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Ni2+ effects on Nicotiana tabacum L. pollen germination and pollen tube growth

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Abstract

To investigate the mechanisms of Ni2+ effects on initiation and maintenance of polar cell growth, we used a well-studied model system—germination of angiosperm pollen grains. In liquid medium tobacco pollen grain forms a long tube, where the growth is restricted to the very tip. Ni2+ did not prevent the formation of pollen tube initials, but inhibited their subsequent growth with IC50 = 550 μM. 1 mM Ni2+ completely blocked the polar growth, but all pollen grains remained viable, their respiration was slightly affected and ROS production did not increase. Addition of Ni2+ after the onset of germination had a bidirectional effect on the tubes development: there was a considerable amount of extra-long tubes, which appeared to be rapidly growing, but the growth of many tubes was impaired. Studying the localization of possible targets of Ni2+ influence, we found that they may occur both in the wall and in the cytoplasm, as confirmed by specific staining. Ni2+ disturbed the segregation of transport vesicles in the tips of these tubes and significantly reduced the relative content of calcium in the aperture area of pollen grains, as measured by X-ray microanalysis. These factors are considered being critical for normal polar cell growth. Ni2+ also causes the deposition of callose in the tips of the tube initials and the pollen tubes that had stopped their growth. We can assume that Ni2+-induced disruption of calcium homeostasis can lead to vesicle traffic impairment and abnormal callose deposition and, consequently, block the polar growth.

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References

  • Bansal P, Sharma P, Goyal V (2002) Impact of lead and cadmium on enzyme of citric acid cycle in germinating pea seeds. Biol Plantarum 45:125–127

    Article  CAS  Google Scholar 

  • Bhandal IS, Bala R (1989) Heavy metal inhibition of in vitro pollen germination and pollen tube growth in Amaryllis vittata (Ait). Curr Sci 58:379–380

    CAS  Google Scholar 

  • Breygina MA, Matveeva NP, Ermakov IP (2009) The role of Cl− in pollen germination and tube growth. Russ J Dev Biol 39:157–164

    Article  Google Scholar 

  • Bushart TJ, Roux SJ (2007) Conserved features of germination and polarized cell growth: a few insights from a pollen–fern spore comparison. Ann Bot 99:9–17

    Article  PubMed  CAS  Google Scholar 

  • Chen C, Huang D, Liu J (2009) Functions and toxicity of nickel in plants: recent advances and future prospects. Clean 37:304–313

    CAS  Google Scholar 

  • Cheung AY, Wu H-M (2008) Structural and signaling networks for the polar cell growth machinery in pollen tubes. Annu Rev Plant Biol 59:547–572

    Article  PubMed  CAS  Google Scholar 

  • Ferguson C, Teeri TT, Siika-aho M, Read SM, Bacic A (1998) Location of cellulose and callose in pollen tubes and grains of Nicotiana tabacum. Planta 206:452–460

    Article  CAS  Google Scholar 

  • Fowler JE, Quatrano RS (1997) Plant cell morphogenesis: plasma membrane interactions with the cytoskeleton and cell wall. Annu Rev Cell Dev Biol 13:697–743

    Article  PubMed  CAS  Google Scholar 

  • Geitmann A, Emons AMC (2000) The cytoskeleton in plant and fungal cell tip growth. J Microsc 198:218–245

    Article  PubMed  CAS  Google Scholar 

  • Geitmann A, Steer M (2006) The architecture and properties of the pollen tube cell wall. In: Malho R (ed) The pollen tube. Springer, Berlin, pp 47–69

    Google Scholar 

  • Gramlich A, Moradi AB, Robinson BH, Kaestner A, Schulin R (2011) Dimethylglyoxime (DMG) staining for semi-quantitative mapping of Ni in plant tissue. Environ Exp Bot 71:232–240

    Article  CAS  Google Scholar 

  • Gür N, Topdemir A (2008) Effects of some heavy metals on in vitro pollen germination and tube growth of apricot (Armenica vulgaris Lam.) and cherry (Cerasus avium L.). World Appl Sci J 4:195–198

    Google Scholar 

  • Halliwell B, Whiteman M (2004) Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean? Br J Pharmacol 142:231–255

