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Responses of Trapa natans L. floating laminae to high concentrations of manganese

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Summary.

The present study focuses on the responses of floating laminae of the Mn-tolerant hydrophyte Trapa natans L. to 1 mM Mn and their ability to accumulate the metal. Studies were carried out first on young floating laminae belonging to the second verticil of 30-day-old plants which originated from fruits that had been maintained in a 1 mM Mn-treated environment and again on the young floating laminae after 10 days of further treatment with 1 mM Mn. Mn storing was observed from the first days after germination, but only 10-day-treated laminae showed the capability to hyperaccumulate the element inside specialised cells (>20000 μg/g [dry weight]). Electron microscopy and the Folin–Ciocalteu reaction for phenolics revealed deposits of chelated material inside vacuoles of the first palisade layer and of idioblasts in the spongy tissue. X-ray microanalysis indicated that the deposits were Mn chelated with phenolic compounds. Numerous trichomes were observed at the lower epidermis of 10-day-treated laminae. They were rich in phenolics and characterised by Mn concretions at their base. As they are associated with a high concentration of the metal in culture water and sediments, trichomes may constitute a morphological differentiation for the secretion of Mn-chelating molecules into the culture water, as a probable “avoidance” mechanism. Finally, monitoring of the photosynthetic apparatus showed that photosynthetic function was not impaired, though differences in development occurred.

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Abbreviations

Chl:

chlorophyll

CP43–47 :

inner antenna of PSII

ICP:

inductively coupled plasma

LHCII:

light-harvesting system of PSII

PSII:

photosystem II

RCII:

reaction centre of PSII

TEM:

transmission electron microscopy

References

  • T Aalto E Yuurola (2002) ArticleTitleA three-dimensional model for CO2 transport in airspaces and mesophyll cells of a silver birch leaf Plant Cell Environ 25 1399–1410 Occurrence Handle10.1046/j.0016-8025.2002.00906.x

    Article  Google Scholar 

  • M Alfonso G Montoya R Cases R Rodriguez R Picorel (1994) ArticleTitleCore antenna complex, CP43 and CP47, of higher plant photosystem II. Spectral properties, pigment stoichiometry, and amino acid composition Biochemistry (Washington) 33 10494–10500 Occurrence Handle10.1021/bi00200a034 Occurrence Handle1:CAS:528:DyaK2cXltlSit7c%3D

    Article  CAS  Google Scholar 

  • AJM Baker SP Mc Grath RD Reeves JAC Smith (2000) Metal hyperaccumulator plants: a review of the ecology and physiology of a biochemical resource for phytoremediation of metal-polluted soils N Terry G Banuleos (Eds) Phytoremediation of contaminated soil and water Lewis Publishers Boca Raton, Fla. 85–107

    Google Scholar 

  • C Baldisserotto L Ferroni V Medici A Pagnoni M Pellizzari MP Fasulo F Fagioli A Bonora S Pancaldi (2004) ArticleTitleSpecific intra-tissue responses to manganese in the floating lamina of Trapa natans L Plant Biol 6 578–589 Occurrence Handle15375729 Occurrence Handle10.1055/s-2004-821089 Occurrence Handle1:CAS:528:DC%2BD2cXpsVSjtb8%3D

    Article  PubMed  CAS  Google Scholar 

  • C Baldisserotto L Ferroni C Andreoli MP Fasulo A Bonora S Pancaldi (2005) ArticleTitleDark-acclimation of the chloroplast in Koliella antarctica exposed to a simulated austral night condition Arct Antarct Alp Res 37 146–156 Occurrence Handle10.1657/1523-0430(2005)037[0146:DOTCIK]2.0.CO;2

    Article  Google Scholar 

  • A Bonora S Pancaldi R Gualandri MP Fasulo (2000) ArticleTitleCarotenoid and ultrastructure variations in plastids of Arum italicum Miller fruit during maturation and ripening J Exp Bot 51 873–884 Occurrence Handle10948213 Occurrence Handle10.1093/jexbot/51.346.873 Occurrence Handle1:CAS:528:DC%2BD3cXjsl2mt70%3D

    Article  PubMed  CAS  Google Scholar 

  • C Bowler W van Camp M van Montagu D Inze (1994) ArticleTitleSuperoxide dismutase in plants Crit Rev Plant Sci 13 199–218 Occurrence Handle1:CAS:528:DyaK2cXmvFOis7w%3D

