Towards deciphering dynamic changes and evolutionary mechanisms involved in the adaptation to low salinities in Ectocarpus (brown algae)

Plant Journal

Volumn 71, Issue 3, 2012, Pages 366-377

  Dittami, Simon M ^a,b,h   Gravot, Antoine ^c,d   Goulitquer, Sophie ^e,i   Rousvoal, Sylvie ^a,b   Peters, Akira F ^f,g   Bouchereau, Alain ^c,d   Boyen, Catherine ^a,b   Tonon, Thierry ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE RENNES 1   (France)

^d UNIVERSITÉ EUROPÉENNE DE BRETAGNE   (France)

^e FACULTÉ DE MÉDECINE ET DES SCIENCES DE LA SANTÉ   (France)

^f Bezhin Rosko   (France)

^g THE LABORATORY   (United Kingdom)

^h UNIVERSITY OF OSLO   (Norway)

ⁱ STATION BIOLOGIQUE   (France)

Author keywords

abiotic stress; adaptation; brown algae; Ectocarpus; primary metabolism; transcriptomic and metabolite profiling

Indexed keywords

ABIOTIC STRESS; ADAPTATION; BROWN ALGAE; ECTOCARPUS; METABOLITE PROFILING;

AMINO ACIDS; BIOMOLECULES; FATTY ACIDS; GENE EXPRESSION; METABOLITES; PHYSIOLOGY; SEAWATER; STRAIN; WATER;

ALGAE;

AMINO ACID; ANION; CATION; FRESH WATER; NITROGEN; OMEGA 3 FATTY ACID; TRANSCRIPTOME;

ARTICLE; BROWN ALGA; CARBOHYDRATE METABOLISM; CLASSIFICATION; DNA MICROARRAY; DNA SEQUENCE; ECOSYSTEM; EVOLUTION; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; METABOLOME; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; PLANT GENOME; SALINITY; SALT TOLERANCE;

AMINO ACIDS; ANIONS; BASE SEQUENCE; BIOLOGICAL EVOLUTION; CARBOHYDRATE METABOLISM; CATIONS; ECOSYSTEM; FATTY ACIDS, OMEGA-3; FRESH WATER; GENE EXPRESSION PROFILING; GENOME, PLANT; METABOLOME; MOLECULAR SEQUENCE DATA; NITROGEN; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHAEOPHYTA; PHYLOGENY; SALINITY; SALT-TOLERANCE; SEQUENCE ANALYSIS, DNA; TRANSCRIPTOME;

ALGAE; ECTOCARPUS; PHAEOPHYCEAE;

EID: 84864443483     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.04982.x     Document Type: Article

References (51)

