The nuclear factor HCF145 affects chloroplast psaA-psaB-rps14 transcript abundance in Arabidopsis thaliana

Plant Journal

Volumn 38, Issue 5, 2004, Pages 740-753

  Lezhneva, Lina ^a   Meurer, Jörg ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Arabidopsis hcf mutants; Chloroplast biogenesis; Photosystem I; Plastid mRNA stability; psaA psaB rps14 operon; Quantitative real time RT PCR

Indexed keywords

CHLOROPHYLL; CHROMOSOMES; DEFECTS; ENZYME KINETICS; FLUORESCENCE; MUTAGENESIS; REACTION KINETICS; SPECTROSCOPIC ANALYSIS;

MUTANTS; PHOTOSYSTEM;

PLANTS (BOTANY);

ARABIDOPSIS PROTEIN; BACTERIAL PROTEIN; CHLORAMPHENICOL; HCF145 PROTEIN, ARABIDOPSIS; MESSENGER RNA; NUCLEAR PROTEIN; PHOTOSYSTEM I, PSAB SUBUNIT; PLANT RNA; PRIMER DNA; PROTEIN SYNTHESIS INHIBITOR; PSI A PROTEIN, SYNECHOCOCCUS; PSI-A PROTEIN, SYNECHOCOCCUS; RIBOSOME RNA;

ARABIDOPSIS; ARTICLE; CHLOROPLAST; DRUG EFFECT; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NUCLEOTIDE SEQUENCE; PHOTOSYSTEM I; PLANT GROWTH; PLANT LEAF; PROTEIN SYNTHESIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BACTERIAL PROTEINS; BASE SEQUENCE; CHLORAMPHENICOL; CHLOROPLASTS; DNA PRIMERS; HYPOCOTYL; NUCLEAR PROTEINS; PHOTOSYSTEM I PROTEIN COMPLEX; PLANT LEAVES; PROTEIN BIOSYNTHESIS; PROTEIN SYNTHESIS INHIBITORS; RNA, MESSENGER; RNA, PLANT; RNA, RIBOSOMAL; TRANSCRIPTION, GENETIC;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); EMBRYOPHYTA; SYNECHOCOCCUS;

EID: 2542590978     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2004.02081.x     Document Type: Article

References (87)

1. Alexander, C., Faber, N. and Klaff, P. (1998) Characterization of protein-binding to the spinach chloroplast psbA mRNA 5′ untranslated region. Nucl. Acids Res. 26, 2265-2272.
2. Allison, L.A. (2000) The role of sigma factors in plastid transcription. Biochimie, 82, 537-548.
3. Baginsky, S., Shteiman-Kotler, A., Liveanu, V., Yehudai-Resheff, S., Bellaoui, M., Settlage, R.E., Shabanowitz, J., Hunt, D.F., Schuster, G. and Gruissem, W. (2001) Chloroplast PNPase exists as a homo-multimer enzyme complex that is distinct from the Escherichia coli degradosome. RNA, 7, 1464-1475.
4. Barkan, A. (1993) Nuclear mutants of maize with defects in chloroplast polysome assembly have altered chloroplast RNA metabolism. Plant Cell, 5, 389-402.
5. Barkan, A. and Goldschmidt-Clermont, M. (2000) Participation of nuclear genes in chloroplast gene expression. Biochimie, 82, 559-572.
6. Baumgartner, B.J., Rapp, J.C. and Mullet, J.E. (1993) Plastid genes encoding the transcription/translation apparatus are differentially transcribed early in barley (Hordeum vulgare) chloroplast development. Evidence for selective stabilization of psbA mRNA. Plant Physiol. 101, 781-791.
7. Bechhofer, D.H. (1993) 5′ mRNA stabilizers. In Control of Messenger RNA Stability (Belasco, J. and Brawerman, G., eds). New York: Academic Press, pp. 31-52.
8. Ben-Shem, A., Frolow, F. and Nelson, N. (2003) Crystal structure of plant photosystem I. Nature, 426, 630-635.
9. Blum, H., Beier, H. and Gross, H.J. (1987) Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis, 8, 93-99.
10. Boudreau, E., Takahashi, Y., Lemieux, C., Turmel, M. and Rochaix, J.D. (1997) The chloroplast ycf3 and ycf4 open reading frames of Chlamydomonas reinhardtii are required for the accumulation of the photosystem I complex. EMBO J. 16, 6095-6104.
11. Boudreau, E., Nickelsen, J., Lemaire, S.D., Ossenbühl, F. and Rochaix, J.D. (2000) The Nac2 gene of Chlamydomonas encodes a chloroplast TPR-like protein involved in psbD mRNA stability. EMBO J. 19, 3366-3376.
12. Chitnis, P.R. (2001) Photosystem I: function and physiology. Annu. Rev. Plant Physiol. Plant. Mol. Biol. 52, 593-626.
13. Culver, G.M. (2003) Assembly of the 30S ribosomal subunit. Biopolymers, 68, 234-249.
14. Dal Bosco, C., Lezhneva, L., Biehl, A., Leister, D., Strotmann, H., Wanner, G. and Meurer, J. (2004) Inactivation of the chloroplast ATP synthase gamma subunit results in high non-photochemical fluorescence quenching and altered nuclear gene expression in Arabidopsis thaliana. J. Biol. Chem. 279, 1060-1069.
15. Deng, X.W., Tonkyn, J.C., Peter, G.F., Thornber, J.P. and Gruissem, W. (1989) Post-transcriptional control of plastid mRNA accumulation during adaptation of chloroplasts to different light quality environments. Plant Cell, 1, 645-654.
16. Drager, R.G., Girard-Bascou, J., Choquet, Y., Kindle, K.L. and Stern, D.B. (1998) In vivo evidence for 5′→3′ exoribonuclease degradation of an unstable chloroplast mRNA. Plant J. 13, 85-96.
17. Drager, R.G., Higgs, D.C., Kindle, K.L. and Stern, D.B. (1999) 5′ to 3′ exoribonucleolytic activity is a normal component of chloroplast mRNA decay pathways. Plant J. 19, 521-531.
18. Drapier, D., Girard-Bascou, J., Stern, D.B. and Wollman, F.A. (2002) A dominant nuclear mutation in Chlamydomonas identifies a factor controlling chloroplast mRNA stability by acting on the coding region of the atpA transcript. Plant J. 31, 687-697.
19. Dreyfus, M. and Régnier, P. (2002) The poly(A) tail of mRNAs: bodyguard in eukaryotes, scavenger in bacteria. Cell, 111, 611-613.
20. Esposito, D., Higgs, D.C., Drager, R.G., Stern, D.B. and Girard-Bascou, J. (2001) A nucleus-encoded supressor defines a new factor which can promote petD mRNA stability in the chloroplast of Chlamydomonas reinhardtii. Curr. Genet. 39, 40-48.
21. Felder, S., Meierhoff, K., Sane, A.P., Meurer, J., Driemel, C., Plücken, H., Klaff, P., Stein, B., Bechtold, N. and Westhoff, P. (2001) The nucleus-encoded HCF107 gene of Arabidopsis provides a link between intercistronic RNA processing and the accumulation of translation-competent psbH transcripts in chloroplasts. Plant Cell, 13, 2127-2141.
