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The Role of Phytochelatins in Plant and Animals

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The Role of Phytochelatins in Plant and Animals 22 REVIEW The role of phytochelatins in plant and animals: A review Miguel Angel Merlosa,b, Petr Micháleka,b, Olga Kryštofováa,b, Ondřej Zítkaa,b, Vojtěch Adama,b, René Kizeka,b a Department of Chemistry and Biochemistry, Mendel University in Brno, Zemedelska 1, CZ-613 00 Brno, Czech Republic - European Union b Central European Institute of Technology, Brno University of Technology, Technicka 3058/10, CZ-616 00 Brno, Czech Republic - European Union The role of phytochelatins in plant and animals: A review Phytochelatins (PCs) are thiol-containing oligomers formed in post-translational synthesis from glutathione. They were firstly described in yeasts Schizosaccharomyces pombe. Subse- quently their presence was monitored in plants, microorganisms, but also in many animal species. It is well known, that in plants PCs exhibit significant function in manner of chela- ting of metals. Since they contain thiol functional groups originated from cysteine moieties they keep a metal homeostasis balanced. Although the presence of genes encoding PCs was confirmed in a few animal species, their function in these organisms was not satisfactorily elucidated. Some studies revealed that PCs in animal species are closely linked with detoxifi- cation processes in similar way as in plants. It was also shown that thiols in invertebrates are utilized as the biomarkers of heavy metals contamination. Accepted: 21. 11. 2014 Keywords: phytochelatin; phytochelatin synthase; heavy metal; plants; animals catalyze the synthesis of heavy metal-binding 1. Phytochelatins and phytochela- PCs3, 4. PCs, cysteine-rich peptides, are produced tin synthase from glutamine, cysteine and glycine. Unlike Increasing emissions of heavy metals such commonmetal-binding structures, MT and as cadmium, mercury, and arsenic into the GSH, PCs are not gene-encoded, but enzyma- environment pose an acute problem for all tically synthesized peptides5. PCs have been organisms. As a mass of protection, many of identified in a wide variety of plant species, them, develop mechanisms of full resistance microorganisms and some invertebrates6-10. or at least exhibit partially resisting toward They are structurally related to glutathione these effects. In this way, based on the chemical (GSH) and were presumed to be the products similarity of the involved metallic species, they of a biosynthetic pathway. Numerous physio- are able, to replace them with viable metals logical, biochemical and genetic studies have necessary for the effective functioning of the confirmed GSH as the substrate for PCs bio- cell. These heavy metals may be bound to the synthesis11,12. The general structure of PCs is functional groups of proteins and modify their (c-Glu-Cys)n-Gly, with increasing repetitions structure and through this also affect their of the dipeptide Glu-Cys linked through a physiological function1, 2. Higher plants, algae, c-carboxylamide bond (Fig 1), where n varies certain yeasts and animals are able to respond from 2 to 11, but typically reaching not further to heavy metals by synthesizing phytochelatins than five13. Except glycine, also other amino (PCs) and related cysteine-rich polypeptides. acid residues can be found on C-terminal end γ γ Phytochelatin synthases are -glutamylcysteine of ( -Glu-Cys)n peptides. Examples of which, (γ-Glu-Cys) dipeptidyl transpeptidases that like Ser, Glu, Gln and Ala are often found at Merlos et al. 23 this position in some plant species, and they 3. Phytochelatins in plants are assumed to be functionally analogous and Contamination of soils with toxic metals has synthesised via essentially similar biochemical often resulted from human activities, especi- pathways14, 15. In in vitro studies of PC synthase ally those related to mining, industrial and expressed in E. coli or in S. cerevisiae, the en- emissions. In this context, phytoremediation zyme was activated to varying extents by Cd, has been developed as a cost effective and en- Cu, Ag, Hg, Zn and Pb ions16-18. PC synthase vironmentally friendly remediation method of genes were also isolated in A.thaliana16 and contaminated soils22, 23. In recent years many T.aestivum18. Genes homologous to those from studies showed the mechanisms of chelation of A.thaliana and T.aestivum were also found in metals-PC24-28. Chelation and sequestration of S.pombe and C.elegans, suggesting the existence metals by particular ligands are also mechani- of PC synthase genes in more species19. sms used by plants to cope with metal stress. Figure 1. a) The general structure of PCs. b) Biosynthesis of phytochelatins. 