1. Akerboom, T.P., and, Sies, H., (1981) Assay of glutathione, glutathione disulfide, and glutathione mixed disulfides in biological samples. Meth. Enzymol. 77, 373-382.
2. Apt, K.E., Clendennen, S.K., Powers, D.A., and, Grossman, A.R., (1995) The gene family encoding the fucoxanthin chlorophyll proteins from the brown alga Macrocystis pyrifera. Mol. Gen. Genet. 246, 455-464.
3. Aquino, R.S., Landeira-Fernandez, A.M., Valente, A.P., Andrade, L.R., and, Mourão, P.A., (2005) Occurrence of sulfated galactans in marine angiosperms: evolutionary implications. Glycobiology, 15, 11-20.
4. Benjamini, Y., and, Hochberg, Y., (1995) Controlling the false discovery rate-a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57, 289-300.
5. Berglin, M., Delage, L., Potin, P., Vilter, H., and, Elwing, H., (2004) Enzymatic cross-linking of a phenolic polymer extracted from the marine alga Fucus serratus. Biomacromolecules, 5, 2376-2383.
6. Bold, H.C., and, Wynne, M.J., (1985) Introduction to the Algae: Structure and Reproduction. Englewood Cliffs, NJ, USA: Prentice-Hall, Inc.
7. Bolton, J.J., (1983) Ecoclinal variation in Ectocarpus siliculosus (Phaeophyceae) with respect to temperature growth optima and survival limits. Mar. Biol. 73, 131-138.
8. Charrier, B., Coelho, S.M., Le Bail, A., Tonon, T., Michel, G., Potin, P., Kloareg, B., Boyen, C., Peters, A.F., and, Cock, J.M., (2008) Development and physiology of the brown alga Ectocarpus siliculosus: two centuries of research. New Phytol. 177, 319-332.
9. Cock, J.M., et al. (2010) The Ectocarpus genome: evolution of a multicellular stramenopile. Nature, 465, 617-621.
10. Davison, I.R., and, Reed, R.H., (1985) The physiological significance of mannitol accumulation in brown algae: the role of mannitol as a compatible solute. Phycologia, 24, 449-457.
11. De Franco, P., Rousvoal, S., Tonon, T., and, Boyen, C., (2009) Whole genome survey of the glutathione transferase family in the brown algal model Ectocarpus siliculosus. Mar. Genomics, 1, 135-148.
12. Dittami, S.M., et al. (2009) Global expression analysis of the brown alga Ectocarpus siliculosus (Phaeophyceae) reveals large-scale reprogramming of the transcriptome in response to abiotic stress. Genome Biol. 10, R66.
13. Dittami, S.M., Proux, C., Rousvoal, S., Peters, A.F., Cock, J.M., Coppee, J.-Y., Boyen, C., and, Tonon, T., (2011a) Microarray estimation of genomic inter-strain variability in the genus Ectocarpus (Phaeophyceae). BMC Mol. Biol. 12, 2.
14. Dittami, S.M., Gravot, A., Renault, D., Goulitquer, S., Eggert, A., Bouchereau, A., Boyen, C., and, Tonon, T., (2011b) Integrative analysis of metabolite and transcript abundance during the short-term response to saline and oxidative stress in the brown alga Ectocarpus siliculosus. Plant, Cell Environ. 34, 629-642.
15. Drummond, A.J., and, Rambaut, A., (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214.
16. Flynn, K.J., Dickson, D.M., and, Al-Amoudi, O.A., (1989) The ratio of glutamine:glutamate in microalgae: a biomarker for N-status suitable for use at natural cell densities. J. Plankton Res. 11, 165-170.
17. Geissler, U., (1983) Die salzbelastete Flusstrecke der Werra-ein Binnenlandstandort für Ectocarpus confervoides (Roth) Kjellmann. Nova Hedwigia, 37, 193-217.
18. Gravot, A., Dittami, S.M., Rousvoal, S., Lugan, R., Eggert, A., Collén, J., Boyen, C., Bouchereau, A., and, Tonon, T., (2010) Diurnal oscillations of metabolite abundances and gene analysis provide new insights into central metabolic processes of the brown alga Ectocarpus siliculosus. New Phytol. 188, 98-110.
19. Guindon, S., and, Gascuel, O., (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biol. 52, 696-704.
20. Irizarry, R.A., Hobbs, B., Collin, F., Beazer-Barclay, Y.D., Antonellis, K.J., Scherf, U., and, Speed, T.P., (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics, 4, 249-264.
21. Jubault, M., Hamon, C., Gravot, A., Lariagon, C., Delourme, R., Bouchereau, A., and, Manzanares-Dauleux, M.J., (2008) Differential regulation of root arginine catabolism and polyamine metabolism in clubroot-susceptible and partially resistant Arabidopsis genotypes. Plant Physiol. 146, 2008-2019.
22. Kloareg, B., and, Quatrano, R.S., (1988) Structure of the cell-walls of marine-algae and ecophysiological functions of the matrix polysaccharides. Oceanogr. Mar. Biol. 26, 259-315.
23. Küpper, F.C., Gaquerel, E., Boneberg, E.-M., Morath, S., Salaün, J.-P., and, Potin, P., (2006) Early events in the perception of lipopolysaccharides in the brown alga Laminaria digitata include an oxidative burst and activation of fatty acid oxidation cascades. J. Exp. Bot. 57, 1991-1999.
24. Le Bail, A., Dittami, S.M., De Franco, P.-O., Rousvoal, S., Cock, J.M., Tonon, T., and, Charrier, B., (2008) Normalisation genes for expression analyses in the brown alga model Ectocarpus siliculosus. BMC Mol. Biol. 9, 75.
25. Lee, C.E., and, Bell, M.A., (1999) Causes and consequences of recent freshwater invasions by saltwater animals. Trends Ecol. Evol. 14, 284-288.
26. Logares, R., Bråte, J., Bertilsson, S., Clasen, J.L., Shalchian-Tabrizi, K., and, Rengefors, K., (2009) Infrequent marine-freshwater transitions in the microbial world. Trends Microbiol. 17, 414-422.
