Contribution of proteomic studies towards understanding plant heavy metal stress response

Frontiers in Plant Science

Volumn 3, Issue JAN, 2013, Pages

  Hossain, Zahed ^a   Komatsu, Setsuko ^b  

^a WEST BENGAL STATE UNIVERSITY   (India)

^b NATIONAL INSTITUTE OF CROP SCIENCE   (Japan)

Author keywords

Antioxidant; Heavy metal; HSPs; Phytochelatins; PR protein; Proteomics

Indexed keywords

EID: 84884208029     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2012.00310     Document Type: Review

References (90)

1. Ahsan, N., Nakamura, T., and Komatsu, S. (2012). Differential responses of microsomal proteins and metabolites in two contrasting cadmium (Cd)-accumulating soybean cultivars under Cd stress. Amino Acids 42, 317-327.
2. Ahsan, N., Lee, D. G., Alam, I., Kim, P. J., Lee, J. J., Ahn, Y. O., et al. (2008). Comparative proteomic study of arsenic-induced differentially expressed proteins in rice roots reveals glutathione plays a central role during As stress. Proteomics 8, 3561-3576.
3. Ahsan, N., Lee, D. G., Kim, K. H., Alam, I., Lee, S. H., Lee, K. W., et al. (2010). Analysis of arsenic stress-induced differentially expressed proteins in rice leaves by two-dimensional gel electrophoresis coupled with mass spectrometry. Chemosphere 78, 224-231.
4. Ahsan, N., Lee, D. G., Lee, S. H., Kang, K. Y., Lee, J. J., Kim, P. J., et al. (2007b). Excess copper induced physiological and proteomic changes in germinating rice seeds. Chemosphere 67, 1182-1193.
5. Ahsan, N., Lee, S. H., Lee, D. G., Lee, H., Lee, S. W., Bahk, J. D., et al. (2007a). Physiological and protein profiles alternation of germinating rice seedlings exposed to acute cadmium toxicity. C. R. Biol. 330, 735-746.
6. Ahsan, N., Renaut, J., and Komatsu, S. (2009). Recent developments in the application of proteomics to the analysis of plant responses to heavy metals. Proteomics 9, 2602-2621.
7. Aina, R., Labra, M., Fumagalli, P., Vannini, C., Marsoni, M., Cucchi, U., et al. (2007). Thiol-peptide level and proteomic changes in response to cadmium toxicity in Oryza sativa L. roots. Environ. Exp. Bot. 59, 381-392.
8. Akiyama, T., Pillai, M. A., and Sentoku N. (2004). Cloning, characterization and expression of OsGLN2, a rice endo-1, 3-beta-glucanase gene regulated developmentally in flowers and hormonally in germinating seeds. Planta 220, 129-139.
9. Alvarez, S., Berla, B. M., Sheffield, J., Cahoon, R. E., Jez, J. M., and Hicks, L. M. (2009). Comprehensive analysis of the Brassica juncea root proteome in response to cadmium exposure by complementary proteomic approaches. Proteomics 9, 2419-2431.
10. Alves, M., Moes, S., Jenö, P., Pinheiro, C., Passarinho, J., and Ricardo, C. P. (2011). The analysis of Lupinus albusroot proteome revealed cytoskeleton altered features due to long-term boron deficiency. J. Proteomics 74, 1351-1363.
11. Barber, D. J. W., and Thomas, J. K. (1978). Reactions of radicals with lecithin bilayers. Radiat. Res. 74, 51-65.
12. Barranco-Medina, S., Lázaro, J. J., and Dietz, K. J. (2009). The oligomeric conformation of peroxiredoxins links redox state to function. FEBS Lett. 583, 1809-1816.
13. Bohnert, H. J., Gong, Q., Li, P., and Ma, S. (2006). Unraveling abiotic stress tolerance mechanisms-getting genomics going. Curr. Opin. Plant Biol. 9, 180-188.
14. Bona, E., Marsano, F., Massa, N., Cattaneo, C., Cesaro, P., Argese, E., et al. (2011). Proteomic analysis as a tool for investigating arsenic stress in Pteris vittata roots colonized or not by arbuscular mycorrhizal symbiosis. J. Proteomics 74, 1338-1350.
15. Bona, E., Marsano, F., Cavaletto, M., and Berta, G. (2007). Proteomic characterization of copper stress response in Cannabis sativa roots. Proteomics 7, 1121-1130.
