Repression of essential chloroplast genes reveals new signaling pathways and regulatory feedback loops in chlamydomonas

Plant Cell

Volumn 25, Issue 1, 2013, Pages 167-186

  Ramundo, Silvia ^a   Rahire, Michèle ^a   Schaad, Olivier ^a   Rochaix, Jean David ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84874513053     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.103051     Document Type: Article

References (74)

1. Allison, L.A., Simon, L.D., and Maliga, P. (1996). Deletion of rpoB reveals a second distinct transcription system in plastids of higher plants. EMBO J. 15: 2802-2809.
2. Asakura, Y., Galarneau, E., Watkins, K.P., Barkan, A., and van Wijk, K.J. (2012). Chloroplast RH3 DEAD box RNA helicases in maize and Arabidopsis function in splicing of specific group II introns and affect chloroplast ribosome biogenesis. Plant Physiol. 159: 961-974.
3. Aseeva, E., Ossenbühl, F., Sippel, C., Cho, W.K., Stein, B., Eichacker, L.A., Meurer, J., Wanner, G., Westhoff, P., Soll, J., and Vothknecht, U.C. (2007). Vipp1 is required for basic thylakoid membrane formation but not for the assembly of thylakoid protein complexes. Plant Physiol. Biochem. 45: 119-128.
4. Barkan, A. (1988). Proteins encoded by a complex chloroplast transcription unit are each translated from both monocistronic and polycistronic mRNAs. EMBO J. 7: 2637-2644.
5. Boudreau, E., Turmel, M., Goldschmidt-Clermont, M., Rochaix, J.D., Sivan, S., Michaels, A., and Leu, S. (1997). A large open reading frame (orf1995) in the chloroplast DNA of Chlamydomonas reinhardtii encodes an essential protein. Mol. Gen. Genet. 253: 649-653.
6. Blamire, J., Flechtner, V.R., and Sager, R. (1974). Regulation of nuclear DNA replication by thechloroplast in Chlamydomonas. Proc. Natl. Acad. Sci. USA 71: 2867-2871.
7. Boynton, J.E., and Gillham, N.W. (1993). Chloroplast transformation in Chlamydomonas. Methods Enzymol. 217: 510-536.
8. Boynton, J.E., Gillham, N.W., and Chabot, J.F. (1972). Chloroplast ribosome deficient mutants in the green alga Chlamydomonas reinhardi and the question of chloroplast ribosome function. J. Cell Sci. 10: 267-305.
9. Bryant, N., Lloyd, J., Sweeney, C., Myouga, F., and Meinke, D. (2011). Identification of nuclear genes encoding chloroplast-localized proteins required for embryo development in Arabidopsis. Plant Physiol. 155: 1678-1689.
10. Choquet, Y., and Wollman, F.A. (2002). Translational regulations as specific traits of chloroplast gene expression. FEBS Lett. 529: 39-42.
11. Chua, N.H., Blobel, G., Siekevitz, P., and Palade, G.E. (1973). Attachment of chloroplast polysomes to thylakoid membranes in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 70: 1554-1558.
12. Church, G.M., and Gilbert, W. (1984). Genomic sequencing. Proc. Natl. Acad. Sci. USA 81: 1991-1995.
13. Croft, M.T., Lawrence, A.D., Raux-Deery, E., Warren, M.J., and Smith, A.G. (2005). Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438: 90-93.
14. Croft, M.T., Moulin, M., Webb, M.E., and Smith, A.G. (2007). Thiamine biosynthesis in algae is regulated by riboswitches. Proc. Natl. Acad. Sci. USA 104: 20770-20775.
15. Drapier, D., Girard-Bascou, J., and Wollman, F.A. (1992). Evidence for nuclear control of the expression of the atpA and atpB chloroplast genes in Chlamydomonas. Plant Cell 4: 283-295.
16. Drzymalla, C., Schroda, M., and Beck, C.F. (1996). Light-inducible gene HSP70B encodes a chloroplast-localized heat shock protein in Chlamydomonas reinhardtii. Plant Mol. Biol. 31: 1185-1194.
17. Durrant, I. (1990). Light-based detection of biomolecules. Nature 346: 297-298.
18. Erickson, J.M., Rahire, M., Malnoë, P., Girard-Bascou, J., Pierre, Y., Bennoun, P., and Rochaix, J.D. (1986). Lack of the D2 protein in a Chlamydomonas reinhardtii psbD mutant affects photosystem II stability and D1 expression. EMBO J. 5: 1745-1754.
19. Falk, J., Schmidt, A., and Krupinska, K. (1993). Characterization of plastid DNA transcription in ribosome deficient plastids of heatbleached barley leaves. J. Plant Physiol. 141: 176-181.
20. Fan, W.H., Woelfle, M.A., and Mosig, G. (1995). Two copies of a DNA element, 'Wendy', in the chloroplast chromosome of Chlamydomonas reinhardtii between rearranged gene clusters. Plant Mol. Biol. 29: 63-80.
21. Feinberg, A.P., and Vogelstein, B. (1983). A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132: 6-13.
22. Finer, J.J., Vain, P., Jones, M.W., and McMullen, M.D. (1992). Development of the particle inflow gun for DNA delivery to plant cells. Plant Cell Rep. 11: 323-328.
23. Fleischmann, T.T., Scharff, L.B., Alkatib, S., Hasdorf, S., Schöttler, M.A., and Bock, R. (2011). Nonessential plastid-encoded ribosomal proteins in tobacco: A developmental role for plastid translation and implications for reductive genome evolution. Plant Cell 23: 3137-3155.
24. Fong, S.E., and Surzycki, S.J. (1992). Chloroplast RNA polymerase genes of Chlamydomonas reinhardtii exhibit an unusual structure and arrangement. Curr. Genet. 21: 485-497.
25. Gagné, G., and Guertin, M. (1992). The early genetic response to light in the green unicellular alga Chlamydomonas eugametos grown under light/dark cycles involves genes that represent direct responses to light and photosynthesis. Plant Mol. Biol. 18: 429-445.
26. Geiss, G.K., et al. (2008). Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat. Biotechnol. 26: 317-325.
27. Göhre, V., Ossenbühl, F., Crèvecoeur, M., Eichacker, L.A., and Rochaix, J.D. (2006). One of two alb3 proteins is essential for the assembly of the photosystems and for cell survival in Chlamydomonas. Plant Cell 18: 1454-1466.
28. Goldschmidt-Clermont, M. (1991). Transgenic expression of aminoglycoside adenine transferase in the chloroplast: A selectable marker of site-directed transformation of chlamydomonas. Nucleic Acids Res. 19: 4083-4089.
29. Gorman, D.S., and Levine, R.P. (1966). Cytochrome f and plastocyanin: Their sequence in the photoelectric transport chain. Proc. Natl. Acad. Sci. USA 54: 1665-1669.
30. Gray, J.C., Sullivan, J.A., Wang, J.H., Jerome, C.A., and MacLean, D. (2003). Coordination of plastid and nuclear gene expression. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358: 135-144, discussion 144-145.
31. Guertin, M., and Bellemare, G. (1979). Synthesis of chloroplast ribonucleic acid in Chlamydomonas reinhardtii toluene-treated cells. Eur. J. Biochem. 96: 125-129.
32. Hajdukiewicz, P.T., Allison, L.A., and Maliga, P. (1997). The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO J. 16: 4041-4048.
33. Harris, E.H. (1989). The Chlamydomonas Source Book: A Comprehensive Guide to Biology and Laboratory Use. (San Diego, CA: Academic Press).
34. Harris, E.H., Boynton, J.E., and Gillham, N.W. (1974). Chloroplast ribosome biogenesis in Chlamydomonas. Selection and characterization of mutants blocked in ribosome formation. J. Cell Biol. 63: 160-179.
35. Held, W.A., Ballou, B., Mizushima, S., and Nomura, M. (1974). Assembly mapping of 30S ribosomal proteins from Escherichia coli. J. Biol. Chem. 240: 3108-3111.
36. Heo, J.M., et al. (2010). A stress-responsive system for mitochondrial protein degradation. Mol. Cell 40: 465-480.
37. Hess, W.R., Hübschmann, T., and Börner, T. (1994a). Ribosome deficient plastids of albostrians barley: Extreme representatives of non-photosynthetic plastids. Endocytobiosis Cell Res. 10: 65-80.
38. Hess, W.R., Müller, A., Nagy, F., and Börner, T. (1994b). Ribosomedeficient plastids affect transcription of light-induced nuclear genes: Genetic evidence for a plastid-derived signal. Mol. Gen. Genet. 242: 305-312.
39. Huang, C., Wang, S., Chen, L., Lemieux, C., Otis, C., Turmel, M., and Liu, X.Q. (1994). The Chlamydomonas chloroplast clpP gene contains translated large insertion sequences and is essential for cell growth. Mol. Gen. Genet. 244: 151-159.
40. Igloi, G.L., and Kössel, H. (1992). The transcriptional apparatus of chloroplasts. Crit. Rev. Plant Sci. 10: 525-558.
41. Klein, U. (2009). Chloroplast transcription. In The Chlamydomonas Sourcebook, D.B. Stern, ed (Amsterdam, The Netherlands: Elsevier), pp. 893-913.
42. Kroll, D., Meierhoff, K., Bechtold, N., Kinoshita, M., Westphal, S., Vothknecht, U.C., Soll, J., and Westhoff, P. (2001). VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formation. Proc. Natl. Acad. Sci. USA 98: 4238-4242.
43. Kuchka, M.R., Goldschmidt-Clermont, M., van Dillewijn, J., and 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: 869-876.
44. Kuchka, M.R., Mayfield, S.P., and 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: 319-324.
45. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
46. Liu, C., Willmund, F., Whitelegge, J.P., Hawat, S., Knapp, B., Lodha, M., and Schroda, M. (2005). J-domain protein CDJ2 and HSP70B are a plastidic chaperone pair that interacts with vesicleinducing protein in plastids 1. Mol. Biol. Cell 16: 1165-1177.
47. Liu, X.Q., Hosler, J.P., Boynton, J.E., and Gillham, N.W. (1989). mRNAs for two ribosomal proteins are preferentially translated in the chloroplast of Chlamydomonas reinhardtii under conditions of reduced protein synthesis. Plant Mol. Biol. 12: 385-394.
48. Lloyd, J., and Meinke, D. (2012). A comprehensive dataset of genes with a loss-of-function mutant phenotype in Arabidopsis. Plant Physiol. 158: 1115-1129.
49. Majeran, W., Wollman, F.A., and Vallon, O. (2000). Evidence for a role of ClpP in the degradation of the chloroplast cytochrome b(6)f complex. Plant Cell 12: 137-150.
50. Maul, J.E., Lilly, J.W., Cui, L., dePamphilis, C.W., Miller, W., Harris, E.H., and Stern, D.B. (2002). The Chlamydomonas reinhardtii plastid chromosome: Islands of genes in a sea of repeats. Plant Cell 14: 2659-2679.
51. Merchant, S., and Bogorad, L. (1987). Metal ion regulated gene expression: Use of a plastocyanin-less mutant of Chlamydomonas reinhardtii to study the Cu(II)-dependent expression of cytochrome c-552. EMBO J. 6: 2531-2535.
52. Minai, L., Wostrikoff, K., Wollman, F.A., and Choquet, Y. (2006). Chloroplast biogenesis of photosystem II cores involves a series of assembly-controlled steps that regulate translation. Plant Cell 18: 159-175.
53. Nickelsen, J., van Dillewijn, J., Rahire, M., and Rochaix, J.-D. (1994). Determinants for stability of the chloroplast psbD RNA are located within its short leader region in Chlamydomonas reinhardtii. EMBO J. 13: 3182-3191.