    CAS  Google Scholar 

  • C Büchel J Barber G Ananyev S Eshaghi R Watt C Dismukes (1999) ArticleTitlePhotoassembly of the manganese cluster and oxygen evolution from monomeric and dimeric CP47-reaction center photosystem II complexes Proc Natl Acad Sci USA 96 14288–14293 Occurrence Handle10588698 Occurrence Handle10.1073/pnas.96.25.14288

    Article  PubMed  Google Scholar 

  • WL Butler (1978) ArticleTitleEnergy distribution in the photochemical apparatus of photosynthesis Annu Rev Plant Physiol 29 345–378 Occurrence Handle10.1146/annurev.pp.29.060178.002021 Occurrence Handle1:CAS:528:DyaE1cXktl2gt7Y%3D

    Article  CAS  Google Scholar 

  • ZQ Cai M Slot ZX Fan (2005) ArticleTitleLeaf development and photosynthetic properties of three tropical tree species with delayed greening Photosynthetica 43 91–98 Occurrence Handle10.1007/s11099-005-1098-3 Occurrence Handle1:CAS:528:DC%2BD2MXjtlehurY%3D

    Article  CAS  Google Scholar 

  • L Chalker-Scott (2002) ArticleTitleDo anthocyanins function as osmoregolators in leaf tissues? Adv Bot Res 37 103–127 Occurrence Handle1:CAS:528:DC%2BD3sXht1OqsLY%3D

    CAS  Google Scholar 

  • KB Clairmont WG Hagar EA Davis (1986) ArticleTitleManganese toxicity to chlorophyll synthesis in tobacco callus Plant Physiol 80 291–293 Occurrence Handle16664602 Occurrence Handle1:CAS:528:DyaL28XhtVersLo%3D

    PubMed  CAS  Google Scholar 

  • CL Emmons DM Peterson GL Paul (1999) ArticleTitleAntioxidant capacity of oat (Avena sativa L.) extracts. 2. In vitro antioxidant activity and contents of phenolic and tocol antioxidants J Agric Food Chem 47 4894–4898 Occurrence Handle10606549 Occurrence Handle10.1021/jf990530i Occurrence Handle1:CAS:528:DyaK1MXnsFOlsLc%3D

    Article  PubMed  CAS  Google Scholar 

  • L Ferroni C Baldisserotto MP Fasulo A Pagnoni S Pancaldi (2004) ArticleTitleAdaptive modifications of the photosynthetic apparatus in Euglena gracilis Klebs exposed to manganese excess Protoplasma 224 167–177 Occurrence Handle15614477 Occurrence Handle10.1007/s00709-004-0072-4 Occurrence Handle1:CAS:528:DC%2BD2cXhtFWqsLfN

    Article  PubMed  CAS  Google Scholar 

  • CD Foy (1988) ArticleTitlePlant adaptation to acid, aluminium-toxic soils Commun Soil Sci Plant Anal 19 959–987 Occurrence Handle1:CAS:528:DyaL1cXltV2gsLw%3D

    CAS  Google Scholar 

  • CD Foy RL Chaney MC White (1978) ArticleTitleThe physiology of metal toxicity in plants Annu Rev Plant Physiol 29 511–566 Occurrence Handle10.1146/annurev.pp.29.060178.002455 Occurrence Handle1:CAS:528:DyaE1cXkslWltLw%3D

    Article  CAS  Google Scholar 

  • H Godmaire C Nalewajko (1990) ArticleTitleStructure and development of secretory trichomes on Myriophyllum spicatum L Aquat Bot 37 99–121 Occurrence Handle10.1016/0304-3770(90)90085-Y

    Article  Google Scholar 

  • A Gonzalez JP Lynch (1999) ArticleTitleSubcellular and tissue Mn compartmentation in bean leaves under Mn toxicity stress Aust J Plant Physiol 26 811–822 Occurrence Handle1:CAS:528:DC%2BD3cXlt1Ogug%3D%3D

    CAS  Google Scholar 

  • KS Gould (2004) ArticleTitleNature’s Swiss army knife: the diverse protective roles of anthocyanins in leaves J Biomed Biotechnol 5 314–320 Occurrence Handle10.1155/S1110724304406147

