Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1986 Oct 1;103(4):1315–1325. doi: 10.1083/jcb.103.4.1315

Biogenesis of photosystem II complexes: transcriptional, translational, and posttranslational regulation

PMCID: PMC2114316  PMID: 3533953

Abstract

The integral membrane proteins of photosystem II (PS II) reaction center complexes are encoded by chloroplast genomes. These proteins are absent from thylakoids of PS II mutants of algae and vascular plants as a result of either chloroplast or nuclear gene mutations. To resolve the molecular basis for the concurrent absence of the PS II polypeptides, protein synthesis rates and mRNA levels were measured in mutants of Chlamydomonas reinhardtii that lack PS II. The analyses show that one nuclear gene product regulates the levels of transcripts from the chloroplast gene encoding the 51-kD chlorophyll a-binding polypeptide (polypeptide 5) but is not involved in the synthesis of other chloroplast mRNAs. Another nuclear product is specifically required for translation of mRNA encoding the 32-34-kD polypeptide, D1. The absence of either D1 or polypeptide 5 does not eliminate the synthesis and thylakoid insertion of two other integral membrane proteins of PS II, the chlorophyll a-binding polypeptide of 46 kD (polypeptide 6) and the 30-kD "D1-like" protein, D2. However, these two unassembled subunits cannot be properly processed and/or are degraded in the mutants even though they reside in the membrane. In addition, pulse labeling of the nuclear mutants and a chloroplast mutant that does not synthesize D1 mRNA indicates that synthesis of polypeptide 5 and D1 is coordinated at the translational level. A model is presented to explain how absence of one of the two proteins could lead to translational arrest of the other.

