Cadmium and zinc induced similar changes in protein and glycoprotein patterns in tobacco (Nicotiana tabacum L.) seedlings and plants

Arhiv za Higijenu Rada i Toksikologiju

Volumn 63, Issue 3, 2012, Pages 321-335

  Peharec Štefanić, Petra ^a   Šikić, Sandra ^b   Cvjetko, Petra ^a   Balen, Biljana ^a  

^a UNIVERSITY OF ZAGREB   (Croatia)

^b Zagreb Institute of Public Health   (Croatia)

Author keywords

Heavy metals; Lectins; Protein pattern

Indexed keywords

CADMIUM; GLYCOPROTEIN; PLANT LECTIN; POLYPEPTIDE; VEGETABLE PROTEIN; ZINC;

ABIOTIC STRESS; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL FACTOR; NONHUMAN; PLANT LEAF; PLANT ROOT; PLANT STRESS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN GLYCOSYLATION; SEEDLING; TOBACCO;

NICOTIANA TABACUM;

CADMIUM; COMPLEX MIXTURES; GENE EXPRESSION REGULATION, PLANT; GLYCOSYLATION; HUMANS; OXIDATIVE STRESS; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; SEEDLING; TOBACCO; ZINC;

EID: 84874337611     PISSN: 00041254     EISSN: None     Source Type: Journal    
DOI: 10.2478/10004-1254-63-2012-2173     Document Type: Article

References (77)

