Recent advances in the analysis of metal hyperaccumulation and hypertolerance in plants using proteomics

Frontiers in Plant Science

Volumn 4, Issue JUL, 2013, Pages

  DalCorso, Giovanni ^a   Fasani, Elisa ^a   Furini, Antonella ^a  

^a UNIVERSITY OF VERONA   (Italy)

Author keywords

Abiotic stress; Heavy metals; Hyperaccumulator hypertolerance; IEF; Proteomics

Indexed keywords

EID: 84895069739     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00280     Document Type: Review

References (57)

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. doi: 10.1007/s00726-010-0809-7
2. 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. doi: 10.1002/pmic.200800478
3. Assunção, A. G. L., Martins, P. D. A. C., Folter, S. D. E., Vooijs, R., Schat, H., and Aarts, M. G. M. (2001). Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens. Plant Cell Environ. 3, 217-226. doi: 10.1111/j.1365-3040.2001.00666.x
4. Baker, A. J. M., McGrath, S. P., Reeves, R. D., and Smith, J. A. C. (2000). "Chapter 5. Metal hyperaccumulator plants: a review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils, " in Phytoremediation of Contamined Soil and Water, eds N. Terry and G. Bañuelos (Boca Raton, FL: CRC Press), 85-107.
5. Becher, M., Talke, I. N., Krall, L., and Krämer, U. (2004). Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J. 37, 251-268. doi: 10.1046/j.1365-313X.2003.01959.x
6. Bona, E., Cattaneo, C., Cesaro, P., Marsano, F., Lingua, G., Cavaletto, M., et al. (2010). Proteomic analysis of Pteris vittata fronds: two arbuscular mycorrhizal fungi differentially modulate protein expression under arsenic contamination. Proteomics 10, 3811-3834. doi: 10.1002/pmic.200900436
7. 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. doi: 10.1016/j.jprot.2011.03.027
8. Boyd, R. S., Davis, M. A., Wall, M. A., and Balkwill, K. (2002). Nickel defends the South African hyperaccumulator Senecio coronatus (Asteraceae) against Helix aspersa (Mullusca: Pulmonidae). Chemoecology 12, 91-97. doi: 10.1007/s00049-002-8331-3
9. Carvalho, A. O., and Gomes, V. M. (2009). Plant defensins-prospects for the biological functions and biotechnological properties. Peptides 30, 1007-1020. doi: 10.1016/j.peptides.2009.01.018
10. Clemens, S., Palmgren, M. G., and Krämer, U. (2002). A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci. 7, 309-315. doi: 10.1016/S1360-138502295-1
11. Deinlein, U., Weber, M., Schmidt, H., Rensch, S., Trampczynska, A., Hansen, T. H., et al. (2012). Elevated nicotianamine levels in Arabidopsis halleri roots play a key role in zinc hyperaccumulation. Plant Cell 24, 708-723. doi: 10.1105/tpc.111.095000
12. 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. doi: 10.1016/j.plantsci.2008.10.008
13. Elbaz, B., Shoshani-Knaani, N., David-Assael, O., Mizrachy-Dagri, T., Mizrahi, K., Saul, H., et al. (2006). High expression in leaves of the zinc hyperaccumulator Arabidopsis halleri of AhMHX, a homolog of an Arabidopsis thaliana vacuolar metal/proton exchanger. Plant Cell Environ. 29, 1179-1190. doi: 10.1111/j.1365-3040.2006.01500.x
14. Ernst, W. H. O. (1990). "Mine vegetation in Europe, " in Heavy Metal Tolerance in Plants: Evolutionary Aspects, ed A. J. Shaw (Boca Raton, FL: CRC Press), 21-37.
