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Effect of zinc on nectar secretion of Hibiscus rosa-sinensis L

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Abstract

Zinc toxicity in secretory cells caused a range of effects, mainly depending on metal concentration. Low concentrations activated nectary function increasing nectar secretion but secretion was greatly inhibited or stopped entirely by ongoing concentration. Water loss rate of zinc treated flower parts was significantly reduced whereas green sepals were dehydrated more rapidly in comparison to colored petals. The content of zinc, calcium, magnesium and manganese increased mainly in sepals under excess of zinc, but in the secreted nectar this metal was not evident. Morphological changes were observed in mucilage cells concerning the mucilage structure and appearance. The parenchymatic, subglandular cells displayed an early vacuolarization and cytoplasm condensation. Secretory hairs appeared to be thinner, the apical cell folded inwards and plasmolytic shrinkage became severe in all cells. The waxy cuticula showed an increased electron density. A plasmalemma detachment from the external cell walls was observed creating a gap between cell wall and plasmalemma. ER cisterns of all treated nectary hairs dominated the cytoplasm and electron dense deposits were seen within its profiles. A great number of other organelles were also present, showing electron dense deposits in their membranes as well. The vacuome was drastically reduced in all cells, except in the subglandular ones and electron dense membrane remnants were observed.

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References

  • Alaoui-Sossé B, Genet P, Vinit-Dunand F, Toussaint M-L, Epron D, Badot P-M (2004) Effect of copper on growth of cucumber plants (Cucumis sativus) and its relationships with carbohydrate accumulation and changes in ion contents. Plant Sci 166:1213–1218

    Article  CAS  Google Scholar 

  • Alkorta I, Hernández-Allica J, Becerril JM, Amezaga I, Albizu I, Onaindia M, Garbisu S (2004) Chelate-enhanced phytoremediation of soils polluted with heavy metals. Rev Environ Sci Biotechnol 3:55–70

    Article  CAS  Google Scholar 

  • Arsovski AA, Villota MM, Rowland O, Subramaniam R, Western TL (2009) Mum enhancers are important for seed coat mucilage production and mucilage secretory cell differentiation in Arabidopsis thaliana. J Exp Bot 60:2601–2612

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Bhattacharyya M, Martin C, Smith A (1993) The importance of starch biosynthesis in the wrinkled weed shape character. Plant Mol Biol 22:525–531

    Article  PubMed  CAS  Google Scholar 

  • Blaylock MJ, Huang JW (2000) Phytoextraction of metals. Raskin I and Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. John Wiley and Sons, Toronto, p 303

    Google Scholar 

  • Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702

    Article  PubMed  CAS  Google Scholar 

  • Calabrese EJ (2001) The future of hormesis: where do we go from here? Crit Rev Toxicol 31:637–648

    Article  PubMed  CAS  Google Scholar 

  • Cavet JS, Borrelly GP, Robinson NJ (2003) Zn, Cu and Co in cyanobacteria: selective control of metal availability. FEMS Microbiol Rev 27:165–181

    Article  PubMed  CAS  Google Scholar 

  • Cedergreen N (2008) Is the growth stimulation by low doses of glyphosate sustained over time? Environ Pollut 156:1099–1104

    Article  PubMed  CAS  Google Scholar 

  • Chen HM, Zheng CR, Tu C, Shen ZG (2000) Chemical methods and phytoremediation of soil contaminated with heavy metals. Chemosphere 41:229–234

    Article  PubMed  CAS  Google Scholar 

  • Chettri MK, Sawidis T (1997) Impact of heavy metals on water loss from lichen thalli. Ecotox Environ Saf 37:103–111

    Article  CAS  Google Scholar 

  • Cobb GP, Sands K, Waters M, Wixson BG, Dorward-King E (2000) Accumulation of heavy metals by vegetables grown in mine wastes. Environ Toxicol Chem 19:600–607

    Article  CAS  Google Scholar 

  • Dean GH, Zheng H, Tewari J (2007) The Arabidopsis MUM2 gene encodes a β-galactosidase required for the production of seed coat mucilage with correct hydration properties. The Plant Cell 19:4007–4021

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Deiana S, Premoli A, Senette C, Gessa C, Marzadori C (2003) Role of uronic acid polymers on the availability of iron to plants. J Plant Nutr 26:1927–1941

    Article  CAS  Google Scholar 

  • Dietz K-J, Tavakoli N, Kluge C, Mimura T, Sharma SS, Harris GC (2001) Significance of the V-type ATPase for the adaptation to stressful growth conditions and its regulation on the molecular and biochemical level. J Exp Bot 52:1969–1980

    Article  PubMed  CAS  Google Scholar 

  • Eide DJ (2006) Zinc transporters and the cellular trafficking of zinc. Bioch Biophys Acta 1763:711–722

    Article  CAS  Google Scholar 

  • El-Ghamery AA, El-Kholy MA, El-Yousser MAA (2003) Evaluation of cytological effects of Zn2+ in relation to germination and root growth of Nigella sativa L. and Triticum aestivum L. Mutat Res 537:29–41

