Journal of Applied Phycology

, Volume 28, Issue 5, pp 2915–2924 | Cite as

Abiotic regulation of growth and fertility in the sporophyte of Dictyota dichotoma (Hudson) J.V. Lamouroux (Dictyotales, Phaeophyceae)

  • Kenny Bogaert
  • Tom Beeckman
  • Olivier De Clerck


While Dictyota dichotoma has been cultured for decades, relatively little is known on the abiotic regulation of its growth, life cycle and release periodicity. Here, we evaluated the different abiotic factors that potentially control growth, survival, fertility and spore release in order to establish efficient culture methods of the sporophyte that allow life cycle control. Vegetative growth is maximal at room temperature (18–20 °C), but cultures can be stored for months at low temperatures (≈8 °C). Red light, increased temperature and nutrient manipulation proved to be excellent triggers inducing sporogenesis. Sporophytes lack any lunar periodicity in spore release in contrast to gametophytes, but surprisingly, release of meiospores follows a similar diurnal cycle. This enables the production of synchronously developing spores during the entire lunar cycle. Interest in this species relates to its potential for commercial applications for phytoremediation, metabolites with therapeutic and anti-biofouling potential, and its usage as a model for developmental research complementary to Fucus.


Dictyota Fertility Abiotic regulation Temperature Light Spore release 



The authors are indebted to the Research Foundation Flanders (FWO) (PhD fellowship to KB).


