Skip to main content
SpringerLink
Log in
Book cover

Systems Biology of Marine Ecosystems pp 99–116Cite as

Volatiles in the Aquatic Marine Ecosystem: Ethylene and Related Plant Hormones and Sporulation in Red Seaweeds

  • Chapter
  • First Online:

Abstract

Reports on the production of volatile compounds in algae have been focused on what they produce rather than on their functions. In this scenario, a myriad of fatty acid derivatives, nitrogen-containing compounds, organic halogen compounds, sulphur compounds and compounds derived from transferase activity have been described. Recently, a broad range of these volatile compounds has also been identified under a physiological complex pattern in algae, inferring that seaweeds must somehow integrate signals not only to reply to environmental status but also as a response to their growth and development capacity. Evidence comes from algal mats, which suffer sudden increments in the number of reproductive structures and correspondingly abrupt decreases in biomass. Specifically, the emission of airborne substances, such as ethylene and dimethylsulphide (DMS), has provided valuable information on their participation in algal physiology. DMS is affected by environmental factors such as light and salinity. In addition, the time course of DMS and ethylene release has revealed that the synthesis of ethylene, via the alternative route of DMSP lyase, is not a priority in the red seaweeds. Furthermore, ethylene has a significant effect on the formation of reproductive structures and the sporulation of the red seaweeds Grateloupia imbricata and Pterocladiella capillacea. Our data suggest that the presence of putative receptors and the response of ethylene could be influenced by the length of exposure to this volatile.

Unfortunately, despite the importance of all these facts in the formation of reproductive structures and spore germination, there is to date scant information at a molecular level, and little is known about the role of genes on these processes. In this chapter, we aim to compile the current knowledge of volatile compounds in algae. We will discuss the relation between the emission of volatiles and algal physiology and mainly focus on the involvement of volatiles in the reproduction of red seaweeds. As far as possible, we will try to unveil the molecular mechanisms of the perception of volatiles.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Abrahamsson K, Ekdahl A, Collén J, Pedersén M (1995) Marine algae. A source of trichloroethylene and perchloroethylene. Limnol Oceanogr 40(7):1321–1326

    Article  CAS  Google Scholar 

  • Andreae MO, Elbert W, de Mora SJ (1995) Biogenic sulfur emissions and aerosols over the tropical South Atlantic: 3. Atmospheric dimethylsulfide, aerosols and cloud condensation nuclei. J Geophys Res 100:11335–11356

    Article  CAS  Google Scholar 

  • Arnold TM, Targett NM, Tanner CE, Hatch WI, Ferrari KE (2001) Evidence for metil jasmonate-induced phlorotannin production in Fucus vesiculosus (Phaeophyceae). J Phycol 37:1025–1029

    Article  Google Scholar 

  • Baldwin IT, Halitschke R, Paschold A, von Dahl CC, Preston CA (2006) Volatile signaling in plant–plant interactions: ‘talking trees’ in the genomics era. Science 311:812–815

    Article  CAS  PubMed  Google Scholar 

  • Bankova V, Stepanov K, Dimitrova-Konaklieva ST, Keremedchieva G, Frette X, Nikolova C, Kujimgiev A, Popov S (2001) Secondary metabolites and lipids in Chara globularis Thuill. Hydrobiologia 457:199–203

    Article  Google Scholar 

  • Barbier G, Oesterhelt C, Larson MD, Halgren RG, Wilkerson C, Garavito RM, Benning C, Weber APM (2005) Comparative genomics of two closely related unicellular thermo-acidophilic red algae, Galdieria sulphuraria and Cyanidioschyzon merolae, reveals the molecular basis of the metabolic flexibility of Galdieria sulphuraria and significant differences in carbohydrate metabolism of both algae. Plant Physiol 137:460–474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baweja P, Sahoo D, Garcia-Jimenez P, Robaina RR (2009) Seaweed tissue culture as applied to biotechnology: problems, achievements and prospects. Phycol Res 57:45–58

    Article  Google Scholar 

  • Bitton R, Ben-Yehuda M, Davidovich M, Balazs Y, Potin P, Delage L, Colin C, Bianco-Peled H (2006) Structure of algal-born phenolic polymeric adhesives. Macromol Biosci 7:1280–1289

    Article  Google Scholar 

  • Bitton R, Berglin M, Elwing H, Colin C, Delage L, Potin P, Bianco-Peled H (2007) The influence of halide-mediated oxidation on algae-born adhesives. Macromol Biosci 7:1280–1289