    Article  PubMed  CAS  Google Scholar 

  • Escalante-Pérez M, Lautner S, Nehls U, Selle A, Teuber M, Schnitzler J, Teichmann T, Fayyaz P, Hartung W, Polle A, Fromm J, Hedrich R, Ache P (2009) Salt affects xylem differentiation of grey poplar (Populus x canescens). Planta 229:299–309

    Article  PubMed  CAS  Google Scholar 

  • Galluzzi L, Maiuri MC, Vitale I, Zischka H, Castedo M, Zitvogel L, Kroemer G (2007) Cell death modalities: classification and pathophysiological implications. Cell Death Differ 14:1237–1243

    Article  PubMed  CAS  Google Scholar 

  • Ge YX, Angenent GC, Wittich PE (2000) NEC1, a novel gene, highly expressed in nectary tissue of Petunia hybrida. Plant J 24:725–734

    Article  PubMed  CAS  Google Scholar 

  • Gerendás J, Schurr U (1999) Physicochemical aspects of ion relations and pH regulation in plants: a quantitative approach. J Exp Bot 50:1101–1114

    Google Scholar 

  • Günthardt-Goerg MS, Vollenweider P (2007) Linking stress with macroscopic and microscopic leaf response in trees: new diagnostic perspectives. Environ Pollut 147:467–488

    Article  PubMed  CAS  Google Scholar 

  • Gustin JL, Loureiro ME, Kim D, Na G, Tikhonova M, Salt DE (2009) MTP1-dependent Zn sequestration into shoot vacuoles suggests dual roles in Zn tolerance and accumulation in Zn-hyperaccumulating plants. Plant J 57:1116–1127

    Article  PubMed  CAS  Google Scholar 

  • Hacisalihoglu G, Kochian LV (2003) How do some plants tolerate low levels of soil zinc? Mechanisms of zinc efficiency in crop plants. New Phytol 159:341–350

    Article  CAS  Google Scholar 

  • Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    Article  PubMed  CAS  Google Scholar 

  • Horner HT, Healy RA, Ren G, Fritz D, Klyne A, Seames C, Thornburg RW (2007) Amyloplast to chromoplast conversion in developing ornamental tobacco floral nectaries provides sugar for nectar and antioxidants for protection. Am J Bot 94:12–24

    Article  PubMed  CAS  Google Scholar 

  • Jiang X, Wang C (2008) Zinc distribution and zinc-binding forms in Phragmites australis under zinc pollution. J Plant Physiol 165:697–704

    Article  PubMed  CAS  Google Scholar 

  • Kabata-Pendias A (2001) Trace elements in soils and plants, 3rd edn. CRC Press, Boca Raton

    Google Scholar 

  • Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534

    Article  PubMed  CAS  Google Scholar 

  • Macquet A, Ralet M-C, Kronenberger J, Marion-Poll A, North HM (2007) In situ, chemical and macromolecular study of the composition of Arabidopsis thaliana seed coat mucilage. Plant Cell Physiol 48:984–999

    Article  PubMed  CAS  Google Scholar 

  • Maeshima M (2000) Vacuolar H+-pyrophosphatase. Biochim Biophys Acta 1465:37–51

    Article  PubMed  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic Press, London

    Google Scholar 

  • Mastroberti AA, de A Mariath JE (2008) Development of mucilage cells of Araucaria angustifolia (Araucariaceae). Protoplasma 232:233–245

    Article  PubMed  CAS  Google Scholar 

  • Mushak P (2013) Limits to chemical hormesis as a dose–response model in health risk assessment. Sci Total Environ 443:643–649

    Article  PubMed  CAS  Google Scholar 

  • Nepi M, Soligo C, Nocentini D, Abate M, Guarnieri M, Cai G, Bini L, Puglia M, Bianchi L, Pacini E (2012) Amino acids and protein profile in floral nectar: much more than a simple reward. Flora 207:475–481

    Article  Google Scholar 

  • Noodelkoska TV, Doran PM (2000) Interactive effects of temperature and metal stress on the growth and some biochemical compounds in wheat seedlings. Environ Pollut 107:315–320

    Article  Google Scholar 

  • O’Brien IE, Murray BG, Baguley BC, Morris BA, Ferguson IB (1998) Major changes in chromatin condensation suggest the presence of an apoptotic pathway in plant cells. Exp Cell Res 241:46–54

    Article  PubMed  Google Scholar 

  • Pan JW, Zhu MY, Chen H (2001) Aluminum-induced cell death in root-tip cells barley. Environ Exp Bot 46:71–79

    Article  PubMed  CAS  Google Scholar 

  • Plum LM, Rink L, Haase H (2010) The essential toxin: impact of zinc on human health. Int J Environ Res Public Health 7:1342–1365

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ren J, Dai WR, Xuan ZY, Yao YN, Korpelainen H, Li CY (2007) The effect of drought and enhanced UV-B radiation on the growth and physiological traits of two contrasting poplar species. For Ecol Manag 239:112–119

    Article  Google Scholar 

  • Sabatini SE, Juarez AB, Eppis MR, Bianchi L, Luquet CM, Rios de Molina MC (2009) Oxidative stress and antioxidant defenses in two green microalgae exposed to copper. Ecotoxicol Environ Saf 72:1200–1206

