ALGAE

The Korean Society of Phycology (한국조류학회(藻類))
권호 표지
DOI QR코드

DOI QR Code

Prostaglandin A2 triggers a strong oxidative burst in Laminaria: a novel defense inducer in brown algae?

  • Zambounis, Antonios (Department of Ichthyology and Aquatic Environment, School of Agricultural Sciences, University of Thessaly) ;
  • Gaquerel, Emmanuel (Station Biologique, UMR 7139 CNRS-Universite Pierre et Marie Curie-Paris VI) ;
  • Strittmatter, Martina (Scottish Association for Marine Science, Scottish Marine Institute) ;
  • Salaun, Jean-Pierre (Station Biologique, UMR 7139 CNRS-Universite Pierre et Marie Curie-Paris VI) ;
  • Potin, Philippe (Station Biologique, UMR 7139 CNRS-Universite Pierre et Marie Curie-Paris VI) ;
  • Kupper, Frithjof C. (Station Biologique, UMR 7139 CNRS-Universite Pierre et Marie Curie-Paris VI)
  • Received : 2011.12.20
  • Accepted : 2012.02.23
  • Published : 2012.03.15
Download PDF
⟨ Previous Next ⟩

Abstract

We report an oxidative burst triggered by prostaglandin $A_2(PGA_2)$ in the brown algal kelp Laminaria digitata, constituting the first such discovery in an alga and the second finding of an oxidative burst triggered by a prostaglandin in a living organism. The response is more powerful than the oxidative burst triggered by most other chemical elicitors in Laminaria. Also, it is dose-dependent and cannot be inhibited by diphenylene iodonium, suggesting that another source than NAD(P)H oxidase is operational in the production of reactive oxygen species. Despite the very strong oxidative response, rather few effects at other levels of signal transduction pathways could be identified. $PGA_2$ does not increase lipolysis (free fatty acids) in Laminaria, and only one oxylipin (15-hydroxyeicosatetraenoic acid; 15-HETE) was found to be upregulated in Laminaria. In a subsequent set of experiments in the genome model Ectocarpus siliculosus, none of 5 selected candidate genes, all established participants in various stress responses, showed any significant differences in their expression profiles.

