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Distinctive Features and Role of Sulfur-Containing Compounds in Marine Plants, Seaweeds, Seagrasses and Halophytes, from an Evolutionary Point of View

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Sabkha Ecosystems

Part of the book series: Tasks for Vegetation Science ((TAVS,volume 47))

Abstract

Many seaweeds, seagrasses and many halophytes, grow in the tidal zone in similar environments. Their every-day-life and their life cycle are influenced by regular flooding during high tide and exposure to the air at low tide. Therefore they are confronted with similar daily changes in the osmotic potential and need to take up nutrients from the water and/or from the sediment. In addition, coastal zones and estuaries are often contaminated with high loads of some nutrients and heavy metals. Sulfur-deficiency is a major issue for land-based agriculture, whereas seawater act as a global sulfur reservoir and sulfur does not limit growth of marine plants. Sulfur-containing compounds and proteins seem to play a pivotal in the adaptation to these environmental conditions. This review highlights the putative roles of sulfur-containing compounds in a comparative way in seaweeds, seagrasses and halophytes. Can we observe similar metabolic and proteomic adaptations in regularly flooded coastal plants? The role of sulfur-containing proteins and of sulfur-containing secondary metabolites and their responsible set of enzymes will be analyzed from an evolutionary point of view. New strategies to increase salt-tolerance in higher plants based on sulfur-containing compounds are discussed.

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References

  1. Glenn EP, Brown JJ (1999) Salt tolerance and crop potential of halophytes. Crit Rev Plant Sci 18:227–255

    Article  Google Scholar 

  2. Michel G, Tonon T, Scornet D, Cock JM, Kloareg B (2010) The cell wall polysaccharide metabolism of the brown alga Ectocarpus siliculosus. Insights into the evolution of extracellular matrix polysaccharides in Eukaryotes. New Phytol 188:82–97

    Article  CAS  Google Scholar 

  3. Schmidt-Nielsen K (1997) Animal physiology: adaptation and environment. Cambridge University Press, Cambridge

    Google Scholar 

  4. Cock JM, Sterck L, Rouzé P et al (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465:617–621

    Article  CAS  Google Scholar 

  5. Nader HB, Medeiros MGL, Paiva JF, Paiva VMP, Jerônimo SMB, Ferreira TMPC, Dietrich CP (1983) A correlation between the sulfated glycosaminoglycan concentration and degree of salinity of the “habitat” in fifteen species of the classes Crustacea, Pelecypoda and Gastropoda. Comp Biochem Physiol B Biochem Mol Biol 76:433–436

    Article  Google Scholar 

  6. Medeiros GF, Mendes A, Castro RAB, Baú EC, Nader HB, Dietrich CP (2000) Distribution of sulfated glycosaminoglycans in the animal kingdom: widespread occurrence of heparin-like compounds in invertebrates. Biochim Biophys Acta 1475:287–294

    Article  CAS  Google Scholar 

  7. Jiao G, Yu G, Zhang J (2011) Chemical structures and bioactivities of sulfated polysaccharides from marine algae. Mar Drugs 9:196–223

    Article  CAS  Google Scholar 

  8. Aquino RS, Grativol C, Mourão PA (2011) Rising from the sea: correlations between sulfated polysaccharides and salinity in plants. PLoS One 6:e18862. doi:10.1371/journal.pone.0018862

    Article  CAS  Google Scholar 

  9. Dantas-Santos N, Gomes DL, Costa LS, Cordeiro SL, Costa MS, Trindade ES, Franco CR, Scortecci KC, Leite EL, Rocha HA (2012) Freshwater plants synthesize sulfated polysaccharides: Heterogalactans from water hyacinth (Eichhornia crassipes). Int J Mol Sci 13:961–976

    Article  CAS  Google Scholar 

  10. Bickel-Sandkötter S (2001) Nutzpflanzen und ihre Inhaltsstoffe. Quelle & Meyer, Wiebelsheim

    Google Scholar 

  11. Uehara T, Takeshita M, Maeda M (1992) Studies on anticoagulant-active arabinan sulfates from the green alga, Codium latum. Carbohydr Res 23:309–311

    Article  Google Scholar 

  12. Matsubara K, Hori K, Matsuura Y, Miyazawa K (2000) Purification and characterization of a fibrinolytic enzyme and identification of fibrinogen clotting enzyme in a marine green alga, Codium divaricatum. Comp Biochem Physiol B Biochem Mol Biol 125:137–143

