Plastid sigma factors: Their individual functions and regulation in transcription

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1847, Issue 9, 2015, Pages 770-778

  Chi, Wei ^a   He, Baoye ^a   Mao, Juan ^a   Jiang, Jingjing ^a   Zhang, Lixin ^a  

^a INSTITUTE OF BOTANY   (China)

Author keywords

Abbreviations ALA aminolevulinic acid; BLRP blue light responsive psbD promoter; CK2 casein kinase 2; CR conserved region; CSK chloroplast sensor kinase; MEcPP methylerythritol cyclodiphosphate; NEP phage type RNA polymerase; PAP ' phosphoadenosine 5' phosphate; PEP plastid encoded RNA polymerase; PhANG photosynthesis associated nuclear gene; ppGpp nucleotide guanosine tetraphosphate; PQ plastoquinone; RNAP RNA polymerase; UCR unconserved region

Indexed keywords

PEPTIDES AND PROTEINS; SIG1 PROTEIN; SIG2 PROTEIN; SIG3 PROTEIN; SIG4 PROTEIN; SIG5 PROTEIN; SIG6 PROTEIN; SIGMA FACTOR; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; CHLAMYDOMONAS REINHARDTII; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASTID; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; PHYSIOLOGY; PROMOTER REGION;

BACTERIA (MICROORGANISMS); CYANOBACTERIA; EMBRYOPHYTA;

PLASTIDS; PROMOTER REGIONS, GENETIC; SIGMA FACTOR; TRANSCRIPTION, GENETIC;

EID: 84931567558     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2015.01.001     Document Type: Review

References (127)

1. A. Barkan Expression of plastid genes: organelle-specific elaborations on a prokaryotic scaffold Plant Physiol. 155 2011 1520 1532
2. K. Liere, A. Weihe, and T. Börner The transcription machineries of plant mitochondria and chloroplasts: composition, function, and regulation J. Plant Physiol. 168 2011 1345 1360
3. N. Sato Was the evolution of plastid genetic machinery discontinuous? Trends Plant Sci. 6 2001 151 155
4. Y. Yagi, and T. Shiina Evolutionary aspects of plastid proteins involved in transcription: the transcription of a tiny genome is mediated by complicated machinery Transcription 3 2012 290 294
5. S. Sekine, S. Tagami, and S. Yokoyama Structural basis of transcription by bacterial and eukaryotic RNA polymerases Curr. Opin. Struct. Biol. 22 2012 110 118
6. A. Feklístov, B.D. Sharon, S.A. Darst, and C.A. Gross Bacterial sigma factors: a historical, structural, and genomic perspective Annu. Rev. Microbiol. 68 2014 357 376
7. S.J. Surzycki, and D.L. Shellenbarger Purification and characterization of a putative sigma factor from Chlamydomonas reinhardtii Proc. Natl. Acad. Sci. U. S. A. 73 1976 3961 3965
8. S. Lerbs, E. Brautigam, and R. Mache DNA-dependent RNA polymerase of spinach chloroplasts: characterization of sigma-like and alpha-like polypeptides Mol. Gen. Genet. 211 1988 459 464
9. S. Bulow, and G. Link Sigma-like activity from mustard (Sinapis alba L.) chloroplasts conferring DNA-binding and transcription specificity to E. coli core RNA polymerase Plant Mol. Biol. 10 1988 349 357
10. B. Liu, and R.F. Troxler Molecular characterization of a positively photoregulated nuclear gene for a chloroplast RNA polymerase sigma factor in Cyanidium caldarium Proc. Natl. Acad. Sci. U. S. A. 93 1996 3313 3318
11. K. Tanaka, K. Oikawa, N. Ohta, H. Kuroiwa, T. Kuroiwa, and H. Takahashi Nuclear encoding of a chloroplast RNA polymerase sigma subunit in a red alga Science 272 1996 1932 1935
12. M.A. Hakimi, I. Privat, J.G. Valay, and S. Lerbs-Mache Evolutionary conservation of C-terminal domains of primary sigma (70)-type transcription factors between plants and bacteria J. Biol. Chem. 275 2000 9215 9221
