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. 1991 Sep 1;114(5):905–915. doi: 10.1083/jcb.114.5.905

Evidence for thylakoid membrane fusion during zygote formation in Chlamydomonas reinhardtii

PMCID: PMC2289111  PMID: 1874788

Abstract

To understand whether fusions of thylakoid membranes from the parental chloroplasts occurred during zygote formation in Chlamydomonas reinhardtii, we performed an ultrastructural analysis of the zygotes produced by crossing mutants lacking photosystem I or II protein complexes, in the absence of de novo chloroplast protein synthesis. Thylakoid membranes from each parent could be distinguished on thin sections due to their organization in "supergrana" in mutants lacking photosystem I centers, by freeze-fracturing due to the absence of most of the exoplasmic-face (EF) particles in mutants lacking photosystem II centers, by immunocytochemistry using antibodies directed against photosystem II subunits. We demonstrate that a fusion of the thylakoid membranes occurred during zygote formation approximately 15 h after mating. These fusions allowed a lateral redistribution of the thylakoid membrane proteins. These observations provide the structural basis for the restoration of photosynthetic electron flow in the mature zygote that we observed in fluorescence induction experiments.

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Selected References

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  1. Bennoun P., Masson A., Delosme M. A method for complementation analysis of nuclear and chloroplast mutants of photosynthesis in chlamydomonas. Genetics. 1980 May;95(1):39–47. doi: 10.1093/genetics/95.1.39. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bulté L., Bennoun P. Translational accuracy and sexual differentiation in Chlamydomonas reinhardtii. Curr Genet. 1990 Aug;18(2):155–160. doi: 10.1007/BF00312603. [DOI] [PubMed] [Google Scholar]
  3. Cavalier-Smith T. Basal body and flagellar development during the vegetative cell cycle and the sexual cycle of Chlamydomonas reinhardii. J Cell Sci. 1974 Dec;16(3):529–556. doi: 10.1242/jcs.16.3.529. [DOI] [PubMed] [Google Scholar]
  4. Cavalier-Smith T. Eelectron microscopy of zygospore formation in Chlamydomonas reinhardii. Protoplasma. 1976;87(4):297–315. doi: 10.1007/BF01624002. [DOI] [PubMed] [Google Scholar]
  5. Cavalier-Smith T. Electron and light microscopy of gametogenesis and gamete fusion in Chlamydomonas reinhardii. Protoplasma. 1975;86(1-3):1–18. doi: 10.1007/BF01275619. [DOI] [PubMed] [Google Scholar]
  6. Cavalier-Smith T. Electron microscopic evidence for chloroplast fusion in zygotes of Chlamydomonas reinhardii. Nature. 1970 Oct 24;228(5269):333–335. doi: 10.1038/228333a0. [DOI] [PubMed] [Google Scholar]
  7. Chua N. H., Bennoun P. Thylakoid membrane polypeptides of Chlamydomonas reinhardtii: wild-type and mutant strains deficient in photosystem II reaction center. Proc Natl Acad Sci U S A. 1975 Jun;72(6):2175–2179. doi: 10.1073/pnas.72.6.2175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Delepelaire P. Partial characterization of the biosynthesis and integration of the Photosystem II reaction centers in the thylakoid membrane of Chlamydomonas reinhardtii. EMBO J. 1984 Apr;3(4):701–706. doi: 10.1002/j.1460-2075.1984.tb01872.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Friedmann I., Colwin A. L., Colwin L. H. Fine-structural aspects of fertilization in Chlamydomonas reinhardi. J Cell Sci. 1968 Mar;3(1):115–128. doi: 10.1242/jcs.3.1.115. [DOI] [PubMed] [Google Scholar]
  10. Goldschmidt-Clermont M., Girard-Bascou J., Choquet Y., Rochaix J. D. Trans-splicing mutants of Chlamydomonas reinhardtii. Mol Gen Genet. 1990 Sep;223(3):417–425. doi: 10.1007/BF00264448. [DOI] [PubMed] [Google Scholar]
  11. Goodenough U. W., Levine R. P. Chloroplast Ultrastructure in Mutant Strains of Chlamydomonas reinhardi Lacking Components of the Photosynthetic Apparatus. Plant Physiol. 1969 Jul;44(7):990–1000. doi: 10.1104/pp.44.7.990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  13. Martin N. C., Goodenough U. W. Gametic differentiation in Chlamydomonas reinhardtii. I. Production of gametes and their fine structure. J Cell Biol. 1975 Dec;67(3):587–605. doi: 10.1083/jcb.67.3.587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Olive J., Wollman F. A., Bennoun P., Recouvreur M. Ultrastructure - function relationship in Chlamydomonas reinhartii thylakoids, by means of a comparison between the wild type and the F34 mutant which lacks the photosystem II reaction center. Mol Biol Rep. 1979 Aug 31;5(3):139–143. doi: 10.1007/BF00778412. [DOI] [PubMed] [Google Scholar]
  15. REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Rochaix J. D., Kuchka M., Mayfield S., Schirmer-Rahire M., Girard-Bascou J., Bennoun P. Nuclear and chloroplast mutations affect the synthesis or stability of the chloroplast psbC gene product in Chlamydomonas reinhardtii. EMBO J. 1989 Apr;8(4):1013–1021. doi: 10.1002/j.1460-2075.1989.tb03468.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Siersma P. W., Chiang K. S. Conservation and degradation of cytoplasmic and chloroplast ribosomes in Chlamydomonas reinhardtii. J Mol Biol. 1971 May 28;58(1):167–185. doi: 10.1016/0022-2836(71)90239-7. [DOI] [PubMed] [Google Scholar]
  18. Staehelin L. A. Reversible particle movements associated with unstacking and restacking of chloroplast membranes in vitro. J Cell Biol. 1976 Oct;71(1):136–158. doi: 10.1083/jcb.71.1.136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Wollman F. A., Diner B. A. Cation control of fluorescence emission, light scatter, and membrane stacking in pigment mutants of Chlamydomonas reinhardi. Arch Biochem Biophys. 1980 May;201(2):646–659. doi: 10.1016/0003-9861(80)90555-x. [DOI] [PubMed] [Google Scholar]
  20. Wollman F. A., Olive J., Bennoun P., Recouvreur M. Organization of the photosystem II centers and their associated antennae in the thylakoid membranes: a comparative ultrastructural, biochemical, and biophysical study of Chlamydomonas wild type and mutants lacking in photosystem II reaction centers. J Cell Biol. 1980 Dec;87(3 Pt 1):728–735. doi: 10.1083/jcb.87.3.728. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. de Vitry C., Olive J., Drapier D., Recouvreur M., Wollman F. A. Posttranslational events leading to the assembly of photosystem II protein complex: a study using photosynthesis mutants from Chlamydomonas reinhardtii. J Cell Biol. 1989 Sep;109(3):991–1006. doi: 10.1083/jcb.109.3.991. [DOI] [PMC free article] [PubMed] [Google Scholar]

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