    Article  CAS  PubMed  Google Scholar 

  • Bleecker AB (2000) ETHYLENE: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18

    Article  CAS  PubMed  Google Scholar 

  • Bouarab K, Adas F, Gaquerel E, Kloareg B, Salaün JP, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bravo-Linares CM, Mudge SM, Loyola-Sepulveda RH (2010) Production of volatile organic compounds (vocs) by temperate macroalgae. The use of solid phase microextraction (spme) coupled to GC-MS as method of analysis. J Chil Chem Soc 55(2):227–232

    Article  CAS  Google Scholar 

  • Bruinsma M, van Broekhoven S, Poelman EH, Posthumus MA, Müller MJ, van Loon JJA, Dicke M (2010) Inhibition of lipoxygenase affects induction of both direct and indirect plant defences against herbivorous insects. Oecologia 162:393–404

    Article  PubMed  Google Scholar 

  • Carpenter LJ, Liss PS (2000) On temperate sources of bromoform and other reactive organic bromines gases. J Geophys Res Atmos 105:20539–205547

    Article  CAS  Google Scholar 

  • Carpenter LJ, Liss PS, Penkett SA (2003) Marine organohalogens in the atmosphere over the Atlantic and Southern Oceans. J Geophys Res 108(D9):4256. doi:10.1029/2002JD002769

    Article  Google Scholar 

  • Christov C, Fournadzieva S, Bozhcova M, Cherkezov N, Pilarski P, Zafirova T (1996) Abscisic acid and jasmonates content during the ontogenesis of Scenedesmus acutus. In: Ordog V, Szigeti J, Pulz O (eds) Proceedings of a conference on progress in plant sciences from plant breeding to growth regulation. Pannon University of Agricultural Sciences, Mosonmagyarovár, pp 155–162

    Google Scholar 

  • Christov C, Pounevacc I, Bozhkova M, Toncheva T, Fournadzieva S, Zafirova T (2001) Influence of temperature and methyl jasmonate on Scenedesmus incrassulatus. Biol Plant 44(3):367–371

    Article  CAS  Google Scholar 

  • Cock JM, Sterck L, Rouze P, Scornet D, Allen AE et al (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465:617–621. doi:10.1038/nature09016

    Article  CAS  PubMed  Google Scholar 

  • Cole KM, Sheath RG (1990) Biology of the red algae. Cambridge University Press, Cambridge, New York, Port Chester, Melbourne, Sydney

    Google Scholar 

  • Collén J, Guisle-Marsollier I, Léger JL, Boyen C (2007) Response of the transcriptome of the intertidal red seaweed Chondrus crispus to controlled and natural stresses. New Phytol 176:45–55

    Article  PubMed  Google Scholar 

  • Dacey JWH, King GM, Wakeham SG (1987) Factors controlling emission of dimethylsulfide from salt marshes. Nature 330:643–645

    Article  CAS  Google Scholar 

  • Devoto A, Turner JG (2003) Regulation of jasmonate-mediated plant responses in Arabidopsis. Ann Bot 92:329–337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujimura T, Kawai T, Kajiwara T, Iwhida Y (1994) Volatile components in protoplasts isolated from the marine brown alga Dictyopteris prolifera (Dictyotales). Papers Plant Tissue Culture Letters 11(1):34–39

    Article  CAS  Google Scholar 

  • Gaquerel E (2005) Caractérisation et rôle des oxylipines dans la signalisation lipidique cellulaire chez le gamétophyte de Chondrus crispus. PhD thesis, Université de Bretagne Occidentale, Brest

    Google Scholar 

  • Gaquerel E, Weinhold A, Baldwin IT (2009) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphigidae) and its natural host Nicotiana attenuata. VIII. An unbiased GCxGC-ToFMS analysis of the plant’s elicited volatile emissions. Plant Physiol 149(3):1408–1423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia-Jimenez P, Robaina RR (2012) Effects of ethylene on tetrasporogenesis in Pterocladiella capillacea (Rhodophyta). J Phycol 48:710–715

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Jimenez P, Robaina RR (2015) On reproduction in red algae: further research needed at the molecular level. Front Plant Sci 6:1–6

    Google Scholar 

  • Garcia-Jimenez P, Brito-Romano O, Robaina RR (2013) Production of volatiles by the red seaweed Gelidium arbuscula (Rhodophyta): emission of ethylene and dimethyl sulphide. J Phycol 49:661–669