13. M. Hanaoka, K. Kanamaru, H. Takahashi, and K. Tanaka Molecular genetic analysis of chloroplast gene promoters dependent on SIG2, a nucleus-encoded sigma factor for the plastid-encoded RNA polymerase in Arabidopsis thaliana Nucleic Acids Res. 31 2003 7090 7098
14. A. Homann, and G. Link DNA-binding and transcription characteristics of three cloned sigma factors from mustard (Sinapis alba L.) suggest overlapping and distinct roles in plastid gene expression Eur. J. Biochem. 270 2003 1288 1300
15. S. Österberg, T. del Peso-Santos, and V. Shingler Regulation of alternative sigma factor use Annu. Rev. Microbiol. 65 2011 37 55
16. K. Isono, M. Shimizu, K. Yoshimoto, Y. Niwa, K. Satoh, A. Yokota, and H. Kobayashi Leaf-specifically expressed genes for polypeptides destined for chloroplasts with domains of sigma70 factors of bacterial RNA polymerases in Arabidopsis thaliana Proc. Natl. Acad. Sci. U. S. A. 94 1997 14948 14953
17. K. Tanaka, Y. Tozawa, N. Mochizuki, K. Shinozaki, A. Nagatani, K. Wakasa, and H. Takahashi Characterization of three cDNA species encoding plastid RNA polymerase sigma factors in Arabidopsis thaliana: evidence for the sigma factor heterogeneity in higher plant plastids FEBS Lett. 413 1997 309 313
18. S. Tan, and R.F. Troxler Characterization of two chloroplast RNA polymerase sigma factors from Zea mays: photoregulation and differential expression Proc. Natl. Acad. Sci. U. S. A. 96 1999 5316 5321
19. K. Oikawa, M. Fujiwara, E. Nakazato, K. Tanaka, and H. Takahashi Characterization of two plastid sigma factors, SigA1 and SigA2, that mainly function in matured chloroplasts in Nicotiana tabacum Gene 261 2000 221 228
20. M. Fujiwara, A. Nagashima, K. Kanamaru, K. Tanaka, and H. Takahashi Three new nuclear genes, sigD, sigE and sigF, encoding putative plastid RNA polymerase sigma factors in Arabidopsis thaliana FEBS Lett. 481 2000 47 52
21. S. Lerbs-Mache Function of plastid sigma factors in higher plants: regulation of gene expression or just preservation of constitutive transcription? Plant Mol. Biol. 76 2011 235 249
22. E.A. Lysenko Plant sigma factors and their role in plastid transcription Plant Cell Rep. 26 2007 845 859
23. J. Schweer Plant sigma factors come of age: flexible transcription factor network for regulated plastid gene expression Endocytobiosis Cell Res. 20 2010 1 12
24. J. Schweer, H. Türkeri, A. Kolpack, and G. Link Role and regulation of plastid sigma factors and their functional interactors during chloroplast transcription - recent lessons from Arabidopsis thaliana Eur. J. Cell Biol. 89 2010 940 946
25. K.S. Murakami, S. Masuda, and S.A. Darst Structural basis of transcription initiation: RNA polymerase holoenzyme at 4 Å resolution Science 296 2002 1280 1284
26. D.G. Vassylyev, S. Sekine, O. Laptenko, J. Lee, M.N. Vassylyeva, S. Borukhov, and S. Yokoyama Crystal structure of a bacterial RNA polymerase holoenzeme at 2.6 Å resolution Nature 417 2002 712 719
27. A. Nagashima, M. Hanaoka, T. Shikanai, M. Fujiwara, K. Kanamaru, H. Takahashi, and K. Tanaka The multiple-stress responsive plastid sigma factor, SIG5, directs activation of the psbD blue light-responsive promoter (BLRP) in Arabidopsis thaliana Plant Cell Physiol. 45 2004 357 368
28. J. Schweer, S. Geimer, J. Meurer, and G. Link Arabidopsis mutants carrying chimeric sigma factor genes reveal regulatory determinants for plastid gene expression Plant Cell Physiol. 50 2009 1382 1386
29. J. Schweer, H. Türkeri, B. Link, and G. Link AtSIG6, a plastid sigma factor from Arabidopsis, reveals functional impact of cpCK2 phosphorylation Plant J. 62 2010 192 202
30. M. Shimizu, H. Kato, T. Ogawa, A. Kurachi, Y. Nakagawa, and H. Kobayashi Sigma factor phosphorylation in the photosynthetic control of photosystem stoichiometry Proc. Natl. Acad. Sci. U. S. A. 107 2010 10760 10764
31. W. Chi, J. Mao, Q. Li, D. Ji, M. Zou, C. Lu, and L. Zhang Interaction of the pentatricopeptide-repeat protein DELAYED GREENING 1 with sigma factor SIG6 in the regulation of chloroplast gene expression in Arabidopsis cotyledons Plant J. 64 2010 14 25
32. W. Reznikov, D.A. Siegle, D.W. Cowing, and C.A. Gross The regulation of transcription initiation in bacteria Annu. Rev. Genet. 19 1985 355 387
33. T. Shiina, Y. Tsunoyama, Y. Nakahira, and M.S. Khan Plastid RNA polymerases, promoters, and transcription regulators in higher plants Int. Rev. Cytol. 244 2005 1 68
34. A.A. Gatenby, J.A. Castleton, and M.W. Saul Expression in E. coli of maize and wheat chloroplast genes for large subunit of ribulose bisphosphate carboxylase Nature 291 1981 117 121
35. D. Bradley, and A.A. Gatenby Mutational analysis of the maize chloroplast ATPase beta subunit gene promoter: the isolation of promoter mutants in E. coli and their characterization in a chloroplast in vitro transcription system EMBO J. 4 1985 3641 3648
36. J. Ortelt, and G. Link Plastid gene transcription: promoters and RNA polymerases Methods Mol. Biol. 1132 2014 47 72
37. U. Klein, J.D. De Camp, and L. Bogorad Two types of chloroplast gene promoters in Chlamydomonas reinhardtii Proc. Natl. Acad. Sci. U. S. A. 89 1992 3453 3457
38. A.D. Blowers, G.S. Ellmore, U. Klein, and L. Bogorad Transcriptional analysis of endogenous and foreign genes in chloroplast transformants of Chlamydomonas Plant Cell 2 1990 1059 1070
39. U. Klein, M.L. Salvador, and L. Bogorad Activity of the Chlamydomonas chloroplast rbcL gene promoter is enhanced by a remote sequence element Proc. Natl. Acad. Sci. U. S. A. 91 1994 10819 10823
40. S. Kasai, S. Yoshimura, K. Ishikura, Y. Takaoka, K. Kobayashi, K. Kato, and A. Shinmyo Effect of coding regions on chloroplast gene expression in Chlamydomonas reinhardtii J. Biosci. Bioeng. 95 2003 276 282
41. G. Link DNA sequence requirements for the accurate transcription of a protein-coding plastid gene in a plastid in vitro system from mustard (Sinapis alba L.) EMBO J. 3 1984 1697 1704
42. W. Gruissem, and G. Zurawski Analysis of promoter regions for the spinach chloroplast rbcL, atpB and psbA genes EMBO J. 4 1985 3375 3383
43. S.K. Boyer, and J.E. Mullet Sequence and transcript map of barley chloroplast psbA gene Nucleic Acids Res. 16 1988 8184
44. A. Eisermann, K. Tiller, and G. Link In vitro transcription and DNA binding characteristics of chloroplast and etioplast extracts from mustard (Sinapis alba) indicate differential usage of the psbA promoter EMBO J. 9 1990 3981 3987
45. J.Y. Suzuki, P. Sriraman, Z. Svab, and P. Maliga Unique architecture of the plastid ribosomal RNA operon promoter recognized by the multisubunit RNA polymerase in tobacco and other higher plants Plant Cell 15 2003 195 205
46. T. Shiina, L. Allison, and P. Maliga rbcL transcript levels in tobacco plastids are independent of light: reduced dark transcription rate is compensated by increased mRNA stability Plant Cell 10 1998 1713 1722