    Article  CAS  Google Scholar 

  13. Lewis LA, McCourt RM (2004) Green algae and the origin of land plants. Am J Bot 91:1535–1556

    Article  Google Scholar 

  14. Donnan FG (1924) The theory of membrane equilibria. Chem Rev 1:73–90

    Article  CAS  Google Scholar 

  15. Dittami SM, Gravot A, Goulitquer S, Rousvoal S, Peters AF, Bouchereau A, Boyen C, Tonon T (2012) Towards deciphering dynamic changes and evolutionary mechanisms involved in the adaptation to low salinities in Ectocarpus (brown algae). Plant J 71:366–377

    CAS  Google Scholar 

  16. Shaw GE (1983) Bio-controlled thermostasis involving the sulfur cycle. Clim Change 5:297–303

    Article  CAS  Google Scholar 

  17. Dacey JWH, Blough NV (1987) Hydroxide decomposition of dimethylsulfoniopropionate to form dimethylsulfide. Geophys Res Lett 14:1246–1249

    Article  CAS  Google Scholar 

  18. Dacey JWH, King GM, Lobel PS (1994) Herbivory by reef fishes and production of dimethylsulfide and acrylic acid. Mar Ecol Prog Ser 112:67–74

    Article  Google Scholar 

  19. Karsten U, Kuck K, Daniel C, Wiencke C, Kirst GO (1994) A method for complete determination of dimethlysulphonio-propionate (DMSP) in marine macroalgae from different geographical regions. Phycologia 33:171–176

    Article  Google Scholar 

  20. Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    Article  CAS  Google Scholar 

  21. Grennan AK (2011) Metallothioneins, a diverse protein family. Plant Physiol 155:1750–1751

    Article  CAS  Google Scholar 

  22. Gullstroem M (2006) Seagrass meadows – community ecology and habitat dynamics. Dissertation, Goteborg University

    Google Scholar 

  23. Halim M, Conte P, Piccolo A (2003) Potential availability of heavy metals to phytoextraction from contaminated soils induced by exogenous humic substances. Chemosphere 52:265–275

    Article  CAS  Google Scholar 

  24. Govindasamy C, Arulpriya M, Ruban P, Francisca JL, Ilayaraja A (2011) Concentration of heavy metals in seagrasses tissue of the Palk Strait, Bay of Bengal. Environ Sci 2:145–153

    CAS  Google Scholar 

  25. Agoramoorthy G, Chen FA, Hsu MJ (2008) Threat of heavy metal pollution in halophytic and mangrove plants of Tamil Nadu, India. Environ Pollut 155:320–326

    Article  CAS  Google Scholar 

  26. Tranchina L, Micciche S, Bartolotta A, Brai M, Mantegna RN (2005) Posidonia oceanica as a historical monitor device of lead concentration in marine environment. Environ Sci Technol 39:3006–3012

    Article  CAS  Google Scholar 

  27. Zhang FQ, Wang YS, Sun CC, Sun Z, Lou P, Dong JD (2012) A novel metallothionein gene from a mangrove plant Kandelia candel. Ecotoxicology 21:1633–1641

    Article  CAS  Google Scholar 

  28. Robinson N (1989) Algal metallothioneins: secondary metabolites and proteins. Appl Phycol 1:5–18

    Article  CAS  Google Scholar 

  29. Ghnaya T, Nouairi I, Slama I, Messedi D, Grignon C, Abdelly C, Ghorbel MH, Daler D (2005) Cadmium effects on growth and mineral nutrition of two halophytes: Sesuvium portulacastrum and Mesembryanthemum crystallinum. J Plant Physiol 162:1133–1140

    Article  CAS  Google Scholar 

  30. Kraus ML (1988) Accumulation and excretion of five heavy metals by the salt marsh cord grass Spartina alterniflora. Bull N J Acad Sci 33:39–43

    Google Scholar 

  31. Pedersen O, Borum J, Duarte CM, Fortes MD (1998) Oxygen dynamics in the rhizosphere of Cymodocea rotundata. Mar Ecol Prog Ser 169:283–288

    Article  CAS  Google Scholar 

  32. Cobbett CS, Goldsbrough P (2002) Phytochelatins and metallothionines: roles in heavy metals detoxification and homeostasis. Annu Rev Plant Biol 53:159–182

    Article  CAS  Google Scholar 

  33. Clemens S (2006) Evolution and function of phytochelatin synthases. J Plant Physiol 163:319–332

    Article  CAS  Google Scholar 

  34. Gupta M, Rai UN, Tripathi RD, Chandra P (1995) Lead induced changes in glutathione and phytochelatin in Hydrilla verticillata (l.f.) Royle. Chemosphere 30:2011–2020

