Advertisement

Molecular and General Genetics MGG

, Volume 231, Issue 3, pp 449–459 | Cite as

Accumulation of chloroplast psbB RNA requires a nuclear factor in Chlamydomonas reinhardtii

  • Caroline Monod
  • Michel Goldschmidt-Clermont
  • Jean-David Rochaix
Article

Summary

We have isolated and characterized a nuclear mutant, 222E, in Chlamydomonas reinhardtii, which is defective in photosystem II (PSII). Polypeptide P5, the product of psbB, is not produced in this mutant, leading to a destabilization of other PSII components. The mutant specifically fails to accumulate psbB transcripts and displays an altered transcription pattern downstream of psbB. Pulse-labelling experiments suggest that mRNA stability and/or processing are affected by the alteration of a nuclear gene product in this mutant. We show that the C. reinhardtii psbB gene is co-transcribed with a small open reading frame that is highly conserved in location and amino acid sequence in land plants. The 5′ and 3′ termini of the psbB transcript have been mapped to 35 bases upstream of the initiation codon and approximately 600 bases downstream of the stop codon. The 3′ flanking region contains two potential stem-loops, of which the larger (with an estimated free energy of −46 kcal) is near the 3′ terminus of the transcript.

Key words

Chloroplast genes Chloroplast mRNA stability RNA 3′ inverted repeat Photosynthetic mutant 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adams CC, Stern DB (1990) Control of mRNA stability in chloroplasts by 3′ inverted repeats: effects of stem and loop mutations on degradation of psbA mRNA in vitro. Nucleic Acids Res 18:6003–6010Google Scholar
  2. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (eds) (1990) Current protocols in molecular biology. Greene Publishing Associates and Wiley-Interscience, New YorkGoogle Scholar
  3. Bennoun P, Delepelaire P (1982) Isolation of photosynthesis mutants in Chlamydomonas. In: Edelman M, Hallick RB, Chua NH (eds) Methods in chloroplast molecular biology. Elsevier Biomedical Press, Amsterdam, pp 25–38Google Scholar
  4. Bennoun P, Spierer-Herz M, Erickson J, Girard-Bascou J, Pierre Y, Delosme M, Rochaix J-D (1986) Characterization of photosystem II mutants of tChlamydomonas reinhardtii lacking the psbA gene. Plant Mol Biol 6:151–160Google Scholar
  5. Bonham-Smith PC, Bourque DP (1989) Translation of chloroplast-encoded mRNA: potential initiation and termination signals. Nucleic Acids Res 17:2057–2080Google Scholar
  6. Bukharov AA, Kolosov VL, Zolotarev AS (1988) Nucleotide sequence of rye chloroplast DNA fragment encoding psbB and psbH genes. Nucleic Acids Res 16:8737Google Scholar
  7. Deng XW, Gruissem W (1987) Control of plastid gene expression during development: the limited role of transcriptional regulation. Cell 49:379–387Google Scholar
  8. de Vitry C, Olive J, Drapier D, Recouvreur M, Wellman FA (1989) Posttranslational events leading to the assembly of photosystem II protein complex: a study using photosynthesis mutants from Chlamydomonas reinhardtii. J Cell Biol 109:991–1006Google Scholar
  9. Dron M, Rahire M, Rochaix J-D (1982) Sequence of the chloroplast DNA region of Chlamydomonas reinhardtii containing the gene of the large subunit of ribulose bisphosphate carboxylase and parts of its flanking genes. J Mol Biol 162:775–793Google Scholar
  10. Erickson JM, Rochaix J-D (1991) The molecular biology of photosystem II. In: Barber J (ed) Topics in photosynthesis, vol 10. Elsevier Science Publishers, AmsterdamGoogle Scholar
  11. Erickson JM, Rahire M, Rochaix J-D (1984) Chlamydomonas reinhardtii gene for the 32000 mol. wt. protein of photosystem II contains four large introns and is located entirely within the chloroplast inverted repeat. EMBO J 3:2753–2762Google Scholar
  12. Erickson JM, Rahire M, Malnoë P, Girard-Bascou J, Pierre Y, Bennoun P, Rochaix J-D (1986) Lack of the D2 protein in a Chlamydomonas reinhardtii psbD mutant affects photosystem 11 stability and D1 expression. EMBO J 5:1745–1754Google Scholar