1. Das P, Samantaray S, Rout GR. Studies on cadmium toxicity in plants: a review. Environ Pollut 1997;98:29-36.
2. Skórzyńska-Polit E, Baszyński T. Differences in sensitivity of the photosynthetic apparatus in Cd-stressed runner bean plants in relation to their age. Plant Sci 1997;128:11-21.
3. Sanità di Toppi L, Gabbrielli R. Response to cadmium in higher plants. Environ Exp Bot 1999;41:105-30.
4. Shah K, Kumar RG, Verma S, Dubey RS. Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 2001;161:1135-44.
5. Romero-Puertas MC, Palma JM, Gómez M, del Río LA, Sandalio LM. Cadmium causes the oxidative modifications of proteins in pea plants. Plant Cell Environ 2002;25:677-86.
6. Aravind P, Prasad MNV. Zinc alleviates cadmium-induced oxidative stress in Ceratophyllum demersum L.: a free floating freshwater macrophyte. Plant Physiol Biochem 2003;41:391-7.
7. Aravind P, Prasad MNV. Modulation of cadmium-induced oxidative stress in Caratophyllum demersum by zinc involves ascorbate-glutathion cycle and glutathione metabolism. Plant Physiol Biochem 2005;43:107-16.
8. Vallee BL, Falchuk KH. The biochemical basis of zinc physiology. Physiol Rev 1993;73:79-118.
9. Ullrich SM, Ramsey MH, Helios-Rybicka E. Total and exchangeable concentrations of heavy metal in soils near Bytom, an area of Pb/Zn mining and smelting in upper Silesia, Poland. Appl Geochem 1999;14:187-96.
10. Wu F, Zhang G. Alleviation of cadmium-toxicity by application of zinc and ascorbic acid in barley. J Plant Nutr 2002;25:2745-61.
11. Hassan MJ, Zhang G, Wu F, Wie K, Chen Z. Zinc alleviates growth inhibition and oxidative stress caused by cadmium in rice. J Plant Nutr Soil Sci 2005;168:255-61.
12. Tkalec M, Prebeg T, Roje V, Pevalek-Kozlina, Ljubešić N. Cadmium induced responses in duckweed Lemna minor L. Acta Physiol Plant 2008;30:881-90.
13. Jomová K, Morovič M. Effect of heavy metal treatment on molecular changes in root tips of Lupinus luteus L. Czech J Food Sci 2009;27(Special issue):S386-9.
14. Siedlecka A. Some aspects of interactions between heavy metals and plant mineral nutrients. Acta Soc Bot Pol 1995;64:265-72.
15. AI-Rumaih MM, Rushdy SS, Warsy AS. Alteration in the protein electrophoretic patterns of cowpea, (Vigna unguiculata L.) treated with cadmium in the presence or absence of gibberellic acid. Saudi J Biol Sci 2002;9:47-56.
16. Sobkowiak R, Deckert J. Proteins induced by cadmium in soybean cells. J Plant Physiol 2006;163:1203-6.
17. Pós V, Hunyadi-Gulyás É, Caiazzo R, Jócsák I, Medzihradszky KF, Lukács N. Induction of pathogenesis-related proteins in intercellular fluid by cadmium stress in barley (Hordeum vulgare L.) - A proteomic analysis. Acta Aliment 2011;40:164-75.
18. Ahsan N, Lee SH, Lee DG, Lee H, Lee SW, Bahk JD, Lee BH. Physiological and protein profiles alternation of germinating rice seedlings exposed to acute cadmium toxicity. C R Biol 2007;330:735-46.
19. Stevens LH, Stoopen GM, Elbers IJ, Molthoff JW, Bakker HAC, Lommen A, Bosch D, Jordi W. Effect of climate conditions and plant developmental stage on the stability of antibodies expressed in transgenic tobacco. Plant Physiol 2000;124:173-82.
20. Elbers I JW, Stoopen GM, Bakker H, Stevens LH, Bardor M, Molthoff JW, Jordi WJRM, Bosch D, Lommen A. Influence of growth conditions and developmental stage on N-glycan heterogeneity of transgenic immunoglobulin G and endogenous proteins in tobacco leaves. Plant Physiol 2001;126:1314-22.
21. Krsnik-Rasol M, Čipčić H, Poljuha D, Hagége D. Electrophoretic protein patterns of sugar beet tissue lines. Phyton 2000;41:13-20.
22. Balen B, Milošević J, Krsnik-Rasol M. Protein and glycoprotein patterns related to morphogenesis in Mammillaria gracillis Pfeiff. tissue culture. Food Technol Biotechnol 2002;40:275-80.
23. Pavoković D, Šola I, Hagége D, Krsnik-Rasol M. Sugarinduced changes in cellular and extracellular protein and glycoprotein patterns of sugarbeet cell lines. Acta Bot Croat 2007;66:127-34.
24. Balen B, Zamfir A, Vakhrushev SY, Krsnik-Rasol M, Peter-Katalinić J. Determination of Mammillaria gracillis N-glycan patterns by ESI Q-TOF mass spectrometry. Croat Chem Acta 2005;78: 463-77.
25. Balen B, Krsnik-Rasol M, Zamfir AD, Milošević J, Vakhrushev SY, Peter-Katalinić J. Glycoproteomic survey of Mammillaria gracillis tissues grown in vitro. J Proteome Res 2006;5:1658-66.
26. Balen B, Krsnik-Rasol M, Zamfir AD, Zadro I, Vakhrushev SY, Peter-Katalinić J. Assessment of N-glycan heterogeneity of cactus glycoproteins by one-dimensional gel electrophoresis and matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. J Biomol Tech 2007;18:150-60.
