Skip to main content
SpringerLink
Log in

Morphological and photosynthetic variations in the process of spermatia formation from vegetative cells in Porphyra yezoensis Ueda (Bangiales, Rhodophyta) and their responses to desiccation

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Porphyra yezoensis has a macroscopic foliage gametophyte phase with only a single cell layer, and is ideally suited for the study of the sexual differentiation process, from the vegetative cell to the spermatia. Firstly, we compared variations in the responses of the vegetative and male sectors to desiccation. Later, cell tracking experiments were carried out during the formation of spermatia from vegetative cells. The two sectors showed similar tolerance to desiccation, and the formation of spermatia from vegetative cells was independent of the degree of desiccation. Both light and scanning electron microscopy (SEM) observations of the differentiation process showed that the formation of spermatia could be divided into six phases: the one-cell, two-cell, four-cell, eight-cell, pre-release and spermatia phases. Photomicrographs of Fluorescent Brightener staining showed that the released spermatia had no cell walls. Photosynthetic data showed that there was a significant rise in Y(II) in the four-cell phase, indicating an increase in photosynthetic efficiency of PSII during this phase. We propose that this photosynthetic rise may be substantial and provide the increased energy needed for the formation and release of spermatia in P. yezoensis.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

APC:

Allophycocyanin

CA:

Carbonic anhydrase

Chl a :

Chlorophyll a

DCMU:

Diuron, 3-(3, 4-dichlorophenyl)-1, 1-dimethylurea

ETR(I):

Relative rates of photosynthetic electron transport of PSI

ETR(II):

Relative rates of photosynthetic electron transport of PSII

F :

The current fluorescence yield

F0:

The intrinsic fluorescence

Fm:

Maximum fluorescence yield

Fm′:

The maximum fluorescence yield in active radiation

Fv:

Variable fluorescence yield

Fv/Fm:

Optimum quantum yield of PSII

PAR:

Photosynthetic active radiation

PC:

Phycocyanin

PE:

Phycoerythrin

PSI (II):

Photosystem I (II)

RWC:

The relative water content

SEM:

Scanning electron microscopy

Y :

Effective quantum yield

Y(I):

Effective quantum yield of PSI

Y(II):

Effective quantum yield of PSII

References

  • Brody M, Emerson R (1959) The quantum yield of photosynthesis in Porphyridium cruentum, and the role of chlorophyll a in the photosynthesis of red algae. J Gen Physiol 43:251–264

    Article  PubMed  CAS  Google Scholar 

  • Bucher M, Brander KA, Sbicego S, Mandel T, Kuhlemeier C (1995) Aerobic fermentation in tobacco pollen. Plant Mol Biol 28:739–750

    Article  PubMed  CAS  Google Scholar 

  • Burritt DJ, Larkindale J, Hurd CL (2002) Antioxidant metabolism in the intertidal red seaweed Stictosiphonia arbuscula following desiccation. Planta 215:829–838

    Article  PubMed  CAS  Google Scholar 

  • Candia A, Lindstrom S, Reyes E (1999) Porphyra sp. (Bangiales, Rhodophyta): reproduction and life form. Hydrobiologia 398(399):115–119

    Article  Google Scholar 

  • Chen YH, Hsu BD (1995) Effects of dehydration on the electron transport of Chlorella. An in vivo fluorescence study. Photosynth Res 46:295–299

    Article  CAS  Google Scholar 

  • Clément C, Chavant L, Burrus M, Audran JC (1994) Anther starch variations in Lilium during pollen development. Sex Plant Reprod 7:347–356

    Article  Google Scholar 

  • Coleman JR (2000) Carbonic anhydrase and its role in photosynthesis. In: Leegood RC, Sharkey TD, Von Caemmerer S (eds) Advances in photosynthesis, vol 9: photosynthesis: physiology and metabolism. Kluwer Academic Publisher, Dordrecht, pp 353–367

    Google Scholar 

  • Davison IR, Pearson GA (1996) Stress tolerance in intertidal seaweeds. J Phycol 32:197–211