47. T.B. Sexton, D.A. Christopher, and J.E. Mullet Light-induced switch in barley psbD-psbC promoter utilization: a novel mechanism regulating chloroplast gene expression EMBO J. 9 1990 4485 4494
48. D.A. Christopher, M. Kim, and J.E. Mullet A novel light-regulated promoter is conserved in cereal and dicot chloroplasts Plant Cell 4 1992 785 798
49. M. Kim, and J.E. Mullet Identification of a sequence-specific DNA binding factor required for transcription of the barley chloroplast blue light-responsive psbD-psbC promoter Plant Cell 7 1995 1445 1457
50. K.Y. To, M.C. Cheng, D.F. Suen, D.P. Mon, L.F. Chen, and S.C. Chen Characterization of the light-responsive promoter of rice chloroplast psbD-C operon and the sequence-specific DNA binding factor Plant Cell Physiol. 37 1996 660 666
51. P.H. Hoffer, and D.A. Christopher Structure and blue-light-responsive transcription of a chloroplast psbD promoter from Arabidopsis thaliana Plant Physiol. 115 1997 213 222
52. M. Kim, K.E. Thum, D.T. Morishige, and J.E. Mullet Detailed architecture of the barley chloroplast psbD-psbC blue light-responsive promoter J. Biol. Chem. 274 1999 4684 4692
53. J. Satoh, K. Baba, Y. Nakahira, Y. Tsunoyama, T. Shiina, and Y. Toyoshima Developmental stage-specific multi-subunit plastid RNA polymerase (PEP) in wheat Plant J. 18 1999 407 415
54. I. Privat, M.A. Hakimi, L. Buhot, J.J. Favory, and S. Lerbs-Mache Characterization of Arabidopsis plastid sigma-like transcription factors SIG1, SIG2 and SIG3 Plant Mol. Biol. 55 2003 385 399
55. Y. Tozawa, M. Teraishi, T. Sasaki, K. Sonoike, Y. Nishiyama, M. Itaya, A. Miyao, and H. Hirochika The plastid sigma factor SIG1 maintains photosystem I activity via regulated expression of the psaA operon in rice chloroplasts Plant J. 52 2007 124 132
56. Y. Onda, Y. Yagi, Y. Saito, N. Takenaka, and Y. Toyoshima Light induction of Arabidopsis SIG1 and SIG5 transcripts in mature leaves: differential roles of cryptochrome 1 and cryptochrome 2 and dual function of SIG5 in the recognition of plastid promoters Plant J. 55 2008 968 978
57. M. Hanaoka, M. Kato, M. Anma, and K. Tanaka SIG1, a sigma factor for the chloroplast RNA polymerase, differently associates with multiple DNA regions in the chloroplast chromosomes in vivo Int. J. Mol. Sci. 13 2012 12182 12194
58. K. Kanamaru, A. Nagashima, M. Fujiwara, H. Shimada, Y. Shirano, K. Nakabayashi, D. Shibara, K. Tanaka, and H. Takahashi An Arabidopsis sigma factor (SIG2)-dependent expression of plastid-encoded tRNAs in chloroplasts Plant Cell Physiol. 42 2001 1034 1043
59. A. Nagashima, M. Hanaoka, R. Motohashi, M. Seki, K. Shinozaki, K. Kanamaru, H. Takahashi, and K. Tanaka DNA microarray analysis of plastid gene expression in an Arabidopsis mutant deficient in a plastid transcription factor sigma, SIG2 Biosci. Biotechnol. Biochem. 68 2004 694 704
60. M. Malik Ghulam, O. Zghidi-Abouzid, E. Lambert, S. Lerbs-Mache, and L. Merendino Transcriptional organization of the large and the small ATP synthase operons, atpI/H/F/A and atpB/E, in Arabidopsis thaliana chloroplasts Plant Mol. Biol. 79 2012 259 272
61. M. Hanaoka, K. Kanamaru, M. Fujiwara, H. Takahashi, and K. Tanaka Glutamyl-tRNA mediates a switch in RNA polymerase use during chloroplast biogenesis EMBO Rep. 6 2005 545 550
62. P.T. Hajdukiewicz, L.A. Allison, and P. Maliga The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids EMBO J. 16 1997 4041 4048