22. Feldmann, K.A. (1991) T-DNA insertion mutagenesis in Arabidopsis: mutational spectrum. Plant J. 1, 71-82.
23. Girard-Bascou, J., Choquet, Y., Schneider, M., Delosme, M. and Dron, M. (1987) Characterization of a chloroplast mutation in the psaA2 gene of Chlamydomonas reinhardtii. Curr. Genet. 12, 489-495.
24. Glick, R.E., McCauley, S.W., Gruissem, W. and Melis, A. (1986) Light quality regulates expression of chloroplast genes and assembly of photosynthetic membrane complexes. Proc. Natl. Acad. Sci. USA, 83, 4287-4291.
25. Gruissem, W. (1989) Chloroplast gene expression: how plants turn their plastids on. Cell, 56, 161-170.
26. Grunberg-Manago, M. (1999) Messenger RNA stability and its role in control of gene expression in bacteria and phages. Annu. Rev. Genet. 33, 193-227.
27. Gutiérrez, R.A., MacIntosh, G.C. and Green, P.J. (1999) Current perspectives on mRNA stability in plants: multiple levels and mechanisms of control. Trends Plant Sci. 4, 429-438.
28. Hayes, R., Kudla, J. and Gruissem, W. (1999) Degrading chloroplast mRNA: the role of polyadenylation. Trends Biochem. Sci. 24, 199-202.
29. Hedtke, B., Legen, J., Weihe, A., Herrmann, R.G. and Börner, T. (2002) Six active phage-type RNA polymerase genes in Nicotiana tabacum. Plant J. 30, 625-637.
30. Herrmann, R.G. and Westhoff, P. (2001) Thylakoid biogenesis and dynamics: the result of a complex phylogenetic puzzle. In Regulation of Photosynthesis (Aro, E.-M. and Andersson, B., eds). Dordrecht: Kluwer Academic Publishers, pp. 1-28.
31. Hicks, A., Drager, R.G., Higgs, D.C. and Stern, D.B. (2002) An mRNA 3′ processing site targets downstream sequences for rapid degradation in Chlamydomonas chloroplasts. J. Biol. Chem. 277, 3325-3333.
32. Hihara, Y. and Sonoike, K. (2001) Regulation, inhibition and protection of photosystem I. In Regulation of Photosynthesis (Aro, E.-M. and Andersson, B., eds). Dordrecht: Kluwer Academic Publishers, pp. 507-531.
33. Horlitz, M. and Klaff, P. (2000) Gene-specific trans-regulatory functions of magnesium for chloroplast mRNA stability in higher plants. J. Biol. Chem. 275, 35638-35645.
34. Jansson, S., Andersen, B. and Scheller, H.V. (1996) Nearest-neighbor analysis of higher-plant photosystem I holocomplex. Plant Physiol. 112, 409-420.
35. Kaberdin, V.R., Miczak, A., Jakobsen, J.S., Lin-Chao, S., McDowall, K.J. and von Gabain, A. (1998) The endoribonucleolytic N-terminal half of Escherichia coli RNase E is evolutionary conserved in Synechocystis sp. and other bacteria but not the C-terminal half, which is sufficient for degradosome assembly. Proc. Natl. Acad. Sci. USA, 29, 11637-11642.
36. Kawaguchi, H., Fukuda, I., Shiina, T. and Toyoshima, Y. (1992) Dynamical behavior of psb gene transcripts in greening wheat seedlings. Part I. Time course of accumulation of the psbA through psbN gene transcripts during light-induced greening. Plant Mol. Biol. 20, 695-704.
37. Kim, M., Christopher, D.A. and Mullet, J.E. (1993) Direct evidence for selective modulation of psbA, rpoA, rbcL and 16S RNA stability during barley chloroplast development. Plant Mol. Biol. 22, 447-463.
38. Klaff, P. (1995) mRNA decay in spinach chloroplasts: psbA mRNA degradation is initiated by endonucleolytic cleavages within the coding region. Nucl. Acids Res. 23, 4885-4892.
39. Klaff, P. and Gruissem, W. (1991) Changes in chloroplast mRNA stability during leaf development. Plant Cell, 3, 517-530.
40. Kubicki, A., Steinmüller, K. and Westhoff, P. (1994) Differential transcription of plastome-encoded genes in the mesophyll and bundle-sheath chloroplasts of the monocotyledonous NADP-malic enzyme-type C4 plants maize and Sorghum. Plant Mol. Biol. 25, 669-679.
41. Kushner, S.R. (2002) mRNA decay in Escherichia coli comes of age. J. Bacteriol. 184, 4658-4665.
42. Kushnir, S., Babiychuk, E., Bannikova, M., Momot, V., Komarnitsky, I., Cherep, N. and Gleba, Y. (1991) Nucleo-cytoplasmic incompatibility in cybrid plants possessing an Atropa genome and a Nicotiana plastome. Mol. Gen. Genet. 225, 225-230.