27. Lugan, R., Niogret, M.-F., Kervazo, L., Larher, F.R., Kopka, J., and, Bouchereau, A., (2009) Metabolome and water status phenotyping of Arabidopsis under abiotic stress cues reveals new insight into ESK1 function. Plant, Cell Environ. 32, 95-108.
28. McCauley, L.A., and, Wehr, J.D., (2007) Taxonomic reappraisal of the freshwater brown algae Bodanella, Ectocarpus, Heribaudiella, and Pleurocladia (Phaeophyceae) on the basis of rbcL sequences and morphological characters. Phycologia, 46, 429-439.
29. Michel, G., Tonon, T., Scornet, D., Cock, J.M., and, 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.
30. Nyvall, P., Corre, E., Boisset, C., Barbeyron, T., Rousvoal, S., Scornet, D., Kloareg, B., and, Boyen, C., (2003) Characterization of mannuronan C-5-epimerase genes from the brown alga Laminaria digitata. Plant Physiol. 133, 726-735.
31. Peters, A.F., Mann, A.D., Cõrdova, C.A., Brodie, J., Correa, J.A., Schroeder, D.C., and, Cock, J.M., (2010a) Genetic diversity of Ectocarpus (Ectocarpales, Phaeophyceae) in Peru and northern Chile, the area of origin of the genome-sequenced strain. New Phytol. 188, 30-41.
32. Peters, A.F., Van Wijk, S.J., Cho, G.-Y., Scornet, D., Hanyuda, T., Kawai, H., Schroeder, D.C., Cock, J.M., and, Boo, S.M., (2010b) Reinstatement of Ectocarpus crouaniorum Thuret in Le Jolis as a third common species of Ectocarpus (Ectocarpales, Phaeophyceae) in Western Europe, and its phenology at Roscoff, Brittany. Phycol. Res. 58, 157-170.
33. Popper, Z.A., Michel, G., Hervé, C., Domozych, D.S., Willats, W.G.T., Tuohy, M.G., Kloareg, B., and, Stengel, D.B., (2011) Evolution and diversity of plant cell walls: from algae to flowering plants. Annu. Rev. Plant Biol. 62, 567-590.
34. Posada, D., (2008) jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25, 1253-1256.
35. Ravanko, O., (1970) Morphological, developmental and taxonomic studies in the Ectocarpus complex (Phaeophyceae). Nova Hedwigia, 20, 179-252.
36. Raven, J.A., and, Falkowski, P.G., (1999) Oceanic sinks for atmospheric CO2. Plant, Cell Environ. 22, 741-755.
37. Reed, R.H., and, Barron, J.A., (1983) Physiological adaptation to salinity change in Pilayella littoralis from marine and estuarine sites. Bot. Mar. 26, 409-416.
38. Reed, R.H., Davison, I.R., Chudek, J.A., and, Foster, R., (1985) The osmotic role of mannitol in the phaeophyta-an appraisal. Phycologia, 24, 35-47.
39. Renault, H., Roussel, V., El Amrani, A., Arzel, M., Renault, D., Bouchereau, A., and, Deleu, C., (2010) The Arabidopsis pop2-1 mutant reveals the involvement of GABA transaminase in salt stress tolerance. BMC Plant Biol. 10, 20.
40. Ritter, A., Goulitquer, S., Salaün, J.-P., Tonon, T., Correa, J.A., and, Potin, P., (2008) Copper stress induces biosynthesis of octadecanoid and eicosanoid oxygenated derivatives in the brown algal kelp Laminaria digitata. New Phytol. 180, 809-821.
41. Roessner, U., Luedemann, A., Brust, D., Fiehn, O., Linke, T., Willmitzer, L., and, Fernie, A., (2001) Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell, 13, 11-29.
42. Rousvoal, S., Groisillier, A., Dittami, S.M., Michel, G., Boyen, C., and, Tonon, T., (2011) Mannitol-1-phosphate dehydrogenase activity in Ectocarpus siliculosus, a key role for mannitol synthesis in brown algae. Planta, 233, 261-273.
43. Russel, G., and, Bolton, J., (1975) Euryhaline ecotypes of Ectocarpus siliculosus (Dillw.) Lyngb. Estuar. Coast. Mar. Sci. 3, 91-94.
44. Saeed, A.I., et al. (2003) TM4: A free, open-source system for microarray data management and analysis. Biotechniques, 34, 374-377.
45. Sealfon, R.S., Hibbs, M.A., Huttenhower, C., Myers, C.L., and, Troyanskaya, O.G., (2006) GOLEM: an interactive graph-based gene-ontology navigation and analysis tool. BMC Bioinformatics, 7, 443.
46. Sigee, D.C., (2005) Freshwater Microbiology: Biodiversity and Dynamic Interactions of Microorganisms in the Aquatic Environment. Chichester: John Wiley and Sons.
47. Silberfeld, T., Leigh, J.W., Verbruggen, H., Cruaud, C., De Reviers, B., and, Rousseau, F., (2010) A multi-locus time-calibrated phylogeny of the brown algae (Heterokonta, Ochrophyta, Phaeophyceae): investigating the evolutionary nature of the "brown algal crown radiation". Mol. Phylogenet. Evol. 56, 659-674.
48. Sørensen, I., Pettolino, F.A., Bacic, A., Ralph, J., Lu, F., O'Neill, M.A., Fei, Z., Rose, J.K.C., Domozych, D.S., and, Willats, W.G.T., (2011) The Charophycean green algae provide insights into the early origins of plant cell walls. Plant J. 68, 201-211.
49. Stache-Crain, B., Müller, D.G., and, Goff, L., (1997) Molecular systematics of Ectocarpus and Kuckuckia (Ectocarpales, Phaeophyceae) inferred from phylogenetic analysis of nuclear- and plastid-encoded DNA sequences. J. Phycol. 33, 152-168.
50. Starr, R.C., and, Zeikus, J.A., (1993) Utex-the culture collection of algae at the University-of-Texas at Austin 1993 List of Cultures. J. Phycol. 29, 1-106.
51. West, J., and, Kraft, G., (1996) Ectocarpus siliculosus (Dillwyn) Lyngb. from Hopkins River Falls, Victoria-the first record of a freshwater brown alga in Australia. Muelleria, 9, 29-33.