Advertisement

Plant Molecular Biology

, Volume 76, Issue 3–5, pp 235–249 | Cite as

Function of plastid sigma factors in higher plants: regulation of gene expression or just preservation of constitutive transcription?

  • Silva Lerbs-Mache
Article

Abstract

Plastid gene expression is rather complex. Transcription is performed by three different RNA polymerases, two of them are nucleus-encoded, monomeric, of the phage-type (named RPOTp and RPOTmp) and one of them is plastid-encoded, multimeric, of the eubacterial-type (named PEP). The activity of the eubacterial-type RNA polymerase is regulated by up to six nucleus-encoded transcription initiation factors of the sigma-type. This complexity of the plastid transcriptional apparatus is not yet well understood and raises the question of whether it is subject to any regulation or just ensures constitutive transcription of the plastid genome. On the other hand, considerable advances have been made during the last years elucidating the role of sigma factors for specific promoter recognition and selected transcription of some plastid genes. Sigma-interacting proteins have been identified and phosphorylation-dependent functional changes of sigma factors have been revealed. The present review aims to summarize these recent advances and to convince the reader that plastid gene expression is regulated on the transcriptional level by sigma factor action.

Keywords

Higher plants Plastid Transcription regulation Sigma factors 

References

  1. Allison LA, Simon LD, Maliga P (1996) Deletion of rpoB reveals a second distinct transcription system in plastids of higher plants. EMBO J 15:2802–2809PubMedGoogle Scholar
  2. Azevedo J, Courtois F, Lerbs-Mache S (2006) Sub-plastidial localization of two different phage-type RNA polymerases in spinach chloroplasts. Nucleic Acids Res 34:436–444PubMedCrossRefGoogle Scholar
  3. Azevedo J, Courtois F, Hakimi MA, Demarsy E, Lagrange T, Alcaraz JP, Pankaj J, Drouard L, Lerbs-Mache S (2008) Intraplastidial trafficking of a phage-type RNA polymerase is mediated by a thylakoid RING-H2 protein. Proc Natl Acad Sci USA 105:9123–9128PubMedCrossRefGoogle Scholar
  4. Baeza L, Bertrand A, Mache R, Lerbs-Mache S (1991) Characterization of a protein binding sequence in the promoter region of the 16S rRNA gene of the spinach chloroplast genome. Nucleic Acids Res 19:3577–3581PubMedCrossRefGoogle Scholar
  5. Bar-Nahum G, Nudler E (2001) Isolation and characterization of σ70-retaining transcription elongation complexes from Escherichia coli. Cell 106:443–451PubMedCrossRefGoogle Scholar
  6. Baumgartner BJ, Rapp JC, Mullet JE (1993) Plastid genes encoding the transcription/translation apparatus are differently transcribed early in barley (Hordeum vulgare) chloroplast development. Plant Physiol 101:781–791PubMedGoogle Scholar
  7. Bergsland KJ, Haselkorn R (1991) Evolutionary relationships among eubacteria, cyanobacteria, and chloropasts: Evidence from the rpoC1 gene of Anabaena sp. Strain PCC 7120. J Bacteriol 173:3446–3455PubMedGoogle Scholar
  8. Bligny M, Courtois F, Thaminy S, Chang CC, Lagrange T, Baruah-Wolff J, Stern D, Lerbs-Mache S (2000) Regulation of plastid rDNA transcription by interaction of CDF2 with two different RNA polymerases. EMBO J 19:1851–1860PubMedCrossRefGoogle Scholar