    Article  Google Scholar 

  • Delivopoulos SG (2000) Ultrastructure of spermatiogenesis in the red alga Osmundea spectabilis var. spectabilis (Rhodomelaceae, Ceramiales, Rhodophyta). Phycologia 39:517–526

    Article  Google Scholar 

  • Delivopoulos SG (2002) Ultrastructure of tetrasporogenesis in the red alga Osmundea spectabilis var. spectabilis (Rhodomelaceae: Ceramiales: Rhodophyta). Mar Biol 140:921–934

    Article  Google Scholar 

  • Delivopoulos SG (2004) Ultrastructure of tetrasporogenesis in the red alga Rhodymenia californica var. attenuata (Rhodymeniaceae, Rhodymeniales, Rhodophyta). Bot Mar 47:222–230

    Article  Google Scholar 

  • Fan XL, Wang GC, Li DM, Xu P, Shen SD (2008) Study on early-stage development of conchospore in Porphyra yezoensis Ueda. Aquaculture 278:143–149

    Article  Google Scholar 

  • Fork DC, Bose S, Herbert SK (1986) Radiationless transitions as a protection mechanism against photoinhibition in higher plants and a red alga. Photosynth Res 10:327–333

    Article  CAS  Google Scholar 

  • Gao S, Chen XY, Yi QQ, Wang GC, Pan GH, Lin AP, Peng G (2010) A strategy for the proliferation of Ulva prolifera, main causative species of green tides, with formation of sporangia by fragmentation. PLoS ONE 5:e8571

    Article  PubMed  Google Scholar 

  • Gasulla F, Gómez de Nova P, Esteban-Carrasco A, Zapata JM, Barreno E, Guéra A (2009) Dehydration rate and time of desiccation affect recovery of the lichenic algae Trebouxia erici: alternative and classical protective mechanisms. Planta 231:195–208

    Article  PubMed  CAS  Google Scholar 

  • Gómez-Pinchetti JL, Ramazanov Z, García-Reina G (1992) Effect of inhibitors of carbonic anhydrase activity on photosynthesis in the red alga Soliera filiformis (Gigartinales: Rhodophyta). Mar Biol 114:335–339

    Article  Google Scholar 

  • Han T, Han Y, Kain JM, Häder D (2003) Thallus differentiation of photosynthesis, growth, reproduction, and UV-B sensitivity in the green alga Ulva pertusa (Chlorophyceae). J Phycol 39:712–721

    Article  Google Scholar 

  • Hawkes MW (1978) Sexual reproduction in Porphyra gardneri (Smith et Hollenberg) Hawkes (Bangiales, Rhodophyta). Phycologia 17:329–353

    Article  Google Scholar 

  • Heber U (2008) Photoprotection of green plants: a mechanism of ultra-fast thermalenergy dissipation in desiccated lichens. Planta 228:641–650

    Article  PubMed  CAS  Google Scholar 

  • Heber U, Bilger W, Bligny R, Lange OL (2000) Phototolerance of lichens, mosses and higher plants in an alpine environment: analysis of photoreactions. Planta 211:770–780

    Article  PubMed  CAS  Google Scholar 

  • Heber U, Bilger W, Shuvalov VA (2006) Thermal energy dissipation in reaction centres and in the antenna of photosystem II protects desiccated poikilohydric mosses against photo-oxidation. J Exp Bot 57:2993–3006

    Article  PubMed  CAS  Google Scholar 

  • Heber U, Bilger W, Türk R, Lange OL (2010) Photoprotection of reaction centres in photosynthetic organisms: mechanisms of thermal energy dissipation in desiccated thalli of the lichen Lobaria pulmonaria. New Phytol 185:459–470

    Article  PubMed  CAS  Google Scholar 

  • Hoekstra FA (1979) Mitochondrial development and activity of binucleate and trinucleate pollen during germination in vitro. Planta 145:25–36

