Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Blue- and green-light signals for gamete release in the brown alga, Silvetia compressa

Abstract

The intertidal brown alga Silvetia compressa releases gametes from receptacles (the reproductive tissue) rapidly upon a dark transfer (following a photosynthesis-dependent period in the light, termed potentiation). In this study, the wavelength-dependence of this process was investigated. During the potentiation period in white light (WL), gametes are not released. However, gametes were released during potentiation in blue light (BL), or in low red light/blue light (RL/BL) ratios, but not in RL alone, high RL/BL ratios, or in broadband blue-green light (B-GL) (presence of BL, but absence of RL). RL was as effective as WL for potentiation, i.e., both lead to gamete release following transfer to darkness. Rates of linear photosynthetic electron transport were similar in RL and BL. Gamete release in BL was inhibited by equal amounts of additional narrow-waveband light between the green and red regions of the spectrum, with light-induced gamete release restricted between <491 nm and 509 nm. Very little light-induced gamete release occurred between 530 nm and 650 nm. It is proposed that a BL-responsive photoreceptor is responsible for light-induced gamete release. Transfer of WL-potentiated receptacles to GL near 530 nm resulted in significant de-potentiation and reduced gamete release during a subsequent dark transfer. This effect was not seen at 509 nm or 560 nm and revealed the presence of a second photoreceptor system repressing or counteracting potentiation in the light. We propose that the restriction of gamete release to periods when irradiance is blue-shifted may constitute a depth-sensing mechanism for this intertidal alga, allowing controlled release of gametes at high tide and/or less turbid periods, thus minimizing gamete dilution, and promoting fertilization success.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3a–c
Fig. 4a, b
Fig. 5
Fig. 6
Fig. 7

References

  1. Assmann SM (1993) Signal transduction in guard cells. Annu Rev Cell Biol 9:345–375

  2. Babcock RC, Bull GD, Harrison PL, Heyward AJ, Oliver JK, Wallace CC, Willis BL (1986) Synchronous spawning of 105 scleractinian coral species on the Great Barrier Reef. Mar Biol 90:379–394

  3. Bamberg E, Tittor J, Oesterhelt D (1993) Light-driven proton or chloride pumping by halorhodopsin. Proc Natl Acad Sci USA 90:639–643

  4. Berndt M-L, Callow JA, Brawley SH (2002) Gamete concentrations and timing and success of fertilization in a rocky shore seaweed. Mar Ecol Prog Ser 226:273–285

  5. Brawley SH (1992) Fertilization in natural populations of the dioecious brown alga Fucus ceranoides and the importance of the polyspermy block. Mar Biol 113:145–157

  6. Brawley SH, Johnson LE, Pearson GA, Speransky V, Li R, Serrão E (1999) Gamete release at low tide in fucoid algae: maladaptive or advantageous? Am Zool 39:218–229

  7. Cho MH, Spalding EP (1996) An anion channel in Arabidopsis hypocotyls activated by blue light. Proc Natl Acad Sci USA 93:8134–8138

  8. Clifton KE (1997) Mass spawning by green algae on coral reefs. Science 275:1116–1118

  9. Denny MW, Shibata MF (1989) Consequences of surf-zone turbulence for settlement and external fertilization. Am Nat 134:859–889

  10. Dring MJ (1989) Stimulation of light-saturated photosynthesis in Laminaria (Phaeophyta) by blue light. J Phycol 25:254–257

  11. Dring MJ, Lüning K (1975) A photoperiodic response mediated by blue-light in the brown alga Scytosiphon lomentaria. Planta 125:25–32

  12. Eckert M, Kaldenhoff R (2000) Light-induced stomatal movement of selected Arabidopsis thaliana mutants. J Exp Bot 51:1435–1442

  13. Forster RM, Dring MJ (1992) Interactions of blue light and inorganic carbon supply in the control of light-saturated photosynthesis in brown algae. Plant Cell Environ 15:241–247

  14. Frechilla S, Zhu J, Talbott LD, Zeiger E (1999) Stomata from npq1, a zeaxanthin-less Arabidopsis mutant, lack a specific response to blue light. Plant Cell Physiol 40:949–954

  15. Frechilla S, Talbott LD, Bogomolni RA, Zeiger E (2000) Reversal of blue light-stimulated stomatal opening by green light. Plant Cell Physiol 41:171–176

  16. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

  17. Harrison PL, Babcock RC, Bull GD, Oliver JK, Wallace CC, Willis BL (1984) Mass spawning in tropical reef corals. Science 223:1186–1189

  18. Haupt W (1983) Movements of chloroplasts under the control of light. Prog Phycol Res 2:227–281

  19. Hedrich R, Marten I (1993) Malate-induced feedback regulation of plasma membrane anion channels could provide a CO2 sensor to guard cells. EMBO J 12:897–901

  20. Hedrich R, Marten I, Lohse G, Dietrich P, Winter H, Lohaus G, Heldt H-W (1994) Malate-sensitive anion channels enable guard cells to sense changes in the ambient CO2 concentration. Plant J 6:741–748

  21. Hedrich R, Neimanis S, Savchenko G, Felle HH, Kaiser WM, Heber U (2001) Changes in apoplastic pH and membrane potential in leaves in relation to stomatal responses to CO2, malate, abscisic acid or interruption of water supply. Planta 213:594–601

  22. Jaffe LF (1954) Stimulation of the discharge of gametangia from a brown alga by a change from light to darkness. Nature 174:743