16. Braconi, D., Bernardini, G., and Santucci, A. (2011). Linking protein oxidation to environmental pollutants: redox proteomic approaches. J. Proteomics 74, 2324-2337.
17. Bubb, J. M., and Lester, J. N. (1991). The impact of heavy metals on lowland rivers and the implications for man and the environment. Sci. Total Environ. 100, 207-233.
18. Cobbett, C. S. (2000). Phytochelatins and their roles in heavy metal detoxification. Plant Physiol. 123, 825-832.
19. Cobbett, C., and Goldsbrough, P. (2002). Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu. Rev. Plant Biol. 53, 159-182.
20. Di Baccio, D., Kopriva, S., Sebastiani, L., and Rennenberg, H. (2005). Does glutathione metabolism have a role in the defence of poplar against zinc excess? New Phytol. 167, 73-80.
21. Didierjean, L., Frendo, P., Nasser, W., Genot, G., Marivet, J., and Burkard, G. (1996). Heavy-metal-responsive genes in maize: identification and comparison of their expression upon various forms of abiotic stress. Planta 199, 1-8.
22. Dietz, K. J. (2003). Plant peroxiredoxins. Annu. Rev. Plant Biol. 54, 93-107.
23. Dietz, K. J., Jacob, S., Oelze, M. L., Laxa, M., Tognetti, V., de Miranda, S. M., et al. (2006). The function of peroxiredoxins in plant organelle redox metabolism. J. Exp. Bot. 57, 1697-1709.
24. Dowling, V. A., and Sheehan, D. (2006). Proteomics as a route to identification of toxicity targets in environmental toxicology. Proteomics 6, 5597-5604.
25. Durand, T. C., Sergeant, K., Planchon, S., Carpin, S., Label, P., Morabito, D., et al. (2010). Acute metal stress in Populus tremula × P. alba (717-1B4 genotype): leaf and cambial proteome changes induced by cadmium(2+). Proteomics 10, 349-368.
26. Durrant, W. E., and Dong, X. (2004). Systemic acquired resistance. Annu. Rev. Phytopathol. 42, 185-209.
27. Duquesnoy, I., Goupil, P., Nadaud, I., Branlard, G., Piquet-Pissaloux, A., and Ledoigt, G. (2009). Identification of Agrostis tenuis leaf proteins in response to As(V) and As(III) induced stress using a proteomics approach. Plant Sci. 176, 206-213.
28. Edreva, A. (2005). Pathogenesis-related proteins. Research progress in the last 15 years. Gen. Appl. Plant Physiol. 31, 105-124.
29. Elvira, M. I., Galdeano, M. M., Gilardi, P., García-Luque, I., and Serra, M. T. (2008). Proteomic analysis of pathogenesis-related proteins (PRs) induced by compatible and incompatible interactions of pepper mild mottle virus (PMMoV) in Capsicum chinense L3 plants. J. Exp. Bot. 59, 1253-1265.
30. Ercal, N., Gurer-Orhan, H., and Aykin-Burns, N. (2001). Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Curr. Top. Med. Chem. 1, 529-539.
31. Espartero, J., Sanchez-Aguayo, I., and Pardo, J. M. (1995). Molecular characterization of glyoxalase-I from a higher plant; upregulation by stress. Plant Mol. Biol. 29, 1223-1233.
32. Farinati, S., DalCorso, G., Bona, E., Corbella, M., Lampis, S., Cecconi, D., et al. (2009). Proteomic analysis of Arabidopsis halleri shoots in response to the heavy metals cadmium and zinc and rhizosphere microorganisms. Proteomics 9, 4837-4850.
33. Fecht-Christoffers, M. M., Braun, H. P., Lemaitre-Guillier, C., VanDorsselaer, A., and Horst, W. J. (2003). Effect of manganese toxicity on the proteome of the leaf apoplast in cowpea. Plant Physiol. 133, 1935-1946.
34. Führs, H., Hartwig, M., Molina, L. E., Heintz, D., Van Dorsselaer, A., Braun, H. P., et al. (2008). Early manganese-toxicity response in Vigna unguiculata L.-a proteomic and transcriptomic study. Proteomics 8, 149-159.
35. Grill, E., Loffler, S., Winnacker, E. L., and Zenk, M. H. (1989). Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific gamma-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc. Natl. Acad. Sci. U.S.A. 86, 6838-6842.