Full Text

The Full Text of this article is available as a PDF (2.9 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Berry J. O., Nikolau B. J., Carr J. P., Klessig D. F. Transcriptional and post-transcriptional regulation of ribulose 1,5-bisphosphate carboxylase gene expression in light- and dark-grown amaranth cotyledons. Mol Cell Biol. 1985 Sep;5(9):2238–2246. doi: 10.1128/mcb.5.9.2238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Collins R. A., Lambowitz A. M. RNA splicing in Neurospora mitochondria. Defective splicing of mitochondrial mRNA precursors in the nuclear mutant cyt18-1. J Mol Biol. 1985 Aug 5;184(3):413–428. doi: 10.1016/0022-2836(85)90291-8. [DOI] [PubMed] [Google Scholar]
  4. Delepelaire P., Chua N. H. Lithium dodecyl sulfate/polyacrylamide gel electrophoresis of thylakoid membranes at 4 degrees C: Characterizations of two additional chlorophyll a-protein complexes. Proc Natl Acad Sci U S A. 1979 Jan;76(1):111–115. doi: 10.1073/pnas.76.1.111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Erickson J. M., Rahire M., Rochaix J. D. Chlamydomonas reinhardii gene for the 32 000 mol. wt. protein of photosystem II contains four large introns and is located entirely within the chloroplast inverted repeat. EMBO J. 1984 Dec 1;3(12):2753–2762. doi: 10.1002/j.1460-2075.1984.tb02206.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fromm H., Devic M., Fluhr R., Edelman M. Control of psbA gene expression: in mature Spirodela chloroplasts light regulation of 32-kd protein synthesis is independent of transcript level. EMBO J. 1985 Feb;4(2):291–295. doi: 10.1002/j.1460-2075.1985.tb03628.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Galloway R. E., Mets L. J. Atrazine, bromacil, and diuron resistance in chlamydomonas: a single non-mendelian genetic locus controls the structure of the thylakoid binding site. Plant Physiol. 1984 Mar;74(3):469–474. doi: 10.1104/pp.74.3.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gorman D. S., Levine R. P. Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Proc Natl Acad Sci U S A. 1965 Dec;54(6):1665–1669. doi: 10.1073/pnas.54.6.1665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Grebanier A. E., Coen D. M., Rich A., Bogorad L. Membrane proteins synthesized but not processed by isolated maize chloroplasts. J Cell Biol. 1978 Sep;78(3):734–746. doi: 10.1083/jcb.78.3.734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hoffman-Falk H., Mattoo A. K., Marder J. B., Edelman M., Ellis R. J. General occurrence and structural similarity of the rapidly synthesized, 32,000-dalton protein of the chloroplast membrane. J Biol Chem. 1982 Apr 25;257(8):4583–4587. [PubMed] [Google Scholar]
  12. Holmes D. S., Quigley M. A rapid boiling method for the preparation of bacterial plasmids. Anal Biochem. 1981 Jun;114(1):193–197. doi: 10.1016/0003-2697(81)90473-5. [DOI] [PubMed] [Google Scholar]
  13. Holschuh K., Bottomley W., Whitfeld P. R. Structure of the spinach chloroplast genes for the D2 and 44 kd reaction-centre proteins of photosystem II and for tRNASer (UGA). Nucleic Acids Res. 1984 Dec 11;12(23):8819–8834. doi: 10.1093/nar/12.23.8819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Inamine G., Nash B., Weissbach H., Brot N. Light regulation of the synthesis of the large subunit of ribulose-1,5-bisphosphate carboxylase in peas: Evidence for translational control. Proc Natl Acad Sci U S A. 1985 Sep;82(17):5690–5694. doi: 10.1073/pnas.82.17.5690. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jolly S. O., McIntosh L., Link G., Bogorad L. Differential transcription in vivo and in vitro of two adjacent maize chloroplast genes: The large subunit of ribulosebisphosphate carboxylase and the 2.2-kilobase gene. Proc Natl Acad Sci U S A. 1981 Nov;78(11):6821–6825. doi: 10.1073/pnas.78.11.6821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kirk M. M., Kirk D. L. Translational regulation of protein synthesis, in response to light, at a critical stage of Volvox development. Cell. 1985 Jun;41(2):419–428. doi: 10.1016/s0092-8674(85)80015-5. [DOI] [PubMed] [Google Scholar]
  17. Leto K. J., Bell E., McIntosh L. Nuclear mutation leads to an accelerated turnover of chloroplast-encoded 48 kd and 34.5 kd polypeptides in thylakoids lacking photosystem II. EMBO J. 1985 Jul;4(7):1645–1653. doi: 10.1002/j.1460-2075.1985.tb03832.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Link G., Coen D. M., Bogorad L. Differential expression of the gene for the large subunit of ribulose bisphosphate carboxylase in maize leaf cell types. Cell. 1978 Nov;15(3):725–731. doi: 10.1016/0092-8674(78)90258-1. [DOI] [PubMed] [Google Scholar]
  19. Marder J. B., Goloubinoff P., Edelman M. Molecular architecture of the rapidly metabolized 32-kilodalton protein of photosystem II. Indications for COOH-terminal processing of a chloroplast membrane polypeptide. J Biol Chem. 1984 Mar 25;259(6):3900–3908. [PubMed] [Google Scholar]
  20. Miller M. E., Jurgenson J. E., Reardon E. M., Price C. A. Plastid translation in organello and in vitro during light-induced development in Euglena. J Biol Chem. 1983 Dec 10;258(23):14478–14484. [PubMed] [Google Scholar]
  21. Mishkind M. L., Schmidt G. W. Posttranscriptional Regulation of Ribulose 1,5-bisphosphate Carboxylase Small Subunit Accumulation in Chlamydomonas reinhardtii. Plant Physiol. 1983 Jul;72(3):847–854. doi: 10.1104/pp.72.3.847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mishkind M. L., Wessler S. R., Schmidt G. W. Functional determinants in transit sequences: import and partial maturation by vascular plant chloroplasts of the ribulose-1,5-bisphosphate carboxylase small subunit of Chlamydomonas. J Cell Biol. 1985 Jan;100(1):226–234. doi: 10.1083/jcb.100.1.226. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Morris J., Herrmann R. G. Nucleotide sequence of the gene for the P680 chlorophyll alpha apoprotein of the photosystem II reaction center from spinach. Nucleic Acids Res. 1984 Mar 26;12(6):2837–2850. doi: 10.1093/nar/12.6.2837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Morrissey J. H. Silver stain for proteins in polyacrylamide gels: a modified procedure with enhanced uniform sensitivity. Anal Biochem. 1981 Nov 1;117(2):307–310. doi: 10.1016/0003-2697(81)90783-1. [DOI] [PubMed] [Google Scholar]
  25. Owens G. C., Ohad I. Phosphorylation of chlamydomonas reinhardi chloroplast membrane proteins in vivo and in vitro. J Cell Biol. 1982 Jun;93(3):712–718. doi: 10.1083/jcb.93.3.712. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Plumley F. G., Schmidt G. W. Rocket and crossed immunoelectrophoresis of proteins solubilized with sodium dodecyl sulfate. Anal Biochem. 1983 Oct 1;134(1):86–95. doi: 10.1016/0003-2697(83)90267-1. [DOI] [PubMed] [Google Scholar]
  27. Sabatini D. D., Kreibich G., Morimoto T., Adesnik M. Mechanisms for the incorporation of proteins in membranes and organelles. J Cell Biol. 1982 Jan;92(1):1–22. doi: 10.1083/jcb.92.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schmidt G. W., Bartlett S. G., Grossman A. R., Cashmore A. R., Chua N. H. Biosynthetic pathways of two polypeptide subunits of the light-harvesting chlorophyll a/b protein complex. J Cell Biol. 1981 Nov;91(2 Pt 1):468–478. doi: 10.1083/jcb.91.2.468. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schmidt G. W., Matlin K. S., Chua N. H. A rapid procedure for selective enrichment of photosynthetic electron transport mutants. Proc Natl Acad Sci U S A. 1977 Feb;74(2):610–614. doi: 10.1073/pnas.74.2.610. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schmidt G. W., Mishkind M. L. Rapid degradation of unassembled ribulose 1,5-bisphosphate carboxylase small subunits in chloroplasts. Proc Natl Acad Sci U S A. 1983 May;80(9):2632–2636. doi: 10.1073/pnas.80.9.2632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Spreitzer R. J., Mets L. Photosynthesis-deficient Mutants of Chlamydomonas reinhardii with Associated Light-sensitive Phenotypes. Plant Physiol. 1981 Mar;67(3):565–569. doi: 10.1104/pp.67.3.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Walter P., Blobel G. Translocation of proteins across the endoplasmic reticulum III. Signal recognition protein (SRP) causes signal sequence-dependent and site-specific arrest of chain elongation that is released by microsomal membranes. J Cell Biol. 1981 Nov;91(2 Pt 1):557–561. doi: 10.1083/jcb.91.2.557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Willey D. L., Auffret A. D., Gray J. C. Structure and topology of cytochrome f in pea chloroplast membranes. Cell. 1984 Feb;36(2):555–562. doi: 10.1016/0092-8674(84)90248-4. [DOI] [PubMed] [Google Scholar]
  34. Williams J. C., Steiner L. A., Ogden R. C., Simon M. I., Feher G. Primary structure of the M subunit of the reaction center from Rhodopseudomonas sphaeroides. Proc Natl Acad Sci U S A. 1983 Nov;80(21):6505–6509. doi: 10.1073/pnas.80.21.6505. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES