Proteomic analysis of eucalyptus leaves unveils putative mechanisms involved in the plant response to a real condition of soil contamination by multiple heavy metals in the presence or absence of mycorrhizal/rhizobacterial additives

Environmental Science and Technology

Volumn 48, Issue 19, 2014, Pages 11487-11496

  Guarino, Carmine ^a   Conte, Barbara ^a   Spada, Valentina ^a   Arena, Simona ^b   Sciarrillo, Rosaria ^a   Scaloni, Andrea ^b  

^a UNIVERSITY OF SANNIO   (Italy)

^b CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADDITIVES; ANTIOXIDANTS; CLONE CELLS; CONTAMINATION; ENZYMES; HEAVY METALS; PEPTIDES; PHOTOSYNTHESIS; PLANT LIFE EXTENSION; PLANTS (BOTANY); PROTEOMICS; SOILS;

COMPARATIVE PROTEOMICS; EUCALYPTUS CAMALDULENSIS; GLUTATHIONE METABOLISM; GROWTH PERFORMANCE; METAL HYPERACCUMULATORS; MOLECULAR MECHANISM; SIGNALING MECHANISMS; SOIL MICRO-ORGANISMS;

SOIL POLLUTION;

ENZYME; GLUTATHIONE; HEAVY METAL; PROTEIN; SOIL; SOIL POLLUTANT; VEGETABLE PROTEIN;

ANTIOXIDANT; BIOACCUMULATION; CHELATING AGENT; EVERGREEN TREE; GENE EXPRESSION; GROWTH RATE; HEAVY METAL; HYPERACCUMULATION; MOLECULAR ANALYSIS; MYCORRHIZA; PHYSIOLOGICAL RESPONSE; PHYTOREMEDIATION; PROTEOMICS; RHIZOBACTERIUM; SOIL MICROORGANISM;

ARBUSCULAR MYCORRHIZA; ARTICLE; CARBON DIOXIDE FIXATION; CONTROLLED STUDY; EUCALYPTUS CAMALDULENSIS; EVOLUTIONARY ADAPTATION; GLUTATHIONE METABOLISM; HARVESTING; NONHUMAN; PHOTOSYNTHESIS; PLANT GROWTH; PLANT GROWTH PROMOTING RHIZOBACTERIA; PLANT LEAF; PLANT RESPONSE; PROTEIN EXPRESSION; PROTEOMICS; RHIZOBIUM; SOIL MICROFLORA; SOIL POLLUTION; ANATOMY AND HISTOLOGY; BIOREMEDIATION; CHEMISTRY; DRUG EFFECTS; ENERGY METABOLISM; ENVIRONMENT; EUCALYPTUS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MYCORRHIZA; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT STEM; PROCEDURES; RHIZOBIACEAE; SOIL; SOIL POLLUTANT; TOXICITY; TWO DIMENSIONAL GEL ELECTROPHORESIS;

EUCALYPTUS;

BIODEGRADATION, ENVIRONMENTAL; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENERGY METABOLISM; ENVIRONMENT; EUCALYPTUS; GLUTATHIONE; METALS, HEAVY; MYCORRHIZAE; PHOTOSYNTHESIS; PLANT LEAVES; PLANT PROTEINS; PLANT STEMS; PROTEOMICS; RHIZOBIACEAE; SOIL; SOIL MICROBIOLOGY; SOIL POLLUTANTS; STRESS, PHYSIOLOGICAL;

EID: 84907938873     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es502070m     Document Type: Article

References (79)