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Jimenez P, Brito-Romano O, Robaina RR (2016) Occurrence of jasmonates during cystocarp development in the red alga Grateloupia imbricata. J Phycol 52:1085–1093

    Article  Google Scholar 

  • Goodwin KD, North WJ, Lidstrom ME (1997) Production of bromoform and dibromomethane by Giant Kelp: factors affecting release and comparison to anthropogenic bromine sources. Limnol Oceanogr 42:1725–1734

    Article  CAS  Google Scholar 

  • Hay ME (1996) Marine chemical ecology: what’s known and what’s next? J Exp Mar Biol Ecol 200:103–134

    Article  CAS  Google Scholar 

  • Holopainen JK (2004) Multiple functions of inducible plant volatiles. Trends Plant Sci 9:529–533

    Article  CAS  PubMed  Google Scholar 

  • Kawasaki W, Matsui K, Akakabe Y, Itai N, Kajiwara T (1998) Volatiles from Zostera marina. Phytochemistry 47(1):27–29

    Article  CAS  Google Scholar 

  • Kim GH, Lee IK (1989) Mixed phases reproduction of Platythamnion yezoense Inagaki in culture. Korean J Phycol 4(2):111–119

    Google Scholar 

  • Klaschka U, Kolossa-Gehring M (2007) Fragrances in the environment: pleasant odours for nature? Environ Sci Pollut Res 14:44–52

    Article  CAS  Google Scholar 

  • Krupina MV, Dathe W (1991) Occurrence of jasmonic acid in the red alga Gelidium latifolium. Z Naturforsch 46:1127–1129

    CAS  Google Scholar 

  • Küpper FC, Gaquerel E, Cosse A, Adas F, Peters AF, Müller DG, Kloareg B, Salaün JP, Potin P (2009) Free fatty acids and methyl jasmonate trigger defense reactions in Laminaria digitata. Plant Cell Physiol 50(4):789–800

    Article  PubMed  Google Scholar 

  • La Barre S, Potin P, Leblanc C, Delage L (2010) The halogenated metabolism of brown algae (Phaeophyta), its biological importance and its environmental significance. Mar Drugs 8(4):988–1010. doi:10.3390/md8040988

    Article  PubMed  PubMed Central  Google Scholar 

  • Leedham Elvidge EC, Phang SM, Sturges WT, Malin G (2015) The effect of desiccation on the emission of volatile bromocarbons from two common temperate macroalgae. Biogeosciences 12:387–398

    Article  Google Scholar 

  • Liechti R, Farmer EE (2006) Jasmonate biochemical pathway. Sci STKE 322:1–3

    Google Scholar 

  • Liechti R, Gfeller A, Farmer EE (2006) Jasmonate signaling pathway. Sci STKE 14. doi:10.1126/stke.3222006cm2

  • Loreto F, Schnitzler JP (2010) Abiotic stress and induced BVOCS. Trends Plant Sci 15:154–166

    Article  CAS  PubMed  Google Scholar 

  • Manley SL, Goodwin K, North WJ (1992) Laboratory production of bromoform, methylene bromide, and methyl iodide by macroalgae and distribution in nearshore southern California waters. Limnol Oceanogr 37:1652–1659

    Article  CAS  Google Scholar 

  • Matsui K (2006) Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Curr Opin Plant Biol 9:274–280

    Article  CAS  PubMed  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  PubMed  Google Scholar 

  • Montero-Fernández M, Robaina RR, Garcia-Jimenez P (2016) In silico characterization of DNA motifs associated with the differential expression of the ornithine decarboxylase gene during in vitro cystocarp development in the red seaweed Grateloupia imbricata. J Plant Physiol 195:31–38

    Article  PubMed  Google Scholar 

  • Mtolera MSP, Collén J, Pedersén M, Ekdahl A, Abrahamsson K, Semesi AK (1996) Stress-induced production of volatile halogenated organic compounds in Eucheuma denticulatum (Rhodophyta) caused by elevated pH and high light intensities. Eur J Phycol 32(1):89–95

    Article  Google Scholar 

  • Müller DG (1989) The role of pheromones in sexual reproduction of brown algae. In: Coleman AW, Goff LJ, Stein-Taylor JR (eds) Algae as experimental systems. Alna r Liss, Inc, New York, pp 201–213

