Photosynthesis-Dependent Extracellular Ca2+ Influx Triggers an Asexual Reproductive Cycle in the Marine Red Macroalga Porphyra yezoensis

Megumu Takahashi, Naotsune Saga, Koji Mikami
DOI: 10.4236/ajps.2010.11001                

Abstract

Asexual propagation to increase the number of gametophytic clones via the growth of asexual haploid spores is a unique survival strategy found in marine multicellular algae. However, the mechanisms regulating the asexual life cycle are largely unknown. Here, factors involved in the regulation of production and discharge of asexual spores, so-called monospores, are identified in the marine red macroalga Porphyra yezoensis. First, enhanced discharge of monospores was found by incubation of gametophytes in ASPMT1, a modified version of the previously established synthetic medium ASP12. Comparison of the compositions of ASPMT1 and our standard medium, ESL, indicated that the Ca2+ concentration in ASPMT1 was three times lower than that in ESL medium. Thus, we modified ASPMT1 by increasing its Ca2+ concentration, resulting in reduction of monospore discharge. These findings demonstrate the role of reduced Ca2+ concentrations in enhancing monospore production and release. Moreover, it was also observed that initiation of asexual life cycle required illumination, was repressed by DCMU, and was induced by a Ca2+ ionophore in the dark. Taken together, these results indicate that photosynthesis-dependent Ca2+ influx triggers the asexual life cycle by promoting the production and discharge of monospores in P. yezoensis.

Keywords

Asexual Life Cycle, Bangiophyceae, Ca2+ Influx, Monospore, Photosynthesis, Porphyra yezoensis, Rhodophyta, Synthetic Medium

