Skip to main content
SpringerLink
Log in

The transcriptional program of synchronous gametogenesis in Chlamydomonas reinhardtii

  • Research Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

Cells of Chlamydomonas reinhardtii undergo gametogenesis to produce sexually competent gametes under nitrogen-starved conditions. By using a synchronized system for gametogenesis of early G1 cells, several previously identified marker genes and 18 novel nitrogen-starved gametogenesis (NSG) genes isolated by macroarray analysis were placed into at least three temporal classes of expression. Early genes are induced transiently in the first 2 h after transfer to nitrogen-free medium. Middle genes are strongly induced between 3 h and 4 h after nitrogen removal, a time corresponding to the acquisition of mating competency, suggesting their involvement in the gamete program. Late genes are induced between 5 h and 8 h after nitrogen removal, a time after the completion of gametic differentiation, suggesting that they are not directly involved in the formation of sexually competent gametes. All of the 18 NSG genes examined are induced in both mating-type plus and minus gametes and about two-thirds of the genes are also expressed in the mitotic cell cycle, especially at S/M phases.

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

References

  • Adair WS, Monk BC, Cohen R, Hwang C, Goodenough UW (1982) Sexual agglutinins from the Chlamydomonas flagellar membrane: partial purification and characterization. J Biol Chem 257:4593–4602

    CAS  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    CAS  PubMed  Google Scholar 

  • Asamizu E, Nakamura Y, Sato S, Fukuzawa H, Tabata S (1999) A large scale structural analysis of cDNAs in a unicellular green alga, Chlamydomonas reinhardtii: generation of 3433 non-redundant expressed sequence tags. DNA Res 6:363–373

    Google Scholar 

  • Asamizu E, Nakamura Y, Miura K, Fukuzawa H, Fujiwara S, Hirono M, Iwamoto K, Matsuda Y, Minagawa J, Shimogawara K, Takahashi Y, Tabata S (2004) Establishment of publicly available cDNA material and information resource of Chlamydomonas reinhardtii (Chlorophyta), to facilitate gene function analysis. Phycologia (in press)

  • Aubourg S, Kreis M, Lecharny A (1999) The DEAD box RNA helicase family in Arabidopsis thaliana. Nucleic Acids Res 27:628–636

    Google Scholar 

  • Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer EL (2002) The Pfam protein families database. Nucleic Acids Res 30:276–280

    Article  CAS  PubMed  Google Scholar 

  • Beck CF, Haring MA (1996) Gametic differentiation of Chlamydomonas. Int Rev Cytol 168:259–302

    CAS  Google Scholar 

  • Benton BK, Reid MS, Okayama H (1993) A Schizosaccharomyces pombe gene that promotes sexual differentiation encodes a helix-loop-helix protein with homology to MyoD. EMBO J 12:135–143

    CAS  PubMed  Google Scholar 

  • Brodsky FM, Chen C-Y, Knuchl C, Towler MC, Wakeham DE (2001) Biological basket weaving: formation and function of clathrin-coated vesicles. Annu Rev Cell Dev Biol 17:517–568

    Article  CAS  PubMed  Google Scholar 

  • Bulté L, Bennoun P (1990) Translational accuracy and sexual differentiation in Chlamydomonas reinhardtii. Curr Genet 18:155–160

    PubMed  Google Scholar 

  • Bulté L, Wollman F-A (1992) Evidence for a selective destabilization of an integral membrane protein, the cytochrome b6/f complex, during gametogenesis in Chlamydomonas reinhardtii. Eur J Biochem 204:327–336

    PubMed  Google Scholar 

  • Chen Q, Silflow CD (1996) Isolation and characterization of glutamine synthetase genes in Chlamydomonas reinhardtii. Plant Physiol 112:987–996

    Article  CAS  PubMed  Google Scholar 

  • Chu S, DeRisi J, Elsen M, Mulholland J, Botstein D, Brown PO, Herskowitz I (1998) The transcriptional program of sporulation in budding yeast. Science 282:699–705

