Advertisement

Dynamic Features of Plastid Genome and Its Transcriptional Control in Plastid Development

  • Kengo KanamaruEmail author
  • Mamoru SugitaEmail author
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 36)

Summary

Land plants usually have different types of plastids, e.g. etioplasts, chloroplasts, amyloplasts, and chromoplasts. Although identical copies of the plastid genome are present in all plastid types, the level and pattern of accumulation of plastid transcripts varies largely among the different plastid types and during plastid differentiation and development. Plastid genomes possess many promoters of widely differing strength, and genes often have multiple initiation sites. Two distinct plastid RNA polymerases, plastid-encoded RNA polymerase (PEP) and nuclear-encoded RNA polymerase (NEP), direct such a complex transcription of plastid genes. Photosynthetic genes, e.g. psbA, psbD and rbcL are mainly transcribed by PEP. Some non-photosynthetic genes such as rpoB and accD are exclusively transcribed by NEP, and rrn and clpP genes are mutually transcribed by both PEP and NEP. The interplay of PEP and NEP results in a highly complex transcript pattern in plastids. PEP controls chloroplast development in leaves and its functional maintenance is primarily mediated by the variation of sigma factors. Arabidopsis thaliana has six nuclear-encoded plastid sigma factors (AtSIG1 to 6). In addition to the temporal dynamics of sigma factors during chloroplast development, the expression profile of each plant sigma factor in organs and cell types is diverse and probably correlated with the major function of each sigma factor. Extensive forward and reverse genetics studies revealed the role and specificity of respective sigma factors in transcription of different plastid genes involved in the biosynthesis and maintenance of the photosynthetic apparatus, during chloroplast development or under various environmental conditions such as light, salt and cold/heat stresses. Thus, transcriptional regulation in plastids, particularly in chloroplasts, is important for fine-tuned plastid gene expression.

Keywords

Sigma Factor Plastid Genome Bundle Sheath Chloroplast Development Plastid Gene 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations:

asRNA

Antisense RNA;

BLRP

Blue light responsive promoter;

BS cell

Bundle sheath cell;

CK

Caseine kinase;

cpCK2

Nuclear-coded plastid-targeted casein kinase 2;

CSK

Chloroplast sensor kinase;

DAPI

4′,6-diamidino-2-phenylindole;

IR

Inverted repeat sequence;

LSC

Large single copy region;

M cell

Mesophyll cell;

ncRNA

Non-coding RNA;

NEP

Nuclear-encoded (plastid) RNA polymerase;

NIP

NEP interacting protein;

ORF

Open reading frame;

PCR

Polymerase chain reaction;

PEP

Plastid-encoded (plastid) RNA polymerase;

PPR

Pentatricopeptide repeat;

PS I

Photosystem I;

PS II

Photosystem II;

pTAC

Plastid transcriptionally active chromosome;

ptDNA

Plastid DNA;

qRT-PCR

Quantitative reverse transcription-PCR;

RPOT

T3/T7 phage-type single-subunit RNA polymerase;

SIB1

Sigma factor-binding protein 1;

SIG

Sigma factor;

snmRNA

Small non-messenger RNA;

SPP

Stromal processing peptidase;

spRNAP-IV

Single-polypeptide nuclear RNA polymerase;

SSC

Small single copy region;

UTR

Untranslated region;

Ycf

The conserved hypothetical open reading frame

Notes

Acknowledgments

This work was supported by Special Coordination Funds for Promoting Science and Technology, Creation of Innovation Centers for Advanced Interdisciplinary Research Areas (Innovative Bioproduction Kobe), MEXT, Japan, to KK and by a Grant-in-Aid for Scientific Research (C) from the Japan Society for the Promotion of Science (JSPS) KAKENHI (20570033) to MS.