1. Waalkes, M. P.; Fox, D. A.; States, J. C.; Patierno, S. R.; McCabe, M. J., Jr. Metals and disorders of cell accumulation: modulation of apoptosis and cell proliferation Toxicol. Sci. 2000, 56 (6) 255-261
2. Hossain, Z.; Komatsu, S. Contribution of proteomic studies towards understanding plant heavy metal stress response Front Plant Sci. 2013, 3, 310
3. Clemens, S. Developing tools for phytoremediation: Towards a molecular understanding of plant metal tolerance and accumulation Int. J. Occup. Med. Environ. Health 2001, 14, 235-239
4. Bubb, J. M.; Lester, J. N. The impact of heavy metals on lowland rivers and the implications for man and the environment Sci. Total Environ. 1991, 100, 207-233
5. Sharma, S. S.; Dietz, K. J. The relationship between metal toxicity and cellular redox imbalance Trends Plant Sci. 2009, 14 (1) 43-50
6. Hall, J. L. Cellular mechanisms for heavy metal detoxification and tolerance J. Exp. Bot. 2002, 53 (366) 1-11
7. Cobbett, C.; Goldsbrough, P. Phytochelatins and metallothioneins: Roles in heavy metal detoxification and homeostasis Annu. Rev. Plant Biol. 2002, 53, 159-182
8. Chekmeneva, E.; Gusmão, R.; Díaz-Cruz, J. M.; Ariño, C.; Esteban, M. From cysteine to longer chain thiols: Thermodynamic analysis of cadmium binding by phytochelatins and their fragments Metallomics 2011, 3 (8) 838-846
9. Brune, A.; Urbach, W.; Dietz, K. J. Differential toxicity of heavy metals is partly related to a loss of preferential extraplasmic compartmentation: A comparison of Cd, Mo, Ni, and Zn-stress New Phytol. 1995, 129, 403-409
10. Karliński, L.; Rudawska, M.; Kieliszewska-Rokicka, B.; Leski, T. Relationship between genotype and soil environment during colonization of poplar roots by mycorrhizal and endophytic fungi Mycorrhiza 2010, 20 (5) 315-324
11. Lingua, G.; D'Agostino, G.; Massa, N.; Antosiano, M.; Berta, G. Mycorrhiza-induced differential response to a yellow disease in tomato Mycorrhiza 2002, 12 (4) 191-198
12. Rodriguez, R.; Redman, R. More than 400 million years of evolution and some plants still can't make it on their own: Plant stress tolerance via fungal symbiosis J. Exp. Bot. 2008, 59 (5) 1109-1114
13. Gamalero, E.; Lingua, G.; Berta, G.; Glick, B. R. Beneficial role of plant growth promoting bacteria and arbuscular mycorrhizal fungi on plant responses to heavy metal stress Can. J. Microbiol. 2009, 55 (5) 501-514
14. Miransari, M. Hyperaccumulators, arbuscular mycorrhizal fungi and stress of heavy metals Biotechnol. Adv. 2011, 29 (6) 645-653
15. Artursson, V.; Finlay, R. D.; Jansson, J. K. Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth Environ. Microbiol. 2006, 8 (1) 1-10
16. Cobbett, C. S. Phytochelatin biosynthesis and function in heavy-metal detoxification Curr. Opin. Plant Biol. 2000, 3 (3) 211-216
17. Verbruggen, N.; Hermans, C.; Schat, H. Molecular mechanisms of metal hyperaccumulation in plants New Phytol. 2009, 181 (4) 759-776
18. Hossain, M. A.; Piyatida, P.; Teixeira da Silva, J. A.; Fujita, M. 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; DOI 10.1155/2012/872875.
19. Bohnert, H. J.; Gong, Q.; Li, P.; Ma, S. Unraveling abiotic stress tolerance mechanisms-getting genomics going Curr. Opin. Plant. Biol. 2006, 9 (2) 180-188
20. Nesatyy, V. J.; Suter, M. J. Analysis of environmental stress response on the proteome level Mass Spectrom. Rev. 2008, 27 (6) 556-574
21. Dowling, V. A.; Sheehan, D. Proteomics as a route to identification of toxicity targets in environmental toxicology Proteomics 2006, 6 (20) 5597-5604
22. Lemos, M. F.; Soares, A. M.; Correia, A. C.; Esteves, A. C. Proteins in ecotoxicology-how, why and why not? Proteomics 2010, 10 (4) 873-887
23. Ahsan, N.; Renaut, J.; Komatsu, S. Recent developments in the application of proteomics to the analysis of plant responses to heavy metals Proteomics 2009, 9 (10) 2602-2621 and references therein