    Article  CAS  PubMed  Google Scholar 

  • Coates JC (2003) Armadillo repeat proteins: beyond the animal kingdom. Trends Cell Biol 13:463–471

    Article  CAS  PubMed  Google Scholar 

  • Davey J (1998) Fusion of a fission yeast. Yeast 14:1529–1566

    Article  CAS  PubMed  Google Scholar 

  • Detmers PA, Goodenough UW, Condeelis J (1983) Elongation of the fertilization tubule in Chlamydomonas: new observations on the core microfilaments and the effect of transient intracellular signals on their structural integrity. J Cell Biol 97:522–532

    Article  CAS  PubMed  Google Scholar 

  • Detmers PA, Carboni JM, Condeelis J (1985) Localization of actin in Chlamydomonas using antiactin and NBD-phallacidin. Cell Motil 5:415–430

    CAS  PubMed  Google Scholar 

  • Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863–14868

    Article  Google Scholar 

  • Fernández E, Schnell R, Ranum LPW, Hussey SC, Silflow CD, Lefebvre PA (1989) Isolation and characterization of the nitrate reductase structural gene in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 86:6449–6453

    PubMed  Google Scholar 

  • Ferris PJ, Goodenough UW (1994) The mating type locus of Chlamydomonas reinhardtii contains highly rearranged DNA sequences. Cell 76:1135–1145

    Article  CAS  PubMed  Google Scholar 

  • Ferris PJ, Goodenough UW (1997) Mating type in Chlamydomonas is specified by mid, the minus dominance gene. Genetics 146:859–869

    CAS  PubMed  Google Scholar 

  • Ferris PJ, Woessner JP, Goodenough UW (1996) A sex recognition glycoprotein is encoded by the plus mating-type gene fus1 of Chlamydomonas reinhardtii. Mol Biol Cell 7:1235–1248

    CAS  PubMed  Google Scholar 

  • Ferris PJ, Woessner JP, Waffenschmidt S, Kilz S, Drees J, Goodenough UW (2001) Glycosylated polyproline II rods with kinks as a structural motif in plant hydroxyproline-rich glycoproteins. Biochemistry 40:2978–2987

    Article  CAS  PubMed  Google Scholar 

  • Ferris PJ, Armbrust EV, Goodenough UW (2002) Genetic structure of the mating-type locus of Chlamydomonas reinhardtii. Genetics 160:181–200

    CAS  PubMed  Google Scholar 

  • Friedmann I, Colwin AL, Colwin LH (1968) Fine structural aspects of fertilization in Chlamydomonas reinhardti. J Cell Sci 3:115–128

    CAS  PubMed  Google Scholar 

  • Frishman D, Argos P (1997) Seventy-five percent accuracy in protein secondary structure prediction. Proteins 27:329–335

    Article  CAS  PubMed  Google Scholar 

  • Goodenough UW (1991) Chlamydomonas mating interactions. In: Dworkin M (ed) Microbial cell–cell interactions. American Society for Microbiology, Washington, D.C., pp 71–112

    Google Scholar 

  • Goodenough UW, Detmers PA, Hwang C (1982) Activation for cell fusion in Chlamydomonas. Analysis of wild-type gametes and nonfusing mutants. J Cell Biol 92:378–386

    Article  CAS  PubMed  Google Scholar 

  • Goodenough UW, Armbrust EV, Cambell AM, Ferris PJ (1995) Molecular genetics of sexuality in Chlamydomonas. Annu Rev Plant Physiol Plant Mol Biol 46:21–44

    Article  CAS  Google Scholar 

  • Grandbastein M-A (1992) Retroelements in higher plants. Trends Genet 8:103–108

    PubMed  Google Scholar 

  • Gromoff ED von, Beck CF (1993) Genes expressed during sexual differentiation of Chlamydomonas reinhardtii. Mol Gen Genet 241:415–421