63. A.V. Bohne, A. Weihe, and T. Börner Transfer RNAs inhibit Arabidopsis phage-type RNA polymerases Endocytobiosis Cell Res. 19 2009 63 69
64. W. Zghidi, L. Merendino, A. Cottet, R. Mache, and S. Lerbs-Mache Nucleus-encoded plastid sigma factor SIG3 transcribes specifically the psbN gene in plastids Nucleic Acids Res. 35 2007 455 464
65. O. Zghidi-Abouzid, L. Merendino, F. Buhr, M. Malik Ghulam, and S. Lerbs-Mache Characterization of plastid psbT sense and antisense RNAs Nucleic Acids Res. 39 2011 5379 5387
66. J.J. Favory, M. Kobayshi, K. Tanaka, G. Peltier, M. Kreis, J.G. Valay, and S. Lerbs-Mache Specific function of a plastid sigma factor for ndhF gene transcription Nucleic Acids Res. 33 2005 5991 5999
67. W.B. Yao, B.Y. Meng, M. Tanaka, and M. Sugiura An additional promoter within the protein-coding region of the psbD-psbC gene cluster in tobacco chloroplast DNA Nucleic Acids Res. 17 1989 9583 9591
68. T. Wada, Y. Tunoyama, T. Shiina, and Y. Toyoshima In vitro analysis of light-induced transcription in the wheat psbD/C gene cluster using plastid extracts from dark-grown and short-term-illuminated seedlings Plant Physiol. 104 1994 1259 1267
69. K.E. Thum, M. Kim, D.T. Morishige, C. Eibl, H.-U. Koop, and J.E. Mullet Analysis of barley chloroplast psbD light-responsive promoter elements in transplastomic tobacco Plant Mol. Biol. 47 2001 353 366
70. Y. Tsunoyama, K. Morikawa, T. Shiina, and Y. Toyoshima Blue light specific and differential expression of a plastid sigma factor, Sig5 in Arabidopsis thaliana FEBS Lett. 516 2002 225 228
71. Y. Tsunoyama, Y. Ishizaki, K. Morikawa, M. Kobori, Y. Nakahira, G. Takeba, Y. Toshinori, and T. Shiina Blue light-induced transcription of plastid-encoded psbD gene is mediated by a nuclear-encoded transcription initiation factor, AtSig5 Proc. Natl. Acad. Sci. U. S. A. 101 2004 3304 3309
72. M.P. Davey, N.I. Susanti, J.J. Wargent, J.E. Findlay, W. Paul Quick, N.D. Paul, and G.I. Jenkins The UV-B photoreceptor UVR8 promotes photosynthetic efficiency in Arabidopsis thaliana exposed to elevated levels of UV-B Photosynth. Res. 114 2012 121 131
73. J. Yao, S. Roy-Chowdhury, and L. Allison AtSig5 is an essential nucleus-encoded Arabidopsis sigma-like factor Plant Physiol. 132 2003 739 747
74. T. Kanazawa, K. Ishizaki, T. Kohchi, M. Hanaoka, and K. Tanaka Characterization of four nuclear-encoded plastid RNA polymerase sigma factor genes in the liverwort Marchantia polymorpha: blue-light- and multiple stress-responsive SIG5 was acquired early in the emergence of terrestrial plants Plant Cell Physiol. 54 2013 1736 1748
75. T. Mochizuki, Y. Onda, E. Fujiwara, M. Wada, and Y. Toyoshima Two independent light signals cooperate in the activation of the plastid psbD blue light-responsive promoter in Arabidopsis FEBS Lett. 571 2004 26 30
76. S.G. Moller, Y.S. Kim, T. Kunkel, and N.H. Chua PP7 is a positive regulator of blue light signaling in Arabidopsis Plant Cell 15 2003 1111 1119
77. D.A. Christopher, and P.H. Hoffer DET1 represses a chloroplast blue light-responsive promoter in a developmental and tissue-specific manner in Arabidopsis thaliana Plant J. 14 1998 1 11
78. Z.B. Noordally, K. Ishii, K.A. Atkins, S.J. Wetherill, J. Kusakina, E.J. Walton, M. Kato, M. Azuma, K. Tanaka, M. Hanaoka, and A.N. Dodd Circadian control of chloroplast transcription by a nuclear-encoded timing signal Science 339 2013 1316 1319