54. Nguyen, A.V., Thomas-Hall, S.R., Malnoë, A., Timmins, M., Mussgnug, J.H., Rupprecht, J., Kruse, O., Hankamer, B., and Schenk, P.M. (2008). Transcriptome for photobiological hydrogen production induced by sulfur deprivation in the green alga Chlamydomonas reinhardtii. Eukaryot. Cell 7: 1965-1979.
55. Rochaix, J.D. (1995). Chlamydomonas reinhardtii as the photosynthetic yeast. Annu. Rev. Genet. 29: 209-230.
56. Rochaix, J.-D., Mayfield, S., Goldschmidt-Clermont, and Erickson, J. (1988). Molecular biology of Chlamydomonas. In Plant Molecular Biology: Practical Approach, C.H. Shaw ed (Oxford: IRL Press), pp. 253-275.
57. Nott, A., Jung, H.S., Koussevitzky, S., and Chory, J. (2006). Plastidto-nucleus retrograde signaling. Annu. Rev. Plant Biol. 57: 739-759.
58. Ohad, I., Siekevitz, P., and Palade, G.E. (1967). Biogenesis of chloroplast membranes. II. Plastid differentiation during greening of a dark-grown algal mutant (Chlamydomonas reinhardi). J. Cell Biol. 35: 553-584.
59. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd ed. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
60. Schroda, M., and Vallon, O. (2009). Chaperones and proteases. In The Chlamydomonas Sourcebook, D.B. Stern, ed (Amsterdam, The Netherlands: Elsevier), pp. 671-729.
61. Shimogawara, K., Fujiwara, S., Grossman, A., and Usuda, H. (1998). High-efficiency transformation of Chlamydomonas reinhardtii by electroporation. Genetics 148: 1821-1828.
62. Smith, A.C., and Purton, S. (2002). The transcriptional apparatus of algal plastids. Eur. J. Phycol. 37: 301-311.
63. Sullivan, J.A., and Gray, J.C. (1999). Plastid translation is required for the expression of nuclear photosynthesis genes in the dark and in roots of the pea lip1 mutant. Plant Cell 11: 901-910.
64. Surzycki, R., Cournac, L., Peltier, G., and Rochaix, J.D. (2007). Potential for hydrogen production with inducible chloroplast gene expression in Chlamydomonas. Proc. Natl. Acad. Sci. USA 104: 17548-17553.
65. Susek, R.E., Ausubel, F.M., and Chory, J. (1993). Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74: 787-799.
66. Svab, Z., and Maliga, P. (1993). High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene. Proc. Natl. Acad. Sci. USA 90: 913-917.
67. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3: RESEARCH0034.
68. Walbot, V., and Coe, E.H. (1979). Nuclear gene iojap conditions a programmed change to ribosome-less plastids in Zea mays. Proc. Natl. Acad. Sci. USA 76: 2760-2764.
69. Wolfe, K.H., Morden, C.W., and Palmer, J.D. (1992). Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc. Natl. Acad. Sci. USA 89: 10648-10652.
70. Xu, R., Bingham, S.E., and Webber, A.N. (1993). Increased mRNA accumulation in a psaB frame-shift mutant of Chlamydomonas reinhardtii suggests a role for translation in psaB mRNA stability. Plant Mol. Biol. 22: 465-474.
71. Young, F.S., and Furano, A.V. (1981). Regulation of the synthesis of E. coli elongation factor Tu. Cell 24: 695-706.
72. Zerges, W., and Rochaix, J.D. (1998). Low density membranes are associated with RNA-binding proteins and thylakoids in the chloroplast of Chlamydomonas reinhardtii. J. Cell Biol. 140: 101-110.
73. Zhao, Q., Wang, J., Levichkin, I.V., Stasinopoulos, S., Ryan, M.T., and Hoogenraad, N.J. (2002). A mitochondrial specific stress response in mammalian cells. EMBO J. 21: 4411-4419.
74. Zicker, A.A., Kadakia, C.S., and Herrin, D.L. (2007). Distinct roles for the 59 and 39 untranslated regions in the degradation and accumulation of chloroplast tufA mRNA: Identification of an early intermediate in the in vivo degradation pathway. Plant Mol. Biol. 63: 689-702.