  1. Abou-El-Wafa GSE, Shaaban M, Shaaban KA, El-Naggar ME, Maier A, Fiebig HH, Laatsch H (2013) Pachydictyols B and C: new diterpenes from Dictyota dichotoma Hudson. Mar Drugs 11:3109–3123CrossRefPubMedPubMedCentralGoogle Scholar
  2. Abrantes JL, Barbosa J, Cavalcanti D, Pereira RC, Frederico Fontes CL, Teixeira VL, Moreno Souza TL, Paixão IC (2010) The effects of the diterpenes isolated from the Brazilian brown algae Dictyota pfaffii and Dictyota menstrualis against the herpes simplex type-1 replicative cycle. Planta Med 76:339–344CrossRefPubMedGoogle Scholar
  3. Albuquerque IRL, Cordeiro SL, Gomes DL, Dreyfuss JL, Filgueira LGA, Leite EL, Nader HB, Rocha HAO (2013) Evaluation of anti-nociceptive and anti-inflammatory activities of a heterofucan from Dictyota menstrualis. Mar Drugs 11:2722–2740CrossRefPubMedPubMedCentralGoogle Scholar
  4. Aravindan S, Delma CR, Thirugnanasambandan SS, Herman TS, Aravindan N (2013) Anti-pancreatic cancer deliverables from sea: first-hand evidence on the efficacy, molecular targets and mode of action for multifarious polyphenols from five different brown algae. PLoS One 8: doi: 10.1371/journal.pone.0061977Google Scholar
  5. Barbosa JP, Fleury BG, da Gama BAP, Teixeira VL, Pereira RC (2007) Natural products as antifoulants in the Brazilian brown alga Dictyota pfaffii (Phaeophyta, Dictyotales). Biochem Syst Ecol 35:549–553CrossRefGoogle Scholar
  6. Bogaert KA, Arun A, Coelho SM, De Clerck O (2013) Brown algae as a model for plant organogenesis. Methods Mol Biol 959:97–125CrossRefPubMedGoogle Scholar
  7. Brownlee C, Bouget FY, Corellou F (2001) Choosing sides: establishment of polarity in zygotes of fucoid algae. Semin Cell Dev Biol 12:345–351CrossRefPubMedGoogle Scholar
  8. Caamal-Fuentes E, Moo-Puc R, Freile-Pelegrín Y, Robledo D (2014) Cytotoxic and antiproliferative constituents from Dictyota ciliolata, Padina sanctae-crucis and Turbinaria tricostata. Pharm Biol 52:1–5CrossRefGoogle Scholar
  9. Carney LT, Edwards S (2010) Role of nutrient fluctuations and delayed development in gametophyte reproduction by Macrocystis pyrifera (Phaeopyceae) in southern California. J Phycol 46:987–996CrossRefGoogle Scholar
  10. Cavalcanti DN, de Oliveira MAR, de Paula JC, Barbosa LS, Fogel T, Pinto MA, Paixao ICNP, Teixeira VL (2011) Variability of a diterpene with potential anti-HIV activity isolated from the Brazilian brown alga Dictyota menstrualis. J Appl Phycol 23:873–876CrossRefGoogle Scholar
  11. Chu S, Zhang Q, Liu S, Zhang S, Tang Y, Lu Z, Yu Y (2011) Trade-off between vegetative regeneration and sexual reproduction of Sargassum thunbergii. Hydrobiologia 678:127–135CrossRefGoogle Scholar
  12. da Gama BAP, Plouguerné E, Pereira RC (2014) The antifouling defence mechanisms of marine macroalgae. Adv Bot Res 71:413–440CrossRefGoogle Scholar
  13. De Andrade ML, De Almeida ACM, Domingos TFS, Ortiz-Ramires F, Cavalcanti DN, Teixeira VL, Fuly AL (2014) Antiplatelet and anticoagulant effects of diterpenes isolated from the marine alga, Dictyota menstrualis. Mar Drugs 12:2471–2484CrossRefGoogle Scholar
  14. Demes KW, Graham MH (2011) Abiotic regulation of investment in sexual versus vegetative reproduction in the clonal kelp Laminaria sinclairii (Laminariales, Phaeophyceae). J Phycol 47:463–470CrossRefPubMedGoogle Scholar
  15. Enoki N, Tsuzuki K, Omura S, Ishida R, Matsumoto T (1983) New antimicrobial diterpenes, dictyol F and epidictyol F, from the brown alga Dictyota dichotoma. Chem Lett 12:1627–1630CrossRefGoogle Scholar
  16. Farnham G, Strittmatter M, Coelho S, Cock JM, Brownlee C (2013) Gene silencing in Fucus embryos: developmental consequences of RNAi-mediated cytoskeletal disruption. J Phycol 49:819–829PubMedGoogle Scholar
  17. Førde H, Forbord S, Handå A, Fossberg J, Arff J, Johnsen G, Reitan KI (2015) Development of bryozoan fouling on cultivated kelp (Saccharina latissima) in Norway. J Appl Phycol. doi: 10.1007/s10811-015-0606-5 Google Scholar
  18. Gomes D, Telles C, Costa M, Almeida-Lima J, Costa LS, Keesen TS, Rocha HA (2015) Methanolic extracts from brown seaweeds Dictyota cilliolata and Dictyota menstrualis induce apoptosis in human cervical adenocarcinoma HeLa cells. Molecules 20:6573–6591CrossRefPubMedGoogle Scholar
  19. Guillemin ML, Valenzuela P, Gaitán-Espitia JD, Destombe C (2014) Evidence of reproductive cost in the triphasic life history of the red alga Gracilaria chilensis (Gracilariales, Rhodophyta). J Appl Phycol 26:569–575CrossRefGoogle Scholar