    Google Scholar 

  • Heslop-Harrison J (1987) Pollen germination and pollen-tube growth. Int Rev Cytol 107:1–78

    Article  Google Scholar 

  • Heslop-Harrison J, Heslop-Harrison Y, Shivanna KR (1984) The evaluation of pollen quality, and a further appraisal of the fluorochromatic (FCR) test procedure. Theor Appl Genet 67:367–375

    Article  Google Scholar 

  • Iwano M, Shiba H, Miwa T, Che FS, Takayama S, Nagai T, Miyawaki A, Isogai A (2004) Ca2+ dynamics in a pollen grain and papilla cell during pollination of Arabidopsis. Plant Physiol 136:3562–3571

    Article  PubMed  CAS  Google Scholar 

  • Jackson SL, Heath IB (1993) Roles of calcium ions in hyphal tip growth. Microbiol Rev 57:367–382

    PubMed  CAS  Google Scholar 

  • Krämer U, Clemens S (2005) Functions and homeostasis of zinc, copper, and nickel in plants. In: Tamás M, Martinoia E (eds) Molecular biology of metal homeostasis and detoxification. Topics in current genetics 14. Springer, Berlin, pp 216–271

    Google Scholar 

  • Krzesłowska M (2011) The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiol Plant 33:35–51

    Article  Google Scholar 

  • Lu H, Shi X, Costa M, Huang C (2005) Carcinogenic effect of nickel compounds. Mol Cell Biochem 279:45–67

    Article  PubMed  CAS  Google Scholar 

  • M’Bemba-Meka P, Lemieux N, Chakrabarti SK (2006) Role of oxidative stress, mitochondrial membrane potential, and calcium homeostasis in human lymphocyte death induced by nickel carbonate hydroxide in vitro. Arch Toxicol 80:405–420

    Article  PubMed  Google Scholar 

  • Macomber L, Hausinger RP (2011) Mechanisms of nickel toxicity in microorganisms. Metallomics 3:1153–1162

    Article  PubMed  CAS  Google Scholar 

  • Malhó R, Read ND, Trewavas AJ, Pais MS (1995) Calcium channel activity during pollen tube growth and reorientation. Plant Cell 7:1173–1184

    PubMed  Google Scholar 

  • Malhó R, Coelho CP, Pierson E, Derksen J (2005) Endocytosis and membrane recycling in pollen tubes. In: Samaj J, Baluska F, Menzel D (eds) Plant endocytosis. Springer, Berlin, pp 277–291

    Chapter  Google Scholar 

  • Meychik NR, Matveyeva NP, Nikolaeva YuI, Chaikova AV, Yermakov IP (2006) Features of ionogenic group composition in polymeric matrix of lily pollen wall. Biochem (Moscow) 71:893–899

    Article  CAS  Google Scholar 

  • Meychik NR, Nikolaeva YuI, Komarynets OV, Ermakov IP (2011) Barrier function of the cell wall during uptake of nickel ions. Russ J Plant Physiol 58:409–414

    Article  CAS  Google Scholar 

  • Mohsenzadeh F, Chehregani A, Yousefi N (2011) Effect of the heavy metals on developmental stages of ovule, pollen, and root proteins in Reseda lutea L. (Resedaceae). Biol Trace Elem Res 143:1777–1788

    Article  PubMed  CAS  Google Scholar 

  • Obejero-Paz CA, Gray IP, Jones SW (2008) Ni2+ block of CaV3.1 (α1G) T-type calcium channels. J Gen Physiol 132:239–250

    Article  PubMed  CAS  Google Scholar 

  • Palanivelu R, Preuss D (2000) Pollen tube targeting and axon guidance: parallels in tip growth mechanisms. Trends Cell Biol 10:517–524

    Article  PubMed  CAS  Google Scholar 

  • Parre E, Geitmann A (2005) Pectin and the role of the physical properties of the cell wall in pollen tube growth of Solanum chacoense. Planta 220:582–592

    Article  PubMed  CAS  Google Scholar 

  • Přibyl P, Cepák V, Zachleder V (2008) Cytoskeletal alterations in interphase cells of the green alga Spirogyra decimina in response to heavy metals exposure: II. The effect of aluminium, nickel and copper. Toxicol In Vitro 22:1160–1168