15. 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. doi: 10.1002/pmic.200900036
16. Farinati, S., DalCorso, G., Panigati, M., and Furini, A. (2011). Interaction between selected bacterial strains and Arabidopsis halleri modulates shoot proteome and cadmium and zinc accumulation. J. Exp. Bot. 62, 3433-3447. doi: 10.1093/jxb/err015
17. Filatov, V., Dowdle, J., Smirnoff, N., Ford-Lloyd, B., Newbury, H. J., and MacNair, M. R. (2006). Comparison of gene expression in segregating families identifies genes and genomic regions involved in a novel adaptation, zinc hyperaccumulation. Mol. Ecol. 15, 3045-3059. doi: 10.1111/j.1365-294X.2006.02981.x
18. Frova, C. (2003). The plant glutathione transferase gene family: genomic structure, functions, expression and evolution. Physiol. Plantarum 119, 469-479. doi: 10.1046/j.1399-3054.2003.00183.x
19. Garbis, S., Lubec, G., and Fountoulakis, M. (2005). Limitations of current proteomics technologies. J. Chromatogr. 1077, 1-18. doi: 10.1016/j.chroma.2005.04.059
20. Hall, J. L. (2002). Cellular mechanisms for heavy metal detoxification and tolerance. J. Exp. Bot. 53, 1-11. doi: 10.1093/jexbot/53.366.1
21. Hanks, J. N., Snyder, A. K., Graham, M. A., Shah, R. K., Blaylock, L. A., Harrison, M. J., et al. (2005). Defensin gene family in Medicago truncatula: structure, expression and induction by signal molecules. Plant Mol. Biol. 58, 385-399. doi: 10.1007/s11103-005-5567-7
22. Hassinen, V. H., Tuomainen, M., Peräniemi, S., Schat, H., Kärenlampi, S. O., and Tervahauta, A I. (2009). Metallothioneins 2 and 3 contribute to the metal-adapted phenotype but are not directly linked to Zn accumulation in the metal hyperaccumulator, Thlaspi caerulescens. J. Exp. Bot. 60, 187-196. doi: 10.1093/jxb/ern287
23. Higuchi, K., Suzuki, K., Nakanishi, H., Yamaguchi, H., Nishizawa, N. K., and Mori, S. (1999). Cloning of nicotianamine synthase genes, novel genes involved in the biosynthesis of phytosiderophores. Plant Physiol. 119, 471-480. doi: 10.1104/pp.119.2.471
24. Hossain, Z., and Komatsu, S. (2012). Contribution of proteomic studies towards understanding plant heavy metal stress response. Front. Plant Sci. 3:310. doi: 10.3389/fpls.2012.00310
25. Ingle, R. A., Mugford, S. T., Rees, J. D., Campbell, M. M., and Smith, J. A. C. (2005a). Constitutively high expression of the histidine biosynthetic pathway contributes to nickel tolerance in hyperaccumulator plants. Plant Cell 17, 2089-2106. doi: 10.1105/tpc.104.030577
26. Ingle, R. A., Smith, J. A. C., and Sweetlove, L. J. (2005b). Responses to nickel in the proteome of the hyperaccumulator plant Alyssum lesbiacum. Biometals 18, 627-641. doi: 10.1007/s10534-005-2999-0
27. Jia, L., He, X., Chen, W., Liu, Z., Huang, Y., and Yu, S. (2013). Hormesis phenomena under Cd stress in a hyperaccumulator-Lonicera japonica Thunb. Ecotoxicology 22, 476-485. doi: 10.1007/s10646-013-1041-5
28. Krämer, U. (2010). Metal hyperaccumulation in plants. Annu. Rev. Plant Biol. 61, 517-534. doi: 10.1146/annurev-arplant-042809-112156