References

  1. Allison LA (2000) The role of sigma factors in plastid transcription. Biochimie 82:537–548PubMedCrossRefGoogle Scholar
  2. 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
  3. Asin-Cayuela J, Gustafsson CM (2007) Mitochondrial transcription and its regulation in mammalian cells. Trends Biochem Sci 32:111–117PubMedCrossRefGoogle Scholar
  4. Axmann IM, Kensche P, Vogel J, Kohl S, Herzel H, Hess WR (2005) Identification of cyanobacterial non-coding RNAs by comparative genome analysis. Genome Biol 6:R73PubMedCrossRefGoogle Scholar
  5. 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
  6. Azevedo J, Courtois F, Hakimi MA, Demarsy E, Lagrange T, Alcaraz JP, Jaiswal P, Maréchal-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
  7. Baba K, Nakano T, Yamagishi K, Yoshida S (2001) Involvement of a nuclear-encoded basic helix-loop-helix protein in transcription of the light-responsive promoter of psbD. Plant Physiol 125:595–603PubMedCrossRefGoogle Scholar
  8. Baba K, Schmidt J, Espinosa-Ruiz A, Villarejo A, Shiina T, Gardeström P, Sane AP, Bhalerao RP (2004) Organellar gene transcription and early seedling development are affected in the rpoT;2 mutant of Arabidopsis. Plant J 38:38–48PubMedCrossRefGoogle Scholar
  9. Baginsky S, Tiller K, Pfannschmidt T, Link G (1999) PTK, the chloroplast RNA polymerase-associated protein kinase from mustard (Sinapis alba), mediates redox control of plastid in vitro transcription. Plant Mol Biol 39:1013–1023PubMedCrossRefGoogle Scholar
  10. Baumgartner BJ, Rapp JC, Mullet JE (1989) Plastid transcription activity and DNA copy number increase early in barley chloroplast development. Plant Physiol 89:1011–1018PubMedCrossRefGoogle Scholar
  11. Bendich AJ (1987) Why do chloroplasts and mitochondria contain so many copies of their genome? Bioessays 6:279–281PubMedCrossRefGoogle Scholar
  12. Bendich AJ (1991) Moving pictures of DNA released upon lysis from bacteria, chloroplasts, and mitochondria. Protoplasma 160:121–130CrossRefGoogle Scholar
  13. Biswal UC, Biswal B, Raval MK (2003) Chloroplast biogenesis. From proplastid to gerontoplast. Kluwer, Dordrecht, p 353CrossRefGoogle Scholar
  14. 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
  15. Bock R (2007) Structure, function, and inheritance of plastid genomes. In: Rock R (ed) Cell and molecular biology of plants. Topics in current genetics. Vol. 19. Springer, Berlin, Heidelberg, pp 29–63Google Scholar
  16. Bollenbach TJ, Sharwood RE, Gutierrez R, Lerbs-Mache S, Stern DB (2009) The RNA-binding proteins CSP41a and CSP41b may regulate transcription and translation of chloroplast-encoded RNAs in Arabidopsis. Plant Mol Biol 69:541–552PubMedCrossRefGoogle Scholar
  17. Bülow S, Link G (1987) DNA-binding proteins of thetranscriptionally active chromosome from mustard (Sinapis alba L.) chloroplasts. Curr Genet 12:157–159Google Scholar
  18. Bünger W, Feierabend J (1980) Capacity for RNA synthesis in 70S ribosome-deficient plastids of heat-bleached rye leaves. Planta 149:163–169CrossRefGoogle Scholar
  19. 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
  20. Cahoon AB, Takacs EM, Sharpe RM, Stern DB (2008) Nuclear, chloroplast, and mitochondrial transcript abundance along a maize leaf developmental gradient. Plant Mol Biol 66:33–46PubMedCrossRefGoogle Scholar
  21. Chang CC, Sheen J, Bligny M, Niwa Y, Lerbs-Mache S, Stern DB (1999) Functional analysis of two maize cDNAs encoding T7-like RNA polymerases. Plant Cell 11:911–926PubMedGoogle Scholar
  22. Chi W, Mao J, Li Q, Ji D, Zou M, Lu C, Zhang L (2010) 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 64:14–25PubMedCrossRefGoogle Scholar
  23. 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
  24. del Campo EM (2009) Post-transcriptional control of chloroplast gene expression. Gene Regul Syst Biol 3:31–47Google Scholar
  25. 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
  26. Deng XW, Gruissem W (1987) Control of plastid gene expression during development: the limited role of transcriptional regulation. Cell 49:379–387PubMedCrossRefGoogle Scholar
  27. Deng XW, Gruissem W (1988) Constitutive transcription and regulation of gene expression in non-photosynthetic plastids of higher plants. EMBO J 7:3301–3308PubMedGoogle Scholar
  28. Deng XW, Wing RA, Gruissem W (1989) The chloroplast genome exists in multimeric forms. Proc Natl Acad Sci USA 86:4156–4160PubMedCrossRefGoogle Scholar