    PubMed  Google Scholar 

  • Grossman AR, Harris EH, Hauser C, Lefebvre PA, Martinez D, Rokhsar D, Shrager J, Silflow CD, Stern D, Vallon O, Zhang Z (2003) Chlamydomonas reinhardtii at the crossroads of genomics. Eukaryot Cell 2:1137–1150

    Article  CAS  PubMed  Google Scholar 

  • Harper JW (2001) Protein destruction: adapting roles for Cks proteins. Curr Biol 11:R431–R435

    Article  CAS  PubMed  Google Scholar 

  • Harper JDI, McCurdy DW, Sanders MA, Salisbury JL, John PCL (1992) Actin dynamics during the cell cycle in Chlamydomonas reinhardtii. Cell Motil Cytoskeleton 22:117–126

    CAS  PubMed  Google Scholar 

  • Harris EH (1989) The Chlamydomonas sourcebook. Academic, San Diego

    Google Scholar 

  • Heijne G von (1985) Signal sequences: the limits of variation. J Mol Biol 184:99–105

    PubMed  Google Scholar 

  • Hirokawa T, Boon-Chieng S, Mitaku S (1998) SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14:378–379

    Article  CAS  PubMed  Google Scholar 

  • Jordan A, Reichard P (1998) Ribonucleotide reductases. Annu Rev Biochem 67:71–98

    Article  CAS  PubMed  Google Scholar 

  • Kassi Y, Adir N, Boger-Nadjar E, Raviv NG, Rubin-Bejerano I, Sagee S, Shenhar G (2003) Transcriptional regulation of meiosis in budding yeast. Int Rev Cytol 224:111–171

    PubMed  Google Scholar 

  • Kato T, Kagami O, Yagi T, Kamiya R (1993) Isolation of two species of Chlamydomonas reinhardtii flagellar mutants, ida5 and ida6, that lack a newly identified heavy chain of the inner dynein arm. Cell Struct Funct 18:371–377

    CAS  PubMed  Google Scholar 

  • Kato-Minoura T, Hirono M, Kamiya R (1997) Chlamydomonas inner-arm dynein mutant, ida5, has a mutation in an actin-encoding gene. J Cell Biol 137:649–656

    Article  CAS  PubMed  Google Scholar 

  • Kinoshita T, Fukuzawa H, Shimada T, Saito T, Matsuda Y (1992) Primary structure and expression of a gamete lytic enzyme in Chlamydomonas reinhardtii: similarity of functional domains to matrix metalloproteases. Proc Natl Acad Sci USA 89:4693–4697

    CAS  PubMed  Google Scholar 

  • Kubo T, Saito T, Fukuzawa H, Matsuda Y (2001) Two tandemly located matrix metalloprotease genes with different expression patterns in the Chlamydomonas sexual cell cycle. Curr Genet 40:136–143

    Article  CAS  PubMed  Google Scholar 

  • Kubo T, Abe J, Saito T, Matsuda Y (2002) Genealogical relationships among laboratory strains of Chlamydomonas reinhardtii as inferred from matrix metalloprotease genes. Curr Genet 41:115–122

    Article  CAS  PubMed  Google Scholar 

  • Kuriyama H, Takano H, Uchida H, Kawano S, Kuroiwa H, Kuroiwa T (1999) Characterization of Chlamydomonas reinhardtii zygote-specific cDNAs that encode novel proteins containing ankyrin repeats and WW domains. Plant Physiol 119:873–884

    Google Scholar 

  • Latterich M, Fröhlich KU, Schekman R (1995) Membrane fusion and the cell cycle: Cdc48p participates in the fusion of ER membranes. Cell 82:885–893

    Article  CAS  PubMed  Google Scholar 

  • Lindauer A, Fraser D, Brüderlein M, Schmitt R (1993) Reverse transcriptase families and a copia-like retrotransposon, Osser, in the green alga Volvox carteri. FEBS Lett 319:261–266

    Article  CAS  PubMed  Google Scholar 

  • Maciver SK, Hussey PJ (2002) The ADF/cofilin family: actin-remodeling proteins. Genome Biol 5:1–12

