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Plant function and evolutionary biology
RESEARCH ARTICLE

Copper in xylem and phloem saps from rice (Oryza sativa): the effect of moderate copper concentrations in the growth medium on the accumulation of five essential metals and a speciation analysis of copper-containing compounds

Yuko Ando A , Shinji Nagata A , Schuichi Yanagisawa A and Tadakatsu Yoneyama A B
+ Author Affiliations
- Author Affiliations

A Department of Applied Biological Chemistry, The University of Tokyo, Yayoi 1-1-1, Bunkyo-Ku, Tokyo 113-8657, Japan.

B Corresponding author. Email: tadakatsu_yoneyama@opal.ocn.ne.jp

Functional Plant Biology 40(1) 89-100 https://doi.org/10.1071/FP12158
Submitted: 27 May 2012  Accepted: 3 October 2012   Published: 2 November 2012

Abstract

Copper (Cu) is an essential element for cereals, playing important roles as a cofactor of several enzymes. Copper and four other metals (Fe, Mn, Zn and Mo) taken up by roots are efficiently delivered to the shoots via xylem and phloem. Here we investigated the concentrations of Cu, Fe, Mn, Zn and Mo in the xylem and phloem saps as well as in tissues of rice (Oryza sativa L.) seedlings when they were grown under different Cu levels in culture solution. Although the Cu concentrations in the roots and the Mn concentrations in the mature shoot tissues were increased with the increase of the Cu level in the culture solution, the concentrations of Cu and the other four metals in the xylem and phloem saps and the Cu contents in the shoot tissues were only slightly affected by moderate increases in the Cu medium level. The results of our analyses using membrane filtration, size-exclusion chromatography and electrospray ionisation time-of-flight mass spectrometry indicate that Cu in the xylem sap is dominantly complexed by 2′-deoxymugineic acid, whereas Cu in the phloem sap is bound to several compounds, i.e. nicotianamine, histidine and other >3-kDa compounds.

Additional keywords: ESI-TOF MS, metals, speciation.


References

Aki T, Shigyo M, Nakano R, Yoneyama T, Yanagisawa S (2008) Nano scale proteomics revealed the presence of regulatory proteins including three FT-like proteins in phloem and xylem saps from rice. Plant & Cell Physiology 49, 767–790.
Nano scale proteomics revealed the presence of regulatory proteins including three FT-like proteins in phloem and xylem saps from rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnvFWns7k%3D&md5=cb58a671d6bb1847ff394207aa10e2d9CAS |

Beneš I, Schreiber K, Ripperger H, Kircheiss A (1983) Metal complex formation of nicotianamine, a possible phytosiderophore. Experientia 39, 261–262.
Metal complex formation of nicotianamine, a possible phytosiderophore.Crossref | GoogleScholarGoogle Scholar |

Bernal M, Cases R, Picorel R, Yruela I (2007) Foliar and root Cu supply affect differently Fe- and Zn-uptake and photosynthetic activity in soybean plants. Environmental and Experimental Botany 60, 145–150.
Foliar and root Cu supply affect differently Fe- and Zn-uptake and photosynthetic activity in soybean plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXislWgsbs%3D&md5=71f89dcde309d9273493f69fd96627d9CAS |

Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat JF, Walker EL (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409, 346–349.
Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7hvVOntA%3D%3D&md5=f5dd3bf5cc5e3f39bc71d2355297e69cCAS |

Dell B (1981) Male-sterility and anther wall structure in copper-deficient plants. Annals of Botany 48, 599–608.

DiDonato RJ, Roberts LA, Sanderson T, Eisley RB, Walker EL (2004) Arabidosis Yellow Stripe-Like2 (YSL2): a metal-regulated gene of nicotianamine-metal complexes. The Plant Journal 39, 403–414.
Arabidosis Yellow Stripe-Like2 (YSL2): a metal-regulated gene of nicotianamine-metal complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsVSqu7w%3D&md5=07d8157dca68dc5ba35235dc130147e5CAS |

Dučić T, Polle A (2005) Transport and detoxification of manganese and copper in plants. Brazilian Journal of Plant Physiology 17, 103–112.
Transport and detoxification of manganese and copper in plants.Crossref | GoogleScholarGoogle Scholar |

Fukumorita T, Chino M (1982) Sugar, amino acid and inorganic contents in rice phloem sap. Plant & Cell Physiology 23, 273–283.