    Article  Google Scholar 

  • EM Gross H Meier G Schilling (1996) ArticleTitleRelease and ecological impact of algicidal hydrolysable polyphenols in Myriophyllum spicatum Phytochemistry 41 133–138 Occurrence Handle10.1016/0031-9422(95)00598-6 Occurrence Handle1:CAS:528:DyaK28XisVWqsA%3D%3D

    Article  CAS  Google Scholar 

  • JL Hall (2002) ArticleTitleCellular mechanisms for heavy metal detoxification and tolerance J Exp Bot 53 1–11 Occurrence Handle11741035 Occurrence Handle10.1093/jexbot/53.366.1 Occurrence Handle1:CAS:528:DC%2BD3MXptlKgtLw%3D

    Article  PubMed  CAS  Google Scholar 

  • NP Hughes RJP Williams (1988) An introduction to manganese biological chemistry RD Graham RJ Hannam NC Uren (Eds) Manganese in soils and plants Kluwer Academic Dordrecht 7–19

    Google Scholar 

  • M Hummel E Kiviat (2004) ArticleTitleReview of world literature on water chestnut with implication for management in North America J Aquat Plant Manage 42 1–17

    Google Scholar 

  • NV Ignatov FF Litvin (1998) ArticleTitleA comparative study of the terminal stages of chlorophyll biosynthesis before and after water (D2O) introduction into greening plant leaves Photosynth Res 56 83–93 Occurrence Handle10.1023/A:1005913616050 Occurrence Handle1:CAS:528:DyaK1cXltlOhsrw%3D

    Article  CAS  Google Scholar 

  • KA Joutei Y Glories M Mercier (1994) ArticleTitleLocalization of tannins in grape berry skins Vitis 33 133–138 Occurrence Handle1:CAS:528:DyaK2MXivFSrtr4%3D

    CAS  Google Scholar 

  • H Kamachi I Komori H Tamura Y Sawa I Karahara Y Honma N Wada T Kawabata K Matsuda S Ikeno M Noguchi H Inoue (2005) ArticleTitleLead tolerance and accumulation in the gametophytes of the fern Athyrium yokoscense J Plant Res 118 137–145 Occurrence Handle15843865 Occurrence Handle10.1007/s10265-005-0202-x Occurrence Handle1:CAS:528:DC%2BD2MXkvVCksbw%3D

    Article  PubMed  CAS  Google Scholar 

  • M Kamal AE Ghaly N Mahmoud R Côté (2004) ArticleTitlePhytoaccumulation of heavy metals by aquatic plants Environ Int 29 1029–1039 Occurrence Handle14680885 Occurrence Handle10.1016/S0160-4120(03)00091-6 Occurrence Handle1:CAS:528:DC%2BD3sXptVSqt7k%3D

    Article  PubMed  CAS  Google Scholar 

  • S Khokhar RKO Apenton (2003) ArticleTitleIron binding characteristics of phenolic compounds: some tentative structure-activity relations Food Chem 81 133–140 Occurrence Handle10.1016/S0308-8146(02)00394-1 Occurrence Handle1:CAS:528:DC%2BD3sXivVegsb4%3D

    Article  CAS  Google Scholar 

  • GH Krause DN Weis (1991) ArticleTitleChlorophyll fluorescence: the basics Annu Rev Plant Physiol Plant Mol Biol 42 313–349 Occurrence Handle10.1146/annurev.pp.42.060191.001525 Occurrence Handle1:CAS:528:DyaK3MXltFSmsrc%3D

    Article  CAS  Google Scholar 

  • PE Kriedemann RD Graham JT Wiskich (1985) ArticleTitlePhotosynthetic dysfunction and in vivo changes in chlorophyll a fluorescence from manganese-deficient wheat leaves Aust J Agric Res 36 157–169 Occurrence Handle10.1071/AR9850157 Occurrence Handle1:CAS:528:DyaL2MXktVeqsLo%3D

    Article  CAS  Google Scholar 

  • Z Krupa M Baranowska D Orzot (1996) ArticleTitleCan anthocyanins be considered as heavy metal stress indicator in higher plants? Acta Physiol Plant 18 147–151 Occurrence Handle1:CAS:528:DyaK28Xltl2mtLs%3D