  29. Dühring U, Axmann IM, Hess WR, Wilde A (2006) An internal antisense RNA regulates expression of the photosynthesis gene isiA. Proc Natl Acad Sci USA 103:7054–7058PubMedCrossRefGoogle Scholar
  30. Egea we I, Barsan C, Bian W, Purgatto E, Latche A, Chervin C, Bouzayen M, Pech JC (2010) Chromoplast differentiation: current status and perspectives. Plant Cell Physiol 51:1601–1611CrossRefGoogle Scholar
  31. Eisermann A, Tiller K, Link G (1990) 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 9:3981–3987PubMedGoogle Scholar
  32. Emanuel C, Weihe A, Graner A, Hess WR, Börner T (2004) Chloroplast development affects expression of phage-type RNA polymerases in barley leaves. Plant J 38:460–472PubMedCrossRefGoogle Scholar
  33. Falcon de Longevialle A, Small IS, Lurin C (2010) Nuclearly encoded splicing factors implicated in RNA splicing in higher plant organelles. Mol Plant 3:691–705CrossRefGoogle Scholar
  34. Falk J, Schmidt A, Krupinska K (1993) Characterization of plastid DNA transcription in ribosome deficient plastids of heat-bleached barley leaves. J Plant Physiol 141:178–181CrossRefGoogle Scholar
  35. Favory JJ, Kobayashi 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
  36. Fujiwara M, Nagashima A, Kanamaru K, Tanaka K, Takahashi H (2000) Three new nuclear genes, sigD, sigE and sigF, encoding putative plastid RNA polymerase σ factors in Arabidopsis thaliana. FEBS Lett 481:47–52PubMedCrossRefGoogle Scholar
  37. Gao L, Su YJ, Wang T (2010) Plastid genome sequencing, comparative genomics, and phylogenomics: current status and prospects. J Syst Evol 48:77–93CrossRefGoogle Scholar
  38. Georg J, Honsel A, Vosse B, Rennenberg H, Herss WR (2010) A long antisense RNA in plant chloroplasts. New Phytol 186:615–622PubMedCrossRefGoogle Scholar
  39. Goldschmitz-Clermont M, Choquet Y, Girard-Bascou J, Michel F, Schimmer-Rahire M, Rochaix JD (1991) A small chloroplast RNA may be required for trans-splicing in Chlamydomonas reinhardtii. Cell 65:135–143CrossRefGoogle Scholar
  40. Gottesman S (2005) Micros for microbes: non-coding regulatory RNAs in bacteria. Trends Genet 21:399–404PubMedCrossRefGoogle Scholar
  41. Gounaris I, Price CA (1987) Plastid transcripts in chloroplasts and chromoplasts of Capsicum annuum. Curr Genet 12:219–224CrossRefGoogle Scholar
  42. Gruber TM, Gross CA (2003) Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 57:441–466PubMedCrossRefGoogle Scholar
  43. Gruissem W, Barkan A, Deng XW, Stern D (1988) Transcriptional and post-transcriptional control of plastid mRNA levels in higher plants. Trends Genet 4:258–263PubMedCrossRefGoogle Scholar
  44. Hajdukiewicz PTJ, Allison LA, 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 16:4041–4048PubMedCrossRefGoogle Scholar
  45. 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
  46. Han CD, Coe EH, Martienssen RA (1992) Molecular cloning and characterization of iojap (ij), a pattern striping gene of maize. EMBO J 11:4037–4046PubMedGoogle Scholar
  47. 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
  48. 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
  49. Hara K, Sugita M, Aoki S (2001) Cloning and characterization of the cDNA for a plastid σ factor 1 from the moss Physcomitrella patens. Biochim Biophys Acta 1517:302–306PubMedCrossRefGoogle Scholar
  50. Harley CB, Reynolds RP (1987) Analysis of E. coli promoter sequences. Nucleic Acids Res 15:2343–2361PubMedCrossRefGoogle Scholar
  51. Hedtke B, Börner T, Weihe A (1997) Mitochondrial and chloroplast phage-type RNA polymerases in Arabidopsis. Science 277:809–811PubMedCrossRefGoogle Scholar
  52. Hedtke B, Börner T, Weihe A (2000) One RNA polymerase serving two genomes. EMBO Rep 1:435–440PubMedCrossRefGoogle Scholar
  53. Hedtke B, Legen J, Weihe A, Herrmann RG, Börner T (2002) Six active phage-type RNA polymerase genes in Nicotiana tabacum. Plant J 30:625–637PubMedCrossRefGoogle Scholar
  54. Herrin D, Nickelsen J (2004) Chloroplast RNA processing and stability. Photosynth Res 82:301–314PubMedCrossRefGoogle Scholar
  55. Herrmann RG, Bohnert HJ, Kowallik KV, Schmitt JM (1975) Size, conformation and purity of chloroplast DNA of some higher plants. Biochim Biophys Acta 378:305–317PubMedCrossRefGoogle Scholar
  56. Hess WR, Börner T (1999) Organellar RNA polymerases of higher plants. Int Rev Cytol 190:1–59PubMedCrossRefGoogle Scholar