24. Villiers, F.; Ducruix, C.; Hugouvieux, V.; Jarno, N.; Ezan, E.; Garin, J.; Junot, C.; Bourguignon, J. Investigating the plant response to cadmium exposure by proteomic and metabolomic approaches Proteomics 2011, 11 (9) 1650-1663 and references therein
25. Visioli, G.; Marmiroli, N. The proteomics of heavy metal hyperaccumulation by plants J. Proteomics 2013, 79, 133-145 and references therein
26. Li, F.; Shi, J.; Shen, C.; Chen, G.; Hu, S.; Chen, Y. Proteomic characterization of copper stress response in Elsholtzia splendens roots and leaves Plant Mol. Biol. 2009, 71, 251-263 and references therein
27. Qureshi, M. I.; D'Amici, G. M.; Fagioni, M.; Rinalducci, S.; Zolla, L. Iron stabilizes thylakoid protein-pigment complexes in Indian mustard during Cd-phytoremediation as revealed by BN-SDS-PAGE and ESI-MS/MS J. Plant Physiol. 2010, 167 (10) 761-770 and references therein
28. Nwugo, C. C.; Huerta, A. J. The effect of silicon on the leaf proteome of rice (Oryza sativa L.) plants under J. Proteome Res. 2011, 10 (2) 518-528
29. Aloui, A.; Recorbet, G.; Robert, F.; Schoefs, B.; Bertrand, M.; Henry, C.; Gianinazzi-Pearson, V.; Dumas-Gaudot, E.; Aschi-Smiti, S. Arbuscular mycorrhizal symbiosis elicits shoot proteome changes that are modified during cadmium stress alleviation in Medicago truncatula BMC Plant Biol. 2011, 11, 75
30. King, D. J.; Doronila, A. I.; Feenstra, C.; Baker, A. J.; Woodrow, I. E. Phytostabilisation of arsenical gold mine tailings using four Eucalyptus species: Growth, arsenic uptake and availability after five years Sci. Total Environ. 2008, 406 (1-2) 35-42
31. Lamb, D. T.; Ming, H.; Megharaj, M.; Naidu, R. Phytotoxicity and accumulation of lead in Australian native vegetation Arch. Environ. Contam. Toxicol. 2010, 58 (3) 613-621
32. Marchiol, L.; Fellet, G.; Boscutti, F.; Montella, C.; Mozzi, R.; Guarino, C. Gentle remediation at formerly "Pertusola Sud" zinc smelter: Evaluation of native species for phytoremediation purposes Ecol. Eng. 2013, 53, 343-353
33. Toro, M.; Azcon, R.; Barea, J. M. Improvement of arbuscular mycorrhiza development by inoculation of soil with phosphate-solubilizing rhizobacteria to improve rock phosphate bioavailability and nutrient cycling Appl. Environ. Microbiol. 1997, 63, 4408-4412
34. Glick, B. R. Phytoremediation: synergistic use of plants and bacteria to clean up the environment Biotechnol. Adv. 2003, 21 (5) 383-393
35. McSpadden Gardener, B. B. Ecology of Bacillus and Paenibacillus spp. in agricultural systems Phytopathology 2004, 94, 1252-1258
36. Glick, B. R. Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase FEMS Microbiol. Lett. 2005, 251 (1) 1-7
37. Miransari, M. Interactions between arbuscular mycorrhizal fungi and soil bacteria Appl. Microbiol. Biotechnol. 2011, 89, 917-930
38. Approvazione ed ufficializzazione dei metodi di analisi microbiologica del suolo (Approval and formalization of the methods of microbiological analysis of soil). DM n.010175 of July 8, 2002. Official Gazette of the Italian Republic; Istituto Poligrafico e Zecca dello Stato: Rome, 2002.
39. Conte, B.; Braglia, R.; Basile, A.; Castaldo Cobianchi, R.; Forni, C. Proteomics and bryophytes: A comparison between different methods of protein extraction to study protein synthesis in the aquatic moss Leptodictyum riparium (Hedw.) Caryologia 2007, 60, 102-105
40. Carpentier, S. C.; Witters, E.; Laukens, K.; Deckers, P.; Swennen, R.; Panis, B. Preparation of protein extracts from recalcitrant plant tissues: An evaluation of different methods for two-dimensional gel electrophoresis analysis Proteomics 2005, 5 (10) 2497-2507
41. Guarino, C.; Arena, S.; De Simone, L.; D'Ambrosio, C.; Santoro, S.; Rocco, M.; Scaloni, A.; Marra, M. Proteomic analysis of the major soluble components in Annurca apple flesh Mol. Nutr. Food Res. 2007, 51 (2) 255-262
42. O'Farrell, P. H. High resolution two-dimensional electrophoresis of proteins J. Biol. Chem. 1975, 250 (10) 4007-4021
