Review of Plant Physiology and Plant Molecular Biology 42, 103–128.
| pH and ionic conditions in the apoplast.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXltFSmsr0%3D&md5=5c40fc4d97a9cd0ef9f91b6eb3bd7d4bCAS |
Guigues S, Bravin M, Garnier C, Masion A, Doelsch E (2014) Isolated cell walls exhibit cation binding properties distinct from those of plant roots. Plant and Soil 381, 367–379.
| Isolated cell walls exhibit cation binding properties distinct from those of plant roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXnslGktLw%3D&md5=f37c048686d4511eb369233f53a69446CAS |
Haynes RJ (1980) Ion exchange properties of roots and ionic interactions within the root apoplasm. Their role in ion accumulation by plants. Botanical Review 46, 75–99.
| Ion exchange properties of roots and ionic interactions within the root apoplasm. Their role in ion accumulation by plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXitFWktrs%3D&md5=afecbae11299f51471e1af894c4d7bfbCAS |
Horst WJ, Wang Y, Eticha D (2010) The role of the root apoplast in aluminium–induced inhibition of root elongation and in aluminium resistance of plants: a review. Annals of Botany 106, 185–197.
| The role of the root apoplast in aluminium–induced inhibition of root elongation and in aluminium resistance of plants: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVWjsbw%3D&md5=c9d616a186e5955f3ff403682e5fb87bCAS | 20237112PubMed |
Iwasaki K, Sakurai K, Takahashi E (1990) Copper binding by the root cell walls of Italian ryegrass and red clover. Soil Science and Plant Nutrition 36, 431–439.
| Copper binding by the root cell walls of Italian ryegrass and red clover.Crossref | GoogleScholarGoogle Scholar |
Kinraide TB (2004) Possible influence of cell walls upon ion concentrations at plasma membrane surfaces. Toward a comprehensive view of cell-surface electrical effects upon ion uptake, intoxication, and amelioration. Plant Physiology 136, 3804–3813.
| Possible influence of cell walls upon ion concentrations at plasma membrane surfaces. Toward a comprehensive view of cell-surface electrical effects upon ion uptake, intoxication, and amelioration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVCjtr%2FK&md5=cc72ae97d66749a412b6cdd7126c4e11CAS | 15489281PubMed |
Konno H, Nakato T, Nakashima S, Katoh K (2005) Lygodium japonicum fern accumulates copper in the cell wall pectin. Journal of Experimental Botany 56, 1923–1931.
| Lygodium japonicum fern accumulates copper in the cell wall pectin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpvFKntb8%3D&md5=f97293caaaea251adfc558e22c6751f9CAS | 15928016PubMed |
Konno H, Nakashima S, Katoh K (2010) Metal-tolerant moss Scopelophila cataractae accumulates copper in the cell wall pectin of the protonema. Journal of Plant Physiology 167, 358–364.
| Metal-tolerant moss Scopelophila cataractae accumulates copper in the cell wall pectin of the protonema.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltFSksrc%3D&md5=5a7fc1deb877968fece8091f2494198aCAS | 19853964PubMed |
Kopittke PM, Menzies NW (2006) Effect of Cu toxicity on growth of cowpea (Vigna unguiculata). Plant and Soil 279, 287–296.
| Effect of Cu toxicity on growth of cowpea (Vigna unguiculata).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsVaru7g%3D&md5=04675e90395d2eac7cfe9848d0636606CAS |
Kopittke PM, Blamey FPC, Menzies NW (2008) Toxicities of soluble Al, Cu, and La include ruptures to rhizodermal and root cortical cells of cowpea. Plant and Soil 303, 217–227.
| Toxicities of soluble Al, Cu, and La include ruptures to rhizodermal and root cortical cells of cowpea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1ShtLk%3D&md5=953d653080fb4c80559b4f11d8d446f6CAS |
Kopittke PM, Menzies NW, de Jonge MD, McKenna BA, Donner E, Webb RI, Paterson DJ, Howard DL, Ryan CG, Glover CJ, Scheckel KG, Lombi E (2011) In situ distribution and speciation of toxic copper, nickel, and zinc in hydrated roots of cowpea. Plant Physiology 156, 663–673.