  57. Hess WR, Prombona A, Fieder B, Subramanian AR, Börner T (1993) Chloroplast rps15 and the rpoB/C1/C2 gene cluster are strongly transcribed in ribosome-deficient plastids: evidence for a functioning non-chloroplast-encoded RNA polymerase. EMBO J 12:563–571PubMedGoogle Scholar
  58. 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
  59. Hricová A, Quesada V, Micol JL (2006) The SCABRA3 nuclear gene encodes the plastid RpoTp RNA polymerase, which is required for chloroplast biogenesis and mesophyll cell proliferation in Arabidopsis. Plant Physiol 141:942–956PubMedCrossRefGoogle Scholar
  60. Ionescu D, Voss B, Oren A, Hess WR, Muro-Pastor AM (2010) Heterocystis-specific transcription of NsiR1, a non-coding RNA encoded in a tandem array of direct repeats in cyanobacteria. J Mol Biol 398:177–188PubMedCrossRefGoogle Scholar
  61. 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
  62. Isono K, Shimizu M, Yoshimoto K, Niwa Y, Satoh K, Yokota A, Kobayashi H (1997) Leaf-specifically expressed genes for polypeptides destined for chloroplasts with domains of σ70 factors of bacterial RNA polymerases in Arabidopsis thaliana. Proc Natl Acad Sci USA 94:14948–14953PubMedCrossRefGoogle Scholar
  63. Jeong SY, Peffer N, Meier I (2004) Phosphorylation by protein kinase CKII modulates the DNA-binding activity of a chloroplast nucleoid-associated protein. Planta 219:298–302PubMedCrossRefGoogle Scholar
  64. Kabeya Y, Hashimoto K, Sato N (2002) Identification and characterization of two phage-type RNA polymerase cDNAs in the moss Physcomitrella patens: implication of recent evolution of nuclear-encoded RNA polymerase of plastids in plants. Plant Cell Physiol 43:245–255PubMedCrossRefGoogle Scholar
  65. Kabeya Y, Kobayashi Y, Suzuki H, Itoh J, Sugita M (2007) Transcription of plastid genes is modulated by two nuclear-encoded α subunits of plastid RNA polymerase in the moss Physcomitrella patens. Plant J 52:730–741PubMedCrossRefGoogle Scholar
  66. Kahlau S, Bock R (2008) Plastid transcriptiomics and translatomics of tomato fruit development and chloroplast-to-chromoplast defferentiation: chromoplast gene expression largely serves the production of a single protein. Plant Cell 20:856–874PubMedCrossRefGoogle Scholar
  67. Kanai R, Edwards GE (1973) Separation of mesophyll protoplasts and bundle sheath cells from maize leaves for photosynthetic studies. Plant Physiol 51:1133–1137PubMedCrossRefGoogle Scholar
  68. Kanai R, Edwards GE (1999) The biochemistry of C4 photosynthesis. In: Sage RF, Monson RK (eds) C4 plant biology (Physiological ecology). Academic, San Diego, pp 49–87CrossRefGoogle Scholar
  69. Kanamaru K, Tanaka K (2004) Roles of chloroplast RNA polymerase sigma factors in chloroplast development and stress response in higher plants. Biosci Biotechnol Biochem 68:2215–2223PubMedCrossRefGoogle Scholar
  70. Kanamaru K, Fujiwara M, Seki M, Katagiri T, Nakamura M, Mochizuki N, Nagatani A, Shinozaki K, Tanaka K, Takahashi H (1999) Plastidic RNA polymerase sigma factors in Arabidopsis. Plant Cell Physiol 40:832–842PubMedCrossRefGoogle Scholar
  71. Kanamaru K, Nagashima A, Fujiwara M, Shimada H, Shirano Y, Nakabayashi K, Shibata 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
  72. Kapoor S, Sugiura M (1999) Identification of two essential sequence elements in the nonconsensus type II PatpB-290 plastid promoter by using plastid transcription extracts from cultured tobacco BY-2 cells. Plant Cell 11:1799–1810PubMedGoogle Scholar
  73. Kapoor S, Suzuki JY, Sugiura M (1997) Identification and functional significance of a new class of non-consensus-type plastid promoters. Plant J 11:327–337PubMedCrossRefGoogle Scholar
  74. Kasai K, Kawagishi-Kobayashi M, Teraischi M, Ito Y, Ochi K, Wakasa K, Tozawa Y (2004) Differential expression of three plastidial sigma factors, OsSIG1, OsSIG2A, and OsSIG2B, during leaf development in rice. Biosci Biotechnol Biochem 68:973–977PubMedCrossRefGoogle Scholar
  75. Kato Y, Murakami S, Yamamoto Y, Chatani H, Kondo Y, Nakano T, Yokota A, Sato F (2004) The DNA-binding protease, CND41, and the degradation of ribuloase-1,5-bisphosphate carboxylase/oxygenase in senescent leaves of tobacco. Planta 220:97–104PubMedCrossRefGoogle Scholar
  76. Kestermann M, Neukirchen S, Kloppstech K, Link G (1998) Sequence and expression characteristics of a nuclear-encoded chloroplast sigma factor from mustard (Sinapis alba). Nucleic Acids Res 26:2747–2753PubMedCrossRefGoogle Scholar