43. D'Ambrosio, C.; Arena, S.; Rocco, M.; Verrillo, F.; Novi, G.; Viscosi, V.; Marra, M.; Scaloni, A. Proteomic analysis of apricot fruit during ripening J. Proteomics 2013, 78, 39-57
44. Adriano, D. C. Trace Elements in Terrestrial Environments Biogeochemistry, Bioavailability, and Risks of Metals, 2 nd ed.; Springer Verlag: New York, 2001.
45. Paz, I. C. P.; Santin, R. C. M.; Guimarães, A. M.; Rosa, O. P. P.; Dias, A. C. F.; Quecine, M. C.; Azevedo, J. L.; Matsumura, A. T. S. Eucalyptus growth promotion by endophytic Bacillus spp Genet. Mol. Res. 2012, 11 (4) 3711-3720
46. Thippeswamy, B.; Shivakumar, C. K.; Krishnappa, M. Bioaccumulation potential of Aspergillus niger and Aspergillus flavus for removal of heavy metals from paper mill effluent J. Environ. Biol. 2012, 33 (6) 1063-1068
47. Lingua, G.; Bona, E.; Todeschini, V.; Cattaneo, C.; Marsano, F.; Berta, G.; Cavaletto, M. Effects of heavy metals and arbuscular mycorrhiza on the leaf proteome of a selected poplar clone: A time course analysis. PLoS One 2012, 7 (6).
48. Arriagada, C.; Aranda, E.; Sampedro, I.; Garcia-Romera, I.; Ocampo, J. A. Interactions of Trametes versicolor, Coriolopsis rigida, and the arbuscular mycorrhizal fungus Glomus deserticola on the Cu tolerance of Eucalyptus globulus Chemosphere 2009, 77, 273-278
49. Abril, N.; Gion, J. M.; Kerner, R.; Müller-Starck, G.; Cerrillo, R. M.; Plomion, C.; Renaut, J.; Valledor, L.; Jorrin-Novo, J. V. Proteomics research on forest trees, the most recalcitrant and orphan plant species Phytochemistry 2011, 72, 1219-1242
50. Jorrin-Novo, J. V.; Maldonado, A. M.; Echevarría-Zomeño, S.; Valledor, L.; Castillejo, M. A.; Curto, M.; Valero, J.; Sghaier, B.; Donoso, G.; Redondo, I. Plant proteomics update (2007-2008). Second generation proteomic techniques, an appropriate experimental design and data analysis to fulfill MIAPE standards, increase plant proteome coverage and biological knowledge J. Proteomics 2009, 72, 285-314
51. Patterson, J.; Ford, K.; Cassin, A.; Natera, S.; Bacic, A. Increased abundance of proteins involved in phytosiderophore production in boron-tolerant barley Plant Physiol. 2007, 144, 1612-1631
52. Zhen, Y.; Qi, J. L.; Wang, S. S.; Su, J.; Xu, G. H.; Zhang, M. S.; Miao, L.; Peng, X. X.; Tian, D.; Yang, Y. H. Comparative proteome analysis of differentially expressed proteins induced by Al toxicity in soybean Physiol. Plant 2007, 131, 542-554
53. Hossain, Z.; Hajika, M.; Komatsu, S. Comparative proteome analysis of high and low cadmium accumulating soybeans under cadmium stress Amino Acids 2012, 43, 2393-2416
54. Schneider, T.; Persson, D. P.; Husted, S.; Schellenberg, M.; Gehrig, P.; Lee, Y.; Martinoia, E.; Schjoerring, J. K.; Meyer, S. A proteomics approach to investigate the process of Zn hyperaccumulation in Noccaea caerulescens (J & C. Presl) F.K. Meyer Plant J. 2013, 73, 131-142
55. Saravanan, R. S.; Rose, J. K. A critical evaluation of sample extraction techniques for enhanced proteomic analysis of recalcitrant plant tissues Proteomics 2004, 4, 2522-2532
56. Zeng, X. W.; Qiu, R. L.; Ying, R. R.; Tang, Y. T.; Tang, L.; Fang, X. H. The differentially-expressed proteome in Zn/Cd hyperaccumulator Arabis paniculata Franch. in response to Zn and Cd Chemosphere 2011, 82 (3) 321-328
57. Ahsan, N.; Nakamura, T.; Komatsu, S. Differential responses of microsomal proteins and metabolites in two contrasting cadmium (Cd)-accumulating soybean cultivars under Cd stress Amino Acids 2012, 42 (1) 317-327
58. Kosová, K.; Vítámvás, P.; Prásil, I. T.; Renaut, J. Plant proteome changes under abiotic stress-contribution of proteomics studies to understanding plant stress response J. Proteomics 2011, 74 (8) 1301-1322
59. McCutcheon, S. C.; Schnoor, J. L. Eds. Phytoremediation: Transformation and Control of Contaminant; Wiley: New York, 2003; pp 863-885.