29. Liu, Y., Ahn, J.-E., Datta, S., Salzman, R. A., Moon, J., Huyghues-Despointes, B., et al. (2005). Arabidopsis vegetative storage protein is an anti-insect acid phosphatase. Plant Physiol. 139, 1545-1556. doi: 10.1104/pp.105.066837
30. Matthes, M. C., Pickett, J. A., and Napier, J. A. (2008). Natural variation in responsiveness of Arabidopsis thalianato methyl jasmonate is developmentally regulated. Planta 228, 1021-1028. doi: 10.1007/s00425-008-0804-3
31. Mendoza-Cózatl, D. G., Butko, E., Springer, F., Torpey, J. W., Komives, E. A., Kehr, J., et al. (2008). Identification of high levels of phytochelatins, glutathione and cadmium in the phloem sap of Brassica napus. A role for thiol-peptides in the long-distance transport of cadmium and the effect of cadmium on iron translocation. Plant J. 54, 249-259. doi: 10.1111/j.1365-313X.2008.03410.x
32. Meyer, C.-L., Peisker, D., Courbot, M., Craciun, A. R., Cazalé, A.-C., Desgain, D., et al. (2011). Isolation and characterization of Arabidopsis halleri and Thlaspi caerulescens phytochelatin synthases. Planta 234, 83-95. doi: 10.1007/s00425-011-1378-z
33. Papoyan, A., and Kochian, L. V. (2004). Identifcation of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. Characterization of a novel heavy metal transporting ATPase. Plant Physiol. 136, 3814-3823. doi: 10.1104/pp.104.044503
34. Plessl, M., Rigola, D., Hassinen, V. H., Tervahauta, A., Kärenlampi, S., Schat, H., et al. (2010). Comparison of two ecotypes of the metal hyperaccumulator Thlaspi caerulescens (J. and C. PRESL) at the transcriptional level. Protoplasma 239, 81-93. doi: 10.1007/s00709-009-0085-0
35. Pollard, A. J., Dandridge Powell, K., Harper, F. A., and Smith, J. A. C. (2002). The genetic basis of metal hyperaccumulation in plants. Crit. Rev. Plant Sci. 21, 539-566. doi: 10.1080/0735-260291044359
36. Richau, K. H., Kozhevnikova, A. D., Seregin, I. V., Vooijs, R., Koevoets, P. L. M., Smith, J. A. C., et al. (2009). Chelation by histidine inhibits the vacuolar sequestration of nickel in roots of the hyperaccumulator Thlaspi caerulescens. New Phytol. 183, 106-116. doi: 10.1111/j.1469-8137.2009.02826.x
37. Rose, J. K. C., Bashir, S., Giovannoni, J. J., Jahn, M. M., and Saravanan, R. S. (2004). Tackling the plant proteome: practical approaches, hurdles and experimental tools. Plant J. 39, 715-733. doi: 10.1111/j.1365-313X.2004.02182.x
38. Roosens, N. H., Bernard, C., Leplae, R., and Verbruggen, N. (2004). Evidence for copper homeostasis function of metallothionein (MT3) in the hyperaccumulator Thlaspi caerulescens. FEBS Lett. 577, 9-16. doi: 10.1016/j.febslet.2004.08.084
39. 2+. J. Exp. Bot. 57, 4003-4013. doi: 10.1093/jxb/erl170
40. 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. doi: 10.1002/pmic.200500543
41. Schneider, T., Persson, D. P., Husted, S., Schellenberg, M., Gehrig, P., Lee, Y., et al. (2013). A proteomics approach to investigate the process of Zn hyperaccumulation in Noccaea caerulescens (J and C. Presl) F.K. Meyer. Plant J. 73, 131-142. doi: 10.1111/tpj.12022
42. Sels, J., Mathys, J., De Coninck, B. M., Cammue, B. P., and De Bolle, M. F. C. (2008). Plant pathogenesis-related (PR) proteins: a focus on PR peptides. Plant Physiol. Biochem. 46, 941-950. doi: 10.1016/j.plaphy.2008.06.011