  9. Bohne AV, Irihimovitch V, Weihe A, Stern DB (2006) Chlamydomonas reinhardtii encodes a single sigma70-like factor which likely functions in chloroplast transcription. Curr Genet 49:333–340PubMedCrossRefGoogle Scholar
  10. Bohne AV, Weihe A, Börner T (2009) Transfer RNAs inhibit Arabidosis phage-type RNA polymerases. Endocytobiosis Cell Res 19:63–69Google Scholar
  11. Brantl S (2007) Regulatory mechanisms employed by cis-encoded antisense RNAs. Curr Opin Microbiol 10:102–109PubMedCrossRefGoogle Scholar
  12. Cahoon AB, Harris FM, Stern DB (2004) Analysis of developing maize plastids reveals two mRNA stability classes correlating with RNA polymerase type. EMBO Rep 5:801–806PubMedCrossRefGoogle Scholar
  13. Carter ML, Smith AC, Kobayashi H, Purton S, Herrin DL (2004) Structure, circadian regulation and bioinformatic analysis of the unique sigma factor gene in Chlamydomonas reinhardtii. Photosynth Res 82:339–349PubMedCrossRefGoogle Scholar
  14. Chen M, Galvao RM, Li M, Burger B, Bugea J, Bolado J, Chory J (2010) Arabidopsis HEMERA/pTAC12 initiates photomorphogenesis by phytochromes. Cell 141:1230–1240PubMedCrossRefGoogle Scholar
  15. Chi W, Mao JM, Li QL, Zou M, Lu C, Zhang L (2010) Interaction of the pentatricopeptide-repeat protein DELAYED GREENING1 with sigma factor SIG6 in the regulation of chloroplast gene expression in Arabidopsis cotyledons. Plant J (in press)Google Scholar
  16. Choquet Y, Wollman FA (2002) Translational regulation as specific traits of chloroplast gene expression. FEBS L 529:39–42CrossRefGoogle Scholar
  17. Coll NS, Danon A, Meurer J, Cho WK, Apel K (2009) Characterization of soldat8, a suppressor of singlet oxygen-induced cell death in Arabidopsis seedlings. Plant Cell Physiol 50:707–718PubMedCrossRefGoogle Scholar
  18. Courties C, Perasso R, Chretiennot-Dinet M-J, Gouy M, Guillou L, Troussellier M (1998) Phylogenetic analysis and genome size of Ostreococcus tauri (Chlorophyta, Prasinophyceae). J Phycol 34:844–849CrossRefGoogle Scholar
  19. Courtois F, Merendino L, Demarsy E, Mache R, Lerbs-Mache S (2007) Phage-type RNA Polymerase RPOTmp transcribes the rrn operon from the PC promoter at early developmental stages in Arabidopsis. Plant Physiol 145:712–721PubMedCrossRefGoogle Scholar
  20. Demarsy E, Courtois F, Azevedo J, Buhot L, Lerbs-Mache S (2006) Building up of the plastid transcriptional machinery during germination and early plant development. Plant Physiol 142:993–1003PubMedCrossRefGoogle Scholar
  21. Desveaux D, Subramaniam R, Després C, Mess J-N, Lévesque C, Fobert PR, Dangl JL, Brisson N (2004) A “Whirly” transcription factor is required for salicylic acid-dependent disease resistance in Arabidopsis. Dev Cell 6:229–240PubMedCrossRefGoogle Scholar
  22. Favory JJ, Kobayshi M, Tanaka K, Peltier G, Kreis M, Valay JG, Lerbs-Mache S (2005) Specific function of a plastid sigma factor for ndhF gene transcription. Nucleic Acids Res 33:5991–5999PubMedCrossRefGoogle Scholar
  23. Givens RM, Lin M-H, Taylor DJ, Mechold U, Berry JO, Hernandez VJ (2004) Inducible expression, enzymatic activity and origin of higher plant homologues of bacterial RelA/SpoT stress proteins in Nicotiana tabacum. J Biol Chem 279:7495–7504PubMedCrossRefGoogle Scholar
  24. Grigorova IL, Phleger NJ, Mutalik VK, Gross CA (2006) Insights into transcriptional regulation and σ competition from an equilibrium model of RNA polymerase binding to DNA. Proc Natl Acad Sci USA 103:5332–5337PubMedCrossRefGoogle Scholar