60. Jing, Y. D.; He, Z. L.; Yang, X. E. Role of soil rhizobacteria in phytoremediation of heavy metal contaminated soils J. Zhejiang Univ. Sci. B 2007, 8 (3) 192-207
61. Fettke, J.; Nunes-Nesi, A.; Fernie, A. R.; Steup, M. Identification of a novel heteroglycan-interacting protein, HIP 1.3, from Arabidopsis thaliana J. Plant Physiol. 2011, 168 (12) 1415-1425
62. Weber, H.; Heim, U.; Borisjuk, L.; Wobus, U. Cell-type specific, coordinate expression of two ADP-glucose pyrophosphorylase genes in relation to starch biosynthesis during seed development of Vicia faba L Planta 1995, 195 (3) 352-361
63. Semane, B.; Dupae, J.; Cuypers, A.; Noben, J. P.; Tuomainen, M.; Tervahauta, A.; Kärenlampi, S.; Van Belleghem, F.; Smeets, K.; Vangronsveld, J. Leaf proteome responses of Arabidopsis thaliana exposed to mild cadmium stress J. Plant Physiol. 2010, 167 (4) 247-254
64. Wang, W.; Vinocur, B.; Shoseyov, O.; Altman, A. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response Trends Plant Sci. 2004, 9, 244-252
65. Sunkar, R.; Bartels, D.; Kirch, H. H. Overexpression of a stress-inducible aldehyde dehydrogenase gene from Arabidopsis thaliana in transgenic plants improves stress tolerance Plant J. 2003, 35 (4) 452-464
66. Barranco-Medina, S.; Lazaro, J. J.; Dietz, K. J. The oligomeric conformation of peroxiredoxins links redox state to function FEBS Lett. 2009, 583, 1809-1816
67. Wang, Y.; Gao, M.; Li, Q.; Wang, L.; Wang, J.; Jeon, J. S.; Qu, N.; Zhang, Y.; He, Z. OsRAR1 and OsSGT1 physically interact and function in rice basal disease resistance Mol. Plant-Microbe Interact. 2008, 21, 294-303
68. Verbruggen, N.; Hermans, C.; Schat, H. Mechanisms to cope with arsenic or cadmium excess in plants Curr. Opin. Plant Biol. 2009, 12 (3) 364-372
69. Sarry, J. E.; Kuhn, L.; Ducruix, C.; Lafaye, A.; Junot, C.; Hugouvieux, V.; Jourdain, A.; Bastien, O.; Fievet, J. B.; Vailhen, D.; Amekraz, B.; Moulin, C.; Ezan, E.; Garin, J.; Bourguignon, J. The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses Proteomics 2006, 6 (7) 2180-2198
70. Marrs, K. A. The functions and regulation of glutathione S-transferases in plants Annu. Rev. Plant Physiol. Plant Mol. Biol. 1996, 47, 127-158
71. Edwards, R.; Dixon, D. P.; Walbot, V. Plant glutathione S-transferases: Enzymes with multiple functions in sickness and in health Trends Plant Sci. 2000, 5, 193-198
72. Rea, P. A.; Li, Z. S.; Lu, Y. P.; Drozdowicz, Y. M.; Martinoia, E. From vacuolar GS-X pumps to multispecific ABC transporters Annu. Rev. Plant Physiol. Plant Mol. Biol. 1998, 49, 727-760
73. Adamis, P. D. B.; Gomes, D. S.; Pinto, M.; Panek, A. D.; Eleutherio, E. C. A. The role of glutathione transferases in cadmium stress Toxicol. Lett. 2004, 154, 81-88
74. Amir, H.; Lagrange, A.; Hassaïne, N.; Cavaloc, Y. Arbuscular mycorrhizal fungi from New Caledonian ultramafic soils improve tolerance to nickel of endemic plant species Mycorrhiza 2013, 23 (7) 585-595
75. Jamil, M.; Zeb, S.; Anees, M.; Roohi, A.; Ahmed, I.; Rehman, S.; Rha, E. Role of Bacillus licheniformis in phytoremediation of nichel contaminated soil cultivated with rice Int. J. Phytorem. 2014, 16, 554-571
76. Glick, B. R. Using soil bacteria to facilitate phytoremediation Biotechnol. Adv. 2010, 28 (3) 367-374
77. Leung, H. M.; Leung, A. O. W.; Ye, Z. H.; Cheung, K. C.; Yung, K. K. L. Mixed arbuscular mycorrhizal (AM) fungal application to improve growth and arsenic accumulation of Pteris vittata (As hyperaccumulator) grown in As-contaminated soil Chemosphere 2013, 92, 1367-1374
78. Sheng, X.; Sun, L.; Huang, Z.; He, L.; Zhang, W.; Chen, Z. Promotion of growth and Cu accumulation of bio-energy crop (Zea mays) by bacteria: Implications for energy plant biomass production and phytoremediation J. Environ. Manage. 2012, 103, 58-64
79. Nakano, M. M.; Zuber, P. Anaerobic Growth of A "Strict Aerobe" (Bacillus subtilis) Annu. Rev. Microbiol. 1998, 52, 165-190