    CAS  Google Scholar 

  • M Kumar S Chikara MK Chand AK Bhatnagar (2002) ArticleTitleAccumulation of lead, cadmium, zinc, and copper in the edible aquatic plants Trapa bispinosa Roxb. and Nelumbo nucifera Gaertn Bull Environ Contam Toxicol 69 649–654 Occurrence Handle12375112 Occurrence Handle10.1007/s00128-002-0110-x Occurrence Handle1:CAS:528:DC%2BD38Xot1CitL0%3D

    Article  PubMed  CAS  Google Scholar 

  • N Lavid Z Barkay E Tel-Or (2001a) ArticleTitleAccumulation of heavy metals in epidermal glands of the waterlily (Nympheaceae) Planta 212 313–322 Occurrence Handle10.1007/s004250000399 Occurrence Handle1:CAS:528:DC%2BD3MXhtV2ksbc%3D

    Article  CAS  Google Scholar 

  • N Lavid A Schwartz E Lewinsohn E Tel-Or (2001b) ArticleTitlePhenols and phenol oxidases are involved in cadmium accumulation in the water plants Nymphoides peltata (Menyanthaceae) and Nymphaeae (Nympheaceae) Planta 214 189–195 Occurrence Handle1:CAS:528:DC%2BD3MXovFKns78%3D

    CAS  Google Scholar 

  • N Lavid A Schwartz O Yarden E Tel-Or (2001c) ArticleTitleThe involvement of polyphenols and peroxidase activities in heavy-metal accumulation by epidermal glands of the waterlily (Nympheaceae) Planta 212 323–331 Occurrence Handle10.1007/s004250000400 Occurrence Handle1:CAS:528:DC%2BD3MXhtV2ktr4%3D

    Article  CAS  Google Scholar 

  • H Lichtenthaler (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes L Packer R Douce (Eds) Plant cell membranes SeriesTitleMethods in enzymology NumberInSeries148 Academic Press London 350–382 Occurrence Handle10.1016/0076-6879(87)48036-1

    Chapter  Google Scholar 

  • FC Lidon FS Henriques (1992) ArticleTitleEffect of excess copper on photosynthetic pigments in rice plants Bot Bull Acad Sin 33 141–149 Occurrence Handle1:CAS:528:DyaK38Xks1Krsr0%3D

    CAS  Google Scholar 

  • FC Lidon MG Teixeira (2000a) ArticleTitleRice tolerance to excess Mn: implications in the chloroplast lamellae and synthesis of a novel Mn protein Plant Physiol Biochem 38 969–978 Occurrence Handle10.1016/S0981-9428(00)01207-9 Occurrence Handle1:CAS:528:DC%2BD3MXlvFeisA%3D%3D

    Article  CAS  Google Scholar 

  • FC Lidon MG Teixeira (2000b) ArticleTitleOxy radicals production and control in the chloroplast of Mn-treated rice Plant Sci 152 7–15 Occurrence Handle10.1016/S0168-9452(99)00179-X Occurrence Handle1:CAS:528:DC%2BD3cXosVChsQ%3D%3D

    Article  CAS  Google Scholar 

  • FC Lidon MG Barreiro C Ramalho (2004) ArticleTitleManganese accumulation in rice: implications for photosynthetic functioning J Plant Physiol 161 1235–1244 Occurrence Handle15602815 Occurrence Handle10.1016/j.jplph.2004.02.003 Occurrence Handle1:CAS:528:DC%2BD2MXhvFensg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • ECHET Lucassen AJP Smolders JGM Roelofs (2000) ArticleTitleIncreased groundwater levels cause iron toxicity in Glyceria fluitans (L.) Aquat Bot 66 321–327 Occurrence Handle10.1016/S0304-3770(99)00083-2 Occurrence Handle1:CAS:528:DC%2BD3cXhvVOksbc%3D

    Article  CAS  Google Scholar 

  • JF Ma (2005) ArticleTitlePhysiological mechanisms of Al resistance in higher plants Soil Sci Plant Nutr 51 609–612 Occurrence Handle10.1111/j.1747-0765.2005.tb00074.x Occurrence Handle1:CAS:528:DC%2BD2MXhtFyqtL3K

    Article  CAS  Google Scholar 

  • SM Macfie GJ Taylor (1992) ArticleTitleThe effects of excess manganese on photosynthetic rate and concentration of chlorophyll in Triticum aestivum grown in solution culture Physiol Plant 85 467–475 Occurrence Handle10.1111/j.1399-3054.1992.tb05813.x Occurrence Handle1:CAS:528:DyaK38XmsVKksb8%3D