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	T. H. Adams, J. K. Wieser and J. H. Yu, “Asexual Sporulation in Aspergillus nidulans,” Microbiology and Molecular Biology Reviews, Vol. 62, No. 1, March 1998, pp. 35-54.
[2]	R. M. McCourt, C. F. Delwiche and K. G. Karol, “Ch- Arophyte Algae and Land Plant Origins,” Trends in Ecology and Evolution, Vol. 19, No. 12, December 2004, pp. 661-666.
[3]	K. J. Niklas and U. Kutschera, “The Evolution of the Land Plant Life Cycle,” New Phytologist, Vol. 185, No. 1, January 2010, pp. 27-41.
[4]	S. M. Coelho, A. F. Peters, B. Charrier, D. Roze, C. Destombe, M. Valero and J. M. Cock, “Complex Life Cycles of Multicellular Eukaryotes: New Approaches Based on the Use of Model Organisms,” Gene, Vol. 406, No. 1-2, December 2007, pp. 152-170.
[5]	K. J. Niklas and U. Kutschera, “The Evolutionary Development of Plant Body Plans,” Functional Plant Biology, Vol. 36, No. 8, August 2009, pp. 682-695.
[6]	F. Magne, “Classification and Phylogeny in the Lower Rhodophyta: A New Proposal,” Journal of Phycology, Vol. 27, No. s3, June 1991, p. 46.
[7]	L. Goosey and R. Sharrock, “The Arabidopsis Compact Inflorescence Genes: Phase-Specific Growth Regulation and the Determination of Inflorescence Architecture,” Plant Journal, Vol. 26, No. 5, June 2001, pp. 549-559.
[8]	G. C. K. Chiang, D. Barua, E. M. Kramer, R. M. Amasino and K. Donohue, “Major Flowering Time Gene, FL- OWERING LOCUS C, Regulates Seed Germination in Arabidopsis Thaliana,” Proceeding of the National Acad- emy of Sciences of the USA, Vol. 106, No. 28, July 2009, pp. 11661-11666.
[9]	K. E. Hubbard, F. C. Robertson, N. Dalchau and A. A. R. Webb, “Systems Analyses of Circadian Networks,” Molecular Biosystems, Vol. 5, No. 12, December 2009, pp. 1502-1511.
[10]	N. Saga and Y. Kitade, “Porphyra: A Model Plant in Marine Sciences,” Fisheries Science, vol. 68, Supplement II, November 2002, pp. 1075-1078.
[11]	A. Miura, “Genetic Analysis of the Variant Color Types of Light Red, Light Green and Light Yellow Phenotypes of Porphyra yezoensis (Rhodophyta, Bangiaceae),” In: H. Hara, ed., Origin and Evolution of Diversity in Plants and Plant Communities, Academic Scientific Book Inc, Tokyo, 1985, pp. 270-284.
[12]	M. Kurogi, “Species of Cultivated Porphyra and Their Life Histories,” Bulletin of Tohoku Regional Fisheries Resear- ch Laboratory, Vol. 18, March 1961, pp. 91-115.
[13]	M. D. Guiry, “The Life-History of Liagora harveyana （Nemaliales, Rhodophyta) from SOUTH-EASTERN AUSTRALIA,” European Journal of Phycology, Vol. 25, No. 4, December 1990, pp. 353-362.
[14]	J. D. Pickett-Heaps, J. A. West, S. M. Wilson and D. L. McBride, “Time-Lapse Videomicroscopy of Cell (Spore) Movement in Red Algae,” European Journal of Phycology, Vol. 36, No. 1, February 2001, pp. 9-22.
[15]	J. C. Ackland, J. A. West and J. Pickett-Heaps, “Actin and Myosin Regulate Pseudopodia of Porphyra pulchella (Rhodophyta) Archeospores,” Journal of Phycology, Vol. 43, No. 1, February 2007, pp. 129-138.
[16]	L. Li, N. Saga and K. Mikami, “Phosphatidylinositol 3- Kinase Activity and Asymmetrical Accumulation of F- Actin are Necessary for Establishment of Cell Polarity in the Early Development of Monospores from the Marine Red Alga Porphyra yezoensis,” Journal of Experimental Botany, Vol. 59, No. 13, October 2008, pp. 3575- 3586.
[17]	K. Mikami, “Migrating Plant Cell: F-Actin Asymmetry Directed by Phosphoinositide Signaling,” In: S. Lansing and T. Rousseau, eds., Cytoskeleton: Cell Movement, Cytokinesis and Organelles Organization, Nova Science Publishers, New York, 2010, pp. 205-218.
[18]	L. Li, N. Saga and K. Mikami, “Ca2+ Influx and Phosphoinositide Signalling Are Essential for the Establishment and Maintenance of Cell Polarity in Monospores from the Red Alga Porphyra yezoensis,” Journal of Experimental Botany, Vol. 60, No. 12, August 2009, pp. 3477-3489.
[19]	K. Mikami, L. Li, M. Takahashi and N. Saga, “Photosynthesis-Dependent Ca2+ Influx and Functional Diversity between Phospholipases in Formation of Cell Polarity in Migrating Cells of Red Algae,” Plant Signaling and Behavior, Vol. 4, No. 9, September 2009, pp. 911-913.