  25. Hakimi MA, Privat I, Valay JG, Lerbs-Mache S (2000) Evolutionary conservation of C-terminal domains of primary sigma70-type transcription factors between plants and bacteria. J Biol Chem 275:9215–9221PubMedCrossRefGoogle Scholar
  26. Hanaoka M, Kanamaru K, Takahashi H, Tanaka K (2003) 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 31:7090–7098PubMedCrossRefGoogle Scholar
  27. Hanaoka M, Kanamaru K, Fujiwara M, Takahashi H, Tanaka K (2005) Glutamyl-tRNA mediates a switch in RNA polymerase use during chloroplast biogenesis. EMBO Rep 6:545–550PubMedCrossRefGoogle Scholar
  28. Hansson A, Amann K, Zygadio A, Meurer J, Scheller HV, Jensen PE (2007) Knock-out of the chloroplast-encoded PSI-J subunit of photosystem I in Nicotiana tabacum. FEBS J 274:1734–1746PubMedCrossRefGoogle Scholar
  29. Hegeman CE, Halter CP, Owens TG, Hanson MR (2005) Expression of complementary RNA from chloroplast transgenes affects editing efficiency of transgene and endogenous chloroplast transcripts. Nucleic Acids Res 33:1454–1464PubMedCrossRefGoogle Scholar
  30. Homann A, Link G (2003) 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 270:1288–1300PubMedCrossRefGoogle Scholar
  31. Igloi GL, Kössel H (1992) The transcriptional apparatus of chloroplasts. Critical Rev Plant Sci 10:525–558CrossRefGoogle Scholar
  32. Iratni R, Baeza L, Andreeva A, Mache R, Lerbs-Mache S (1994) Regulation of rDNA transcription in chloroplasts: promoter exclusion by constitutive repression. Genes Dev 8:2928–2938PubMedCrossRefGoogle Scholar
  33. Ishizaki Y, Tsunoyama Y, Hatano K, Ando K, Kato K, Shinmyo A, Kobori M, Takeba G, Nakahira Y, Shiina T (2005) A nuclear-encoded sigma factor, Arabidopsis SIG6, recognizes sigma-70 type chloroplast promoters and regulates early chloroplast development in cotyledons. Plant J 42:133–144PubMedCrossRefGoogle Scholar
  34. Jishage M, Ishihama A (1995) Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli: Intracellular levels of σ70 and σ38. J Bacteriol 177:6832–6835PubMedGoogle Scholar
  35. Jishage M, Iwata A, Ueda S, Ishihama A (1996) Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli: Intracellular levels of four species of sigma subunits under various growth conditions. J Bacteriol 178:5447–5451PubMedGoogle Scholar
  36. Kanamaru K, Fujiwara M, Seki M, Katagiri T, Nakamura M, Mochizuki N, Nagatani A, Shinozaki K, Tanaka K, Takahashi H (1999) Plastidic RNA polymerase σ factors in Arabidopsis. Plant Cell Physiol 40:832–842PubMedGoogle Scholar
  37. Kanamaru K, Nagashima A, Fujiwara M, Shimada H, Shirano Y, Nakabayashi K, Shibara D, Tanaka K, Takahashi H (2001) An Arabidopsis sigma factor (SIG2)-dependent expression of plastid-encoded tRNAs in chloroplasts. Plant Cell Physiol 42:1034–1043PubMedCrossRefGoogle Scholar
  38. Kasai K, Kanno T, Endo Y, Wasaka K, Tozawa Y (2004) Guanosine tetra- and pentaphosphate synthetase activity in chloroplasts of a higher plant: association with 70S ribosomes and inhibition by tetracycline. Nucleic Acids Res 32:5732–5741PubMedCrossRefGoogle Scholar
  39. Kashino Y, Koike H, Yoshio M, Egashira H, Ikeuchi M, Pakrasi HB, Satoh K (2002) Low-molecular-mass polypeptide components of a photosystem II preparation from the thermophilic cyanobacterium Thermosynechococcus vulcanus. Plant Cell Physiol 43:1366–1373PubMedCrossRefGoogle Scholar
  40. Khaklova O, Bock R (2006) Elimination of deleterious mutations in plastid genomes by gene conversion. Plant J 46:85–94CrossRefGoogle Scholar