Keywords

References

  1. Zar, J. H. 1999. Biostatistical analysis. Prentice Hall, Upper Saddle River, NJ, 929 pp.
  2. Arimura, G., Ozawa, R., Shimoda, T., Nishioka, T., Boland, W. & Takabayashi, J. 2000. Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 406:512-515. https://doi.org/10.1038/35020072
  3. Arnold, T. M., Targett, N. M., Tanner, C. E., Hatch, W. I. & Ferrari, K. E. 2001. Evidence for methyl jasmonate-induced phlorotannin production in Fucus vesiculosus (Phaeophyceae). J. Phycol. 37:1026-1029. https://doi.org/10.1046/j.1529-8817.2001.01130.x
  4. Baldauf, S. L. 2003. The deep roots of eukaryotes. Science 300:1703-1706. https://doi.org/10.1126/science.1085544
  5. Baldridge, C. W. & Gerard, R. W. 1933. The extra respiration of phagocytosis. Am. J. Physiol. 103:235-236.
  6. Bestwick, C., Bolwell, P., Mansfield, J., Nicole, M. & Wojtaszek, P. 1999. Generation of the oxidative burst - scavenging for the truth. Trends Plant Sci. 4:88-89. https://doi.org/10.1016/S1360-1385(99)01385-0
  7. Bolwell, G. P., Davies, D. R., Gerrish, C., Auh, C. -K. & Murphy, T. M. 1998. Comparative biochemistry of the oxidative burst produced by rose and French bean cells reveals two distinct mechanisms. Plant Physiol. 116:1379-1385. https://doi.org/10.1104/pp.116.4.1379
  8. Bouarab, K., Adas, F., Gaquerel, E., Kloareg, B., Salaün, J. -P. & Potin, P. 2004. The innate immunity of a marine red alga involves oxylipins from both the eicosanoid and octadecanoid pathways. Plant Physiol. 135:1838-1848. https://doi.org/10.1104/pp.103.037622
  9. Bouarab, K., Potin, P., Correa, J. & Kloareg, B. 1999. Sulfated oligosaccharides mediate the interaction between a marine red alga and its green algal pathogenic endophyte. Plant Cell 11:1635-1650. https://doi.org/10.1105/tpc.11.9.1635
  10. Carpenter, L. J., Malin, G., Liss, P. S. & Kupper, F. C. 2000. Novel biogenic iodine-containing trihalomethanes and other short-lived halocarbons in the coastal East Atlantic. Global Biogeochem. Cycles 14:1191-1204. https://doi.org/10.1029/2000GB001257
  11. Charrier, B., Coelho, S. M., Le Bail, A., Tonon, T., Michel, G., Potin, P., Kloareg, B., Boyen, C., Peters, A. F. & Cock, J. M. 2008. Development and physiology of the brown alga Ectocarpus siliculosus: two centuries of research. New Phytol. 177:319-332. https://doi.org/10.1111/j.1469-8137.2007.02304.x
  12. Cock, J. M., Sterck, L., Rouze, P., Scornet, D., Allen, A. E., Amoutzias, G., Anthouard, V., Artiguenave, F., Aury, J. -M., Badger, J. H., Beszteri, B., Billiau, K., Bonnet, E., Bothwell, J. H., Bowler, C., Boyen, C., Brownlee, C., Carrano, C. J., Charrier, B., Cho, G. Y., Coelho, S. M., Collén, J., Corre, E., Da Silva, C., Delage, L., Delaroque, N., Dittami, S. M., Doulbeau, S., Elias, M., Farnham, G., Gachon, C. M. M., Gschloessl, B., Heesch, S., Jabbari, K., Jubin, C., Kawai, H., Kimura, K., Kloareg, B., Kupper, F. C., Lang, D., Le Bail, A., Leblanc, C., Lerouge, P., Lohr, M., Lopez, P. J., Martens, C., Maumus, F., Michel, G., Miranda-Saavedra, D., Morales, J., Moreau, H., Motomura, T., Nagasato, C., Napoli, C. A., Nelson, D. R., Nyvall-Collén, P., Peters, A. F., Pommier, C., Potin, P., Poulain, P., Quesneville, H., Read, B., Rensing, S. A., Ritter, A., Rousvoal, S., Samanta, M., Samson, G., Schroeder, D. C., Ségurens, B., Strittmatter, M., Tonon, T., Tregear, J. W., Valentin, K., Von Dassow, P., Yamagishi, T., Van de Peer, Y. & Wincker, P. 2010. The Ectocarpus genome and the independent evolution of multicellularity in the brown algae. Nature 465:617-621. https://doi.org/10.1038/nature09016
  13. Collen, J., Pedersén, M. & Bornman, C. H. 1994. A stress-induced oxidative burst in Eucheuma platycladum (Rhodophyta). Physiol. Plant. 92:417-422. https://doi.org/10.1111/j.1399-3054.1994.tb08830.x
  14. Colombo, M. L., Rise, P., Giavarini, F., De Angelis, L., Galli, C. & Bolis, C. L. 2006. Marine macroalgae as sources of polyunsaturated fatty acids. Plant Foods Hum. Nutr. 61:67-72.
  15. Cosse, A., Leblanc, C. & Potin, P. 2007. Dynamic defense of marine macroalgae against pathogens: from early activated to gene-regulated responses. Adv. Bot. Res. 46:221-266. https://doi.org/10.1016/S0065-2296(07)46006-2
  16. Dang, H. T., Lee, H. J., Yoo, E. S., Hong, J., Choi, J. S. & Jung, J. H. 2010. The occurrence of 15-keto-prostaglandins in the red alga Gracilaria verrucosa. Arch. Pharm. Res. 33:1325-1329. https://doi.org/10.1007/s12272-010-0905-y
  17. De Franco, P. -O., Rousvoal, S., Tonon, T. & Boyen, C. 2008. Whole genome survey of the glutathione transferase family in the brown algal model Ectocarpus siliculosus. Mar. Genomics 1:135-148. https://doi.org/10.1016/j.margen.2009.01.003
  18. Dittami, S. M., Scornet, D., Petit, J. L., Ségurens, B., Da Silva, C., Corre, E., Dondrup, M., Glatting, K. H., König, R., Sterck, L., Rouzé, P., Van de Peer, Y., Cock, J. M., Boyen, C. & Tonon, T. 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. https://doi.org/10.1186/gb-2009-10-6-r66
  19. Dring, M. J. 2005. Stress resistance and disease resistance in seaweeds: the role of reactive oxygen metabolism. Adv. Bot. Res. 43:175-207. https://doi.org/10.1016/S0065-2296(05)43004-9
  20. Ellertsdottir, E. & Peters, A. F. 1997. High prevalence of infection by endophytic brown algae in populations of Laminaria spp. (Phaeophyceae). Mar. Ecol. Prog. Ser. 146:135-143. https://doi.org/10.3354/meps146135
  21. Farmer, E. & Schulze-Lefert, P. 2005. Biotic interactions: from molecular networks to inter-organismal communities. Curr. Opin. Plant Biol. 8:343-345. https://doi.org/10.1016/j.pbi.2005.05.011
  22. Farmer, E. E., Alméras, E. & Krishnamurthy, V. 2003. Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr. Opin. Plant Biol. 6:372-378. https://doi.org/10.1016/S1369-5266(03)00045-1
  23. Funk, C. D. 2001. Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294:1871-1875. https://doi.org/10.1126/science.294.5548.1871
  24. Gachon, C. M. M., Sime-Ngando, T., Strittmatter, M., Chambouvet, A. & Kim, G. H. 2010. Algal diseases: spotlight on a black box. Trends Plant Sci. 15:633-640. https://doi.org/10.1016/j.tplants.2010.08.005
  25. Gaquerel, E., Herve, C., Labrière, C., Boyen, C., Potin, P. & Salaun, J. P. 2007. Evidence for oxylipin synthesis and induction of a new polyunsaturated fatty acid hydroxylase activity in Chondrus crispus in response to methyljasmonate. Biochim. Biophys. Acta 1771:565-575. https://doi.org/10.1016/j.bbalip.2007.02.007
  26. Gerhart, D. J. 1984. Prostaglandin $A_2$: an agent of chemical defense in the Caribbean gorgonian Plexaura homomalla. Mar. Ecol. Prog. Ser. 19:181-187. https://doi.org/10.3354/meps019181
  27. Gerwick, W. H. 1994. Structure and biosynthesis of marine algal oxylipins. Biochim. Biophys. Acta 1211:243-255. https://doi.org/10.1016/0005-2760(94)90147-3
  28. Glazener, J. A., Orlandi, E. W., Harmon, G. L. & Baker, C. J. 1991. An improved method for monitoring active oxygen in bacteria-treated suspension cells using luminol-dependent chemiluminescence. Physiol. Mol. Plant Pathol. 39:123-133. https://doi.org/10.1016/0885-5765(91)90023-B
  29. Gleason, F. H., Küpper, F. C., Amon, J. P., Picard, K., Gachon, C. M. M., Marano, A. V., Sime-Ngando, T. & Lilje, O. 2011. Zoosporic true fungi in marine ecosystems: a review. Mar. Freshw. Res. 62:383-393. https://doi.org/10.1071/MF10294
  30. Higa, T. & Kuniyoshi, M. 2000. Toxins associated with medicinal and edible seaweeds. J. Toxicol. Toxin Rev. 19:119-137. https://doi.org/10.1081/TXR-100100317
  31. Hofmann, M. & Eichenberger, W. 1997. Lipid and fatty acid composition of the marine brown alga Dictyopteris membranacea. Plant Cell Physiol. 38:1046-1052. https://doi.org/10.1093/oxfordjournals.pcp.a029270
  32. Hsu, B. -Y., Tsao, C. -Y., Chiou, T. -K. & Hwang, D. -F. 2008. Factors affecting $PGE_2$ production in seaweed Gracilaria tenuistipitata. J. Food Drug Anal. 16:59-65.
  33. Huang, W. -C., Chio, C. -C., Chi, K. -H., Wu, H. -M. & Lin, W. -W. 2002. Superoxide anion-dependent Raf/MEK/ERK activation by peroxisome proliferator activated receptor $\gamma$ agonists 15-deoxy-${\Delta}^{12,14}$-prostaglandin $J_2$, ciglitazone, and GW1929. Exp. Cell Res. 277:192-200. https://doi.org/10.1006/excr.2002.5546
  34. Imbs, A. B., Vologodskaya, A. V., Nevshupova, N. V., Khotimchenko, S. V. & Titlyanov, E. A. 2001. Response of prostaglandin content in the red alga Gracilaria verrucosa to season and solar irradiance. Phytochemistry 58:1067-1072. https://doi.org/10.1016/S0031-9422(01)00321-1
  35. Jaworek, J., Bonior, J., Tomaszewska, R., Jachimczak, B., Kot, M., Bielański, W., Pawlik, W. W., Sendur, R., Stachura, J., Konturek, P. C. & Konturek, S. J. 2001. Involvement of cyclooxygenase-derived prostaglandin $E_2$ and nitric oxide in the protection of rat pancreas afforded by low dose of lipopolysaccharide. J. Physiol. Pharmacol. 52:107-126.
  36. Kliewer, S. A., Lenhard, J. M., Wilson, T. M., Patel, I., Morris, D. C. & Lehmann, J. M. 1995. A prostaglandin $J_2$ metabolite binds peroxisome proliferator-activated receptor $\gamma$ and promotes adipocyte differentiation. Cell 83:813-819. https://doi.org/10.1016/0092-8674(95)90194-9
  37. Kupper, F. C., Carpenter, L. J., McFiggans, G. B., Palmer, C. J., Waite, T. J., Boneberg, E. -M., Woitsch, S., Weiller, M., Abela, R., Grolimund, D., Potin, P., Butler, A., Luther, G. W., Kroneck, P. M. H., Meyer-Klaucke, W. & Feiters, M. C. 2008. Iodide accumulation provides kelp with an inorganic antioxidant impacting atmospheric chemistry. Proc. Natl. Acad. Sci. U. S. A. 105:6954-6958. https://doi.org/10.1073/pnas.0709959105
  38. Kupper, F. C., Gaquerel, E., Boneberg, E. -M., Morath, S., Salaün, J. -P. & 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. https://doi.org/10.1093/jxb/erj146
  39. Kupper, F. C., Gaquerel, E., Cosse, A., Adas, F., Peters, A. F., Müller, D. G., Kloareg, B., Salaün, J. -P. & Potin, P. 2009. Free fatty acids and methyl jasmonate trigger defense reactions in Laminaria digitata. Plant Cell Physiol. 50:789-800. https://doi.org/10.1093/pcp/pcp023
  40. Kupper, F. C., Kloareg, B., Guern, J. & Potin, P. 2001. Oligoguluronates elicit an oxidative burst in the brown algal kelp Laminaria digitata. Plant Physiol. 125:278-291. https://doi.org/10.1104/pp.125.1.278
  41. Kupper, F. C., Müller, D. G., Peters, A. F., Kloareg, B. & Potin, P. 2002. Oligoalginate recognition and oxidative burst play a key role in natural and induced resistance of sporophytes of Laminariales. J. Chem. Ecol. 28:2057-2081. https://doi.org/10.1023/A:1020706129624
  42. Le Bail, A., Dittami, S. M., De Franco, P. O., Rousvoal, S., Cock, M. J., Tonon, T. & Charrier, B. 2008. Normalisation genes for expression analyses in the brown alga model Ectocarpus siliculosus. BMC Mol. Biol. 9:75. https://doi.org/10.1186/1471-2199-9-75
  43. Miller, C. C., Ziboh, V. A., Wong, T. & Fletcher, M. P. 1990. Dietary supplementation with oils rich in (n-3) and (n-6) fatty acids influences in vivo levels of epidermal lipoxygenase products in guinea pigs. J. Nutr. 120:36-44. https://doi.org/10.1093/jn/120.1.36
  44. Mittler, R., Vanderauwera, S., Gollery, M. & Van Breusegem, F. 2004. Reactive oxygen gene network of plants. Trends Plant Sci. 9:490-498. https://doi.org/10.1016/j.tplants.2004.08.009
  45. Muller, D. G., Gachon, C. M. M. & Kupper, F. C. 2008. Axenic clonal cultures of filamentous brown algae: initiation and maintenance. Cah. Biol. Mar. 49:59-65.
  46. Muller, D. G. & Knippers, R. 2001. Phaeovirus. In Tidona, C. & Darai, G. (Eds.) The Springer Index of Viruses. Springer Verlag, Berlin, Heidelberg, New York, pp. 732-736.
  47. O'Donnell, V., Tew, D. G., Jones, O. T. G. & England, P. J. 1993. Studies on the inhibitory mechanism of iodonium compounds with special reference to neutrophil NADPH oxidase. Biochem. J. 290:41-49. https://doi.org/10.1042/bj2900041
  48. Orozco-Cardenas, M. L., Narvaez-Vasquez, J. & Ryan, C. A. 2001. Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13:179-191. https://doi.org/10.1105/tpc.13.1.179
  49. Ottonello, L., Morone, M. P., Dapino, P. & Dallegri, F. 1995. Cyclic AMP-elevating agents down-regulate the oxidative burst induced by granulocyte-macrophage colony-stimulating factor (GM-CSF) in adherent neutrophils. Clin. Exp. Immunol. 101:502-506. https://doi.org/10.1111/j.1365-2249.1995.tb03141.x
  50. Pan, Z., Camara, B., Gardner, H. W. & Backhaus, R. A. 1998. Aspirin inhibition and acetylation of the plant cytochrome P450, allene oxide synthase, resembles that of animal prostaglandin endoperoxide H synthase. J. Biol. Chem. 273:18139-18145. https://doi.org/10.1074/jbc.273.29.18139
  51. Peters, A. F., Marie, D., Scornet, D., Kloareg, B. & Cock, J. M. 2004. Proposal of Ectocarpus siliculosus (Ectocarpales, Phaeophyceae) as a model organism for brown algal genetics and genomics. J. Phycol. 40:1079-1088. https://doi.org/10.1111/j.1529-8817.2004.04058.x
  52. Pfaffl, M. W., Horgan, G. W. & Dempfle, L. 2002. Relative expression software tool (REST${\copyright}$) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30:e36. https://doi.org/10.1093/nar/30.9.e36
  53. Potin, P., Bouarab, K., Salaun, J. -P., Pohnert, G. & Kloareg, B. 2002. Biotic interactions of marine algae. Curr. Opin. Plant Biol. 5:308-317. https://doi.org/10.1016/S1369-5266(02)00273-X