36. Gygi, S. P., Rochon, Y., Franza, B. R., and Aebersold, R. (1999). Correlation between protein and mRNA abundance in yeast. Mol. Cell. Biol. 19, 1720-1730.
37. Hajduch, M., Rakwal, R., Agrawal, G. K., Yonekura, M., and Pretova, A. (2001). High-resolution two-dimensional electrophoresis separation of proteins from metal-stressed rice (Oryza sativa L.) leaves: drastic reductions/fragmentation of ribulose-1, 5-bisphosphate carboxylase/oxygenase and induction of stress-related proteins. Electro-phoresis 22, 2824-2831.
38. Hall, J. L. (2002). Cellular mechanisms for heavy metal detoxification and tolerance. J. Exp. Bot. 53, 1-11.
39. Hensel, G., Kunze, G., and Kunze, I. (1999). Expression of the tobacco gene CBP20 in response to developmental stage, wounding, salicylic acid and heavy metals. Plant Sci. 148, 165-174.
40. Hishiya, S., Hatakeyama, W., Mizota, Y., Hosoya-Matsuda, N., Motohashi, K., Ikeuchi, M., et al. (2008). Binary reducing equivalent pathways using NADPH-thioredoxin reductase and ferredoxin-thioredoxin reductase in the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Cell Physiol. 49, 11-18.
41. Hossain, M. A., Piyatida, P., Teixeira da Silva, J. A., and Fujita, M. (2012a). Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J. Bot. 2012, 1-37.
42. Hossain, Z., Hajika, M., and Komatsu, S. (2012b). Comparative proteome analysis of high and low cadmium accumulating soybeans under cadmium stress. Amino Acids 43, 2393-2416.
43. Hossain, Z., Lopez-Climent, M. F., Arbona, V., Perez-Clemente, R. M., and Gomez-Cadenas, A. (2009). Modulation of the antioxidant system in citrus under waterlogging and subsequent drainage. J. Plant Physiol. 166, 1391-1404.
44. Hossain, Z., Makino, T., and Komatsu, S. (2012c). Proteomic study of β-aminobutyric acid-mediated cadmium stress alleviation in soybean. J. Proteomics 75, 4151-4164.
45. Hossain, Z., Nouri, M. Z., and Komatsu, S. (2012d). Plant cell organelle proteomics in response to abiotic stress. J. Proteome Res. 11, 37-48.
46. Hradilova, J., Rehulka, P., Rehulkova, H., Vrbova, M., Griga, M., and Brzobohaty, B. (2010). Comparative analysis of proteomic changes in contrasting flax cultivars upon cadmium exposure. Electrophoresis 31, 421-431.
47. Jang, H. H., Lee, K. O., Chi, Y. H., Jung, B. G., Park, S. K., Park, J. H., et al. (2004). Two enzymes in one; two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function. Cell 117, 625-635.
48. Jwa, N. S., Agrawal, G. K., Tamogami, S., Yonekura, M., Han, O., Iwahashi, H., et al. (2006). Role of defense/stress related marker genes, proteins and secondary metabolites in defining rice self-defense mechanisms. Plant Physiol. Biochem. 44, 261-273.
49. Kieffer, P., Dommes, J., Hoffmann, L., Hausman, J. F., and Renaut, J. (2008). Quantitative changes in protein expression of cadmium-exposed poplar plants. Proteomics 8, 2514-2530.
50. Kieffer, P., Planchon, S., Oufir, M., Ziebel, J., Dommes, J., Hoffmann, L., et al. (2009). Combining proteomics and metabolite analyses to unravel cadmium stress-response in poplar leaves. J. Proteome Res. 8, 400-417.
51. Komatsu, S., and Ahsan, N. (2009). Soybean proteomics and its application to functional analysis. J. Proteomics 72, 325-336.
52. Kasprzewska, A. (2003). Plant chitinases-regulation and function. Cell. Mol. Biol. Lett. 8, 809-824.
53. Labra, M., Gianazza, E., Waitt, R., Eberini, I., Sozzi, A., Regondi, S., et al. (2006). Zea mays L. protein changes in response to potassium dichromate treatments. Chemosphere 62, 1234-1244.
54. Lee, K., Bae, D. W., Kim, S. H., Han, H. J., Liu, X., Park, H. C., et al. (2010). Comparative proteomic analysis of the short-term responses of rice roots and leaves to cadmium. J. Plant Physiol. 167, 161-168.