  41. Kubota Y, Miyao A, Hirochika H, Tozawa Y, Yasuda H, Tsunoyama Y, Niwa Y, Imamura S, Shirai M, Asayama M (2007) Two novel nuclear genes, OsSIG5 and OsSIG6, encoding potential plastid sigma factors of RNA polymerase in rice: Tissue-specific and light-responsive gene expression. Plant Cell Physiol 48:186–192PubMedCrossRefGoogle Scholar
  42. Lerbs-Mache S (2000) Regulation of rDNA transcription in plastids of higher plants. Biochimie 82:525–535PubMedCrossRefGoogle Scholar
  43. Liere K, Börner T (2007) Transcription and transcriptional regulation in plastids. In: Bock R (ed) Topics in current genetics, vol 19, pp 121–174Google Scholar
  44. Lonetto M, Gribskov M, Gross CA (1992) The sigma 70 family: sequence conservation and evolutionary relationships. J Bacteriol 174:3843–3849PubMedGoogle Scholar
  45. Loschelder H, Schweer J, Link B, Link G (2006) Dual temporal role of plastid sigma factor 6 in Arabidopsis development. Plant Physiol 142:642–650PubMedCrossRefGoogle Scholar
  46. Lung B, Zemann A, Madej MJ, Schuelke M, Techritz S, Ruf S, Bock R, Hüttenhofer A (2006) Identification of small non-coding RNAs from mitochondria and chloroplasts. Nucleic Acids Res 34:3842–3852PubMedCrossRefGoogle Scholar
  47. Lysenko EA (2007) Plant sigma factors and their role in plastid transcription. Plant Cell Rep 26:845–859PubMedCrossRefGoogle Scholar
  48. Mache R, Cottet A, Hakimi AM, Lerbs-Mache S (2002) The Plant sigma factors: structure and phylogenetic origin. Genome Lett 1,2:71–76. The Journal ceased activity in 2003. Reprints are available at http://www.aspbs.com/genomelett/contents_genomelett.htm
  49. Maier UG, Bozarth A, Funk HT, Zauner S, Rensing SA, Schmitz-Linneweber C, Börner T, Tillich M (2008) Complex chloroplast RNA metabolism: just debugging the genetic programme? BMC Biol 6:36PubMedCrossRefGoogle Scholar
  50. Marles-Wright J, Lewis RJ (2007) Stress responses of bacteria. Curr Opin Struct Biol 17:755–760PubMedCrossRefGoogle Scholar
  51. Masuda S, Mizusawa K, Narisawa T, Tozawa Y, Ohta H, Takamiya K-I (2008) The bacterial stringent response, conserved in chloroplasts, controls plant fertilization. Plant Cell Physiol 49:135–141PubMedCrossRefGoogle Scholar
  52. Morikawa K, Ito S, Tsunoyama Y, Nakahira Y, Shiina T, Toyoshima Y (1999) Circadian-regulated expression of a nuclear-encoded plastid σ factor gene (sigA) in wheat seedlings. FEBS Lett 451:275–278PubMedCrossRefGoogle Scholar
  53. Morikawa K, Shiina T, Murakami S, Toyoshima Y (2002) Novel nuclear-encoded protein interacting with a plastid sigma factor, Sig1, in Arabidopsis thaliana. FEBS Lett 514:300–304PubMedCrossRefGoogle Scholar
  54. Muller HJ (1964) The relation of recombination to mutational advance. Mutat Res 1:2–9Google Scholar
  55. Mullet JE (1993) Dynamic regulation of chloroplast transcription. Plant Physiol 103:309–313PubMedCrossRefGoogle Scholar
  56. Nagashima A, Hanaoka M, Motohashi R, Seki M, Shinozaki K, Kanamaru K, Takahashi H, Tanaka K (2004a) DNA microarray analysis of plastid gene expression in an Arabidopsis mutant deficient in a plastid transcription factor sigma, SIG2. Biosci Biotechnol Biochem 68:694–704PubMedCrossRefGoogle Scholar
  57. Nagashima A, Hanaoka M, Shikanai T, Fujiwara M, Kanamaru K, Takahashi H, Tanaka K (2004b) The multiple-stress responsive plastid sigma factor, SIG5, directs activation of the psbD blue light-responsive promoter (BLRP) in Arabidopsis thaliana. Plant Cell Physiol 45:357–368PubMedCrossRefGoogle Scholar