    Google Scholar 

  • Niki T, Kunugi M, Otsuki A (2000) DMSP-lyase activity in five marine phytoplankton species: its potential importance in DMS production. Mar Biol 136:759–764

    Article  CAS  Google Scholar 

  • Osborne DJ, McManus MT (2005) Hormones, signals and target cells in plant development. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Otte ML, Wilson G, Morris JT, Moran BM (2004) Dimethylsulphoniopropionate (DMSP) and related compounds in higher plants. J Exp Bot 55:1919–1925

    Article  CAS  PubMed  Google Scholar 

  • Paul C, Pohnert G (2011) Production and role of volatile halogenated compounds from marine algae. Nat Prod Rep 28:186–195

    Article  CAS  PubMed  Google Scholar 

  • Pirjola L, O’Dowd CD, Brooks IM, Kulmala M (2000) Can new particle formation occur in the clean marine boundary layer? J Geophys Res 105:26531–26546

    Article  CAS  Google Scholar 

  • Plettner I, Steinke M, Malin G (2005) Ethene (ethylene) production in the marine macroalga Ulva (Enteromorpha) intestinales L. (Chlorophyta, Ulvophyceae): effect of light stress and co-production with dimethylsulphide. Plant Cell Environ 28:1136–1145

    Article  CAS  Google Scholar 

  • Qualley A, Dudareva N (2010) Plant volatiles. eLS. doi:10.1002/9780470015902.a0000910

  • Reis VM, Oliveira LS, Passos RMF, Viana NB, Mermelstein C (2013) Traffic of secondary metabolites to cell surface in the red alga Laurencia dendroidea depends on a two-step transport by the cytoskeleton. PLoS One 8(5):e63929. doi:10.1371/journal.pone.0063929

    Article  PubMed  PubMed Central  Google Scholar 

  • Roje S (2006) S-Adenosyl-L-methionine: beyond the universal methyl group donor. Phytochemistry 67:1686–1698

    Article  CAS  PubMed  Google Scholar 

  • Sacramento AT, Garcia-Jimenez P, Alcazar R, Tiburcio AF, Robaina RR (2004) Influence of polyamines on the sporulation of Grateloupia (Halymeniaceae, Rhodophyta). J Phycol 40:887–894

    Article  CAS  Google Scholar 

  • Salgado LT, Cinelli LP, Viana NB, Tomazetto de Carvalho R, Mourão P, Teixeira VL, Farina M, Amado Filho GM (2009) Vanadium bromoperoxidase catalyzes the formation of high-molecular-weight complexes between brown algal phenolic substances and alginates. J Phycol 45:193–202

    Article  CAS  PubMed  Google Scholar 

  • Sasaki Y, Asamizu E, Shibata D, Nakamura Y, Kaneko T, Awai K, Amagai M, Kuwata C, Tsugane T, Masuda T, Shimada H, Takamiya K, Ohta H, Tabata S (2001) Monitoring of methyl jasmonate-responsive genes in Arabidopsis by cDNA macroarray: self-activation of jasmonic acid biosynthesis and crosstalk with other phytohormone signaling pathways. DNA Res 8:153–161

    Article  CAS  PubMed  Google Scholar 

  • Schall C, Laturnus F, Heumann KG (1994) Biogenic volatile organoiodine and organobromine compounds released from polar macroalgae. Chemosphere 28:1315–1324

    Article  CAS  Google Scholar 

  • Stefels J (2000) Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J Sea Res 43:183–197

    Article  CAS  Google Scholar 

  • Steinke M, Daniel C, Kirst GO (1996) DMSP lyase in marine macro- and microalgae: intraspecific differences in cleavage activity. In: Kiene RP, Visscher PT, Keller M, Kirst GO (eds) Biological and environmental chemistry of DMSP and related sulfonium compounds. Plenum, New York, pp 317–324

    Chapter  Google Scholar 

  • Sunda W, Kieber DJ, Kiene RP, Huntsman S (2002) An antioxidant function for DMSP and DMS in marine algae. Nature 418:317–320

    Article  CAS  PubMed  Google Scholar 

  • Takamo K, Igarashi S, Mikai H, Hino S (2003) Causation of reversal simultaneity for diatom biomass and density of Phormidium tenue during the warm season in eutrophic Lake Barato, Japan. Limnology 4:73–78