    Article  CAS  Google Scholar 

  • Israel A, Beer S (1992) Photosynthetic carbon acquisition in the red alga Gracilaria conferta. II. Rubisco carboxylase kinetics, carbonic anhydrase and HCO3–uptake. Mar Biol 112:697–700

    Article  CAS  Google Scholar 

  • Jacob A, Wiencke C, Lehmann H, Kirst GO (1992) Physiology and ultrastructure of desiccation in the green alga Prasiola crispa from Antarctica. Bot Mar 35:297–304

    Article  Google Scholar 

  • Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c 1 and c 2 in higher plants, algae, and natural phytoplankton. Biochem Physiol Pflanzen 167:191–194

    CAS  Google Scholar 

  • Kim GH, Fritz L (1993) Ultrastructure and cytochemistry of early spermatangial development in Antithamnion nipponicum (Ceramiaceae, Rhodophyta). J Phycol 29:797–805

    Article  Google Scholar 

  • Kitade Y, Taguchi G, Shin JA, Saga N (1998) Porphyra monospore system (Bangiales, Rhodophyta): a model for the developmental biology of marine plants. Phycol Res 46:17–20

    Article  Google Scholar 

  • Krause GH, Weis E (1984) Chlorophyll fluorescence as a tool in plant physiology. II. Interpretation of fluorescence signals. Photosynth Res 5:139–157

    Article  CAS  Google Scholar 

  • Kugrens P (1974) Light and electron microscopic studies of the development and liberation of Lanczewskia gardneri Setch. Spermatia (Rhodophyta). Phycologia 13:295–306

    Article  Google Scholar 

  • Kursar TA, Alberte RS (1983) Photosynthetic unit organization in a red alga. Relationships between light harvesting pigments and reaction centers. Plant Physiol 72:409–414

    Article  PubMed  CAS  Google Scholar 

  • Kursar TA, Vander MJ, Alberte RS (1983) Light-harvesting system of the red alga Gracilaria tikvahiae. I. Biochemical analysis of pigment mutations. Plant Physiol 73:353–360

    Article  PubMed  CAS  Google Scholar 

  • Lin AP, Wang C, Qiao HJ, Pan GH, Wang GC, Song LY, Wang ZY, Sun S, Zhou BC (2009a) Study on the photosynthetic performances of Enteromorpha prolifera collected from the surface and bottom of the sea of Qingdao sea area. Chin Sci Bull 54:399–404

    Article  CAS  Google Scholar 

  • Lin AP, Wang GC, Yang F, Pan GH (2009b) Photosynthetic parameters of sexually different parts of Porphyra katadai var. hemiphylla (Bangiales, Rhodophyta) during dehydration and re-hydration. Planta 229:803–810

    Article  PubMed  CAS  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  PubMed  CAS  Google Scholar 

  • Nelson WA, Brodie J, Guiry MD (1999) Terminology used to describe reproduction and life history stages in the genus Porphyra (Bangiales, Rhodophyta). J Appl Phycol 11:407–410

    Article  Google Scholar 

  • Öquist G, Fork DC (1982) Effects of desiccation on the excitation energy distribution from phycoerythrin to the two photosystems the red alga Porphyra perforata. Physiol Plant 56:56–62

    Article  Google Scholar 

  • Ramus J, Beale SI, Mauzerall D (1976) Correlation of changes in pigment content with photosynthetic capacity of seaweeds as a function of water depth. Mar Biol 37:231–238

    Article  CAS  Google Scholar 

  • Rowan KS (1989) Photosynthetic pigments of algae. Cambridge University Press, Cambridge

    Google Scholar 

  • Schreiber U (2004) Pulse-Amplitude-Modulation (PAM) fluorometry and saturation pulse method: an overview. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis. Springer, New York, pp 279–319

    Google Scholar 

  • Schreiber U, Klughammer C (2008) Saturation pulse method for assessment of energy conversion in PS I. PAM Appl Notes 1:11–14

    Google Scholar 

  • Shafer DJ, Sherman TD, Wyllie-Echeverria S (2007) Do desiccation tolerances control the vertical distribution of intertidal seagrasses? Aquat Bot 87:161–166