55. Liu, J. J., and Ekramoddoullah, A. (2006). The family 10 of plant pathogenesis-related proteins: their structure, regulation, and function in response to biotic and abiotic stresses. Physiol. Mol. Plant Pathol. 68, 3-13.
56. Luque-Garcia, J. L., Cabezas-Sanchez, P., and Camara, C. (2011). Proteomics as a tool for examining the toxicity of heavy metals. Trends Anal. Chem. 30, 703-716.
57. Ma, J. F., Ryan, P. R., and Delhaize, E. (2001). Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci. 6, 273-278.
58. Maksymiec, W. (2007). Signaling responses in plants to heavy metal stress. Acta Physiol. Plant. 29, 177-187.
59. Murphy, A., and Taiz, L. (1995). Comparison of metallothionein gene expression and nonprotein thiols in ten Arabidopsis ecotypes. Correlation with copper tolerance. Plant Physiol. 109, 945-954.
60. Pandey, S., Rai, R., and Rai, L. C. (2012). Proteomics combines morphological, physiological and biochemical attributes to unravel the survival strategy of Anabaena sp. PCC7120 under arsenic stress. J. Proteomics 75, 921-937.
61. Patterson, J., Ford, K., Cassin, A., Natera, S., and Bacic, A. (2007). Increased abundance of proteins involved in phytosiderophore production in boron-tolerant barley. Plant Physiol. 144, 1612-1631.
62. Perfus-Barbeoch, L., Leonhardt, N., Vavasseur, A., and Forestier, C. (2002). Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant J. 32, 539-548.
63. Rakwal, R., Agrawal, G. K., and Yonekura, M. (1999). Separation of proteins from stressed rice (Oryza sativa L.) leaf tissues by two-dimensional polyacrylamide gel electrophoresis: induction of pathogenesis-related and cellular protectant proteins by jasmonic acid, UV irradiation and copper chloride. Electrophoresis 20, 3472-3478.
64. Requejo, R., and Tena, M. (2006). Maize response to acute arsenic toxicity as revealed by proteome analysis of plant shoots. Proteomics 6, S156-S162.
65. Ritter, A., Ubertini, M., Romac, S., Gaillard, F., Delage, L., Mann, A., et al. (2010). Copper stress proteomics highlights local adaptation of two strains of the model brown alga Ectocarpus siliculosus. Proteomics 10, 2074-2088.
66. Rodríguez-Celma, J., Rellan-Alvarez, R., Abadia, A., Abadia, J., and Lopez-Millan, A. F. (2010). Changes induced by two levels of cadmium toxicity in the 2-DE protein profile of tomato roots. J. Proteomics 73, 1694-1706.
67. Salt, D. E., and Rauser, W. E. (1995). MgATP-dependent transport of phytochelatins across the tonoplast of oat roots. Plant Physiol. 107, 1293-1301.
68. Sanita Di Toppi, L., and Gabbrielli, R. (1999). Response to cadmium in higher plants. Environ. Exp. Bot. 41, 105-130.
69. Saravanan, R. S., and Rose, J. K. (2004). A critical evaluation of sample extraction techniques for enhanced proteomic analysis of recalcitrant plant tissues. Proteomics 4, 2522-2532.
70. Sarowar, S., Kim, Y. J., Kim, E. N., Kim, K. D., Hwang, B. K., Islam, R., et al. (2005). Overexpression of a pepper basic pathogenesis-related protein 1 gene in tobacco plants enhances resistance to heavy metal and pathogen stresses. Plant Cell Rep. 24, 216-224.
71. Sarry, J. E., Kuhn, L., Ducruix, C., Lafaye, A., Junot, C., Hugouvieux, V., et al. (2006). The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics 6, 2180-2198.
72. Schneider, T., Schellenberg, M., Meyer, S., Keller, F., Gehrig, P., Riedel, K., et al. (2009). Quantitative detection of changes in the leaf-mesophyll tonoplast proteome in dependency of a cadmium exposure of barley (Hordeum vulgare L.) plants. Proteomics 9, 2668-2677.
73. Semane, B., Dupae, J., Cuypers, A., Noben, J. P., Tuomainen, M., Tervahauta, A., et al. (2010). Leaf proteome responses of Arabidopsis thaliana exposed to mild cadmium stress. J. Plant Physiol. 167, 247-254.