    Article  CAS  Google Scholar 

  • SM Macfie EA Cossins GJ Taylor (1994) ArticleTitleEffects of excess manganese on production of organic acids in Mn-tolerant and in Mn-sensitive cultivars of Triticum aestivum L. (wheat) J Plant Physiol 143 135–144 Occurrence Handle1:CAS:528:DyaK2cXitFSgt7k%3D

    CAS  Google Scholar 

  • DP Maljuga (1947) ArticleTitleChemical composition of soils and plants as indicators of prospecting for metals Izv Akad Nauk SSSR, Ser Geogr Geofiz 11 135–138

    Google Scholar 

  • AL Mancinelli F Rossi A Moroni (1991) ArticleTitleCryptochrome, phytochrome, and anthocyanin production Plant Physiol 96 1079–1085 Occurrence Handle16668301 Occurrence Handle1:CAS:528:DyaK3MXmtVensbw%3D

    PubMed  CAS  Google Scholar 

  • AR Menon M Yatazawa (1984) ArticleTitleNature of manganese complexes in manganese accumulator plant – Acanthopanax sciadophylloides J Plant Nutr 7 961–974

    Google Scholar 

  • JS Moroni KG Briggs GJ Taylor (1991) ArticleTitleChlorophyll content and leaf elongation rate in wheat seedlings as a measure of manganese tolerance Plant Soil 136 1–9 Occurrence Handle10.1007/BF02465214 Occurrence Handle1:CAS:528:DyaK3MXltlajur8%3D

    Article  CAS  Google Scholar 

  • WC Mueller AD Greenwood (1978) ArticleTitleUltrastructure of phenolic-storing cells fixed with caffeine J Exp Bot 29 757–764 Occurrence Handle10.1093/jxb/29.3.757

    Article  Google Scholar 

  • RO Nable RL Houtz GM Cheniae (1988) ArticleTitleEarly inhibition of photosynthesis during development of Mn toxicity in tobacco Plant Physiol 86 1136–1142 Occurrence Handle16666045 Occurrence Handle1:CAS:528:DyaL1cXktVWqtbY%3D

    PubMed  CAS  Google Scholar 

  • D Neumann U zur Nieden O Lichtenberger I Leopold (1995) ArticleTitleHow does Armeria maritima tolerate high heavy metal concentrations? J Plant Physiol 146 704–717 Occurrence Handle1:CAS:528:DyaK2MXotlOnsrY%3D

    CAS  Google Scholar 

  • A Nissim-Levi S Kagan R Ovadia M Oren-Shamir (2003) ArticleTitleEffects of temperature, UV-light and magnesium on anthocyanin pigmentation in cocoplum leaves J Hortic Sci Biotech 78 61–64 Occurrence Handle1:CAS:528:DC%2BD3sXitVCisrg%3D

    CAS  Google Scholar 

  • S Pancaldi A Bonora R Gualandri R Gerdol R Manservigi MP Fasulo (1998) ArticleTitleIntra-tissue characteristics of chloroplasts in the lamina and petiole of mature winter leaf of Arum italicum Miller Bot Acta 111 267–272

    Google Scholar 

  • S Pancaldi C Baldisserotto L Ferroni A Bonora MP Fasulo (2002) ArticleTitleRoom temperature microspectrofluorimetry as a useful tool for studying the assembly of the PSII chlorophyll-protein complexes in single living cells of etiolated Euglena gracilis Klebs during the greening process J Exp Bot 53 1753–1763 Occurrence Handle12147725 Occurrence Handle10.1093/jxb/erf031 Occurrence Handle1:CAS:528:DC%2BD38Xmt12nsLs%3D

    Article  PubMed  CAS  Google Scholar 

  • JK Pittman (2005) ArticleTitleManaging the manganese: molecular mechanisms of manganese transport and homeostasis New Phytol 167 733–742 Occurrence Handle16101910 Occurrence Handle10.1111/j.1469-8137.2005.01453.x Occurrence Handle1:CAS:528:DC%2BD2MXhtVGisbfE