    Article  Google Scholar 

  • Tugwell S, Branch GM (1989) Differential polyphenolic distribution among tissues in the kelps Ecklonia maxima, Laminaria pallida and Macrocystis angustifolia in relation to plant-defense theory. J Exp Mar Biol Ecol 129:219–230. doi:10.1016/0022-0981(89) 90104-4

    Article  CAS  Google Scholar 

  • Ueda J, Miyamoto K, Sato T, Momotani Y (1991a) Identification of jasmonic acid from Euglena gracilis Z as a plant growth regulator. Agric Biol Chem 55(1):275–276

    CAS  Google Scholar 

  • Ueda J, Miyamoto K, Aoki M, Hirata T, Sato T, Momotani Y (1991b) Identification of jasmonic acid in Chlorella and Spirulina. Bull Univ Osaka Prefect Ser B Agric Biol 43:103–108

    CAS  Google Scholar 

  • Uji T, Matsuda R, Takechi K, Takano H, Mizuta H, Takio S (2016) Ethylene regulation of sexual reproduction in the marine red alga Pyropia yezoensis (Rhodophyta). J Appl Phycol 28:3501. doi:10.1007/s10811-016-0904-6

    Article  CAS  Google Scholar 

  • Van Alstyne KL, Houser LT (2003) Dimethylsulfide release during macroinvertebrate grazing and its role as an activated chemical defense. Mar Ecol Prog Ser 250:175–181

    Article  Google Scholar 

  • van Rijssel M, Gieskes WC (2002) Temperature, light, and the dimethylsulfoniopropionate (DMSP) content of Emiliania huxleyi (Prymnesiophyceae). J Sea Res 48:17–27

    Article  Google Scholar 

  • Vanden Driessche T, De Vries PG, Guisset JL (1997) Differentiation, growth and morphogenesis: Acetabularia as a model system. New Phytol 135:1–20

    Article  Google Scholar 

  • Vanden Driessche T, Kevers C, Collet M, Gaspar T (1998) Acetabularia mediterranea and ethylene: production in relation with development, circadian rhythms in emission, and response to external application. J Plant Physiol 133:635–639

    Article  Google Scholar 

  • Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weinberger F, Lion U, Delage L, Kloareg B, Potin P, Beltrán J, Flores V, Faugeron S, Correa J, Pohnert G (2011) Up-regulation of lipoxygenase, phospholipase, and oxylipin-production in the induced chemical defense of the red alga Gracilaria chilensis against epiphytes. J Chem Ecol 37:677–686

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto M, Baldermann S, Yoshikawa K, Fujita A, Mase N, Watanabe N (2014) Determination of volatile compounds in four commercial samples of Japanese green algae using solid phase microextraction gas chromatography mass spectrometry. Sci World J 2014:289780. doi:10.1155/2014/289780

    Article  Google Scholar 

  • Yang SF, Hoffmann NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35:155–189

    Article  CAS  Google Scholar 

  • Yoch DC, Ansede JH, Rabinowitz S (1997) Evidence for intracellular and extracellular dimethylsulfoniopropionate (DMSP) lyases and DMSP uptake sites in two species of marine bacteria. Appl Environ Microbiol 63:3182–3188

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Olegario Brito-Romano for his skilful technical assistance. This work has been carried out at the Biology Department of the Facultad de Ciencias del Mar, Universidad de Las Palmas de Gran Canaria.

Author information

Authors and Affiliations

  1. Department Biology, Facultad de Ciencias del Mar, Universidad de Las Palmas de Gran Canaria, Las Palmas de Gran Canaria, Canary Islands, 35017, Spain

    P. Garcia-Jimenez & R. R. Robaina

Authors
  1. P. Garcia-Jimenez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. R. Robaina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. Garcia-Jimenez .

Editor information

Editors and Affiliations

  1. Climate Change Cluster, Faculty of Science, University of Technology Sydney (UTS), Sydney, New South Wales, Australia

    Manoj Kumar

  2. Climate Change Cluster, Faculty of Science, University of Technology Sydney (UTS), Sydney, New South Wales, Australia

    Peter Ralph

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Garcia-Jimenez, P., Robaina, R.R. (2017). Volatiles in the Aquatic Marine Ecosystem: Ethylene and Related Plant Hormones and Sporulation in Red Seaweeds. In: Kumar, M., Ralph, P. (eds) Systems Biology of Marine Ecosystems. Springer, Cham. https://doi.org/10.1007/978-3-319-62094-7_5

Download citation

Publish with us

Policies and ethics

Search

Navigation