74. Sharma, S. S., and Dietz, K. J. (2009). The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci. 14, 43-50.
75. Sharmin, S. A., Alam, I., Kim, K. H., Kim, Y. G., Kim, P. J., Bahk, J. D., et al. (2012). Chromium-induced physiological and proteomic alterations in roots of Miscanthus sinensis. Plant Sci. 187, 113-126.
76. Tuomainen, M. H., Nunan, N., Lehesranta, S. J., Tervahauta, A. I., Hassinen, V. H., Schat, H., et al. (2006). Multivariate analysis of protein profiles of metal hyperaccumulator Thlaspi caerulescens accessions. Proteomics 6, 3696-3706.
77. van Hoof, N. A., Hassinen, V. H., Hakvoort, H. W., Ballintijn, K. F., Schat, H., Verkleij, J. A., et al. (2001). Enhanced copper tolerance in Silene vulgaris (Moench) Garcke populations from copper mines is associated with increased transcript levels of a 2b-type metallothionein gene. Plant Physiol. 126, 1519-1526.
78. Van Loon, L., and Van Strien, E. (1999). The families of pathogenesis related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol. Mol. Plant Pathol. 55, 85-97.
79. Van Loon, L. C. (1997). Induced resistance in plants and the role of pathogenesis-related proteins. Eur. J. Plant Pathol. 103, 753-765.
80. Vannini, C., Marsoni, M., Domingo, G., Antognoni, F., Biondi, S., and Bracale, M. (2009). Proteomic analysis of chromate-induced modifications in Pseudokirchneriella subcapitata. Chemosphere 76, 1372-1379.
81. Verbruggen, N., Hermans, C., and Schat, H. (2009). Mechanisms to cope with arsenic or cadmium excess in plants. Curr. Opin. Plant Biol. 12, 364-372.
82. Villiers, F., Ducruix, C., Hugouvieux, V., Jarno, N., Ezan, E., Garin, J., et al. (2011). Investigating the plant response to cadmium exposure by proteomic and metabolomic approaches. Proteomics 11, 1650-1663.
83. Wang, L., Zhao, J.-Y., Wu, S.-M., Pan, J.-L., Huang, Z.-B., Wu, Z.-K., et al. (2011). No statistic correlation between superoxide dismutase and peroxidase activities and aluminum-induced lipid peroxidation in maize, implying limited roles of both enzymes in prevention against aluminum-induced lipid peroxidation. Am. J. Plant Sci. 2, 156-164.
84. Wang, W., Vinocur, B., Shoseyov, O., and Altman, A. (2004). Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci. 9, 244-252.
85. Welch, R. M., and Norvell, W. A. (1999) "Mechanisms of cadmium uptake, translocation and deposition in plants, " in Cadmium in Soils and Plants, eds M. J. McLaughlin and B. R. Singh (Dordrecht: The Kluwer Academic Publishers), 125-150.
86. Yadav, S. K., Singla-Pareek, S. L., Ray, M., Reddy, M. K., and Sopory, S. K. (2005). Methylglyoxal levels in plants under salinity stress are dependent on glyoxalase I and glutathione. Biochem. Biophys. Res. Commun. 337, 61-67.
87. Yang, Z., and Chu, C. (2011). "Towards understanding plant response to heavy metal stress, " in Abiotic Stress in Plants-Mechanisms and Adaptations, eds A. Shanker and B. Venkateswarlu (Shanghai: InTech). Available at: http://www.intechopen.com/books/abiotic-stress-in-plants-mechanisms-and-adaptations
88. Yang, Q., Wang, Y., Zhang, J., Shi, W., Qian, C., and Peng, X. (2007). Identification of aluminum-responsive proteins in rice roots by a proteomic approach: cysteine synthase as a key player in Al response. Proteomics 7, 737-749.
89. Zhang, H., Lian, C., and Shen, Z. (2009). Proteomic identification of small, copper-responsive proteins in germinating embryos of Oryza sativa. Ann. Bot. 103, 923-930.
90. Zhen, Y., Qi, J. L., Wang, S. S., Su, J., Xu, G. H., Zhang, M. S., et al. (2007). Comparative proteome analysis of differentially expressed proteins induced by Al toxicity in soybean. Physiol. Plant 131, 542-554.