  58. Narusaka M, Kawai K, Izawa N, Seki M, Shinozaki K, Seo S, Kobayashi M, Shiraishi T, Narusaka Y (2008) Gene coding for SigA-binding protein from Arabidopsis appears to be transcriptionally up-regulated by salicylic acid and NPR1-dependent mechanisms. J Gen Plant Pathol 74:345–354CrossRefGoogle Scholar
  59. Nishimura Y, Kikis EA, Zimmer SL, Komine Y, Stern D (2004) Antisense transcript and RNA processing alterations suppress instability of polyadenylated mRNA in Chlamydomonas chloroplasts. Plant Cell 16:2849–2869PubMedCrossRefGoogle Scholar
  60. Nyström T (2004) Growth versus maintenance: a trade-off dictated by RNA polymerase availability and sigma factors competition. Mol Microbiol 54:855–862PubMedCrossRefGoogle Scholar
  61. Ohnishi N, Takahashi Y (2001) PsbT polypeptide is required for efficient repair of photodamaged photosystem II reaction center. J Biol Chem 276:33798–33804PubMedCrossRefGoogle Scholar
  62. Oikawa K, Fujiwara M, Nakazato E, Tanaka K, Takahashi H (2000) Characterization of two plastid σ factors, SigA1 and SigA2, that mainly function in matured chloroplasts in Nicotiana tabacum. Gene 261:221–228PubMedCrossRefGoogle Scholar
  63. Olinares PD, Ponnala L, van Wijk KJ (2010) Megadalton complexes in the chloroplast stroma of Arabidopsis thaliana characterized by size exclusion chromatography, mass spectrometry, and hierarchical clustering. Mol Cell Proteomics 9:1594–1615PubMedCrossRefGoogle Scholar
  64. Onda Y, Yagi Y, Saito Y, Takenaka N, Toyoshima Y (2008) 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 55:968–978PubMedCrossRefGoogle Scholar
  65. Osanai T, Imashimizu M, Seki A, Tabata S, Imamura S, Asayama M, Ikeuchi M, Tanaka K (2009) ChlH, the H subunit of the Mg-chelatase, is an anti-sigma factor for SigE in Synechocystis sp. PCC 6803Google Scholar
  66. Peltier J-B, Cai Y, Sun Q, Zabrouskov V, Giacomelli L, Rudella A, Ytterberg AJ, Rutschow H, van Wijk KJ (2006) The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts. Mol Cell Proteomics 5:114–133PubMedGoogle Scholar
  67. Pfalz J, Liere K, Kandlbinder A, Dietz K-J, Oelmüller R (2006) pTAC2, -6, and -12 are components of the transcriptionally active chromosome that are required for plastid gene expression. Plant Cell 18:176–197PubMedCrossRefGoogle Scholar
  68. Pfannschmidt T, Nilsson A, Allen JF (1999) Photosynthetic control of chloroplast gene expression. Nature 397:625–628CrossRefGoogle Scholar
  69. Prikryl J, Watkins KP, Friso G, van Wijk KL, Barkan A (2008) A member of the Whirly family is a multifunctional RNA- and DNA-binding protein that is essential for chloroplast biogenesis. Nucleic Acids Res 36:51152–55165CrossRefGoogle Scholar
  70. Privat I, Hakimi MA, Buhot L, Favory JJ, Lerbs-Mache S (2003) Characterization of Arabidopsis plastid sigma-like transcription factors SIG1, SIG2 and SIG3. Plant Mol Biol 55:385–399CrossRefGoogle Scholar
  71. Repoila F, Darfeuille F (2019) Small regulatory non-coding RNAs in bacteria:physiology and mechanistic aspects. Biol Cell 101:117–131CrossRefGoogle Scholar
  72. Reppas NB, Wade JT, Church GM, Struhl K (2008) The transition between transcriptional initiation and elongation in E. coli is highly variable and often rate limiting. Mol Cell 24:747–757CrossRefGoogle Scholar