  54. Reymond, P. & Farmer, E. E. 1998. Jasmonate and salicylate as global signals for defense gene expression. Curr. Opin. Plant Biol. 1:404-411. https://doi.org/10.1016/S1369-5266(98)80264-1
  55. Ritter, A., Goulitquer, S., Salaun, J. -P., Tonon, T., Correa, J. A. & 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. https://doi.org/10.1111/j.1469-8137.2008.02626.x
  56. Ritter, A., Ubertini, M., Romac, S., Gaillard, F., Delage, L., Mann, A., Cock, J. M., Tonon, T., Correa, J. A. & Potin, P. 2010. Copper stress proteomics highlights local adaptation of two strains of the model brown alga Ectocarpus siliculosus. Proteomics 10:2074-2088. https://doi.org/10.1002/pmic.200900004
  57. Ross, C., Kupper, F. C. & Jacobs, R. S. 2006. Involvement of reactive oxygen species and reactive nitrogen species in the wound response of Dasycladus vermicularis. Chem. Biol. 13:353-364. https://doi.org/10.1016/j.chembiol.2006.01.009
  58. Ross, C., Küpper, F. C., Vreeland, V., Waite, J. H. & Jacobs, R. S. 2005. Evidence of a latent oxidative burst in relation to wound repair in the giant unicellular chlorophyte Dasycladus vermicularis. J. Phycol. 41:531-541. https://doi.org/10.1111/j.1529-8817.2005.04072.x
  59. Sajiki, J. 1997. Effects of acetic acid treatment on the concentrations of arachidonic acid and prostaglandin E2 in the red algae, Gracilaria asiatica and G. rhodocaudata. Fish. Sci. 63:128-131. https://doi.org/10.2331/fishsci.63.128
  60. Schultz, J. C. & Appel, H. M. 2004. Cross-kingdom cross-talk: hormones shared by plants and their insect herbivores. Ecology 85:70-77. https://doi.org/10.1890/02-0704
  61. Spolaore, P., Joannis-Cassan, C., Duran, E. & Isambert, A. 2006. Commercial applications of microalgae. J. Biosci. Bioeng. 101:87-96. https://doi.org/10.1263/jbb.101.87
  62. Starr, R. C. & Zeikus, J. A. 1987. UTEX: the culture collection of algae at the University of Texas at Austin. J. Phycol. 23(Suppl):1-47. https://doi.org/10.1111/j.1529-8817.1987.tb04493.x
  63. Strittmatter, M., Gachon, C. M. M. & Küpper, F. C. 2009. Ecology of lower oomycetes. In Lamour, K. & Kamoun, S. (Eds.) Oomycete Genetics and Genomics: Diversity, Plant and Animal Interactions, and Toolbox. John Wiley and Sons, Hoboken, NJ, pp. 25-46.
  64. Turlings, T. C. J., Alborn, H. T., Loughrin, J. H. & Tumlinson, J. H. 2000. Volicitin, an elicitor of maize volatiles in oral secretion of Spodoptera exigua: isolation and bioactivity. J. Chem. Ecol. 26:189-202. https://doi.org/10.1023/A:1005449730052
  65. Vaidya, S., Somers, E. P., Wright, S. D., Detmers, P. A. & Bansal, V. S. 1999. 15-deoxy-${\Delta}^{12,14}$-prostaglandin $J_2$ inhibits the ${\beta}_2$ integrin-dependent oxidative burst: involvement of a mechanism distinct from peroxisome proliferator-activated receptor $\gamma$ ligation. J. Immunol. 163:6187-6192.
  66. Weinberger, F. & Friedlander, M. 2000a. Endogenous and exogenous elicitors of a hypersensitive response in Gracilaria conferta (Rhodophyta). J. Appl. Phycol. 12:139-145. https://doi.org/10.1023/A:1008119125911
  67. Weinberger, F. & Friedlander, M. 2000b. Response of Gracilaria conferta (Rhodophyta) to oligoagars results in defense against agar-degrading epiphytes. J. Phycol. 36:1079-1086. https://doi.org/10.1046/j.1529-8817.2000.00003.x
  68. Weinberger, F., Friedlander, M. & Hoppe, H. -G. 1999. Oligoagars elicit a physiological response in Gracilaria conferta (Rhodophyta). J. Phycol. 35:747-755. https://doi.org/10.1046/j.1529-8817.1999.3540747.x
  69. West, J. A. & McBride, D. L. 1999. Long-term and diurnal carpospore discharge patterns in the Ceramiaceae, Rhodomelaceae and Delesseriaceae (Rhodophyta). Hydrobiologia 398/399:101-113. https://doi.org/10.1023/A:1017025815001
  70. Whalen, K. E., Lane, A. L., Kubanek, J. & Hahn, M. E. 2010. Biochemical warfare on the reef: the role of glutathione transferases in consumer tolerance of dietary prostaglandins. PLoS One 5:e8537. https://doi.org/10.1371/journal.pone.0008537
  71. Wiesemeier, T., Jahn, K. & Pohnert, G. 2008. No evidence for the induction of brown algal chemical defense by the phytohormones jasmonic acid and methyl jasmonate. J. Chem. Ecol. 34:1523-1531. https://doi.org/10.1007/s10886-008-9568-2
  72. Wojtaszek, P. 1997. Oxidative burst: an early plant response to pathogen infection. Biochem. J. 322(Pt 3):681-692.
  73. Wright, E. P. 1877. On a species of Rhizophydium parasitic on species of Ectocarpus, with notes on the fructification of the Ectocarpi. Trans. R. Ir. Acad. 26:369-380.