43. Lee, H., Bingham, S.E. and Webber, A.N. (1996) Function of 3′ non-coding sequences and stop codon usage in expression of the chloroplast psaB gene in Chlamydomonas reinhardtii. Plant Mol. Biol. 31, 337-354.
44. Legen, J., Misera, S., Herrmann, R.G. and Meurer, J. (2001) Map positions of 69 Arabidopsis thaliana genes of all known nuclear encoded constituent polypeptides and various regulatory factors of the photosynthetic membrane: a case study. DNA Res. 8, 53-60.
45. Legen, J., Kemp, S., Krause, K., Profanter, B., Herrmann, R.G. and Maier, R.M. (2002) Comparative analysis of plastid transcription profiles of entire plastid chromosomes from tobacco attributed to wild-type and PEP-deficient transcription machineries. Plant J. 31, 171-188.
46. Lezhneva, L., Amann, K. and Meurer, J. (2004) The universally conserved HCF101 protein is involved in assembly of [4Fe-4S]-cluster-containing complexes in Arabidopsis thaliana chloroplasts. Plant J. 37, 174-185.
47. Meurer, J., Berger, A. and Westhoff, P. (1996a) A nuclear mutant of Arabidopsis with impaired stability on distinct transcripts of the plastid psbB, psbD/C, ndhH, and ndhC operons. Plant Cell, 8, 1193-1207.
48. Meurer, J., Meierhoff, K. and Westhoff, P. (1996b) Isolation of high-chlorophyll-fluorescence mutants of Arabidopsis thaliana and their characterisation by spectroscopy, immunoblotting and northern hybridisation. Planta, 198, 385-396.
49. Meurer, J., Lezhneva, L., Amann, K., Godel, M., Bezhani, S., Sherameti, I. and Oelmüller, R. (2002) A peptide chain release factor 2 affects the stability of UGA-containing transcripts in Arabidopsis chloroplasts. Plant Cell, 14, 3255-3269.
50. Monde, R.A., Schuster, G. and Stern, D.B. (2000) Processing and degradation of chloroplast mRNA. Biochimie, 82, 573-582.
51. Mullet, J.E. (1993) Dynamic regulation of chloroplast transcription. Plant Physiol. 103, 309-313.
52. Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
53. Nickelsen, J. (1999) Transcripts containing the 5′ untranslated regions of the plastid genes psbA and psbB from higher plants are unstable in Chlamydomonas reinhardtii chloroplasts. Mol. Gen. Genet. 262, 768-771.
54. Nickelsen, J. (2000) Mutations at three different nuclear loci of Chlamydomonas suppress a defect in chloroplast psbD mRNA accumulation. Curr. Genet. 37, 136-142.
55. Nickelsen, J. (2003) Chloroplast RNA-binding proteins. Curr. Genet. 43, 392-399.
56. 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.
57. Nickelsen, J., Fleischmann, M., Boudreau, E., Rahire, M. and Rochaix, J.D. (1999) Identification of cis-acting RNA leader elements required for chloroplast psbD gene expression in Chlamydomonas. Plant Cell, 11, 957-970.
58. 63 of barley (Hordeum vulgare) contains low amounts of active but unstable photosystem I. Physiol. Plant. 98, 637-644.
59. Nierhaus, K.H. and Wittmann, H.G. (1980) Ribosomal function and its inhibition by antibiotics in prokaryotes. Naturwissenschaften, 67, 234-250.
60. Ossenbühl, F. and Nickelsen, J. (2000) Cis- and trans-acting determinants for translation of psbD mRNA in Chlamydomonas reinhardtii. Mol. Cell Biol. 20, 8134-8142.
61. Pfannschmidt, T., Nilsson, A. and Allen, J.F. (1999) Photosynthetic control of chloroplast gene expression. Nature, 397, 625-628.
62. Plücken, H., Müller, B., Grohmann, D., Westhoff, P. and Eichacker, L.A. (2002) The HCF136 protein is essential for assembly of the photosystem II reaction center in Arabidopsis thaliana. FEBS Lett. 532, 85-90.
63. Rapp, J.C., Baumgartner, B.J. and Mullet J. (1992) Quantitative analysis of transcription and RNA levels of 15 barley chloroplast genes. Transcription rates and mRNA levels vary over 300-fold; predicted mRNA stabilities vary 30-fold. J. Biol. Chem. 267, 21404-21411.
64. Régnier, P. and Arraiano, C.M. (2000) Degradation of mRNA in bacteria: emergence of ubiquitous features. Bioessays, 22, 235-244.
65. Rochaix, J.D. (2001) Post-transcriptional control of chloroplast gene expression. From RNA to photosynthetic complex. Plant Physiol. 125, 142-144.
66. Salvador, M.L. and Klein, U. (1999) The redox state regulates RNA degradation in the chloroplast of Chlamydomonas reinhardtii. Plant Physiol. 121, 1367-1374.