27. Balen B, Peharec P, Krsnik-Rasol M. Developmentally specific soluble and membrane proteins and glycoproteins in Mammillaria gracillis Pfeiff. (Cactaceae) tissue culture. Acta Bot Croat 2008;67:221-7.
28. Koiwa H, Li F, McCully MG, Mendoza I, Koizumi N, Manabe Y, Nakagawa Y, Zhu J, Rus A, Pardo JM, Bressan RA, Hasegawa PM. The STT3a subunit isoform of the Arabidopsis oligosaccharyltransferase controls adaptive responses to salt/osmotic stress. Plant Cell 2003;15:2273-84.
29. Kang JS, Frank J, Kang CH, Kajiura H, Vikram M, Ueda A, Kim S, Bahk JD, Triplett B, Fujiyama K, Lee SY, von Schaewen A, Koiwa H. Salt tolerance of Arabidopsis thaliana requires maturation of N glycosylated proteins in the Golgi. Proc Natl Acad Sci USA 2008;105:5933-8.
30. Komatsu S, Yamada E, Furukawa K. Cold stress changes the concanavalin A-positive glycosylation pattern of proteins expressed in the basal parts of rice leaf sheaths. Amino Acids 2009;36:115-23.
31. Carpena RO, Vázquez S, Esteban E, Fernández-Pascual M, de Felipe MR, Zornoza P. Cadmium-stress in white lupin: effects on nodule structure and functioning. Plant Physiol Biochem 2003;41:911-9.
32. Zhang M, Henquet M, Chen Z, Zhang H, Zhang Y, Ren X, van der Krol S, Gonneau M, Bosch D, Gong Z. LEW3, encoding a putative alpha-1,2- mannosyltransferase (ALG11) in N-linked glycoprotein, plays vital roles in cell-wall biosynthesis and the abiotic stress response in Arabidopsis thaliana. Plant J 2009;60:983-99.
33. Johnson KL, Jones BJ, Bacic A, Schultz CJ. The fasciclinlike arabinogalactan proteins of Arabidopsis. A multigene family of putative cell adhesion molecules. Plant Physiol 2003;133:1911-25.
34. Havir EA, Brisson LF, Zelitch I. Distribution of catalase isoforms in Nicotiana tabacum. Phytochemistry 1996;41:699-702.
35. Ganapathi TR, Suprasanna P, Rao PS, Bapat VA. Tobacco (Nicotiana tabacum L.) - A model system for tissue culture interventions and genetic engineering. Indian J Biotechnol 2004;3:171-84.
36. Garnier L, Simon-Plas F, Thuleau P, Agnel JP, Blein JP, Ranjeva R, Montillet JL. Cadmium affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity. Plant Cell Environ 2006;29:1956-69.
37. Gratão PL, Pompeu GB, Capaldi FR, Vitorello VA, Lea PJ, Azevedo RA. Antioxidant response of Nicotiana tabacum cv. Bright Yellow 2 cells to cadmium and nickel stress. Plant Cell Tiss Organ Cult 2008;94:73-83.
38. Murashige T, Skoog F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Plant Physiol 1962;15:473-97.
39. Gichner T, Ptácek O, Stavreva DA, Plewa MJ. Comparison of DNA damage in plants as measured by single cell gel electrophoresis and somatic leaf mutations induced by monofunctional alkylating agents. Environ Mol Mutagen 1999;33:279-86.
40. Staples RC, Stahmann MA. Changes in proteins and several enzymes in susceptible bean leaves after infection by the bean rust fungus. Phytopatology 1964;54:760-4.
41. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-54.
42. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227:680-5.
43. Blum H, Beier H, Gross HJ. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 1987;8:93-9.
44. Hrubá P, Tupý J. N-glycoproteins specific for different stages of microspore and pollen development in tobacco. Plant Sci 1999;141:29-40.
45. Yamashita K, Totani K, Ohkura T, Takasaki S, Goldstein IJ, Kobata A. Carbohydrate binding properties of complex-type oligosaccharides on immobilized Datura stramonium lectin. J Biol Chem 1987;262:1602-7.
46. Mérant C, Messouak A, Cadoré JL, Monier JC. PNA-binding glycans are expressed at high levels on horse mature and immature T lymphocytes and a subpopulation of B lymphocytes. Glycoconj J 2005;22:27-34.
47. Shah MM, Fujiyama K, Flynn CR, Joshi L. Sialylated endogenous glycoconjugates in plant cells. Nature Biotechnol 2003;21:1470-1.
48. Rangan L, Vogel C, Srivastava AK. Analysis of context sequence surrounding translation initiation site from complete genome of model plants. Mol Biotechnol 2008;39:207-13.
49. Zhang W, Wu Y, Schnable JC, Zeng Z, Freeling M, Crawford GE, Jiang J. High-resolution mapping of open chromatin in the rice genome. Genome Res 2012;22:151-62.
50. Kyndt T, Denil S, Haegeman A, Trooskens G, De Meyer T, Van Criekinge W, Gheysen G. Transcriptome analysis of rice mature root tissue and root tips in early development by massive parallel sequencing. J Exp Bot 2012;63: 2141-57.