  77. Kobayashi Y, Dokiya Y, Sugita M (2001) Dual targeting of phage-type RNA polymerase to both mitochondria and plastids is due to alternative translation initiation in single transcripts. Biochem Biophys Res Commun 289:1106–1113PubMedCrossRefGoogle Scholar
  78. Krause K, Maier RM, Kofer W, Krupinska K, Herrmann RG (2000) Disruption of plastid-encoded RNA polymerase genes in tobacco: expression of only a distinct set of genes is not based on selective transcription of the plastid chromosome. Mol Gen Genet 263:1022–1030PubMedCrossRefGoogle Scholar
  79. Kravchenko JE, Rogozin IB, Koonin EV, Chumakov PM (2005) Transcription of mammalian messenger RNAs by a nuclear RNA polymerase of mitochondrial origin. Nature 436:735–739PubMedCrossRefGoogle Scholar
  80. Krupinska K, Apel K (1989) Light-induced transformation of etioplasts to chloroplasts of barley without transcriptional control of plastid gene expression. Mol Gen Genet 219:467–473CrossRefGoogle Scholar
  81. 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
  82. Kühn K, Bohne AV, Liere K, Weihe A, Börner T (2007) Arabidopsis phage-type RNA polymerases: accurate in vitro transcription of organellar genes. Plant Cell 19:959–971PubMedCrossRefGoogle Scholar
  83. Kühn K, Richter U, Meyer EH, Delannoy E, Longevialle AF, O’Toole N, Börner T, Millar AH, Small ID, Whelan J (2009) Phage-type RNA polymerase RPOTmp performs gene-specific transcription in mitochondria of Arabidopsis thaliana. Plant Cell 21:2762–2779PubMedCrossRefGoogle Scholar
  84. Kuroiwa T (1991) The replication, differentiation, and inheritance of plastids with emphasis on the concept of organelle nuclei. Int Rev Cytol 128:1–62CrossRefGoogle Scholar
  85. Kusumi K, Yara A, Mitsui N, Tozawa Y, Iba K (2004) Characterization of a rice nuclear-encoded plastid RNA polymerase gene OsRpoTp. Plant Cell Physiol 45:1194–1201PubMedCrossRefGoogle Scholar
  86. Lahiri SD, Allison LA (2000) Complementary expression of two plastid-localized sigma-like factors in maize. Plant Physiol 123:883–894PubMedCrossRefGoogle Scholar
  87. Lamppa GK, Bendich AJ (1979) Changes in chloroplast DNA levels during development of pea (Pisum sativum). Plant Physiol 64:126–130PubMedCrossRefGoogle Scholar
  88. Lawrence ME, Possingham JV (1985) Microspectro­fluorometric measurement of chloroplast DNA in dividing and expanding leaf cells of Spinacia oleracea. Plant Physiol 81:708–710Google Scholar
  89. Legen J, Kemps S, Krause K, Profanter B, Hermann RG, Maier RM (2002) Comparative analysis of plastid transcription profiles of entire plastid chromosomes from tobacco attributed to wild-type and PEP-deficient transcription machineries. Plant J 31:171–188PubMedCrossRefGoogle Scholar
  90. Lerbs-Mache S (1993) The 110-kDa polypeptide of spinach plastid DNA-dependent RNA polymerase: single-subunit enzyme or catalytic core of multimeric enzyme complexes? Proc Natl Acad Sci USA 90:5509–5513PubMedCrossRefGoogle Scholar
  91. Lerbs-Mache S (2011) Function of plastid sigma factors in higher plants: regulation of gene expression or just preservation of constitutive transcription? Plant Mol Biol 76:235–249Google Scholar
  92. Li W, Ruf S, Bock R (2006) Constancy of organellar genome copy numbers during leaf development and senescence in higher plants. Mol Genet Genomics 275:185–192PubMedCrossRefGoogle Scholar
  93. Liere K, Maliga P (1999) In vitro characterization of the tobacco rpoB promoter reveals a core sequence motif conserved between phage-type plastid and plant mitochondrial promoters. Plant Cell 18:249–257Google Scholar
  94. Liere K, Kaden D, Maliga P, Börner T (2004) Overexpression of phage-type RNA polymerase RpoTp in tobacco demonstrates its role in chloroplast transcription by recognizing a distinct promoter type. Nucleic Acids Res 32:1159–1165PubMedCrossRefGoogle Scholar
  95. Lilly JW, Havey MJ, Jackson S, Jiang J (2001) Cytogenomic analyses reveal the structural plasticity of the chloroplast genome in higher plants. Plant Cell 13:245–254PubMedGoogle Scholar
  96. Link G (2003) Redox regulation of chloroplast transcription. Antioxid Redox Signal 5:79–88PubMedCrossRefGoogle Scholar
  97. Link G, Coen DM, Bogorad L (1978) Differential expression of the gene for the large subunit of ribulose bisphosphate carboxylase in maize leaf cell types. Cell 15:725–731PubMedCrossRefGoogle Scholar
  98. Liu B, Troxler RF (1996) Molecular characterization of a positively photoregulated nuclear gene for a chloroplast RNA polymerase σ factor in Cyanidium caldarium. Proc Natl Acad Sci USA 93:3313–3318PubMedCrossRefGoogle Scholar