  13. Fukuzawa H, Kohchi T, Sano T, Shirai H, Umesono K, Inokuchi H, Ozeki H, Ohyama K (1988) Structure and organization of Marchantia polymorpha chloroplast genome III. Gene organization of the large single copy region from rbcL to trnI(CAU). J Mol Biol 203:333–351Google Scholar
  14. Goldschmidt-Clermont M (1986) The two genes for the small subunit of RuBP carboxylase/oxygenase are closely linked in Chlamydomonas reinhardtii. Plant Mol Biol 6:13–21Google Scholar
  15. Gorman DS, Levine RP (1965) Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 54:1665–1669Google Scholar
  16. Gruissem W (1989) Chloroplast gene expression: how plants turn their plastids on. Cell 56:161–170Google Scholar
  17. Gruissem W, Barkan A, Deng XW, Stern D (1988) Transcriptional and post-transcriptional control of plastid mRNA levels in higher plants. Trends Genet 4:258–263Google Scholar
  18. Guertin M, Bellemare G (1979) Synthesis of chloroplast ribonucleic acid in Chlamydomonas reinhardtii toluene-treated cells. Eur J Biochem 96:125–129Google Scholar
  19. Harris EH (1989) The Chlamydomonas sourcebook. A comprehensive guide to biology and laboratory use. Academic Press, San Diego, USAGoogle Scholar
  20. Harris EH, Boynton JE, Gillham NW (1987) Chlamydomonas reinhardtii. In: O'Brien SJ (ed) Genetic maps 1987. A compilation of linkage and restriction maps of genetically studied organisms, vol 4. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  21. Hanley-Bowdoin L, Chua NH (1987) Chloroplast promoters. Trends Biochem Sci 12:67–70Google Scholar
  22. Hawley DK, McClure WR (1983) Compilation and analysis of Escherichia coli promoter DNA sequences. Nucleic Acids Res 11:2237–2255Google Scholar
  23. Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun CR, Meng BY, Li YQ, Kanno A, Nishizawa Y, Hirai A, Shinozaki K, Sugiura M (1989) The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet 217:185–194Google Scholar
  24. Hird SM, Webber AN, Wilson RJ, Dyer TA, Gray JC (1991) Differential expression of the psbB and psbH genes encoding the 47 kDa chlorophyll a-protein and the 10 kDa phosphoprotein of photosystem II during chloroplast development in wheat. Curr Genet 19:199–206Google Scholar
  25. Jensen KH, Herrin DL, Plumley FG, Schmidt GW (1986) Biogenesis of photosystem II complexes: transcriptional, translational, and posttranslational regulation. J Cell Biol 103:1315–1325Google Scholar
  26. Kates JR, Jones RE (1964) The control of gametic differentiation in liquid cultures of Chlamydomonas. J Cell Comp Physiol 63:157–164Google Scholar
  27. Keller M, Weil JH, Krishnan Nair CK (1989) Nucleotide sequence of the psbB gene of Euglena gracilis. Plant Mol Biol 13:723–725Google Scholar
  28. Kuchka MR, Mayfield SP, Rochaix J-D (1988) Nuclear mutations specifically affect the synthesis and/or degradation of the chloroplast-encoded D2 polypeptide of photosystem II in Chlamydomonas reinhardtii. EMBO J 7:319–324Google Scholar
  29. Kuchka MR, Goldschmidt-Clermont M, van Dillewijn J, Rochaix J-D (1989) Mutation at the Chlamydomonas nuclear NAC2 locus specifically affects stability of the chloroplast psbD transcript encoding polypeptide D2 of PS II. Cell 58:869–876Google Scholar
  30. Levine RP, Ebersold WT (1960) The genetics and cytology of Chlamydomonas. Annu Rev Microbiol 14:197–216Google Scholar
  31. Mayfield SP, Bennoun P, Rochaix J-D (1987) Expression of the nuclear encoded OEE1 protein is required for oxygen evolution and stability of photosystem II particles in Chlamydomonas reinhardtii. EMBO J 6:313–318Google Scholar
  32. Morris J, Herrmann RG (1984) Nucleotide sequence of the gene for the P680 chlorophyll a apoprotein of the photosystem II reaction center from spinach. Nucleic Acids Res 12:2837–2850Google Scholar
  33. Mullet JE, Klein RR (1987) Transcription and RNA stability are important determinants of higher plant chloroplast RNA levels. EMBO J 6:1571–1579Google Scholar
  34. Nickelsen J, Link G (1989) Interaction of a 3′ RNA region of the mustard trnK gene with chloroplast proteins. Nucleic Acids Res 17:9637–9648Google Scholar
  35. Nickelsen J, Link G (1991) RNA-protein interactions at transcript 3′ ends and evidence for trnK-psbA cotranscription in mustard chloroplasts. Mol Gen Genet 228:89–96Google Scholar