    Article  PubMed  CAS  Google Scholar 

  • UN Rai S Sinha (2001) ArticleTitleDistribution of metals in aquatic edible plants: Trapa natans (Roxb.) Makino and Ipomoea aquatica Forsk Environ Monit Assess 70 214–252 Occurrence Handle10.1023/A:1010727325662

    Article  Google Scholar 

  • UN Rai S Sinha P Chandra (1996) ArticleTitleMetal biomonitoring in water resources of Eastern Gats, Koraput (Orissa), India by aquatic plants Environ Monit Assess 43 125–137 Occurrence Handle10.1007/BF00398603 Occurrence Handle1:CAS:528:DyaK28XntVCqt70%3D

    Article  CAS  Google Scholar 

  • M Roitto P Rautio R Julkunen-Tiitto E Kukkola S Huttenen (2005) ArticleTitleChanges in the concentrations of phenolics and photosynthates in Scots pine (Pinus sylvestris L.) seedlings exposed to nickel and copper Environ Pollut 137 603–609 Occurrence Handle16005771 Occurrence Handle10.1016/j.envpol.2005.01.046 Occurrence Handle1:CAS:528:DC%2BD2MXlvFygu7c%3D

    Article  PubMed  CAS  Google Scholar 

  • DE Salt RD Smith I Raskin (1998) ArticleTitlePhytoremediation Annu Rev Plant Physiol Plant Mol Biol 49 643–668 Occurrence Handle15012249 Occurrence Handle10.1146/annurev.arplant.49.1.643 Occurrence Handle1:CAS:528:DyaK1cXjvVSgs7g%3D

    Article  PubMed  CAS  Google Scholar 

  • S Santabarbara KV Neverov FM Garlaschi G Zucchelli RC Jennings (2001) ArticleTitleInvolvement of uncoupled antenna chlorophylls in photoinhibition in thylakoids FEBS Lett 491 109–113 Occurrence Handle11226430 Occurrence Handle10.1016/S0014-5793(01)02174-3 Occurrence Handle1:CAS:528:DC%2BD3MXhsFShsL4%3D

    Article  PubMed  CAS  Google Scholar 

  • G Santandrea S Schiff A Bennici (1998) ArticleTitleEffects of manganese on Nicotiana species in vitro and characterization of regenerated Mn-tolerant tobacco plants Plant Sci 132 71–82 Occurrence Handle10.1016/S0168-9452(97)00268-9 Occurrence Handle1:CAS:528:DyaK1cXhvVSnsb0%3D

    Article  CAS  Google Scholar 

  • G Santandrea T Pandolfi A Bennici (2000) ArticleTitleA physiological characterization of Mn-tolerant tobacco plants selected by in vitro culture Plant Sci 150 163–170 Occurrence Handle10.1016/S0168-9452(99)00180-6 Occurrence Handle1:CAS:528:DyaK1MXnslynuro%3D

    Article  CAS  Google Scholar 

  • B Schoefs F Frank (1998) ArticleTitleChlorophyll synthesis in dark-grown pine primary needles Plant Physiol 118 1159–1168 Occurrence Handle9847090 Occurrence Handle10.1104/pp.118.4.1159 Occurrence Handle1:CAS:528:DyaK1MXnsw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • D Strack E Busch E Klein (1989) ArticleTitleAnthocyanin patterns in European orchids and their taxonomic and phylogenetic relevance Phytochemistry 28 2127–2139 Occurrence Handle10.1016/S0031-9422(00)97931-7 Occurrence Handle1:CAS:528:DyaK3cXhvVyntA%3D%3D

    Article  CAS  Google Scholar 

  • C Sundqvist C Dahlin (1997) ArticleTitleWith chlorophyll pigments from prolamellar bodies to light-harvesting complexes Physiol Plant 100 748–759 Occurrence Handle10.1111/j.1399-3054.1997.tb00002.x Occurrence Handle1:CAS:528:DyaK2sXlvFCitLw%3D

    Article  CAS  Google Scholar 

  • G Suvarnalatha L Rajendran GA Ravishankar LV Venkataraman (1994) ArticleTitleElicitation of anthocyanin production in cell-cultures of carrot (Daucus carota L.) by using elicitors and abiotic stress Biotechnol Lett 16 1275–1280 Occurrence Handle1:CAS:528:DyaK2MXjtFOlsr0%3D