    Article  Google Scholar 

  • Smith CM, Berry JA (1986) Recovery of photosynthesis after exposure of intertidal algae to osmotic and temperature stress: comparative studies of species whit differing distributional limits. Oecologia 70:6–12

    Article  Google Scholar 

  • Smith CM, Satoh K, Fork DC (1986) The effects of osmotic tissue dehydration and air drying on morphology and energy transfer in two species of Porphyra. Plant Physiol 80:843–847

    Article  PubMed  CAS  Google Scholar 

  • Stengel DB, Dring MJ (1998) Seasonal variation in the pigment content and photosynthesis of different thallus regions of Ascophyllum nodosum (Fucales, Phaeophyta) in relation to position in the canopy. Phycologia 37:259–268

    Article  Google Scholar 

  • Sussman M, Mieog JC, Doyle J, Victor S, Willis BL, Bourne DG (2009) Vibrio zinc-metalloprotease causes photoinactivation of coral endosymbionts and coral tissue lesions. PLoS ONE 4:e4511

    Article  PubMed  Google Scholar 

  • Szabo E, Colman B (2007) Isolation and characterization of carbonic anhydrases from the marine diatom Phaeodactylum tricornutum. Physiol Plant 129:484–492

    Article  CAS  Google Scholar 

  • Tadege M, Kuhlemeier C (1997) Aerobic fermentation during tobacco pollen development. Plant Mol Biol 35:343–354

    Article  PubMed  CAS  Google Scholar 

  • Van van Norman RW, French CS, Macdowall FDH (1948) The absorption and fluorescence spectra of two red marine algae. Plant Physiol 23:455–466

    Article  PubMed  CAS  Google Scholar 

  • Wang SJ, Xu ZD (1984) Ultrastructural studies on the reproductive organs of Porphyra haitanensis T. J. Chang et B. F. Zheng. Hydrobiologia 116/117:213–217

    Article  Google Scholar 

  • Wilbur KM, Anderson NG (1948) Electrometric and colorimetric determination of carbonic anhydrase. J Biol Chem 176:147–154

    PubMed  CAS  Google Scholar 

  • Xu HP, Weterings K, Vriezen W, Feron R, Xue YB, Derksen J, Mariani C (2002) Isolation and characterization of male-germ-cell transcripts in Nicotiana tabacum. Sex Plant Reprod 14:339–346

    Article  Google Scholar 

  • Yokoya NS, Necchi O, Martins AP, Gonzalez SF, Plastino EM (2007) Growth responses and photosynthetic characteristics of wild and phycoerythrin-deficient strains of Hypnea musciformis (Rhodophyta). J Appl Phycol 19:197–205

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 30830015, 40806063, 41176134, 30970302, 41106131, 41176137).

Author information

Authors and Affiliations

  1. College of Marine Science and Engineering, Tianjin University of Science & Technology, 300457, Tianjin, China

    Rui-Ling Yang & Guang-Hua Pan

  2. Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, 266071, Qingdao, China

    Wei Zhou, Guang-Ce Wang & Lin-Wen He

  3. Graduate School, The Chinese Academy of Sciences, 100039, Beijing, China

    Wei Zhou & Lin-Wen He

  4. Marine Fisheries Institute of Jiangsu, 226007, Nantong, China

    Wei Zhou

  5. School of Life Science, Soochow University, 215123, Jiangsu, China

    Song-Dong Shen

Authors
  1. Rui-Ling Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wei Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Song-Dong Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guang-Ce Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lin-Wen He
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Guang-Hua Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Guang-Ce Wang.

Additional information

R.-L. Yang and W. Zhou contributed equally to this publication.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yang, RL., Zhou, W., Shen, SD. et al. Morphological and photosynthetic variations in the process of spermatia formation from vegetative cells in Porphyra yezoensis Ueda (Bangiales, Rhodophyta) and their responses to desiccation. Planta 235, 885–893 (2012). https://doi.org/10.1007/s00425-011-1549-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-011-1549-y

Keywords

Search

Navigation