79. Y. Tozawa, K. Tanaka, H. Takahashi, and K. Wakasa Nuclear encoding of a plastid sigma factor in rice and its tissue- and light-dependent expression Nucleic Acids Res. 26 1998 415 419
80. K. Kanamaru, M. Fujiwara, M. Seki, T. Katagiri, M. Nakamura, N. Mochizuki, A. Nagatani, K. Shinozaki, K. Tanaka, and H. Takahashi Plastidic RNA polymerase sigma factors in Arabidopsis Plant Cell Physiol. 40 1999 832 842
81. S.D. Lahiri, J. Yao, C. McCumbers, and L.A. Allison Tissue-specific and light-dependent expression within a family of nuclear-encoded sigma-like factors from Zea mays Mol. Cell Biol. Res. Commun. 1 1999 14 20
82. K. Morikawa, S. Ito, Y. Tsunoyama, Y. Nakahira, T. Shiina, and Y. Toyoshima Circadian regulated expression of a nuclear encoded plastid sigma factor gene (sigA) in wheat seedlings FEBS Lett. 451 1999 275 278
83. K. Ichikawa, M. Sugita, T. Imaizumi, M. Wada, and S. Aoki Differential expression on a daily basis of plastid sigma factor genes from the moss Physcomitrella patens. Regulatory interactions among PpSig5, the circadian clock, and blue light signaling mediated by cryptochromes Plant Physiol. 136 2004 4285 4298
84. K. Ichikawa, A. Shimizu, R. Okada, S.B. Satbhai, and S. Aoki The plastid sigma factor SIG5 is involved in the diurnal regulation of the chloroplast gene psbD in the moss Physcomitrella patens FEBS Lett. 582 2008 405 409
85. M.L. Rugnone, A. Faigón Soverna, S.E. Sanchez, R.G. Schlaen, C.E. Hernando, D.K. Seymour, E. Mancini, A. Chernomoretz, D. Weigel, P. Más, and M.J. Yanovsky LNK genes integrate light and clock signaling networks at the core of the Arabidopsis oscillator Proc. Natl. Acad. Sci. U. S. A. 110 2013 12120 121205
86. Y. Ishizaki, Y. Tsunoyama, K. Hatano, K. Ando, A. Shinmyo, M. Kobori, G. Takeba, Y. Nakahira, and T. Shiina A nuclear-encoded sigma factor, Arabidopsis SIG6, recognizes sigma-70 type chloroplast promoters and regulates early chloroplast development in cotyledons Plant J. 42 2005 133 144
87. H. Loschelder, J. Schweer, B. Link, and G. Link Dual temporal role of plastid sigma factor 6 in Arabidopsis development Plant Physiol. 142 2006 642 650
88. J. Schweer, H. Loschelder, and G. Link A promoter switch that can rescue a plant sigma factor mutant FEBS Lett. 580 2006 6617 6622
89. K.X. Chan, P.A. Crisp, G.M. Estavillo, and B.J. Pogson Chloroplast-to-nucleus communication: current knowledge, experimental strategies and relationship to drought stress signaling Plant Signal. Behav. 5 2010 1575 1582
90. W. Chi, X. Sun, and L. Zhang Intracellular signaling from plastid to nucleus Annu. Rev. Plant Biol. 64 2013 559 582
91. J.D. Woodson, J.M. Perez-Ruiz, R.J. Schmitz, J.R. Ecker, and J. Chory Sigma factor-mediated plastid retrograde signals control nuclear gene expression Plant J. 73 2013 1 13
92. E. Ankele, P. Kindgren, E. Pesquet, and A. Strand In vivo visualization of Mg-protoporphyrin IX, a coordinator of photosynthetic gene expression in the nucleus and the chloroplast Plant Cell 19 2007 1964 1979
93. N. Mochizuki, R. Tanaka, A. Tanaka, T. Masuda, and A. Nagatani The steady-state level of Mg-protoporphyrin IX is not a determinant of plastid-to-nucleus signaling in Arabidopsis Proc. Natl. Acad. Sci. U. S. A. 105 2008 15184 15189
94. M. Moulin, A.C. McCormac, M.J. Terry, and A.G. Smith Tetrapyrrole profiling in Arabidopsis seedlings reveals that retrograde plastid nuclear signaling is not due to Mg-protoporphyrin IX accumulation Proc. Natl. Acad. Sci. U. S. A. 105 2008 15178 15183