    Google Scholar 

  • Martin NC, Goodenough UW (1975) Gametic differentiation in Chlamydomonas reinhardti. I. Production of gametes and their fine structure. J Cell Biol 67:587–605

    Article  CAS  PubMed  Google Scholar 

  • Martin NC, Chiang K-S, Goodenough UW (1976) Turnover of chloroplast and cytoplasmic ribosomes during gametogenesis in Chlamydomonas reinhardti. Dev Biol 51:190–201

    CAS  PubMed  Google Scholar 

  • Matsuda Y (1998) Gametolysin. In: Barrett A, Woessner F, Rawlings N (eds) Handbook of proteolytic enzymes. Academic, New York, pp 1140–1143

    Google Scholar 

  • Matsuda Y, Tamaki S, Tsubo Y (1978) Mating type specific induction of cell wall lytic factor by agglutination of gametes in Chlamydomonas reinhardtii. Plant Cell Physiol 19:1253–1261

    Google Scholar 

  • Matsuda Y, Saito T, Koseki M, Shimada T (1990) The Chlamydomonas non-synchronous and synchronous gametogenesis as analyzed by the activities of cell body-agglutinin and cell wall lytic enzyme (Life Sci Adv). Plant Physiol 9:1–6

    Google Scholar 

  • Matsuda Y, Shimada T, Sakamoto Y (1992) Ammonium ions control gametic differentiation and dedifferentiation in Chlamydomonas reinhardtii. Plant Cell Physiol 33:909–914

    CAS  Google Scholar 

  • Matsuda Y, Koseki M, Shimada T, Saito T (1995) Purification and characterization of a vegetative lytic enzyme responsible for liberation of daughter cells during the proliferation of Chlamydomonas reinhardtii. Plant Cell Physiol 36:681–689

    CAS  PubMed  Google Scholar 

  • McClintock B (1984) The significance of responses of the genome to challenge. Science 236:792–801

    Google Scholar 

  • Merchán F, Ende H van den, Fernández E, Beck CF (2001) Low-expression genes induced by nitrogen starvation and subsequent sexual differentiation in Chlamydomonas reinhardtii, isolated by the differential display technique. Planta 213:309–317

    Article  PubMed  Google Scholar 

  • Misamore MJ, Gupta S, Snell WJ (2003) The Chlamydomonas Fus1 protein is present on the mating type plus fusion organelle and required for critical membrane adhesion event during fusion with minus gametes. Mol Biol Cell 14:2530–2542

    Article  CAS  PubMed  Google Scholar 

  • Miura K, Yamano T, Yoshioka S, Kohinata T, Inoue Y, Taniguchi F, Asamizu E, Nakamura Y, Tabata S, Yamato KT, Ohyama K, Fukuzawa H (2004) Expression profiling-based identification of CO2-responsive genes regulated by CCM1 controlling a carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Physiol 135:1595–1607

    Article  CAS  PubMed  Google Scholar 

  • Mol CD, Harris JM, McIntosh EM, Tainer JA (1996) Human dUTP pyrophosphatase: uracil recognition by a beta hairpin and active sites formed by three separate subunits. Structure 4:1077–1092

    Article  CAS  PubMed  Google Scholar 

  • Morgenstern B, Atchley WR (1999) Evolution of bHLH transcription factors: modular evolution by domain shuffling? Mol Biol Evol 16:1654–1663

    CAS  PubMed  Google Scholar 

  • Nelson MA, Metzenberg RL (1992) Sexual development genes of Neurospora crassa. Genetics 132:149–162

    CAS  PubMed  Google Scholar 

  • Peifer M, Berg S, Reynolds AB (1994) A repeating amino acid motif shared by proteins with diverse cellular roles. Cell 76:789–791

    Article  CAS  PubMed  Google Scholar 

  • Picard-Bennoun M, Bennoun P (1985) Change in cytoplasmic ribosome properties during gametogenesis in the alga Chlamydomonas reinhardtii. Curr Genet 9:239–243