43. Shen, Z. G., Zhao, F. J., and McGrath, S. (1997). Uptake and transport of zinc in the hyperaccumulator Thiaspi caerulescens and the non-hyperaccumulator Thiaspi ochroleucum. Plant Cell Environ. 20, 898-906. doi: 10.1046/j.1365-3040.1997.d01-134.x
44. Speers, A. E., and Wu, C. C. (2007). Proteomics of integral membrane proteins-theory and application. Chem. Rev. 107, 3687-3714. doi: 10.1021/cr068286z
45. Sunkar, R., Bartels, D., and Kirch, H. H. (2003). Overexpression of a stress-inducible aldehyde dehydrogenase gene from Arabidopsis thaliana in transgenic plants improves stress tolerance. Plant J. 35, 452-464. doi: 10.1046/j.1365-313X.2003.01819.x
46. Tolrà, R. P., Poschenrieder, C., Alonso, R., Barceló, D., and Barceló, J. (2001). Influence of zinc hyperaccumulation on glucosinolates in Thlaspi caerulescens. New Phytol. 151, 621-626. doi: 10.1046/j.0028-646x.2001.00221.x
47. Tuomainen, M., Tervahauta, A., Hassinen, V., Schat, H., Koistinen, K. M., Lehesranta, S., et al. (2010). Proteomics of Thlaspi caerulescens accessions and an inter-accession cross segregating for zinc accumulation. J. Exp. Bot. 61, 1075-1087. doi: 10.1093/jxb/erp372
48. 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. doi: 10.1002/pmic.200501357
49. van de Mortel, J. E., Almar Villanueva, L., Schat, H., Kwekkeboom, J., Coughlan, S., Moerland, P. D., et al. (2006). Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol. 142, 1127-1147. doi: 10.1104/pp.106.082073
50. van de Mortel, J. E., Schat, H., Moerland, P. D., Ver Loren van Themaat, E., van der Ent, S., Blankestijn, H., et al. (2008). Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd-hyperaccumulator Thlaspi caerulescens. Plant Cell Environ. 31, 301-324. doi: 10.1111/j.1365-3040.2007.01764.x
51. Verbruggen, N., Hermans, C., and Schat, H. (2009). Molecular mechanisms of metal hyperaccumulation in plants. New Phytol. 181, 759-776. doi: 10.1111/j.1469-8137.2008.02748.x
52. Visioli, G., and Marmiroli, N. (2013). The proteomics of heavy metal hyperaccumulation by plants. J. Proteomics 79, 133-145. doi: 10.1016/j.jprot.2012.12.006
53. Visioli, G., Vincenzi, S., Marmiroli, M., and Marmiroli, N. (2012). Correlation between phenotype and proteome in the Ni hyperaccumulator Noccaea caerulescens subsp. caerulescens. Environ. Exp. Bot. 77, 156-164. doi: 10.1016/j.envexpbot.2011.11.016
54. Weber, M., Harada, E., Vess, C., Roepenack-Lahaye, E. V., and Clemens, S. (2004). Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J. 37, 269-281. doi: 10.1046/j.1365-313X.2003.01960.x
55. Wittig, I., and Schägger, H. (2009). Native electrophoretic techniques to identify protein-protein interactions. Proteomics 9, 5214-5223. doi: 10.1002/pmic.200900151
56. Zeng, X.-W., Qiu, R.-L., Ying, R.-R., Tang, Y.-T., Tang, L., and Fang, X.-H. (2011). The differentially-expressed proteome in Zn/Cd hyperaccumulator Arabis paniculata Franch. in response to Zn and Cd. Chemosphere 82, 321-328. doi: 10.1016/j.chemosphere.2010.10.030
57. Zhao, L., Sun, Y.-L., Cui, S.-X., Chen, M., Yang, H.-M., Liu, H.-M., et al. (2011). Cd-induced changes in leaf proteome of the hyperaccumulator plant Phytolacca americana. Chemosphere 85, 56-66. doi: 10.1016/j.chemosphere.2011.06.029