    Article  PubMed  Google Scholar 

  • Ragsdale SW (2009) Nickel-based enzymatic systems. J Biol Chem 284:18571–18575

    Article  PubMed  CAS  Google Scholar 

  • Reese RN, Roberts LW (1985) Effects of cadmium on whole cell and mitochondrial respiration in tobacco cell suspension cultures (Nicotiana tabacum L. var. xanthi). J Plant Physiol 120:123–130

    Article  CAS  Google Scholar 

  • Sabrine H, Afif H, Mohamed B, Hamadi B, Maria H (2010) Effects of cadmium and copper on pollen germination and fruit set in pea (Pisum sativum L.). Sci Hortic 125:551–555

    Article  CAS  Google Scholar 

  • Samaj J (2005) Methods and molecular tools for studying endocytosis in plants—an overview. In: Samaj J, Baluska F, Menzel D (eds) Plant endocytosis. Springer, Berlin, pp 1–17

    Chapter  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sheng S, Perry CJ, Kleyman TR (2002) External nickel inhibits epithelial sodium channel by binding to histidine residues within the extracellular domains of α and γ subunits and reducing channel open probability. J Biol Chem 277:50098–50111

    Google Scholar 

  • Sheng X, Zhang S, Jiang L, Li K, Gao Y, Li X (2012) Lead stress disrupts the cytoskeleton organization and cell wall construction during Picea wilsonii pollen germination and tube growth. Biol Trace Elem Res 146:86–93

    Google Scholar 

  • Smirnova AV, Matveyeva NP, Polesskaya OG, Yermakov IP (2009) Generation of reactive oxygen species during pollen grain germination. Russ J Develop Biol 40:345–353

    Article  CAS  Google Scholar 

  • Speranza A, Ferri P, Battistelli M, Falcieri E, Crinelli R, Scoccianti V (2007) Both trivalent and hexavalent chromium strongly alter in vitro germination and ultrastructure of kiwifruit pollen. Chemosphere 66:1165–1174

    Article  PubMed  CAS  Google Scholar 

  • Speranza A, Taddei AR, Gambellini G, Ovidi E, Scoccianti V (2009) The cell wall of kiwifruit pollen tubes is a target for chromium toxicity: alterations to morphology, callose pattern and arabinogalactan protein distribution. Plant Biol 11:179–193

    Article  PubMed  CAS  Google Scholar 

  • Tuna AL, Bürün B, Yokaş Ü, Çoban E (2002) The effects of heavy metals on pollen germination and pollen tube length in the tobacco plant. Turk J Biol 26:109–113

    CAS  Google Scholar 

  • Xiong ZT, Peng YH (2001) Response of pollen germination and tube growth to cadmium with special reference to low concentration exposure. Ecotoxicol Environ Saf 48:51–55

    Article  PubMed  CAS  Google Scholar 

  • Yusuf M, Fariduddin Q, Hayat S, Ahmad A (2011) Nickel: an overview of uptake, essentiality and toxicity in plants. Bull Environ Contam Toxicol 86:1–17

    Article  PubMed  CAS  Google Scholar 

  • Zonia L (2010) Spatial and temporal integration of signalling networks regulating pollen tube growth. J Exp Bot 61:1939–1957

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the Russian Foundation for Basic Research (projects 11-04-00605-a and 10-04-00945-a).

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Authors and Affiliations

  1. Department of Plant Physiology, School of Biology, Lomonosov Moscow State University, 119991, Moscow, Russia

    Maria Breygina, Natalie Matveyeva, Svetlana Polevova, Natalie Meychik, Yulia Nikolaeva, Anna Mamaeva & Igor Yermakov

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  1. Maria Breygina
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  2. Natalie Matveyeva
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  3. Svetlana Polevova
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  4. Natalie Meychik
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  5. Yulia Nikolaeva
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  7. Igor Yermakov
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Correspondence to Maria Breygina.

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Breygina, M., Matveyeva, N., Polevova, S. et al. Ni2+ effects on Nicotiana tabacum L. pollen germination and pollen tube growth. Biometals 25, 1221–1233 (2012). https://doi.org/10.1007/s10534-012-9584-0

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  • DOI: https://doi.org/10.1007/s10534-012-9584-0

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