95. S. Oh, and B.L. Montgomery Phytochrome-induced SIG2 expression contributes to photoregulation of phytochrome signalling and photomorphogenesis in Arabidopsis thaliana J. Exp. Bot. 64 2013 5457 5472
96. S. Oh, and B.L. Montgomery Phytochrome-dependent coordinate control of distinct aspects of nuclear and plastid gene expression during anterograde signaling and photomorphogenesis Front. Plant Sci. 5 2014 171
97. R. Meskauskiene, M. Nater, D. Goslings, F. Kessler, R. op den Camp, and K. Apel FLU: a negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana Proc. Natl. Acad. Sci. U. S. A. 98 2001 12826 12831
98. N.S. Coll, A. Danon, J. Meurer, W.K. Cho, and K. Apel Characterization of soldat8, a suppressor of singlet oxygen-induced cell death in Arabidopsis seedlings Plant Cell Physiol. 50 2009 707 718
99. T.A. Beardslee, S. Roy-Chowdhury, P. Jaiswal, L. Buhot, S. Lerbs-Mache, D.B. Stern, and L.A. Allison A nucleus-encoded maize protein with sigma factor activity accumulates in mitochondria and chloroplasts Plant J. 31 2002 199 209
100. F. Yu, J. Shi, J. Zhou, J. Gu, Q. Chen, J. Li, W. Cheng, D. Mao, L. Tian, B.B. Buchanan, L. Li, L. Chen, D. Li, and S. Luan ANK6, a mitochondrial ankyrin repeat protein, is required for male-female gamete recognition in Arabidopsis thaliana Proc. Natl. Acad. Sci. U. S. A. 107 2010 22332 22337
101. S for degradation by ClpXP Genes Dev. 15 2001 627 637
102. M.D. Blankschien, J.H. Lee, E.D. Grace, C.W. Lennon, J.A. Halliday, W. Ross, R.L. Gourse, and C. Herman Super DksAs: substitutions in DksA enhancing its effects on transcription initiation EMBO J. 28 2009 1720 1731
103. S. Baginsky, K. Tiller, and G. Link Transcription factor phosphorylation by a protein kinase associated with chloroplast RNA polymerase from mustard (Sinapis alba) Plant Mol. Biol. 34 1997 181 189
104. K. Ogrzewalla, M. Piotrowski, S. Reinbothe, and G. Link The plastid transcription kinase from mustard (Sinapis alba L.). A nuclear-encoded CK2-type chloroplast enzyme with redox-sensitive function Eur. J. Biochem. 269 2002 3329 3337
105. F. Meggio, and L.A. Pinna One-thousand-and-one substrates of protein kinase CK2? FASEB J. 17 2003 349 368
106. T. Pfannschmidt, and K. Liere Redox regulation and modification of proteins controlling chloroplast gene expression Antioxid. Redox Signal. 7 2005 607 618
107. B.B. Buchanan, and Y. Balmer Redox regulation: a broadening horizon Annu. Rev. Plant Biol. 56 2005 187 220
108. S. Puthiyaveetil, T.A. Kavanagh, P. Cain, J.A. Sullivan, C.A. Newell, J.C. Gray, C. Robinson, M. van der Giezen, M.B. Rogers, and J.F. Allen The ancestral symbiont sensor kinase CSK links photosynthesis with gene expression in chloroplasts Proc. Natl. Acad. Sci. U. S. A. 105 2008 10061 10066
109. S. Puthiyaveetil, I.M. Ibrahim, B. Jelicic, A. Tomasic, H. Fulgosi, and J.F. Allen Transcriptional control of photosynthesis genes: the evolutionarily conserved regulatory mechanism in plastid genome function Genome Biol. Evol. 2 2010 888 896
110. S. Puthiyaveetil, I.M. Ibrahim, and J.F. Allen Oxidation-reduction signalling components in regulatory pathways of state transitions and photosystem stoichiometry adjustment in chloroplasts Plant Cell Environ. 35 2012 347 359
111. J.D. Rochaix Redox regulation of thylakoid protein kinases and photosynthetic gene expression Antioxid. Redox Signal. 18 2013 2184 2201