    Article  PubMed  CAS  Google Scholar 

  • Sagardoy F, Morales F, Lopez-Millan AF, Abadıa A, Abadıa J (2009) Effects of zinc toxicity on sugar beet (Beta vulgaris L.) plants grown in hydroponics. Plant Biol 11:339–350

    Article  PubMed  CAS  Google Scholar 

  • Sawidis T (1991) A histochemical study of nectaries of Hibiscus rosa-sinensis. J Exp Bot 42:1477–1487

    Article  Google Scholar 

  • Sawidis T (1998) The subglandular tissue of Hibiscus rosa-sinensis nectaries. Flora 193:327–335

    Google Scholar 

  • Sawidis T (2008) Effect of cadmium on pollen germination and tube in Lilium longiflorum and Nicotiana tabacum. Protoplasma 233:95–106

    Article  PubMed  CAS  Google Scholar 

  • Sawidis T, Reiss H-D (1995) Effects of heavy metals on pollen tube growth and ultrastructure. Protoplasma 185:113–122

    Article  CAS  Google Scholar 

  • Sawidis T, Eleftheriou EP, Tsekos I (1987) The floral nectaries of Hibiscus rosa-sinensis L.: I. Development of the secretory hairs. Ann Bot 59:643–652

    Google Scholar 

  • Sawidis T, Eleftheriou EP, Tsekos I (1989) The floral nectaries of Hibiscus rosa-sinensis L.: III. A morphometric and ultrastructural approach. Nord J Bot 9:63–71

    Article  Google Scholar 

  • Schiariti A, Juarez AB, Rodrıguez MC (2004) Effects of sublethal concentrations of copper on three strains of green microalgae under autotrophic and mixotrophic culture conditions. Algol Stud 114:43–157

    Article  Google Scholar 

  • Singh RP, Agrawal M (2007) Effects of sewage sludge amendment on heavy metal accumulation and consequent responses of Beta vulgaris plants. Chemosphere 67:2229–2240

    Article  PubMed  CAS  Google Scholar 

  • Souza JF, Rauser WE (2003) Maize and radish sequester excess cadmium and zinc in different ways. Plant Sci 165:1009–1022

    Article  CAS  Google Scholar 

  • Srivastava AK, Ramaswamy NK, Mukhopadhyaya R, Chiramal Jincy MG, D’Souza SF (2009) Thiourea modulates the expression and activity profile of mtATPase under salinity stress in seeds of Brassica juncea. Ann Bot 103:403–410

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Stebbing ARD (1998) A theory for growth hormesis. Mutat Res 403:249–258

    Article  PubMed  CAS  Google Scholar 

  • Sze H, Schumacher K, Muller ML, Padmanaban S, Taiz L (2002) A simple nomenclature for a complex proton pump: VHA genes encode the vacuolar H(+)-ATPase. Trends Plant Sci 7:157–161

    Article  PubMed  CAS  Google Scholar 

  • Tewari RK, Hahn EJ, Paek KY (2008) Modulation of copper toxicity induced oxidative damage by nitric oxide supply in the adventitious roots of Panax ginseng. Plant Cell Rep 27:171–181

    Article  PubMed  CAS  Google Scholar 

  • Van Assche F, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13:195–206

    Article  Google Scholar 

  • Vankar PS, Sarswat R, Sahu R (2012) Biosorption of zinc ions from aqueous solutions onto natural dye waste of Hibiscus rosa sinensis: thermodynamic and kinetic studies. Environ Progr Sustain Energy 31:89–99

    Article  CAS  Google Scholar 

  • Vermes I, Haanen C, Reutelingsperger C (2000) Flow cytometry of apoptotic cell death. J. Immunol Methods 243:167–190

    Article  CAS  Google Scholar 

  • Verstraeten SV, Zago MP, Mackenzie GG, Keen CL, Oteiza PI (2004) Influence of zinc deficiency on cell-membrane fluidity in Jurkat, 3T3 and IMR-32 cells. Biochem J 378:579–587

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wang C, Zhang SH, Wang PF, Qian J, Hou J, Zhang WJ, Lu J (2009) Excess Zn alters the nutrient uptake and induces the antioxidative responses in submerged plant Hydrilla verticillata (L.f.) Royle. Chemosphere 76:938–945

    Article  PubMed  CAS  Google Scholar 

  • Zhu J-K, Hasegawa PM, Bressan RA (1997) Molecular aspects of osmotic stress in plants. CRC Crit Rev Plant Sci 16:253–277

    Article  CAS  Google Scholar 

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Correspondence to Thomas Sawidis.

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Handling Editor: Peter Nick

Dedicated to Em. Prof. Dr. Eberhard Schnepf — teacher, colleague and friend.

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Sawidis, T., Papadopoulou, A. & Voulgaropoulou, M. Effect of zinc on nectar secretion of Hibiscus rosa-sinensis L. Protoplasma 251, 575–589 (2014). https://doi.org/10.1007/s00709-013-0557-0

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