  73. Rochaix JD (2002) The three genomes of Chlamydomonas. Photosynthesis Res 73:285–293CrossRefGoogle Scholar
  74. Sato M, Takahashi K, Ochiai Y, Hosaka T, Ochi K, Nabeta K (2009) Bacterial alarmone, guanosine 5’-diphosphate 3’-diphosphate (ppGpp), predominantly binds the beta’ subunit of plastid-encoded plastid RNA polymerase in chloroplasts. Chembiochem 10:1227–1233PubMedCrossRefGoogle Scholar
  75. Schröter Y, Steiner S, Matthäi K, Pfannschmidt T (2010) Analysis of oligomeric protein complexes in the chloroplast sub-proteome of nucleic acid-binding proteins from mustard reveals potential redox regulators of plastid gene expression. Proteomics 10:2191–2204PubMedCrossRefGoogle Scholar
  76. Schweer J (2010) Plant sigma factors come of age: flexible transcription factor network for regulated plastid gene expression. Endocytobiosis Cell Res 20:1–20CrossRefGoogle Scholar
  77. Schweer J, Loschelder H, Link G (2006) A promoter switch can rescue a plant sigma factor mutant. FEBS L 580:6617–6622CrossRefGoogle Scholar
  78. Schweer J, Geimer S, Meurer J, Link G (2009) Arabidopsis mutants carrying chimeric sigma factor genes reveal regulatory determinants for plastid gene expression. Plant Cell Physiol 50:1382–1386PubMedCrossRefGoogle Scholar
  79. Schweer J, Türkeri H, Link B, Link G (2010) AtSIG6, a plastid sigma factor from Arabidopsis, reveals functional impact of cpCK2 phosphorylation. Plant J 62:192–202PubMedCrossRefGoogle Scholar
  80. Sharma UK, Chatterji D (2010) Transcriptional switching in Escherichia coli during stress and starvation by modulation of σ70 activity. FEMS Microbiol Rev (under press)Google Scholar
  81. Shepherd N, Dennis P, Bremer H (2001) Cytoplasmic RNA polymerase in Escherichia coli. J Bacteriol 183:2527–2534PubMedCrossRefGoogle Scholar
  82. Shiina T, Tsunoyama Y, Nakahira Y, Khan MS (2005) Plastid RNA polymerases, promoters and transcription regulators in higher plants. Int Rev Cytol 244:1–68PubMedCrossRefGoogle Scholar
  83. Shimizu M, Kato H, Ogawa T, Kurachi A, Nakagawa Y, Kobayashi H (2010) Sigma factor phosphorylation in the photosynthetic control of photosystem stoichiometry. Proc Natl Acad Sci USA 107:10760–10764PubMedCrossRefGoogle Scholar
  84. Shirano Y, Shimada H, Kanamaru K, Fujiwarra M, Tanaka K, Takahashi H, Unno K, Sato S, Tabata S, Hayashi H, Miyake C, Yokota A, Shibata D (2000) Chloroplast development in Arabidopsis thaliana requires the nuclear-encoded transcription factor Sigma B. FEBS Lett 485:178–182PubMedCrossRefGoogle Scholar
  85. Sriraman P, Silhavy D, Maliga P (1998) Transcription from heterologous rRNA operon promoters in chloroplasts reveals requirement for specific activating factors. Plant Physiol 117:1495–1499PubMedCrossRefGoogle Scholar
  86. Stahl DJ, Rodermel SR, Bogorad L, Subramanian AR (1993) Co-transcription pattern of an introgressed operon in the maize chloroplast genome comprising four ATP synthase subunit genes and the ribosomal rps2. Plant Mol Biol 21:1069–1076PubMedCrossRefGoogle Scholar
  87. Suzuki JY, Ytterberg AJ, Beardslee T, Allison LA, van Wijk KJ, Maliga P (2004) Affinity purification of he tobacco plastid RNA polymerase and in vitro reconstitution of the holoenzyme. Plant J 40:164–172PubMedCrossRefGoogle Scholar
  88. Swiatecka-Hagenbruch M, Emanuel C, Hedtke B, Liere K, Börner T (2008) Impaired function of the phage-type RNA polymerase RpoTp in transcription of chloroplast genes is compensated by a second phage-type RNA polymerase. Nucleic Acids Res 36:785–792PubMedCrossRefGoogle Scholar