Graham RD, Stangoulis JCR (2003) Trace element uptake and distribution in plants. Journal of Plant Nutrition 133, 1502s–1505s.

Hayashi H, Chino M (1990) Chemical-composition of phloem sap from the uppermost internode of the rice plant. Plant & Cell Physiology 31, 247–251.

Himelblau E, Amasino RM (2000) Delivering copper within plant cells. Current Opinion in Plant Biology 3, 205–210.

Kato M, Ishikawa S, Inagaki K, Chiba C, Hayashi H, Yanagisawa S, Yoneyama T (2010) Possible chemical forms of cadmium and varietal differences in cadmium concentrations in the phloem sap from rice plants (Oryza sativa L.). Soil Science and Plant Nutrition 56, 839–847.
Possible chemical forms of cadmium and varietal differences in cadmium concentrations in the phloem sap from rice plants (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVOrsrk%3D&md5=7b4be428e032edb7ad7289712fa86d99CAS |

Kawabe S, Fukumorita T, Chino M (1980) Collection of rice phloem sap from stylets of homopterous insects severed by Yag laser. Plant & Cell Physiology 21, 1319–1327.

Kawai S, Kamei S, Matsuda Y, Ando R, Kondo S, Ishizawa A, Alam S (2001) Concentrations of iron and phytosiderophores in xylem sap of iron-deficient barley plants. Soil Science and Plant Nutrition 47, 265–272.
Concentrations of iron and phytosiderophores in xylem sap of iron-deficient barley plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXltV2murs%3D&md5=53a1dede1a8394df7008d4676d01fa44CAS |

Kitagishi K, Yamane I (Eds) (1981) ‘Heavy metal pollution in soils of Japan.’ (Japan Science Society Press: Tokyo)

Koike S, Inoue H, Mizuno D, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2004) OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem. The Plant Journal 39, 415–424.
OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsVSqu70%3D&md5=75a34b9c1d6121db422e10bb46934340CAS |

Köster J, Shi R, von Wirén N, Weber G (2011) Evaluation of different column types for the hydrophilic interaction chromatographic separation of iron-citrate and copper-histidine species from plants. Journal of Chromatography. A 1218, 4934–4943.
Evaluation of different column types for the hydrophilic interaction chromatographic separation of iron-citrate and copper-histidine species from plants.Crossref | GoogleScholarGoogle Scholar |

Krämer U, Howells CJD, 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 |

Kuper J, Llamas A, Hecht H-J, Mendel RR, Schwarz G (2004) Structure of the molybdopterin-bound Cnx1G domain links molybdenum and copper metabolism. Nature 430, 803–806.
Structure of the molybdopterin-bound Cnx1G domain links molybdenum and copper metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmsVGlsr0%3D&md5=a53ff64c474a9b1b56c52957e5d5ca13CAS |

Macfie SM, Tarmohamed Y, Welbourn PM (1994) Effects of cadmium, cobalt, copper, and nickel on growth of the green-alga Chlamydomonas-reinhardtii – the influences of the cell-wall and pH. Archives of Environmental Contamination and Toxicology 27, 454–458.
Effects of cadmium, cobalt, copper, and nickel on growth of the green-alga Chlamydomonas-reinhardtii – the influences of the cell-wall and pH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmvFCltLs%3D&md5=3acd265d81c01f449d0582fa0dc4754eCAS |

Marschner H (1995) ‘Mineral nutrition of higher plants.’ (Academic Press: London)

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=00b62d388ce357a1b7192ec099f937a3CAS |

Murakami T, Ise K, Hayakawa M, Kamei S, Takagi S (1989) Stabilities of metal complexes of mugineic acids and their specific affinities for iron(III). Chemistry Letters 12, 2137–2140.
Stabilities of metal complexes of mugineic acids and their specific affinities for iron(III).Crossref | GoogleScholarGoogle Scholar |

Nakamura S, Hayashi H, Mori S, Chino M (1993) Protein-phosphorylation in the sieve tubes of rice plants. Plant & Cell Physiology 34, 927–933.