    CAS  Google Scholar 

  • Pozuelo M, Merchán F, Macías MI, Beck CF, Galván A, Fernández E (2000) The negative effect of nitrate on gametogenesis is independent of nitrate assimilation in Chlamydomonas reinhardtii. Planta 211:287–292

    Article  CAS  PubMed  Google Scholar 

  • Quesada A, Fernández E (1994) Expression of nitrate assimilation related genes in Chlamydomonas reinhardtii. Plant Mol Biol 24:185–194

    CAS  PubMed  Google Scholar 

  • Quesada A, Galván A, Fernández E (1994) Identification of nitrate transporter genes in Chlamydomonas reinhardtii. Plant J 5:407–419

    CAS  PubMed  Google Scholar 

  • Quirk S, Maciver SK, Ampe C, Doberstein SK, Kaiser DA, Van Damme J, Vandekerckhove JS, Pollard TD (1993) Primary structure of and studies on Acanthamoeba actophorin. Biochemistry 32:8525–8533

    CAS  PubMed  Google Scholar 

  • Rodriguez H, Haring MA, Beck CF (1999) Molecular characterization of two light-induced, gamete-specific genes from Chlamydomonas reinhardtii that encode hydroxyproline-rich proteins. Mol Gen Genet 261:267–274

    Article  CAS  PubMed  Google Scholar 

  • Rost B, Liu J (2003) The PredictProtein server. Nucleic Acids Res 31:3300–3304

    Article  CAS  PubMed  Google Scholar 

  • Sager R, Granick S (1953) Nutritional studies with Chlamydomonas reinhardti. Ann N Y Acad Sci 56:831–838

    CAS  PubMed  Google Scholar 

  • Sager R, Granick S (1954) Nutritional control of sexuality in Chlamydomonas reinhardti. J Gen Physiol 37:729–742

    Article  CAS  PubMed  Google Scholar 

  • Saito T, Matsuda Y (1984) Sexual agglutinin of mating-type minus gametes in Chlamydomonas reinhardtii: purification and characterization of minus agglutinin and comparison with plus agglutinin. Arch Microbiol 139:95–99

    CAS  Google Scholar 

  • Saito T, Matsuda Y (1991) Isolation and characterization of Chlamydomonas temperature-sensitive mutants affecting gametic differentiation under nitrogen-starved conditions. Curr Genet 19:65–71

    CAS  PubMed  Google Scholar 

  • Saito T, Inoue M, Yamada M, Matsuda Y (1998) Control of gametic differentiation and activity by light in Chlamydomonas reinhardtii. Plant Cell Physiol 39:8–15

    CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.

    Google Scholar 

  • Schlösser UG (1981) Algal wall-degrading enzymes—autolysines. In: Tanner W, Loewus FA (eds) Encyclopedia of plant physiology new series, vol 13B. Springer, Berlin Heidelberg New York, pp 333–351

    Google Scholar 

  • Schlösser UG (1984) Species-specific sporangium autolysins (cell wall-dissolving enzymes) in the genus Chlamydomonas. In: Irvine DEG, John DM (eds) Systematics of the green algae. Academic, London, pp 409–418

    Google Scholar 

  • Schnell RA, Lefebvre PA (1993) Isolation of the Chlamydomonas regulatory gene NIT2 by transposon tagging. Genetics 134:737–747

    CAS  PubMed  Google Scholar 

  • Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 95:5857–5864

    Article  CAS  PubMed  Google Scholar 

  • Sedwick SG, Smerdon SJ (1999) The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem Sci 24:311–316

    Article  PubMed  Google Scholar 

  • Shrager J, Hauser C, Chang C-W, Harris EH, Davies J, McDermott J, Tamse R, Zhang Z, Grossman AR (2003) Chlamydomonas reinhardtii genome project: a guide to the generation and use of the cDNA information. Plant Physiol 131:401–408