  99. Loschelder H, Homann A, Ogrzewalla K, Link G (2004) Proteomics-based sequence analysis of plant gene expression – the chloroplast transcription apparatus. Phytochemistry 65:1785–1793PubMedCrossRefGoogle Scholar
  100. 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
  101. Lung B, Zemann A, Madej MJ, Schuelke M, Techritz S, Ruf S, Bock R (2006) Identification of small non-coding RNAs from mitochondria and chloroplasts. Nucleic Acids Res 34:3842–3852PubMedCrossRefGoogle Scholar
  102. Lysenko EA (2007) Plant sigma factors and their role in plastid transcription. Plant Cell Rep 26:845–859PubMedCrossRefGoogle Scholar
  103. 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
  104. Maliga P (1998) Two plastid RNA polymerases of higher plants: an evolving story. Trends Plant Sci 3:4–6CrossRefGoogle Scholar
  105. Manning JE, Wolstenholme DR, Ryan RS, Hunter JA, Richards OC (1971) Circular chloroplast DNA from Euglena gracilis. Proc Natl Acad Sci USA 68:1169–1173PubMedCrossRefGoogle Scholar
  106. Marker C, Zemann A, Terhörst T, Kiefmann M, Kastenmayer JP, Green P, Bachellerie JP, Brosius J, Hüttenhofer A (2002) Experimental RNomics: identification of 140 candidates for small non-messenger RNAs in the plant Arabidopsis thaliana. Curr Biol 12:2002–2013PubMedCrossRefGoogle Scholar
  107. Monde RA, Schuster G, Stern DB (2000) Processing and degradation of chloroplast mRNA. Biochimie 82:573–582PubMedCrossRefGoogle Scholar
  108. Morikawa K, Shiina T, Murakami S, Toyoshima Y (2002) Novel nuclear-encoded proteins interacting with a plastid sigma factor Sig1, in Arabidopsis thaliana. FEBS Lett 514:300–304PubMedCrossRefGoogle Scholar
  109. Mullet JE (1988) Chloroplast development and gene expression. Annu Rev Plant Physiol Plant Mol Biol 39:475–502CrossRefGoogle Scholar
  110. Mullet JE (1993) Dynamic regulation of chloroplast transcription. Plant Physiol 103:309–313PubMedCrossRefGoogle Scholar
  111. Mullet JE, Klein RR (1987) Transcription and RNA stability are important determinants of higher plant chloroplast RNA levels. EMBO J 6:1571–1579PubMedGoogle Scholar
  112. 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, SIG2. Biosci Biotechnol Biochem 68:694–704PubMedCrossRefGoogle Scholar
  113. 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
  114. Nakamura T, Schuster G, Sugiura M, Sugita M (2004) Chloroplast RNA-binding and pentatricopeptide repeat proteins. Biochem Soc Trans 32(Pt 4):571–574PubMedGoogle Scholar
  115. Nakamura T, Naito K, Yokota N, Sugita C, Sugita M (2007) A cyanobacterial non-coding RNA, Yfr1, is required for growth under multiple stress conditions. Plant Cell Physiol 48:1309–1318PubMedCrossRefGoogle Scholar
  116. 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
  117. Ogrzewalla K, Piotrowski M, Reinbothe S, Link G (2002) The plastid transcription kinase from mustard (Sinapis alba L.). A nuclear-encoded CK2-type chloroplast enzyme with redox-sensitive function. Eur J Biochem 269:3329–3337PubMedCrossRefGoogle Scholar
  118. Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T et al (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322:562–574CrossRefGoogle Scholar
  119. 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
  120. 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
  121. Pfalz J, Liere K, Kandlbinder A, Dietz KJ, Oelmüller R (2006) pTAC2, -6, and −12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell 18:176–197PubMedCrossRefGoogle Scholar
  122. Pfannschmidt T, Link G (1997) The A and B forms of plastid DNA-dependent RNA polymerase from mustard (Sinapis alba L.) transcribe the same genes in a different developmental context. Mol Gen Genet 257:35–44PubMedCrossRefGoogle Scholar
  123. Phinney BS, Thelen JJ (2005) Protomic characterization of a triton-insoluble fraction from chloroplasts defines a novel group of proteins associated with macromolecular structures. J Proteome Res 4:497–506PubMedCrossRefGoogle Scholar
  124. Piechulla B, Imlay C, Gruissem W (1985) Plastid gene expression during fruit ripening in tomato. Plant Mol Biol 5:373–385CrossRefGoogle Scholar
  125. Privat I, Hakimi MA, Buhot L, Favory J-J, Lerbs-Mache S (2003) Characterization of Arabidopsis plastid sigma-like transcription factors SIG1, SIG2 and SIG3. Plant Mol Biol 51:385–399PubMedCrossRefGoogle Scholar