Nishiyama R, Kato M, Nagata S, Yanagisawa S, Yoneyama T (2012) Identification of Zn-nicotianamine and Fe-2′-deoxymugineic acid in the phloem sap from rice plants (Oryza sativa L.). Plant & Cell Physiology 53, 381–390.
Identification of Zn-nicotianamine and Fe-2′-deoxymugineic acid in the phloem sap from rice plants (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xis1aruro%3D&md5=d8586c41cee67d8126829801f68bc95cCAS |

Noma M, Noguchi M (1976) Occurrence of nicotianamine in higher plants. Phytochemistry 15, 1701–1702.
Occurrence of nicotianamine in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXhtlymtg%3D%3D&md5=01274d3e5213b829c32746bf18728a6bCAS |

Noma M, Noguchi M, Tamaki E (1971) A new amino acid, nicotianamine, from tobacco leaves. Tetrahedron Letters 12, 2017–2020.
A new amino acid, nicotianamine, from tobacco leaves.Crossref | GoogleScholarGoogle Scholar |

Nomoto K, Mino Y, Ishida T, Yoshioka H, Ota N, Inoue M, Takagi S, Takemoto T (1981) X-ray crystal-structure of the copper(II) complex of mugineic acid, a naturally-occurring metal chelator of graminaceous plants. Journal of the Chemical Society. Chemical Communications 7, 338–339.
X-ray crystal-structure of the copper(II) complex of mugineic acid, a naturally-occurring metal chelator of graminaceous plants.Crossref | GoogleScholarGoogle Scholar |

Nozoye T, Nagasaka S, Kobayashi T, Takahashi M, Sato T, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK (2011) Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. The Journal of Biological Chemistry 286, 5446–5454.
Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvVCjsrg%3D&md5=0a0c0516c17916a8cb7f4670e0c78c75CAS |

Pätsikkä E, Kairavuo M, Šeršen F, Aro E-M, Tyystjärvi E (2002) Excess copper predisposes photosystem II to photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll. Plant Physiology 129, 1359–1367.
Excess copper predisposes photosystem II to photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll.Crossref | GoogleScholarGoogle Scholar |

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=f4028b9ecf10695d8ce2154474e4000aCAS |

Pich A, Scholz G, Stephan UW (1994) Iron-dependent changes of heavy metals, nicotianamine, and citrate in different plant organs and in the xylem exudate of two tomato genotypes. Nicotianamine as possible copper translocator. Plant and Soil 165, 189–196.
Iron-dependent changes of heavy metals, nicotianamine, and citrate in different plant organs and in the xylem exudate of two tomato genotypes. Nicotianamine as possible copper translocator.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjtF2isb4%3D&md5=ca4b2c2b924d1f6f732e53ce763731fdCAS |

Rellán-Álvarez R, Abadía J, Álvarez-Fernández A (2008) Formation of metal-nicotianamine complexes as affected by pH, ligand exchange with citrate and metal exchange. A study by electrospray ionization time-of-flight mass spectrometry. Rapid Communications in Mass Spectrometry 22, 1553–1562.
Formation of metal-nicotianamine complexes as affected by pH, ligand exchange with citrate and metal exchange. A study by electrospray ionization time-of-flight mass spectrometry.Crossref | GoogleScholarGoogle Scholar |

Rudolph A, Becker R, Scholz G, Prochazka Z, Toman J, Macek T, Herout V (1985) The occurrence of the amino-acid nicotianamine in plants and microorganisms - a reinvestigation. Biochemie und Physiologie der Pflanzen 180, 557–563.

Schaaf G, Ludewig U, Erenoglu BE, Mori S, Kitahara T, von Wirén N (2004) ZmYS1 functions as a proton-coupled symporter for phytosiderophore- and nicotianamine-chelated metals. Journal of Biological Chemistry 279, 9091–9096.
ZmYS1 functions as a proton-coupled symporter for phytosiderophore- and nicotianamine-chelated metals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhs1Omsrs%3D&md5=59b0581f018d9a35e596f4642a82cfdfCAS |

Schmidke I, Stephan UW (1995) Transport of metal micronutrients in the phloem of castor bean (Ricinus communis) seedlings. Physiologia Plantarum 95, 147–153.
Transport of metal micronutrients in the phloem of castor bean (Ricinus communis) seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhvVyhtQ%3D%3D&md5=ce7696db091553bc5a8d2f29c15ab1e8CAS |