  89. Takahashi K, Kasai K, Ochi K (2004) Identification of the bacterial alarmone guanosine 5’ diphosphate 3’-diphosphate (ppGpp) in plants. Proc Natl Acad Sci USA 101:4320–4324PubMedCrossRefGoogle Scholar
  90. Tarrant MK, Cole PA (2009) The chemical biology of protein phosphorylation. Annu Rev Biochem 78:797–825PubMedCrossRefGoogle Scholar
  91. Tozawa Y, Teraishi M, Sasaki T, Sonoike K, Nishiyama Y, Itaya M, Miyao A, Hirochika H (2007a) The plastid sigma factor SIG1 maintains photosystem I activity via regulated expression of the psaA operon in rice chloroplasts. Plant J 52:124–132PubMedCrossRefGoogle Scholar
  92. Tozawa Y, Nozawa A, Kanno T, Narisawa T, Masuda S, Kasai K, Nanamiya H (2007b) Calcium-activated (p)ppGpp synthetase in chloroplasts of land plants. J Biol Chem 282:35536–35545PubMedCrossRefGoogle Scholar
  93. Tsunoyama Y, Morikawa K, Shiina T, Toyoshima Y (2002) Blue light specific and differential expression of a plastid sigma factor, Sig5 in Arabidopsis thaliana. FEBS Lett 516:225–228PubMedCrossRefGoogle Scholar
  94. Tsunoyama Y, Ishizaki Y, Morikawa K, Kobori M, Nakahira Y, Takeba G, Toshinori Y, Shiina T (2004) Blue light-induced transcription of plastid-encoded psbD gene is mediated by a nuclear-encoded transcription initiation factor, AtSig5. Proc Natl Acad Sci USA 101:3304–3309PubMedCrossRefGoogle Scholar
  95. Van der Biezen EA, Sun J, Coleman MJ, Bibb MJ, Jones JDG (2000) Arabidopsis RelA/SpoT homologd implicate (p)ppGpp in plant signalling. Proc Natl Acad Sci USA 97:3747–3752PubMedCrossRefGoogle Scholar
  96. Wade JT, Roa DC, Grainger DC, Hurd D, Busby SJW, Struhl K, Nudler E (2006) Extensive functional overlap between s factors in Escherichia coli. Nat Struct Mol Biol 13:806–814PubMedCrossRefGoogle Scholar
  97. Wagner EGH, Darfeuille F (2006) Small regulatory RNAs in bacteria. In: Nellen W, Hammann C (eds) Small RNAs: analysis and regulatory functions. Springer, Berlin, pp 1–30Google Scholar
  98. Weaver KE (2007) Emerging plasmid-encoded antisense RNA regulated systems. Curr Opin Microbiol 10:110–118PubMedCrossRefGoogle Scholar
  99. Wösten MM (1998) Eubacterial sigma factors. FEMS Microbiol Rev 22:127–150PubMedCrossRefGoogle Scholar
  100. Xie YD, Li W, Guo D, Dong J, Zhang Q, Fu Y, Ren D, Peng M, Xia Y (2010) The Arabidopsis gene SIGMA FACTOR-BINDING PROTEIN 1 plays a role in the salicylate- and jasmonate-mediated defence responses. Plant Cell Environ 33:828–839PubMedGoogle Scholar
  101. Xiong J-Y, Lai C-X, Qu Z, Yang X-Y, Qin X-H, Liu G-Q (2009) Recruitment of AtWHY1 and AtWHY3 by a distal element upstream of the kinesin gene AtKP1 to mediate transcriptional repression. Plant Mol Biol 71:437–449PubMedCrossRefGoogle Scholar
  102. Yao J, Roy-Chowdhury S, Allison L (2003) AtSig5 is an essential nucleus-encoded Arabidopsis σ-like factor. Plant Physiol 132:739–747PubMedCrossRefGoogle Scholar
  103. Zghidi W, Merendino L, Cottet A, Mache R, Lerbs-Mache S (2007) Nucleus-encoded plastid sigma factor SIG3 transcribes specifically the psbN gene in plastids. Nucleic Acids Res 35:455–464PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Laboratoire de Physiologie Cellulaire Végétale, Centre National de la Recherche Scientifique, CEA-Grenoble, UMR 5168Université Joseph FourierGrenoble cedexFrance

Personalised recommendations