  126. Puthiyaveetil S, Ibrahim IM, Jelicic B, Tomasic A, Fulgosi H, Allen JF (2010) Transcriptional control of photosynthesis genes: the evolutionarily conserved regulatory mechanism in plastid genome function. Genome Biol Evol 2:888–896PubMedCrossRefGoogle Scholar
  127. Pyke K (2007) Plastid biogenesis and differentiation. In: Bock R (ed) Cell and molecular biology of plastids, vol 19, Topics in current genetics. Springer, Berlin, pp 1–28CrossRefGoogle Scholar
  128. Ravi V, Khurana JP, Tyagi AK, Khurana P (2008) An update on chloroplast genomes. Plant Syst Evol 271:101–122CrossRefGoogle Scholar
  129. Richter U, Kiessling J, Hedtke B, Decker E, Reski R, Börner T, Weihe A (2002) Two RpoT genes of Physcomitrella patens encode phage-type RNA polymerases with dual targeting to mitochondria and plastids. Gene 290:95–105PubMedCrossRefGoogle Scholar
  130. Sager R, Ishida MR (1963) Chloroplast DNA in Chlamydomonas. Proc Natl Acad Sci USA 50:725–730PubMedCrossRefGoogle Scholar
  131. Sakai A (2001) In vitro transcription/DNA synthesis using isolated organelle-nuclei: application to the analysis of the mechanisms that regulate organelle genome function. J Plant Res 114:199–211CrossRefGoogle Scholar
  132. Sakai A, Miyazawa Y, Suzuki T, Sasaki N, Kawano S, Kuroiwa T (1999) Plastid gene expression during amyloplast formation in cultured tobacco cells. J Plant Physiol 154:71–78CrossRefGoogle Scholar
  133. Salvador ML, Klein U, Bogorad L (1998) Endogenous fluctuations of DNA topology in the chloroplast of Chlamydomonas reinhardtii. Mol Cell Biol 18:7235–7242PubMedGoogle Scholar
  134. Sato S, Nakamura Y, Kaneko T, Asamizu E, Tabata S (1999) Complete structure of the chloroplast genome of Arabidopsis thaliana. DNA Res 6:283–290PubMedCrossRefGoogle Scholar
  135. Satoh J, Baba K, Nakahira Y, Tsunoyama Y, Shiina T, Toyoshima Y (1999) Developmental stage-specific multi-subunit plastid RNA polymerase (PEP) in wheat. Plant J 18:407–416PubMedCrossRefGoogle Scholar
  136. Schliebner I, Pribil M, Zuhlke J, Dietzmann A, Leister D (2008) A survey of chloroplast protein kinases and phosphatases in Arabidopsis thaliana. Curr Genomics 9:184–190PubMedCrossRefGoogle Scholar
  137. Schmitz-Linneweber C, Small I (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 13:663–670PubMedCrossRefGoogle Scholar
  138. Schön A, Krupp G, Gough S, Berry-Lowe S, Kannangara CG, Söll D (1986) The RNA required in the first step of chlorophyll biosynthesis is a chloroplast glutamate tRNA. Nature 322:281–284PubMedCrossRefGoogle Scholar
  139. 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 regulator of plastid gene expression. Proteomics 10:2191–2204PubMedCrossRefGoogle Scholar
  140. Schweer J (2010) Plant sigma factors come of age: flexible transcription factor network for regulated plastid gene expression. Endocyt Cell Res 20:1–20CrossRefGoogle Scholar
  141. Schweer J, Loschelder H, Link G (2006) A promoter switch that can rescue a plant sigma factor mutant. FEBS Lett 580:6617–6622PubMedCrossRefGoogle Scholar
  142. 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
  143. Sekine K, Hase T, Sato N (2002) Reversible DNA compaction by sulfite reductase regulates transcriptional activity of chloroplast nucleoids. J Biol Chem 277:24399–24404PubMedCrossRefGoogle Scholar
  144. Serino G, Maliga P (1998) RNA polymerase subunits encoded by the plastid rpo genes are not shared with the nucleus-encoded plastid enzyme. Plant Physiol 117:1165–1170PubMedCrossRefGoogle Scholar
  145. Sharpe RM, Mahajan A, Takacs EM, Stern DB and Cahoon AB (2011) Developmental and cell type characterization of bundle sheath and mesophyll chloroplast transcript abundance in maize. Curr Genet 57:89–102Google Scholar
  146. Sheen J (1999) C gene expression. Annu Rev Plant Physiol Plant Mol Biol 50:187–217PubMedCrossRefGoogle Scholar
  147. 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
  148. Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N et al (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043–2049PubMedGoogle Scholar
  149. Shirano Y, Shimada H, Kanamaru K, Fujiwara 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
  150. Sologub M, Litonin D, Anikin M, Mustaev A, Temiakov D (2009) TFB2 is a transient component of the catalytic site of the human mitochondrial RNA polymerase. Cell 139:934–944PubMedCrossRefGoogle Scholar
  151. Sriraman P, Silhavy D, Maliga P (1998) The phage-type PclpP-53 plastid promoter comprises sequences downstream of the transcription initiation site. Nucleic Acids Res 26:4874–4879PubMedCrossRefGoogle Scholar