Scholz G, Becker R, Pich A, Stephan UW (1992) Nicotianamine – a common constituent of strategies I and II of iron acquisition by plants: a review. Journal of Plant Nutrition 15, 1647–1665.
Nicotianamine – a common constituent of strategies I and II of iron acquisition by plants: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXmtFKj&md5=f4658ac0b6750e81dc82103e16bf6b0bCAS |

Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. Journal of Experimental Botany 57, 711–726.
The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XitVOqtrk%3D&md5=c16bb7f276da559ae1b2d4af6882173fCAS |

Shojima S, Nishizawa NK, Fushiya S, Nozoe S, Irifune T, Mori S (1990) Biosynthesis of phytosiderophores: in vitro biosynthesis of 2′-deoxymugineic acid from L-methionine and nicotianamine. Plant Physiology 93, 1497–1503.
Biosynthesis of phytosiderophores: in vitro biosynthesis of 2′-deoxymugineic acid from L-methionine and nicotianamine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXls12jtb4%3D&md5=b3efa9c46fbf8e2ba404a05cd4d6c837CAS |

Sillén LG, Martell AE (1964) ‘Stability constants of metal-ion complexes. Special publication 17.’ (The Chemical Society: London)

Stephan UW, Schmidke I, Stephan VW, Scholz G (1996) The nicotianamine molecule is made-to-measure for complexation of metal micronutrients in plants. Biometals 9, 84–90.
The nicotianamine molecule is made-to-measure for complexation of metal micronutrients in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xnt1yjuw%3D%3D&md5=aa63a43f73db30bdf78d773aad63d2c9CAS |

Takagi S (1976) Naturally occurring iron-chelating compounds in oat- and rice-root washings. Soil Science and Plant Nutrition 22, 423–433.
Naturally occurring iron-chelating compounds in oat- and rice-root washings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXlt1Ojsg%3D%3D&md5=f752db73e43d502479275b201e95a596CAS |

Takagi S, Nomoto K, Takemoto T (1984) Physiological aspect of mugineic acid, a possible phytosiderophore of graminaceous plants. Journal of Plant Nutrition 7, 469–477.
Physiological aspect of mugineic acid, a possible phytosiderophore of graminaceous plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXlt12lt7c%3D&md5=875358749020ea4aa31884ef312657b7CAS |

Takahashi M, Terada Y, Nakai I, Nakanishi H, Yoshimura E, Mori S, Nishizawa NK (2003) Role of nicotianamine in the intracellular delivery of metals and plant reproductive development. The Plant Cell 15, 1263–1280.
Role of nicotianamine in the intracellular delivery of metals and plant reproductive development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkvVeksbo%3D&md5=5d22fefabaafb1db63ed6c79dbfc5beeCAS |

von Wirén N, Klair S, Bansal S, Briat J-F, Khodr H, Shioiri T, Leigh RA, Hider RC (1999) Nicotianamine chelates both FeIII and FeII. Implications for metal transport in plants. Plant Physiology 119, 1107–1114.
Nicotianamine chelates both FeIII and FeII. Implications for metal transport in plants.Crossref | GoogleScholarGoogle Scholar |

White PJ, Broadley MR (2009) Biofortification of crops with seven mineral elements often lacking in human diets – iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytologist 182, 49–84.
Biofortification of crops with seven mineral elements often lacking in human diets – iron, zinc, copper, calcium, magnesium, selenium and iodine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksVKhtbw%3D&md5=f49ab32b73eb30cfe4183f475491f682CAS |

White MC, Baker FD, Chaney RL, Decker AM (1981) Metal complexation in xylem fluid. II. Theoretical equilibrium model and computational computer program. Plant Physiology 67, 301–310.
Metal complexation in xylem fluid. II. Theoretical equilibrium model and computational computer program.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXhvVylsLs%3D&md5=5cf158f22baf9c4ae7cf666ef746f419CAS |

Xuan Y, Scheuermann EB, Meda AR, Jacob P, von Wirén N, Weber G (2007) CE of phytosiderophores and related metal species in plants. Electrophoresis 28, 3507–3519.
CE of phytosiderophores and related metal species in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1ersrzM&md5=8e180af0c348d8563c0282c129b7f81eCAS |

Yruela I (2009) Copper in plants: acquisition, transport and interactions. Functional Plant Biology 36, 409–430.
Copper in plants: acquisition, transport and interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsVGhsr8%3D&md5=3036ff3d1a44764ca5be2f420ff427c6CAS |