    Google Scholar 

  • Siersma PW, Chiang K-S (1971) Conservation and degradation of cytoplasmic and chloroplast ribosomes in Chlamydomonas reinhardtii. J Mol Biol 58:167–185

    CAS  PubMed  Google Scholar 

  • Skromne I, Sánchez O, Aguirre J (1995) Starvation stress modulates the expression of the Aspergillus nidulans brlA regulatory gene. Microbiology 141:21–28

    CAS  PubMed  Google Scholar 

  • Smith EF, Lefebvre PA (1996) PF16 encodes a protein with armadillo repeats and localizes to a single microtubule of the central apparatus in Chlamydomonas flagella. J Cell Biol 132:359–370

    Article  CAS  PubMed  Google Scholar 

  • Smith EF, Lefebvre PA (2000) Defining functional domains within PF16: a central apparatus component required for flagellar motility. Cell Motil Cytoskeleton 46:157–165

    Article  CAS  PubMed  Google Scholar 

  • Snell WJ, Eskue WA, Buchanan MJ (1989) Regulated secretion of a serine protease that activates an extracellular matrix-degrading metalloprotease during fertilization in Chlamydomonas. J Cell Biol 109:1689–1694

    Article  CAS  PubMed  Google Scholar 

  • Sugase Y, Hirono M, Kindle KL, Kamiya R (1996) Cloning and characterization of the actin-encoding gene of Chlamydomonas reinhardtii. Gene 168:117–121

    Article  CAS  PubMed  Google Scholar 

  • Vallon O, Bulté L, Kuras R, Olive J, Wollman FA (1993) Extensive accumulation of an extracellular l-amino-acid oxidase during gametogenesis of Chlamydomonas reinhardtii. Eur J Biochem 215:351–360

    CAS  PubMed  Google Scholar 

  • Voges D, Zwickl P, Baumeister W (1999) The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu Rev Biochem 68:1015–1068

    Article  CAS  PubMed  Google Scholar 

  • Voytas DF, Cummings MP, Konieczny A, Ausubel FM, Rodermel SR (1992) copia-like retrotransposons are ubiquitous among plants. Proc Natl Acad Sci USA 89:7124–7128

    CAS  PubMed  Google Scholar 

  • Xiong Y, Eickbush TH (1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 9:3353–3362

    CAS  PubMed  Google Scholar 

  • Ye Y, Meyer HH, Rapoport TA (2001) The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 414:652–656

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Forde BG (2000) Regulation of Arabidopsis root development by nitrate availability. J Exp Bot 51:51–59

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Drs. Erika Asamizu and Satoshi Tabata (Kazusa DNA Institute) for providing EST clones and Drs. Patrick Ferris and Ursula Goodenough (Washington University) for MTA1. We also thank Patrick Ferris for his critical reading of the manuscript.

Author information

Authors and Affiliations

  1. Department of Molecular Science, Graduate School of Science and Technology, Kobe University, Nada-ku, Kobe 657-8501, Japan

    J. Abe, T. Kubo & Y. Takagi

  2. Department of Applied Science, Faculty of Science, Okayama University of Science, Okayama 700-0005, Japan

    T. Saito

  3. Division of Integral Life Science, Graduate School of Biostudies, Kyoto University, Kyoto 606-8502, Japan

    K. Miura & H. Fukuzawa

  4. Department of Biology, Faculty of Science, Kobe University, Nada-ku, Kobe 657-8501, Japan

    Y. Matsuda

Authors
  1. J. Abe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. Kubo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Y. Takagi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. T. Saito
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. K. Miura
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. H. Fukuzawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Y. Matsuda
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Y. Matsuda.

Additional information

Communicated by F.-A. Wollman

Rights and permissions

Reprints and permissions

About this article

Cite this article

Abe, J., Kubo, T., Takagi, Y. et al. The transcriptional program of synchronous gametogenesis in Chlamydomonas reinhardtii. Curr Genet 46, 304–315 (2004). https://doi.org/10.1007/s00294-004-0526-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-004-0526-4

Keywords

Search

Navigation