112. J.D. Rochaix, S. Lemeille, A. Shapiguzov, I. Samol, G. Fucile, A. Willig, and M. Goldschmidt-Clermont Protein kinases and phosphatases involved in the acclimation of the photosynthetic apparatus to a changing light environment Philos. Trans. R. Soc. Lond. B Biol. Sci. 367 2012 3466 3474
113. J. Marles-Wright, and R.J. Lewis Stress responses of bacteria Curr. Opin. Struct. Biol. 17 2007 755 760
114. K. Morikawa, T. Shiina, S. Murakami, and Y. Toyoshima Novel nuclear-encoded proteins interacting with a plastid sigma factor, Sig1, in Arabidopsis thaliana FEBS Lett. 514 2002 300 304
115. Y.D. Xie, W. Li, D. Guo, J. Dong, Q. Zhang, Y. Fu, D. Ren, M. Peng, and Y. Xia The Arabidopsis gene SIGMA FACTOR-BINDING PROTEIN 1 plays a role in the salicylate- and jasmonatemediated defence responses Plant Cell Environ. 33 2010 828 839
116. W. Chi, J. Ma, D. Zhang, J. Guo, F. Chen, C. Lu, and L. Zhang The pentratricopeptide repeat protein DELAYED GREENING1 is involved in the regulation of early chloroplast development and chloroplast gene expression in Arabidopsis Plant Physiol. 147 2008 573 584
117. E.A. Van der Biezen, J. Sun, M.J. Coleman, M.J. Bibb, and J.D.G. Jones Arabidopsis RelA/SpoT homologs implicate (p)ppGpp in plant signaling Proc. Natl. Acad. Sci. U. S. A. 97 2000 3747 3752
118. R.M. Givens, M.-H. Lin, D.J. Taylor, U. Mechold, J.O. Berry, and V.J. Hernandez Inducible expression, enzymatic activity and origin of higher plant homologues of bacterial RelA/SpoT stress proteins in Nicotiana tabacum J. Biol. Chem. 279 2004 7495 7504
119. K. Kasai, T. Kanno, Y. Endo, K. Wasaka, and Y. Tozawa Guanosine tetra- and pentaphosphate synthetase activity in chloroplasts of a higher plant: association with 70S ribosomes and inhibition by tetracycline Nucleic Acids Res. 32 2004 5732 5741
120. Y. Tozawa, A. Nozawa, T. Kanno, T. Narisawa, S. Masuda, K. Kasai, and H. Nanamiya Calcium-activated (p)ppGpp synthetase in chloroplasts of land plants J. Biol. Chem. 282 2007 35536 35545
121. K. Takahashi, K. Kasai, and K. Ochi Identification of the bacterial alarmone guanosine 5' diphosphate 3'-diphosphate (ppGpp) in plants Proc. Natl. Acad. Sci. U. S. A. 101 2004 4320 4324
122. M. Sato, K. Takahashi, Y. Ochiai, T. Hosaka, K. Ochi, and K. Nabeta Bacterial alarmone, guanosine 5'-diphosphate 3'-diphosphate (ppGpp), predominantly binds the beta' subunit of plastid encoded plastid RNA polymerase in chloroplasts Chembiochem 10 2009 1227 1233
123. A. Sakai, H. Takano, and T. Kuroiwa Organelle nuclei in higher plants: structure, composition, function, and evolution Int. Rev. Cytol. 238 2004 59 118
124. P. Jeannette, and P. Thomas Essential nucleoid proteins in early chloroplast development Trends Plant Sci. 18 2013 186 194
125. W. Majeran, G. Friso, Y. Asakura, X. Qu, M. Huang, L. Ponnala, K.P. Watkins, A. Barkan, and K.J. van Wijk Nucleoid-enriched proteomes in developing plastids and chloroplasts from maize leaves: a new conceptual framework for nucleoid functions Plant Physiol. 158 2012 156 189
126. U.G. Maier, A. Bozarth, H.T. Funk, S. Zauner, S.A. Rensing, C. Schmitz-Linneweber, T. Börner, and M. Tillich Complex chloroplast RNA metabolism: just debugging the genetic programme? BMC Biol. 6 2008 36
127. L. Lefebvre-Legendre, L. Merendino, C. Rivier, and M. Goldschmidt-Clermont On the complexity of chloroplast RNA metabolism: psaA trans-splicing can be bypassed in Chlamydomonas Mol. Biol. Evol. 31 2015 2697 2707