  23. Johnson LE, Brawley SH (1998) Dispersal and recruitment in a canopy-forming intertidal alga, Pelvetia compressa (Phaeophyceae). Oecologia 117:517–526

  24. Kinoshita T, Doi M, Suetsugu N, Kawaga T, Shimazaki KI (2001) Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414:656–660

  25. Kropf DL (1992) Establishment and expression of cellular polarity in fucoid zygotes. Microbiol Rev 56:316–339

  26. Levitan DR, Petersen C (1995) Sperm limitation in the sea. Trends Ecol Evol 10:228–231

  27. Morgan SG (1995) The timing of larval release. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC, Boca Raton, pp 157–191

  28. Nuccitelli R, Jaffe LF (1975) The pulse current pattern generated by developing fucoid eggs. J Cell Biol 64:636–643

  29. Nuccitelli R, Jaffe LF (1976) Current pulses involving chloride and potassium efflux relieve excess pressure in Pelvetia embryos. Planta 131:315–320

  30. Nultsch W (1984) Circadian rhythms in chromatophore movements of Dictyota dichotoma. Mar Biol 81:217–222

  31. Pearson GA, Brawley SH (1996) Reproductive ecology of Fucus distichus (Phaeophyceae): an intertidal alga with successful external fertilization. Mar Ecol Prog Ser 143:211–223

  32. Pearson GA, Brawley SH (1998) A model for signal transduction during gamete release in the fucoid alga Pelvetia compressa. Plant Physiol 118:305–313

  33. Pearson GA, Serrão EA, Brawley SH (1998) Control of gamete release in fucoid algae: sensing hydrodynamic conditions via carbon acquisition. Ecology 79:1725–1739

  34. Robinson KR, Miller BJ (1997) The coupling of cyclic GMP and photopolarization of Pelvetia zygotes. Dev Biol 187:125–130

  35. Robinson KR, Lorenzi R, Ceccarelli N, Gualtieri P (1998) Retinal identification in Pelvetia fastigiata. Biochem Biophys Res Commun 243:776–778

  36. Robinson KR, Wozniak M, Pu R, Messerli M (1999) Symmetry breaking in the zygotes of the fucoid algae: controversies and recent progress. Curr Topic Dev Biol 44:101–125

  37. Schmid R, Dring MJ (1992) Circadian rhythm and fast responses to blue light of photosynthesis in Ectocarpus (Phaeophyta, Ectocarpales). I. Characterization of the rhythm and the blue-light response. Planta 187:53–59

  38. Schmid R, Dring MJ (1993) Rapid, blue-light-induced acidifications at the surface of Ectocarpus and other marine macroalgae. Plant Physiol 101:907–913

  39. Schmid R, Dring MJ (1996) Blue light and carbon acquisition in brown algae: an overview and recent developments. Sci Mar 60 [Suppl. 1]:115–124

  40. Schmid R, Dring MJ, Forster RM (1994) Kinetics of blue-light stimulation and circadian rhythmicity of light-saturated photosynthesis in brown algae: a species comparison. J Phycol 30:612–621

  41. Schwartz A, Ilan N, Schwarz M, Scheaffer J, Assmann SM, Schroeder JI (1995) Anion-channel blockers inhibit S-type anion channels and abscisic acid responses in guard cells. Plant Physiol 109:651–658

  42. Serrão EA, Pearson GA, Kautsky L, Brawley SH (1996) Successful external fertilization in turbulent environments. Proc Natl Acad Sci USA 93:5286–5290

  43. Serrão EA, Alice LA, Brawley SH (1999) Evolution of the Fucaceae (Phaeophyceae) inferred from nrDNA-ITS. J Phycol 35:382–394

  44. Speransky VV, Brawley SH, McCully ME (2001) Ion fluxes and modification of the extracellular matrix during gamete release in fucoid algae. J Phycol 37:555–573

  45. Togashi T, Cox PA (2001) Tidal-linked synchrony of gamete release in the marine green alga, Monostroma angicava Kjellman. J Exp Mar Biol Ecol 264:117–131

  46. Yoshioka E (1988) Spawning periodicities coinciding with semidiurnal tidal rhythms in the chiton Acanthopleura japonica. Mar Biol 98:381–385

  47. Yund PO (2000) How severe is sperm limitation in natural populations of marine free-spawners? Trends Ecol Evol 15:10–13

  48. Zeiger E, Zhu J (1998) Role of zeaxanthin in blue light photoreception and the modulation of light-CO2 interactions in guard cells. J Exp Bot 49:433–442

Download references

Acknowledgements

G.P., E.S., and M.D. express our gratitude to Professor Paul Galland for hosting our visits to his laboratory in Marburg, his generosity in allowing us access to equipment, as well as helpful discussions. Many and ever-reliable algal collections were made by Diana Steller, University of California at Santa Cruz, Calif., USA. Silvia Busch (Philipps-Universitaet, Marburg, Germany) provided fine selections of bread for breakfast. Funding by the COST-49 program (EU), the Portuguese Science Foundation (FCT) project GAMETE (POCTI/BSE/39431/2001), and an FCT and European Social Fund (FSE) fellowship to G.P.

Author information

Correspondence to Gareth A. Pearson.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Pearson, G.A., Serrão, E.A., Dring, M. et al. Blue- and green-light signals for gamete release in the brown alga, Silvetia compressa . Oecologia 138, 193–201 (2004). https://doi.org/10.1007/s00442-003-1424-z

Download citation

Keywords

  • External fertilization
  • Intertidal seaweed
  • Photoreceptor
  • Reproductive biology
  • Spawning