[20]	Y. Kitade, G. Taguchi, J. A. Shin and N. Saga, “Porphyra Monospore System (Bangiales, Rhodophyta): A Model for the Developmental Biology of Marine Plans,” Phycological Research, Vol. 46, No. 1, March 1998, pp. 17-20.
[21]	S. Y. Li, “The Ecological Characteristics of Monospores of Porphyra yezoensis Ueda and their Use in Cultivation,” Hydrobiologia, Vol. 116/117, No. 1, September 1984, pp. 255-258.
[22]	H. Mizuta, H. Yasui and N. Saga, “A Simple Method to Mass Monospores in the Thallus of Porphyra yezoensis Ueda,” Journal of Applied Phycology, Vol. 15, No. 4, July 2003, pp. 345-349.
[23]	X. H. Yan, Y. Fujita and Y. Aruga, “High Monospore- Producing Mutants Obtained by Treatment with MNNG in Porphyra yezoensis Ueda (Bangiales, Rhodophyta),” Hydrobiologia, Vol. 512, No. 1-3, January 2004, pp. 133- 140.
[24]	G. R. Seely, W. E. Vidaver and M. J. Duncan, “Preparative and Analytical Extraction of Pigments from Brown Algae with Dimethyl Sulfoxide,” Marine Biology, Vol. 12, No. 2, January 1972, pp. 184-188.
[25]	S. Beer and A. Eshel, “Determining Phycoerythrin and Phycocyanin Concentrations in Aqueous Crude Extracts of Red Algae,” Australian Journal of Marine and Freshwater Research, Vol. 36, No. 6, September 1985, pp. 785-792.
[26]	Y. Kitade, S. Fukuda, M. Nakajima, T. Watanabe and N. Saga, “Isolation of a cDNA Encoding a Homolog of Actin from Porphyra yezoensis (Rhodophyta),” Journal of Applied Phycology, Vol. 14, No. 2, April 2002, pp. 135-141.
[27]	L. Provasoli, J. J. A. McLaughlin and M. R. Droop, “The Development of Artificial Media for Marine Algae,” Archiv für Mikrobiologie, Vol. 25, No. 4, December 1957, pp. 392-428.
[28]	L. Provasoli, “Growing Marine Seaweeds,” In: A. D. De Virville and J. Feldman, eds., Proceedings of the Fourth International Seaweed Symposium, Pergamon Press, Oxford, 1963, pp.9-17.
[29]	N. Saga, T. Motomura and Y. Sakai, “Induction of Callus from the Marine Brown Alga Dictyosiphon foeniculaceus,” Plant and Cell Physiology, Vol. 23, No. 4, June 1982, pp. 727-730.
[30]	N. S. Yokoya, “Apical Callus Formation and Plant Regeneration Controlled by Plant Growth Regulators on Axenic Culture of Red Alga Gracilariopsis tenuifrons (Gracilariales, Rhodophyta),” Phycological Research, Vol. 48, No. 3, September 2000, pp. 133-142.
[31]	S. Shen, L. He, P. Xu and J. Zhu, “Effect of Nitrogen and Phosphorus on the Development and Differentiation of Vegetative Cells of Porphyra yezoensis on Solid Agar Medium,” Botanica Marina, Vol. 49, No. 5/6, December 2006, pp. 372-378.
[32]	J. T. Hafting, “Effect of Tissue Nitrogen and Phosphorus Quota on Growth of Porphyra yezoensis Blades in Suspension Cultures,” Hydrobiologia, Vol. 398/399, No. 0, April 1999, pp. 305-314.
[33]	M. Kakinuma, D. Coury, C. Nakamoto, K. Sakaguchi and H. Amano, “Molecular Analysis of Physiological Responses to Changes in Nitrogen in a Marine Macroalga, Porphyra yezoensis (Rhodophyta),” Cell Biology and Toxicology, Vol. 24, No. 6, December 2008, pp. 629-639.
[34]	K. Charnofsky, L. R. Towill and M. R. Sommerfeld, “Li- Ght Requirements for Monospore Germination in Bangia atropurpurea (Rhodophyta),” Journal of Phycology, Vol. 18, No. 3, September 1982, pp. 417-422.
[35]	N. J. Butterfield, “Bangiomorpha pubescens n. gen., n. sp.: Implications for the Evolution of Sex, Multicellularity, and the Mesoproterozoic/Neoproterozoic Radiation of Eukaryotes,” Paleobiology, Vol. 26, No. 3, September 2000, pp. 386-404.
[36]	G. Tripodi and F. de Masi, “Unusual Structure in the Spermatial Vesicles of the Red Alga Erythrocystis montagnei,” Plant Systematics and Evolution, Vol. 143, No. 3, September 1983, pp. 197-206.
[37]	M. N. Clayton, “Propagules of Marine Macroalgae: Stru- Cture and Development,” European Journal of Phycology, Vol. 27, No. 3, September 1992, pp. 219-232.
[38]	C. S. Thornber, “Functional Properties of the Isomorphic Biphasic Algal Life Cycle,” Integrative and Comparative Biology, Vol. 46, No. 5, October 2006, pp. 605-614.