  152. Steiner S, Dietzel L, Schroter Y, Fey V, Wagner R, Pfannschmidt T (2009) The role of phosphorylation in redox regulation of photosynthesis genes psaA and psbA during photosynthetic acclimation of mustard. Mol Plant 2:416–429PubMedCrossRefGoogle Scholar
  153. Stern DB, Goldschmidt-Clermont M, Hanson MR (2010) Chloroplast RNA metabolism. Annu Rev Plant Biol 61:125–155PubMedCrossRefGoogle Scholar
  154. Sugita M, Sugiura M (1996) Regulation of gene expression in chloroplasts of higher plants. Plant Mol Biol 32:315–326PubMedCrossRefGoogle Scholar
  155. Sugita M, Svab Z, Maliga P, Sugiura M (1997) Targeted deletion of sprA from the tobacco plastid genome indicates that the encoded small RNA is not essential for pre-16S rRNA maturation in plastids. Mol Gen Genet 257:23–27PubMedCrossRefGoogle Scholar
  156. Sugiura M (1992) The chloroplast genome. Plant Mol Biol 19:149–168PubMedCrossRefGoogle Scholar
  157. Sugiura C, Kobayashi Y, Aoki S, Sugita C, Sugita M (2003) Complete chloroplast DNA sequence of the moss Physcomitrella patens: evidence for the loss and relocation of rpoA from the chloroplast to the nucleus. Nucleic Acids Res 31:5324–5331PubMedCrossRefGoogle Scholar
  158. 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
  159. Tan S, Troxler RF (1999) Characterization of two chloroplast RNA polymerase sigma factors from Zea mays: photoregulation and differential expression. Proc Natl Acad Sci USA 96:5316–5321PubMedCrossRefGoogle Scholar
  160. Tan X-Y, Liu X-L, Wang W, Jia D-J, Chen L-Q, Zhang X-Q, Ye D (2010) Mutations in the Arabidopsis nuclear-encoded mitochondrial phage-type RNA polymerase gene RPOTm led to defects in pollen tube growth, female gametogenesis and embryogenesis. Plant Cell Physiol 51:635–649PubMedCrossRefGoogle Scholar
  161. Tanaka K, Oikawa K, Ohta N, Kuroiwa H, Kuroiwa T, Takahashi H (1996) Nuclear encoding of a chloroplast RNA polymerase sigma subunit in a red alga. Science 272:1932–1935PubMedCrossRefGoogle Scholar
  162. Tanaka K, Tozawa Y, Mochizuki N, Shinozaki K, Nagatani A, Wakasa K, Takahashi H (1997) 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 413:309–313PubMedCrossRefGoogle Scholar
  163. Tillich M, Beick S, Schmitz-Linneweber C (2010) Chloroplast RNA-binding proteins. Repair and regulation of chloroplast transcripts. RNA Biol 7:1–7CrossRefGoogle Scholar
  164. Tozawa Y, Tanaka K, Takahashi H, Wakasa K (1998) Nuclear encoding of a plastid sigma factor in rice and its tissue- and light-dependent expression. Nucleic Acids Res 26:415–419PubMedCrossRefGoogle Scholar
  165. Tozawa Y, Teraishi M, Sasaki T, Sonoike K, Nishiyama Y, Itaya M, Miyao A, Hirochika H (2007) 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
  166. Tsunoyama Y, Ishizaki Y, Morikawa K, Kobori M, Nakahira Y, Takeba G, Toyoshima 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
  167. Vera A, Sugiura M (1994) A novel RNA gene in the tobacco plastid genome: its possible role in the maturation of 16S rRNA. EMBO J 13:2211–2217PubMedGoogle Scholar
  168. Weihe A, Börner T (1999) Transcription and architecture of promoters in chloroplasts. Trends Plant Sci 4:169–170PubMedCrossRefGoogle Scholar
  169. Woodson JD, Chory J (2008) Coordination of gene expression between organellar and nuclear genomes. Nature Rev Genet 9:383–395PubMedCrossRefGoogle Scholar
  170. Wu CY, Lin CH, Chen LJ (1997) Identification of the transcription start site for the spinach chloroplast serine tRNA gene. FEBS Lett 418:157–161PubMedCrossRefGoogle Scholar
  171. 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
  172. Yin C, Richter U, Börner T, Weihe A (2010) Evolution of plant phage-type RNA polymerases: the genome of the basal angiosperm Nuphar advena encodes two mitochondrial and one plastid phage-type RNA polymerases. BMC Evol Biol 10:379–389PubMedCrossRefGoogle Scholar
  173. 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
  174. Zoschke R, Liere K, Börner T (2007) From seedling to mature plant: Arabidopsis plastidial genome copy number, RNA accumulation and transcription are differentially regulated during leaf development. Plant J 50:710–722PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Laboratory of Biological Chemistry, Graduate School of Agricultural ScienceKobe UniversityKobeJapan
  2. 2.Center for Gene ResearchNagoya UniversityNagoyaJapan

Personalised recommendations