  20. Gupta S, Abu-Ghannam N (2011) Bioactive potential and possible health effects of edible brown seaweeds. Trends Food Sci Technol 22:315–326CrossRefGoogle Scholar
  21. Hable WE, Hart PE (2010) Signaling mechanisms in the establishment of plant and fucoid algal polarity. Mol Reprod Dev 77:751–758CrossRefPubMedGoogle Scholar
  22. Hannachi Y, Rezgui A, Dekhil AB, Boubaker T (2015) Removal of cadmium (II) from aqueous solutions by biosorption onto the brown macroalga (Dictyota dichotoma). Desalin Water Treat 54:1663–1673Google Scholar
  23. Heesch H, Day JG, Yamagishi T, Kawai H, Müller DG, Küpper FC (2012) Cryopreservation of the model alga Ectocarpus (Phaeophyceae). Cryo Letters 33:327–336PubMedGoogle Scholar
  24. Herren LW, Walters LJ, Beach KS (2006) Fragment generation, survival, and attachment of Dictyota spp. at Conch Reef in the Florida Keys, USA. Coral Reefs 25:287–295CrossRefGoogle Scholar
  25. Hoffmann A (1988) Daylength and light responses in growth and fertility of Glossophora kunthii (Phaeophyta, Dictyotales) from Pacific South America. J Phycol 24:203–208CrossRefGoogle Scholar
  26. Hoffmann A (1989) Temperature, photoperiod and light interaction on growth and fertility of Glossophora kunthii (Phaeophyta, Dictyotales) from central Chile. J Phycol 25:129–133CrossRefGoogle Scholar
  27. Hoyt WD (1910) Alternation of generations and sexuality in Dictyota dichotoma. Bot Gaz 49:55–57CrossRefGoogle Scholar
  28. Hoyt WD (1927) The periodic fruiting of Dictyota and its relation to the environment. Am J Bot 14:592–619CrossRefGoogle Scholar
  29. Hwang I-K, Kim H-S, Lee WJ (2005) Polymorphism in the brown alga Dictyota dichotoma (Dictyotales, Phaeophyceae) from Korea. Mar Biol 147:999–1015CrossRefGoogle Scholar
  30. Jongaramruong J, Kongkam N (2007) Novel diterpenes with cytotoxic, anti-malarial and anti-tuberculosis activities from a brown alga Dictyota sp. J Asian Nat Prod Res 9:743–751CrossRefPubMedGoogle Scholar
  31. Kim JY, Alamsjah MA, Hamada A, Fujita Y, Ishibashi F (2006) Algicidal diterpenes from the brown alga Dictyota dichotoma. Biosci Biotechnol Biochem 70:2571–2574CrossRefPubMedGoogle Scholar
  32. Kumke J (1973) Beiträge zur Periodizität der Oogon-Entleerung bei Dictyota dichotoma (Phaeophyta). Z Pflanzenphysiol 70:191–210CrossRefGoogle Scholar
  33. Laib E, Leghouchi E (2012) Cd, Cr, Cu, Pb, and Zn concentrations in Ulva lactuca, Codium fragile, Jania rubens, and Dictyota dichotoma from Rabta Bay, Jijel (Algeria). Environ Monit Assess 184:1711–1718CrossRefPubMedGoogle Scholar
  34. Lüning K (1980) Critical levels of light and temperature regulating the gametogenesis of three Laminaria species (Phaeophyceae). J Phycol 16:1–15CrossRefGoogle Scholar
  35. Miceli LA, de Souza AMT, Rodrigues CR, Paixao ICNP, Teixeira VL, Castro HC (2012) HIV-1 reverse transcriptase: a potential target for marine products. Brazilian J Pharmacogn 22:881–888Google Scholar
  36. Müller D (1962) Über jahres- und lunarperiodische Ersheinungen bei einigen Braunalgen. Bot Mar 4:140–155CrossRefGoogle Scholar
  37. Müller S, Clauss H (1976) Aspects of photomorphogenesis in the brown alga Dictyota dichotoma. Z Pflanzenphysiol 78:461–465CrossRefGoogle Scholar
  38. Obeso J (2002) The costs of reproduction in plants. New Phytol 155:321–348CrossRefGoogle Scholar
  39. Othmani A, Bouzidi N, Viano Y, Alliche Z, Seridi H, Blache Y, El Hattab M, Briand J, Culioli G (2014) Anti-microfouling properties of compounds isolated from several Mediterranean Dictyota spp. J Appl Phycol 26:1573–1584Google Scholar
  40. Pearson GA, Serrão EA (2006) Revisiting synchronous gamete release by fucoid algae in the intertidal zone: fertilization success and beyond? Integr Comp Biol 46:587–597CrossRefPubMedGoogle Scholar
  41. Pereira HS, Leão-Ferreira LR, Moussatché N, Teixeira VL, Cavalcanti DN, Costa LJ, Diaz R, Frugulhetti IC (2004) Antiviral activity of diterpenes isolated from the Brazilian marine alga Dictyota menstrualis against human immunodeficiency virus type 1 (HIV-1). Antiviral Res 64:69–76PubMedGoogle Scholar
  42. Pereira H, Barreira L, Figueiredo F, Custódio L, Vizetto-Duarte C, Polo C, Rešek E, Engelen A, Varela J (2012) Polyunsaturated fatty acids of marine macroalgae: potential for nutritional and pharmaceutical applications. Mar Drugs 10:1920–1935CrossRefPubMedPubMedCentralGoogle Scholar