51. Qureshi MI, Qadir S, Zolla L. Proteomics-based dissection of stress-responsive pathways in plants. J Plant Physiol 2007;164:1239-60.
52. Porubleva L, Chitnis PR. Proteomics: A powerful tool in the post-genomic era. Indian J Biochem Biophys 2000;37:360-8.
53. Sanita di Toppi L, Gabbrielli R. Response to cadmium in higher plants. Environ Exp Bot 1999;41:105-30.
54. Cobbett CS. Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 2000;123:825-32.
55. Delhaize E, Robinson NJ, Jackson PJ. Effects of cadmium on gene expression in cadmium-tolerant and cadmiumsensitive Datura innoxia cells. Plant Mol Biol 1989;12:487-97.
56. Grünhage L, Weigel H, Ilge D, Jäger H. Isolation and partial characterization of a cadmium-binding protein from Pisum sativum. J Plant Physiol 1985;119:327-34.
57. Evans IM, Gatehouse LN, Gatehouse JA, Robinson NJ, Croy RRD. A gene from pea (Pisum sativum L.) with homology to metallothionein genes. FEBS Letters 1990;262:29-32.
58. Zeng XW, Qiu RL, Ying RR, Tang YT, Tang L, Fang XH. The differentially-expressed proteome in Zn/Cd hyperaccumulator Arabis paniculata Franch. in response to Zn and Cd. Chemosphere 2011;82:321-8.
59. Hirano Y, Tsumuraya Y, Hashimoto Y. Characterization of spinach leaf α-l-arabinofuranosidases and β-galactosidases and their synergistic action on an endogenous arabinogalactanprotein. Physiol Plant 1994;92:286-96.
60. Kataoka T, Furukawa J, Nakanishi TM. The decrease of extracted apoplast protein in soybean root tip by aluminium treatment. Biol Plant 2003;36:445-9.
61. Scheel T, Pritsch K, Schloter M, Kalbitz K. Precipitation of enzymes and organic matter by aluminum - Impacts on carbon mineralization. J Plant Nutr Soil Sci 2008;171:900-7.
62. Maksymiec W. Signaling responses in plants to heavy metal stress. Acta Physiol Plant 2007;29:177-87.
63. Hossain Z, Nouri M-Z, Komatsu S. Plant cell organelle proteomics in response to abiotic stress. J Proteome Res 2012;11:37-48.
64. Almagro L, Gómez Ros LV, Belchi-Navarro S, Bru R, Ros Barceló A, Pedreño MA. Class III peroxidases in plant defence reactions. J Exp Bot 2009;60:377-90.
65. Hirabayashi J. Lectin-based structural glycomics: Glycoproteomics and glycan profiling. Glycoconj J 2004;21:35-40.
66. Kuno A, Uchiyama N, Koseki-Kuno S, Ebe Y, Takashima S, Yamada M, Hirabayashi J. Evanescent-field fluorescenceassisted lectin microarray: a new strategy for glycan profiling. Nat Methods 2005;2:851-6.
67. Zhang H, Ohyama K, Boudet J, Chen Z, Yang J, Zhang M, Muranaka T, Maurel C, Zhu JK, Gong Z. Dolichol biosynthesis and its effects on the unfolded protein response and abiotic stress resistance in Arabidopsis. Plant Cell 2008;20:1879-98.
68. Fitchette AC, Gomord V, Chekkafi A, Faye L. Distribution of xylosylation and fucosylation in the plant Golgi apparatus. Plant J 1994;5:673-82.
69. Oxley D, Munro SL, Craik DJ, Bacic A. Structure of Nglycans on the S3- and S6-allele stylar self-incompatibility ribonucleases of Nicotiana alata. Glycobiology 1996;6:611-8.
70. Frank J, Kaulfürst-Soboll H, Rips S, von Schaewen A. Comparative analyses of Arabidopsis complex glycan1 mutants and genetic interaction with staurosporin and temperature sensitive3a. Plant Physiol 2008;148:1354-67.
71. von Schaewan A, Frank J, Koiwa H. Role of complex N-glycans in plant stress tolerance. Plant Signal Behav 2008;3:871-3.
72. Seifert GJ, Roberts K. The biology of arabinogalactan proteins. Annu Rev Plant Biol 2007;58:137-61.
73. Gomord V, Fitchette AC, Menu-Bouaouiche L, Saint-Jore- Dupas C, Plasson C, Michaud D, Faye L. Plant-specific glycosylation patterns in the context of therapeutic protein production. Plant Biotechnol J 2010;8:564-87.
74. Arillo A, Margiocco C. Melodia F. The gill sialic acid content as an index of environmental stress in rainbow trout, Salmo gairdneri, Richardson. J Fish Biol 1979;15:405-10.
75. Honglertsakul C, Opanuraks J, Kittikowit W, Boonla C, Wunsuwan R, Tosukhowong P. Increased urinary excretions of oxidative stress biomarkers and sialic acid associated with severity of bladder tumors. Thai J Surg 2007;28:133-7.
76. Goswami K, Nandeesha H, Koner BC, Nandakumar DN. A comparative study of serum protein-bound sialic acid in benign and malignant prostatic growth: possible role of oxidative stress in sialic acid homeostasis. Prostate Cancer Prostatic Dis 2007;10:356-9.
77. Erdogan HM, Karapehlivan M, Citil M, Atakisi O, Uzlu E, Unver A. Serum sialic acid and oxidative stress parameters changes in cattle with leptospirosis. Vet Res Commun 2008;32:333-9.