Cited by

  1. Methyl Jasmonate-Induced Lipidomic and Biochemical Alterations in the Intertidal MacroalgaGracilaria dura(Gracilariaceae, Rhodophyta) vol.56, pp.10, 2015, https://doi.org/10.1093/pcp/pcv115
  2. Quantification of Selected Endogenous Hydroxy-oxylipins from Tropical Marine Macroalgae vol.16, pp.1, 2014, https://doi.org/10.1007/s10126-013-9533-0
  3. Biologically Active Oxylipins from Enzymatic and Nonenzymatic Routes in Macroalgae vol.14, pp.1, 2016, https://doi.org/10.3390/md14010023
  4. In vivo speciation studies and antioxidant properties of bromine in Laminaria digitata reinforce the significance of iodine accumulation for kelps vol.64, pp.10, 2013, https://doi.org/10.1093/jxb/ert110
  5. Morphology and phytogeography of Laminaria appressirhiza and L. inclinatorhiza (Phaeophyceae) from the Sea of Okhotsk vol.27, pp.3, 2012, https://doi.org/10.4490/algae.2012.27.3.139
  6. Emission of volatile halogenated compounds, speciation and localization of bromine and iodine in the brown algal genome model Ectocarpus siliculosus vol.23, pp.7, 2018, https://doi.org/10.1007/s00775-018-1539-7
  7. Evolution and Expansion of the Prokaryote-Like Lipoxygenase Family in the Brown Alga Saccharina japonica vol.8, pp.None, 2017, https://doi.org/10.3389/fpls.2017.02018
  8. Prostaglandins in Marine Organisms: A Review vol.17, pp.7, 2012, https://doi.org/10.3390/md17070428