2. Phytochelatins inmicroorganisms The two best-characterized metal-binding Interestingly, although PC(n=2) has been ligands in plant cells are the PCs and metallo- described in the yeast S. cerevisiae, there is no thioneins 29-31. Naturally hyperaccumulating homologue of the PC-synthase genes in the plants do not overproduce PCs as part of their S. cerevisiae genome. An alternative pathway mechanism against toxic metals and this fea- for PCs biosynthesis which has been in S. po- ture appears to be an inducible rather than a mbe has been proposed. However, it can be a constitutive mechanism, observed especially similar pathway that functions in S. cerevisiae in metal non-tolerant plants8. too20. A study shows that the two vacuolar se- Several studies of plants that overexpressed rine carboxypeptidases are responsible for PC γ-glutamyl-cysteine synthetase or transgenic synthesis in S. cerevisiae. Therefore, the finding plants expressing bacterial γ-glutamyl-cysteine of a PCS-like activity of these enzymes in vivo synthetase evaluated its effect on metal toleran- discloses another route for PC biosynthesis in ce based on the assumption that higher levels of eukaryotes21. GSH and PCs will lead to more efficient metal sequestration32. Bacopa monnieri, a wetland 24 Journal of Metallomics and Nanotechnologies 2014, 4, 22—27 macrophyte is well known for its accumulation 4.1 Fuctionsl of PCs in animals potential of metals and metal tolerance and Biochemical studies have also shown that thus is suitable in phytoremediation. Aquatic these PCS genes are functional: the Caenor- plants respond to metal stress by increased habditis elegans PC synthase produces PCs production of PCs as well as other antioxidants. when it is expressed in an appropriate host, B. monnieri is wellknown for the accumulation and knocking out the gene increases the sen- potential of various heavy metals and warrants sitivity of C. elegans to cadmium37. In several its evaluation for metal tolerance and detoxifi- studies PCs have been measured by direct bio- cation mechanism for its suitability in phytore- chemical analysis of C. elegans tissue extracts, mediation9. Arabidopsis thaliana showed that and found that cadmium exposure did indeed Cd is immediately scavenged by thiols in root increase PCs levels in C. elegans. PC2, PC3, and cells, in particular PCs, at the expense of GSH. PC4 have all been found, with PC2 the highest At the same time, a redox signal is suggested concentration6, 38, 39. Therefore, these studies to be generated by a decreased GSH pool in showed conclude that PCs production plays a combination with an altered GSH:GSSG ratio major role in protecting C. elegans against cad- 24 in order to increase the antioxidant capacity . mium toxicity. PC2 and PC3 were increased in Overexpression of PCs synthase in Arabidopsis autochthonous Lumbricus rubellus populations led to 20-100 times more biomass on 250 and sampled from contaminated sites36. 300 μM arsenate than in the wild type. Also, The yeast (i.e. S. pombe) possesses an ATP- the accumulation of thiol-peptides was 10 ti- -binding cassette (ABC) transporter, Hmt1, mes higher when after the exposure to Cd and which was originally thought to play a possible arsenic, compared to the wild type. Gamma- role in translocation of PCs–metal complexes -glutamyl cysteine, which is a substrate for PC to the vacuole. However, while knocking out synthesis, increased rapidly, after arsenate or the C. elegans HMT-1 (CeHMT-1) the sensiti- cadmium exposure. Overexpression of this vity toward cadmium does increase, and the gene can be useful for phytoremediating33. Also, increase is greater than could be explained by Legumes are also capable for synthesising ho- a lack of PCS alone40. mophytochelatins in response to heavy metal It is important to say that MTs are widely esta- stress32. Citrus plants were able to synthesize blished as a key metal detoxification system in PCs in response to heavy metal intoxication26. animals, even though they certainly have many In wheat, PCs–heavy metal complexes have other biological functions as well. Until now, been reported to accumulate in the vacuole. there is very little known about how MTs and Retention of Cd in the root cell vacuoles might PCs may complement each other for dealing influence the symplastic radial Cd transport to with toxic metals36. the xylem and further transport to the shoot, resulting in genotypic differences in grain Cd 5. Methods for phytochelatins de- accumulation34. termination Recently, Wood et al., showed the analytical 4. Phytochelatins in animals methodology for quantification of PCs and their PCs proteins have been broadly described metal(loid) complexes41. The classical approach and characterized in plants, yeasts, algae, fungi to the analysis of PCs is by reversed phase HPLC and bacteria, as well as nematodes and trema- with post-column derivatization of the sulfhyd- todes35. PC synthase genes are also present in ryl groups and spectrophotometric detection animal species from several different phyla. PCs (but this is not specific to PCs). Independent synthesis appears not to be transcriptionally studies showed a sensitive method for deter- regulated in animals36. Originally it is thought mination of PCs by HPLC with fluorescence to be found only in plants and yeast, but PC detection42, 43. A simple sensitive method for synthase genes have been found in species that the identification, sequencing and quantitative span almost the whole animal tree of life. determination of PCs in plants by electrospray Merlos et al.
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