  36. Offermann-Steinhard K, Herrmann RG (1990) Nucleotide sequences of psbB and psbH, the plastid encoded genes for CP47 and the 10 kDa phosphoprotein of photosystem II in Oenothera hookeri and argillicola. Nucleic Acids Res 18:6452Google Scholar
  37. Reverdatto SV, Andreeva AV, Buryakova AA, Chakhmakhcheva OG, Efimov VA (1989) Nucleotide sequence of the 5.2 kbp barley chloroplast DNA fragment, containing psbB-psbH-petB-petD gene cluster. Nucleic Acids Res 17:2859–2860Google Scholar
  38. Rochaix J-D (1981) Organization, function and expression of the chloroplast DNA of Chlamydomonas reinhardtii. Experientia 37:323–440Google Scholar
  39. Rochaix J-D, Erickson J (1988) Function and assembly of photosystem II: genetic and molecular analysis. Trends Biochem Sci 13:56–59Google Scholar
  40. Rochaix J-D, Mayfield S, Goldschmidt-Clermont M, Erickson J (1988) Molecular biology of Chlamydomonas. In: Shaw CH (ed) Plant molecular biology, a practical approach. IRL Press, Oxford, pp 253–275Google Scholar
  41. Rochaix J-D, Kuchka M, Mayfield S, Schirmer-Rahire M, Girard-Bascou J, Bennoun P (1989) Nuclear and chloroplast mutations affect the synthesis or stability of the chloroplast psbC gene product in Chlamydomonas reinhardtii. EMBO J 8:1013–1021Google Scholar
  42. Rock CD, Barkan A, Taylor WC (1987) The maize plastid psbB-psbF-petB-petD gene cluster: spliced and unspliced petB and petD RNAs encode alternative products. Curr Genet 12:69–77Google Scholar
  43. Schmidt GW, Matlin KS, Chua NH (1977) A rapid procedure for selective enrichment of photosynthetic electron transport mutants. Proc Natl Acad Sci USA 74:610–614Google Scholar
  44. Schuster G, Gruissem W (1991) Chloroplast mRNA 3′ end processing requires a nuclear-encoded RNA-binding protein. EMBO J 10:1493–1502Google Scholar
  45. Shepherd HS, Boynton JE, Gillham NW (1979) Mutations in nine chloroplast loci of Chlamydomonas affecting different photosynthetic functions. Proc Natl Acad Sci USA 76:1353–1357Google Scholar
  46. Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043–2049Google Scholar
  47. Sieburth LE, Berry-Lowe S, Schmidt GW (1991) Chloroplast RNA stability in Chlamydomonas: rapid degradation of psbB and psbC transcripts in two nuclear mutants. Plant Cell 3:175–189Google Scholar
  48. Stern DB, Gruissem W (1987) Control of plastid gene expression: 3′ inverted repeats act as mRNA processing and stabilizing elements, but do not terminate transcription. Cell 51:1145–1157Google Scholar
  49. Stern DB, Gruissem W (1989) Chloroplast mRNA 3′ end maturation is biochemically distinct from prokaryotic mRNA processing. Plant Mol Biol 13:615–625Google Scholar
  50. Stern DB, Jones H, Gruissem W (1989) Function of plastid mRNA 3′ inverted repeats. J Biol Chem 264:18742–18750Google Scholar
  51. Stern DB, Radwanski ER, Kindle KL (1991) A 3′ stem/loop structure of the Chlamydomonas chloroplast atpB gene regulates mRNA accumulation in vivo. Plant Cell 3:285–297Google Scholar
  52. Tinoco I Jr, Borer PN, Dengler B, Levin MD, Uhlenbeck OC, Crothers DM, Bralla J (1973) Improved estimation of secondary structure in ribonucleic acids. Nature New Biol 246:40–41Google Scholar
  53. Vermaas WFJ, Williams JGK, Rutherford AW, Mathis P, Arntzen CJ (1986) Genetically engineered mutant of the cyanobacterium Synechocystis 6803 lacks the photosystem II chlorophyll-binding protein CP-47. Proc Natl Acad Sci USA 83:9474–9477Google Scholar
  54. Vermaas WFJ, Williams JGK, Arntzen CJ (1987) Sequencing and modification of psbB, the gene encoding the CP-47 protein of photosystem II, in cyanobacterium Synechocystis 6803. Plant Mol Biol 8:317–326Google Scholar
  55. Woessner JP, Masson A, Harris EH, Bennoun P, Gillham NW, Boynton JE (1984) Molecular and genetic analysis of the chloroplast ATPase of Chlamydomonas. Plant Mol Biol 3:177–190Google Scholar

Copyright information

© Springer-Verlag 1992

Authors and Affiliations

  • Caroline Monod
    • 1
  • Michel Goldschmidt-Clermont
    • 1
  • Jean-David Rochaix
    • 1
  1. 1.Departments of Molecular Biology and Plant BiologyUniversity of GenevaGeneva 4Switzerland

Personalised recommendations