| In situ distribution and speciation of toxic copper, nickel, and zinc in hydrated roots of cowpea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFWrsbo%3D&md5=331a906b7a980539f266bc025430db3aCAS | 21525332PubMed |
Krzesłowska M (2011) The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiologiae Plantarum 33, 35–51.
| The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy.Crossref | GoogleScholarGoogle Scholar |
Lee WM, An YJ, Yoon H, Kweon HS (2008) Toxicity and bioavailability of copper nanoparticles to the terrestrial plants mung bean (Phaseolus radiatus) and wheat (Triticum aestivum): plant agar test for water-insoluble nanoparticles. Environmental Toxicology and Chemistry 27, 1915–1921.
| Toxicity and bioavailability of copper nanoparticles to the terrestrial plants mung bean (Phaseolus radiatus) and wheat (Triticum aestivum): plant agar test for water-insoluble nanoparticles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVersLnI&md5=924ad2169c13ed6d97605e7f6fb0f230CAS | 19086317PubMed |
Lequeux H, Hermans C, Lutts S, Verbruggen N (2010) Response to copper excess in Arabidopsis thaliana: Impact on the root system architecture, hormone distribution, lignin accumulation and mineral profile. Plant Physiology and Biochemistry 48, 673–682.
| Response to copper excess in Arabidopsis thaliana: Impact on the root system architecture, hormone distribution, lignin accumulation and mineral profile.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXosVyht7s%3D&md5=97d6281548c5a26985538fd633325ea0CAS | 20542443PubMed |
Li Z, Wu L, Hu P, Luo Y, Christie P (2013) Copper changes the yield and cadmium/zinc accumulation and cellular distribution in the cadmium/zinc hyperaccumulator Sedum plumbizincicola. Journal of Hazardous Materials 261, 332–341.
| Copper changes the yield and cadmium/zinc accumulation and cellular distribution in the cadmium/zinc hyperaccumulator Sedum plumbizincicola.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1KqsrrO&md5=9a36d4fd7e2650aef310046bb3b1eb50CAS | 23959253PubMed |
Liu D, Kottke I (2004) Subcellular localization of copper in the root cells of Allium sativum by electron energy loss spectroscopy (EELS). Bioresource Technology 94, 153–158.
| Subcellular localization of copper in the root cells of Allium sativum by electron energy loss spectroscopy (EELS).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkt1Cmtbc%3D&md5=3ce2bca03fdb9d3d3608e090bbdef282CAS | 15158507PubMed |
Liu T, Shen C, Wang Y, Huang C, Shi J (2014) New insights into regulation of proteome and polysaccharide in cell wall of Elsholtzia splendens in response to copper stress. PLoS One 9, e109573
| New insights into regulation of proteome and polysaccharide in cell wall of Elsholtzia splendens in response to copper stress.Crossref | GoogleScholarGoogle Scholar | 25340800PubMed |
Lou L, Shen Z, Li X (2004) The copper tolerance mechanisms of Elsholtzia haichowensis, a plant from copper–enriched soils. Environmental and Experimental Botany 51, 111–120.
| The copper tolerance mechanisms of Elsholtzia haichowensis, a plant from copper–enriched soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFCjt7o%3D&md5=0b8d5231362af96fcd3e539f3deee169CAS |
Marschner H (1995) ‘Mineral nutrition of higher plants.’ (2nd edn) (Academic Press: London)
Meychik NR, Yermakov IP (1999) A new approach to the investigation on the ionogenic groups of root cell walls. Plant and Soil 217, 257–264.
| A new approach to the investigation on the ionogenic groups of root cell walls.Crossref | GoogleScholarGoogle Scholar |
Meychik NR, Yermakov IP (2001) Ion exchange properties of plant root cell walls. Plant and Soil 234, 181–193.
| Ion exchange properties of plant root cell walls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnsVemsb0%3D&md5=7c834bc5ff773e4f69e318ed13f17794CAS |
Meychik NR, Yermakov IP, Prokoptseva OS (2003) Diffusion of an organic cation into root cell walls. Biochemistry 68, 760–771.
| Diffusion of an organic cation into root cell walls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXns1Sltb0%3D&md5=4a1e616ee6417fc7d72a4d0b9c630e3bCAS | 12946258PubMed |
Meychik NR, Matveyeva NP, Nikolaeva YuI, Chaikova AV, Yermakov IP (2006) Features of ionogenic group composition in polymeric matrix of lily pollen wall. Biochemistry 71, 893–899.
| Features of ionogenic group composition in polymeric matrix of lily pollen wall.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVOms74%3D&md5=d0f828aeeb188aa5fbc3f7250af6db36CAS | 16978153PubMed |
Meychik NR, Nikolaeva YuI, Yermakov IP (2009) Nonaqueous titration of amino groups in polymeric matrix of plant cell walls. Biochemistry (Moscow) 74, 933–937.
| Nonaqueous titration of amino groups in polymeric matrix of plant cell walls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVaqs7nO&md5=2eddda61c826ff6a07331c2a6a508007CAS | 19817695PubMed |
Meychik N, Nikolaeva Y, Kushunina M, Yermakov I (2014) Are the carboxyl groups of pectin polymers the only metal-binding sites in plant cell walls? Plant and Soil 381, 25–34.
| Are the carboxyl groups of pectin polymers the only metal-binding sites in plant cell walls?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmsVCju7w%3D&md5=55f17fff8cf08b300e3527e64dabc5eaCAS |
Michaud AM, Chappellaz C, Hinsinger P (2008) Copper phytotoxicity affects root elongation and iron nutrition in durum wheat (Triticum turgidum durum L.). Plant and Soil 310, 151–165.
| Copper phytotoxicity affects root elongation and iron nutrition in durum wheat (Triticum turgidum durum L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpslWksrg%3D&md5=1d501acc45b048856b9cc6d0ad0525bdCAS |
Nishizono H, Ichikawa H, Suziki S, Ishii F (1987) The role of the root cell wall in the heavy metal tolerance of Athyrium yokoscense. Plant and Soil 101, 15–20.
| The role of the root cell wall in the heavy metal tolerance of Athyrium yokoscense.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXltlWhsrk%3D&md5=52941026d11b6f8612bba88cbf9c4551CAS |
Ouzounidou G, Ciamporova M, Moustakas M, Karataglis S (1995) Responses of maize (Zea mays L.) plants to copper stress. I. Growth, mineral content and ultrastructure of roots. Environmental and Experimental Botany 35, 167–176.
| Responses of maize (Zea mays L.) plants to copper stress. I. Growth, mineral content and ultrastructure of roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmslOrtrk%3D&md5=ceb0a75cee908c3012106ca534a37394CAS |
Peng H, Yang X, Tian S (2005) Accumulation and ultrastructural distribution of copper in Elsholtzia splendens. Journal of Zhejiang University. Science. B. 6, 311–318.
| Accumulation and ultrastructural distribution of copper in Elsholtzia splendens.Crossref | GoogleScholarGoogle Scholar | 15822140PubMed |
Redjala T, Sterckeman T, Skiker S, Echevarria G (2010) Contribution of apoplast and symplast to short term nickel uptake by maize and Leptoplax emarginata roots. Environmental and Experimental Botany 68, 99–106.
| Contribution of apoplast and symplast to short term nickel uptake by maize and Leptoplax emarginata roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Wit77L&md5=dcd8488bc65fa0c138fc39b9232b1350CAS |
Sattelmacher B (2001) The apoplast and its significance for plant mineral nutrition. New Phytologist 149, 167–192.
| The apoplast and its significance for plant mineral nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtlKmu7w%3D&md5=afbc0dc47093f352c7fd182c2a2d88ddCAS |
Schmohl N, Pilling J, Fisahn J, Horst WJ (2000) Pectin methylesterase modulates aluminium sensitivity in Zea mays and Solanum tuberosum. Physiologia Plantarum 109, 419–427.
| Pectin methylesterase modulates aluminium sensitivity in Zea mays and Solanum tuberosum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsl2isr8%3D&md5=b38951a7f36084e56f1afb6add50243aCAS |
Seregin IV, Kozhevnikova AD (2011) Histochemical methods for detection of heavy metals and strontium in the tissues of higher plants. Russian Journal of Plant Physiology: A Comprehensive Russian Journal on Modern Phytophysiology 58, 721–727.
| Histochemical methods for detection of heavy metals and strontium in the tissues of higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXns12nt7o%3D&md5=a916569f19d6e063ed559682561e5d7fCAS |
Taylor GJ, Foy CD (1985) Differential uptake and toxicity of ionic and chelated copper in Triticum aestivum. Canadian Journal of Botany 63, 1271–1275.
| Differential uptake and toxicity of ionic and chelated copper in Triticum aestivum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlt1agurs%3D&md5=075d387d79bcab4fe615825e2a636ef6CAS |
Vogel J (2008) Unique aspects of the grass cell wall. Current Opinion in Plant Biology 11, 301–307.
| Unique aspects of the grass cell wall.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsVGmu7s%3D&md5=bc6ade94bbfd9ec5d74c8190b5bde54dCAS | 18434239PubMed |
Wei L, Luo Ch, Li X, Shen Zh (2008) Copper accumulation and tolerance in Chrysanthemum coronarium L. and Sorghum sudanense L. Archives of Environmental Contamination and Toxicology 55, 238–246.
| Copper accumulation and tolerance in Chrysanthemum coronarium L. and Sorghum sudanense L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsVWjs74%3D&md5=9eda80d0e195bb1da634ac382febfb70CAS | 18183449PubMed |
White PJ (2001) The pathways of calcium movement to the xylem. Journal of Experimental Botany 52, 891–899.
| The pathways of calcium movement to the xylem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXltVejtb0%3D&md5=6bab02a54de5fb0387d215635863f3a1CAS | 11432906PubMed |
White PJ, Whiting SN, Baker AJM, Broadley MR (2002) Does zinc move apoplastically to the xylem in roots of Thlaspi caerulescens? New Phytologist 153, 201–207.
| Does zinc move apoplastically to the xylem in roots of Thlaspi caerulescens? Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitVSnt7s%3D&md5=593edbb68c9ef332dc1eac166daf472fCAS |
Yu Q, Kuo J, Tang C (2001) Using confocal laser scanning microscopy to measure apoplastic pH change in roots of Lupinus angustifolius L. in response to high pH. Annals of Botany 87, 47–52.
| Using confocal laser scanning microscopy to measure apoplastic pH change in roots of Lupinus angustifolius L. in response to high pH.Crossref | GoogleScholarGoogle Scholar |
Zhang Q, Cheetamun R, Dhugga KS, Rafalski JA, Tingey SV, Shirley NJ, Taylor J, Hayes K, Beatty M, Bacic A, Burton RA, Fincher GB (2014) Spatial gradients in cell wall composition and transcriptional profiles along elongating maize internodes. BMC Plant Biology 14, 27
| Spatial gradients in cell wall composition and transcriptional profiles along elongating maize internodes.Crossref | GoogleScholarGoogle Scholar | 24423166PubMed |
Zhao FJ, Hamon RE, Lombi E, McLaughlin MJ, McGrath SP (2002) Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. Journal of Experimental Botany 53, 535–543.
| Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitVegtL8%3D&md5=19822b4dd1cc53c15caa004ccfc0357aCAS | 11847252PubMed |