  43. Peters AF, Marie D, Scornet D, KLoareg B, Cock M (2004) Proposal of Ectocarpus siliculosus (Ectocarpales, Phaeophyceae) as a model organism for brown algal genetics and genomics. J Phycol 40:1079–1088CrossRefGoogle Scholar
  44. Phillips JA, Clayton MN, Maier I, Boland W, Müller DG (1990) Sexual reproduction in Dictyota diemensis (Dictyotales, Phaeophyta). Phycologia 29:367–379CrossRefGoogle Scholar
  45. Rabanal M, Ponce NMA, Navarro DA, Gómez RM, Stortz CA (2014) The system of fucoidans from the brown seaweed Dictyota dichotoma: chemical analysis and antiviral activity. Carbohydr Polym 101:804–811CrossRefPubMedGoogle Scholar
  46. Rasher DB, Hay ME (2010) Chemically rich seaweeds poison corals when not controlled by herbivores. Proc Natl Acad Sci 107:9683–9688CrossRefPubMedPubMedCentralGoogle Scholar
  47. Rasher DB, Stout EP, Engel S, Kubanek J, Hay ME (2011) Macroalgal terpenes function as allelopathic agents against reef corals. Proc Natl Acad Sci 108:17726–17731CrossRefPubMedPubMedCentralGoogle Scholar
  48. Richardson JP (1979) Overwintering of Dictyota dichotoma (Phaeophyceae) near its northern distribution limit on the east coast of North America. J Phycol 15:22–26CrossRefGoogle Scholar
  49. Santelices B (1990) Patterns of reproduction, dispersal and recruitment in seaweeds. Oceanogr Mar Biol 28:177–276Google Scholar
  50. Santelices B (2002) Recent advances in fertilization ecology of macroalgae. J Phycol 38:4–10CrossRefGoogle Scholar
  51. Schreiber E (1935) Über Kultur und Geschlechtsbestimmung von Dictyota dichotoma. Planta 24:266–275CrossRefGoogle Scholar
  52. Soares DC, Calegari-Silva TC, Lopes UG, Teixeira VL, Paixao ICNP, Cime-Santos C, Bou-Habib DC, Saraiva EM (2012) Dolabelladienetriol, a compound from Dictyota pfaffii algae, inhibits the infection by Leishmania amazonensis. PLoS Negl Trop Dis 6:e1787CrossRefPubMedPubMedCentralGoogle Scholar
  53. Tringali C, Piattelli M, Nicolosi G, Hostettmann K (1986) Molluscicidal and antifungal activity of diterpenoids from brown algae of the family Dictyotaceae. Planta Med 5:404–406CrossRefPubMedGoogle Scholar
  54. Tronholm A, Steen F, Tyberghein L, Leliaert F, Verbruggen H, Siguan MAR, De Clerk O (2010) Species delimitation, taxonomy, and biogeography of Dictyota in Europe (Dictyotales, Phaeophyceae). J Phycol 46:1301–1321CrossRefGoogle Scholar
  55. Viano Y, Bonhomme D, Camps M, Briand JF, Ortalo-Magné A, Blache Y, Piovetti L, Culioli G (2009) Diterpenoids from the Mediterranean brown alga Dictyota sp. evaluated as antifouling substances against a marine bacterial biofilm. J Nat Prod 72:1299–1304CrossRefPubMedGoogle Scholar
  56. Vielhaben V (1963) Zur Deutung des semilunaren Fortpflanzungszyklus von Dictyota dichotoma. Z Bot 51:156–173Google Scholar
  57. Wang B, Zhang E, Gu Y, Ning S, Wang Q, Zhou J (2011) Cryopreservation of brown algae gametophytes of Undaria pinnatifida by encapsulation–vitrification. Aquaculture 317:89–93CrossRefGoogle Scholar
  58. West JA, McBride DL (1999) Long-term and diurnal carpospore discharge patterns in the Ceramiaceae, Rhodomelaceae and Delesseriaceae (Rhodophyta). Hydrobiologia 398:101–114CrossRefGoogle Scholar
  59. Wiesemeier T, Hay M, Pohnert G (2007) The potential role of wound-activated volatile release in the chemical defence of the brown alga Dictyota dichotoma: blend recognition by marine herbivores. Aquat Sci 69:403–412CrossRefGoogle Scholar
  60. Williams LJ (1905) Studies in the Dictyotaceae. III. The periodicity of the sexual cells in Dictyota dichotoma. Ann Bot 19:531–560Google Scholar
  61. Yang Z (2008) Cell polarity signaling in Arabidopsis. Annu Rev Cell Dev Biol 24:551–575CrossRefPubMedPubMedCentralGoogle Scholar
  62. Zhou X, Liu J, Yang B, Lin X, Yang XW, Liu Y (2013) Marine natural products with anti-HIV activities in the last decade. Curr Med Chem 20:953–973PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Kenny Bogaert
    • 1
  • Tom Beeckman
    • 2
    • 3
  • Olivier De Clerck
    • 1
  1. 1.Department of BiologyGhent UniversityGhentBelgium
  2. 2.Department of Plant Systems BiologyGhent UniversityGhentBelgium
  3. 3.Department of Plant Biotechnology and BioinformaticsGhent UniversityGhentBelgium

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