67. Salvador, M.L., Klein, U. and Bogorad, L. (1993) Light-regulated and endogenous fluctuations of chloroplast transcript levels in Chlamydomonas. Regulation by transcription and RNA degradation. Plant J. 3, 213-219.
68. Schuster, G. and Bock, R. (2001) Editing, polyadenylation and degradation of mRNA in the chloroplast. In Regulation of Photosynthesis (Aro, E.-M. and Andersson, B., eds). Dordrecht: Kluwer Academic Publishers, pp. 121-136.
69. Schwabe, T.M. and Kruip, J. (2000) Biogenesis and assembly of photosystem I. Indian J. Biochem. Biophys. 37, 351-359.
70. Selinger, D.W., Saxena, R.M., Cheung, K.J., Church, G.M. and Rosenow, C. (2003) Global RNA half-life analysis in Escherichia coli reveals positional patterns of transcript degradation. Genome Res. 13, 216-223.
71. Shiina, T., Allison, L. and Maliga, P. (1998) rbcL transcript levels in tobacco plastids are independent of light: reduced dark transcription rate is compensated by increased mRNA stability. Plant Cell, 10, 1713-1722.
72. Singh, M., Boutanaev, A., Zucchi, P. and Bogorad, L. (2001) Gene elements that affect the longevity of rbcL sequence-containing transcripts in Chlamydomonas reinhardtii chloroplasts. Proc. Natl. Acad. Sci. USA, 98, 2289-2294.
73. Smart, L.B. and McIntosh, L. (1993) Genetic inactivation of the psaB gene in Synechocystis sp. PCC 6803 disrupts assembly of photosystem I. Plant Mol. Biol. 21, 177-180.
74. Smart, L.B., Anderson, S.L. and McIntosh, L. (1991) Targeted genetic inactivation of the photosystem I reaction center in the cyanobacterium Synechocystis sp. PCC 6803. EMBO J. 10, 3289-3296.
75. Stubbe, W. (1989) Oenothera - an ideal system for studying the interaction of genome and plastome. Plant Mol. Biol. Rep. 7, 245-257.
76. Sugita, M. and Sugiura, M. (1996) Regulation of gene expression in chloroplasts of higher plants. Plant Mol. Biol. 32, 315-326.
77. Summer, H., Pfannschmidt, T. and Link, G. (2000) Transcripts and sequence elements suggest differential promoter usage within the ycf3-psaAB gene cluster on mustard (Sinapis alba L.) chloroplast DNA. Curr. Genet. 37, 45-52.
78. Tanaka, K., Oikawa, K., Ohta, N., Kuroiwa, H., Kuroiwa, T. and Takahashi, H. (1996) Nuclear encoding of a chloroplast RNA polymerase sigma subunit in a red alga. Science, 272, 1932-1935.
79. Thomas, E.J. and Ortiz, W. (1995) Loss of chloroplast transcripts for proteins associated with photosystem II: an early event during heat-bleaching in Euglena gracilis. Plant Mol. Biol. 27, 317-325.
80. Vaistij, F.E., Boudreau, E., Lemaire, S.D., Goldschmidt-Clermont, M. and Rochaix, J.D. (2000a) Characterization of Mbb1, a nucleus-encoded tetratricopeptide-like repeat protein required for expression of the chloroplast psbB/psbT/psbH gene cluster in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA, 97, 14813-14818.
81. Vaistij, F.E., Goldschmidt-Clermont, M., Wostrikoff, K. and Rochaix, J.D. (2000b) Stability determinants in the chloroplast psbB/T/H mRNAs of Chlamydomonas reinhardtii. Plant J. 21, 469-482.
82. Wimberly, B.T., Brodersen, D.E., Clemons, W.M., Jr, Morgan-Warren, R.J., Carter, A.P., Vonrhein, C., Hartsch, T. and Ramakrishnan, V. (2000) Structure of the 30S ribosomal subunit. Nature, 407, 327-339.
83. Wittwer, C.T., Herrmann, M.G., Moss, A.A. and Rasmussen, R.P. (1997a) Continuous fluorescence monitoring of rapid cycle DNA amplification. Biotechniques, 22, 130-131, 134-138.
84. Wittwer, C.T., Ririe, K.M., Andrew, R.V., David, D.A., Gundry, R.A. and Balis, U.J. (1997b) The LightCycler: a microvolume multi-sample fluorimeter with rapid temperature control. Biotechniques, 22, 176-181.
85. Yamaguchi, K., von Knoblauch, K. and Subramanian, A.R. (2000) The plastid ribosomal proteins. Identification of all the proteins in the 30S subunit of an organelle ribosome (chloroplast). J. Biol. Chem. 275, 28455-28465.
86. Yang, J., Schuster, G. and Stern, D.B. (1996) CSP41, a sequence-specific chloroplast mRNA binding protein, is an endoribonuclease. Plant Cell, 8, 1409-1420.
87. Zuo, Y. and Deutscher, M.P. (2001) Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. Nucl. Acids Res. 29, 1017-1026.