    Article  CAS  Google Scholar 

  35. Rai UN, Tripathi RD, Gupta M, Chandra P (1995) Induction of phytochelatins under cadmium stress in water lettuce (Pistia stratiotes). J Environ Sci Health A 30:2007–2026

    Google Scholar 

  36. Tripathi RD, Rai UN, Gupta M, Chandra P (1996) Induction of phytochelatins in Hydrilla verticillata (l.f.) Royle under cadmium stress. Bull Environ Contam Toxicol 56:505–512

    Article  CAS  Google Scholar 

  37. Gupta M, Tripathi RD, Rai UN, Chandra P (1998) Role of glutathione and phytochelatin in Hydrilla verticillata (l.f.) Royle and Vallisneria spiralis L. under mercury stress. Chemosphere 37:785–800

    Article  CAS  Google Scholar 

  38. Srivastava S, Mishra S, Tripathi RD, Dwivedi S, Trivedi PK, Tandon PK (2007) Phytochelatins and antioxidant systems respond differentially during arsenite and arsenate stress in Hydrilla verticillata (l.f.) Royle. Environ Sci Technol 41:2930–2936

    Article  CAS  Google Scholar 

  39. Pawlik-Skowrońska B, Pirszel J, Brown MT (2007) Concentrations of phytochelatins and glutathione found in natural assemblages of seaweeds depend on species and metal concentrations of the habitat. Aquat Toxicol 83:190–199

    Article  Google Scholar 

  40. Alvarez-Legorreta T, Mendoza-Cozatl D, Moreno-Sanchez R, Gold-Bouchot G (2008) Thiol peptides induction in the seagrass Thalassia testudinum (Banks ex König) in response to cadmium exposure. Aquat Toxicol 86:12–19

    Article  CAS  Google Scholar 

  41. Ferrat L, Wyllie-Echeverria S, Rex GC, Pergent-Martini C, Pergent G, Zou J, Romeo M, Pasqualini V, Fernandez C (2012) Posidonia oceanica and Zostera marina as potential biomarkers of heavy metal contamination in coastal systems. In: Voudouris K (ed) Ecological water quality-water treatment and reuse, ISBN: 978-953-51-0508-4. InTech

    Google Scholar 

  42. Worden AZ, Lee JH, Mock T et al (2009) Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324:268–272

    Article  CAS  Google Scholar 

  43. Bowler C, Allen AE, Badger JH et al (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–244

    Article  CAS  Google Scholar 

  44. Gonzalez-Mendoza D, Moreno AQ, Zapata-Perez O (2007) Coordinated responses of phytochelatin synthase and metallothionein genes in black mangrove, Avicennia germinans, exposed to cadmium and copper. Aquat Toxicol 83:306–314

    Article  CAS  Google Scholar 

  45. Taji T, Sakurai T, Mochida K et al (2008) Large-scale collection and annotation of full-length enriched cDNAs from a model halophyte, Thellungiella halophila. BMC Plant Biol 8:115

    Article  Google Scholar 

  46. He Z, Li J, Zhang H, Ma M (2005) Different effects of calcium and lanthanum on the expression of phytochelatin synthase gene and cadmium absorption in Lactuca sativa. Plant Sci 168:309–318

    Article  CAS  Google Scholar 

  47. Theologis A, Ecker JR, Palm CJ et al (2000) Sequence and analysis of chromosome 1 of the plant Arabidopsis thaliana. Nature 408:816–820

    Article  Google Scholar 

  48. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  Google Scholar 

  49. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  50. Schwartz RM, Dayhoff MO (1978) Matrices for detecting distant relationships. In: Dayhoff MO (ed) Atlas of protein sequence and structure. National Biomedical Research Foundation, Washington, DC

    Google Scholar 

  51. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 10:2731–2739

    Article  Google Scholar 

  52. Cobbett CS (2000) Phytochelatin biosynthesis and function in heavy-metal detoxification. Curr Opin Plant Biol 3:211–216

    Article  CAS  Google Scholar 

  53. Cherian MG, Kang YJ (2006) Metallothionein and liver cell regeneration. Exp Biol Med 231:138–144

    CAS  Google Scholar 

  54. Blindauer CA, Schmid R (2010) Cytosolic metal handling in plants: determinants for zinc specificity in metal transporters and metallothioneins. Metallomics 2:510–529