    CAS  Google Scholar 

  • N Takamura Y Kadono M Fukushima M Nakagawa BHO Kim (2003) ArticleTitleEffects of aquatic macrophytes on water quality and phytoplankton communities in shallow lakes Ecol Res 18 381–395 Occurrence Handle10.1046/j.1440-1703.2003.00563.x Occurrence Handle1:CAS:528:DC%2BD3sXnsVSnurk%3D

    Article  CAS  Google Scholar 

  • IR Vassiliev Z Kolber KD Wyman D Mauzerall VK Shukla PG Falkowsky (1995) ArticleTitleEffects of iron limitation on photosystem II composition and light utilization in Dunaliella tertiolecta Plant Physiol 109 963–972 Occurrence Handle12228645 Occurrence Handle1:CAS:528:DyaK2MXpsVOrsb0%3D

    PubMed  CAS  Google Scholar 

  • YS Velioglu G Mazza L Gao BD Oomah (1998) ArticleTitleAntioxidant activity and total phenolics in selected fruits, vegetables, and grain products J Agric Food Chem 46 4113–4117 Occurrence Handle10.1021/jf9801973 Occurrence Handle1:CAS:528:DyaK1cXlsFKgs7g%3D

    Article  CAS  Google Scholar 

  • JL Walworth ME Sumner (1988) ArticleTitleFoliar diagnosis. A review Adv Plant Nutr 3 193–241

    Google Scholar 

  • RE Wilkinson K Ohki (1988) ArticleTitleInfluence of manganese deficiency and toxicity on isoprenoid synthesis Plant Physiol 87 841–846 Occurrence Handle16666235 Occurrence Handle1:CAS:528:DyaL1cXls12nsbc%3D

    PubMed  CAS  Google Scholar 

  • AH Wissemeier WJ Horst (1992) ArticleTitleEffect of light intensity on manganese toxicity symptoms and callose formation in cowpea (Vigna unguiculata) Plant Soil 143 299–309 Occurrence Handle10.1007/BF00007886 Occurrence Handle1:CAS:528:DyaK38Xlt1ygtbw%3D

    Article  CAS  Google Scholar 

  • GS Woodall GR Stewart (1998) ArticleTitleDo anthocyanins play a role in UV protection of the red juvenile leaves of Syzygium? J Exp Bot 49 1447–1450 Occurrence Handle10.1093/jexbot/49.325.1447 Occurrence Handle1:CAS:528:DyaK1cXlsVOkt7c%3D

    Article  CAS  Google Scholar 

  • SG Xue YX Chen RD Reeves AJM Baker Q Lin DR Fernando (2004) ArticleTitleManganese uptake and accumulation by the hyperaccumulator plant Phytolacca acinosa Roxb. (Phytolaccaceae) Environ Pollut 131 393–399 Occurrence Handle15261402 Occurrence Handle10.1016/j.envpol.2004.03.011 Occurrence Handle1:CAS:528:DC%2BD2cXlvVWgtrs%3D

    Article  PubMed  CAS  Google Scholar 

  • J Zavoda T Cutright J Szpak E Fallon (2001) ArticleTitleUptake, selectivity, and inhibition of hydroponic treatment of contaminants J Environ Eng 127 502–508 Occurrence Handle10.1061/(ASCE)0733-9372(2001)127:6(502) Occurrence Handle1:CAS:528:DC%2BD3MXktVWkurw%3D

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Laboratory of Plant Cytophysiology, Department of Natural and Cultural Resources, University of Ferrara, Ferrara

    C. Baldisserotto, L. Ferroni, E. Anfuso, M. P. Fasulo & S. Pancaldi

  2. Laboratory of Atomic Spectroscopy, Department of Chemistry, University of Ferrara, Ferrara

    A. Pagnoni

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  1. C. Baldisserotto
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  2. L. Ferroni
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  3. E. Anfuso
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  4. A. Pagnoni
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  5. M. P. Fasulo
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  6. S. Pancaldi
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Corresponding author

Correspondence to M. P. Fasulo.

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Correspondence and reprints: Department of Natural and Cultural Resources, University of Ferrara, Corso Ercole I d’Este 32, 44100 Ferrara, Italy.

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Baldisserotto, C., Ferroni, L., Anfuso, E. et al. Responses of Trapa natans L. floating laminae to high concentrations of manganese. Protoplasma 231, 65–82 (2007). https://doi.org/10.1007/s00709-007-0242-2

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