    Article  CAS  Google Scholar 

  55. Blindauer AC, Leszczyszyn IO (2010) Metallothioneins: unparalleled diversity in structures and functions for metal ion homeostasis and more. Nat Prod Rep 27:720–741

    Article  CAS  Google Scholar 

  56. Clemens S, Persoh D (2009) Multi-tasking phytochelatin synthases. Plant Sci 177:266–271

    Article  CAS  Google Scholar 

  57. Guo WL, Meetam M, Goldsbrough PB (2008) Examining the specific contribution of individual Arabidopsis metallothioneins to copper distribution and metal tolerance. Plant Physiol 146:1697–1706

    Article  CAS  Google Scholar 

  58. Morris CA, Nicolaus B, Sampson V, Harwood JL, Kille P (1999) Identification and characterization of a recombinant metallothionein protein from a marine alga, Fucus vesiculosus. Biochemistry 338:553–560

    Article  CAS  Google Scholar 

  59. Giordani T, Natali L, Maserti BE, Taddei S, Cavallini A (2000) Characterization and expression of DNA sequences encoding putative type-II metallothionines in seagrass Posidonia oceanica. Plant Physiol 123:1571–1581

    Article  CAS  Google Scholar 

  60. Cozza R, Pangaro T, Maestrini P, Giordani T, Natali L, Cavallini A (2006) Isolation of putative type 2 metallothionein encoding sequences and spatial expression pattern in the seagrass Posidonia oceanica. Aquat Bot 85:317–323

    Article  CAS  Google Scholar 

  61. Zhou R, Zeng K, Wu W, Chen X, Yang Z, Shi S, Wu CI (2007) Population genetics of speciation in nonmodel organisms: I. Ancestral polymorphism in mangroves. Mol Biol Evol 24:2746–2754

    Article  CAS  Google Scholar 

  62. Huang GY, Wang YS, Ying GG (2011) Cadmium-inducible BgMT2, a type 2 metallothionein gene from mangrove species (Bruguiera gymnorrhiza), its encoding protein shows metal-binding ability. Exp Mar Biol Ecol 405:128–132

    Article  CAS  Google Scholar 

  63. Usha B, Keeran NS, Harikrishnan M, Kavitha K, Parida A (2011) Characterization of a type 3 metallothionein isolated from Porteresia coarctata. Biol Plant 55:119–124

    Article  CAS  Google Scholar 

  64. Huang GY, Wang YS, Ying GG, Dang AC (2012) Analysis of type 2 metallothionein gene from mangrove species (Kandelia candel). Trees. doi:10.1007/s00468-012-0727-2

    Google Scholar 

  65. Takeda M, Uno Y, Kanechi M, Inagaki N (2003) Analyses of nine cDNAs for salt-inducible gene in the halophyte Sea Aster (Aster tripolium L.). Plant Biotechnol 20:317–322

    Article  CAS  Google Scholar 

  66. Chaturvedi AK, Mishra A, Tiwari V, Jha B (2012) Cloning and transcript analysis of type 2 metallothionein gene (SbMT-2) from extreme halophyte Salicornia brachiata and its heterologous expression in E. coli. Gene 499:280–287

    Article  CAS  Google Scholar 

  67. Inan G, Zhang Q, Li P et al (2004) Salt cress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. Plant Physiol 135:1718–1737

    Article  CAS  Google Scholar 

  68. Carpene E, Andreani G, Isani G (2007) Metallothionein functions and structural characteristics. J Trace Elem Med Biol 21:35–39

    Article  CAS  Google Scholar 

  69. Reusch TBH, Veron AS, Preuss C, Weiner J, Wissler L, Beck A, Klages S, Kube M, Reinhardt R, Bornberg-Bauer E (2008) Comparative analysis of expressed sequence tag (EST) libraries in the seagrass Zostera marina subjected to temperature stress. Mar Biotechnol 10:297–309

    Article  CAS  Google Scholar 

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Nguyen, XV., Klein, M., Riemenschneider, A., Papenbrock, J. (2014). Distinctive Features and Role of Sulfur-Containing Compounds in Marine Plants, Seaweeds, Seagrasses and Halophytes, from an Evolutionary Point of View. In: Khan, M.A., Böer, B., Öztürk, M., Al Abdessalaam, T.Z., Clüsener-Godt, M., Gul, B. (eds) Sabkha Ecosystems. Tasks for Vegetation Science, vol 47. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-7411-7_21

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