Role and regulation of plastid sigma factors and their functional interactors during chloroplast transcription - Recent lessons from Arabidopsis thaliana

European Journal of Cell Biology

Volumn 89, Issue 12, 2010, Pages 940-946

  Schweer, Jennifer ^a   Türkeri, Hacer ^a   Kolpack, Andrea ^a   Link, Gerhard ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Arabidopsis mutants; Chloroplast transcription; Multi site phosphorylation control; Plant sigma factors; Plastid transcription kinase; Sigma interacting proteins

Indexed keywords

PROTEIN SERINE THREONINE KINASE; SIGMA FACTOR;

ARABIDOPSIS; CHLOROPLAST; NONHUMAN; PLASTID; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SHORT SURVEY; TRANSCRIPTION REGULATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLASTS; MODELS, BIOLOGICAL; PLASTIDS; SIGMA FACTOR; TRANSCRIPTION, GENETIC;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 78149411702     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejcb.2010.06.016     Document Type: Short Survey

References (81)

1. Abdallah F., Salamini F., Leister D. A prediction of the size and evolutionary origin of the proteome of chloroplasts of Arabidopsis. Trends Plant Sci. 2000, 5:141-142.
2. Baena-Gonzalez E., Baginsky S., Mulo P., Summer H., Aro E.M., Link G. Chloroplast transcription at different light intensities. Glutathione-mediated phosphorylation of the major RNA polymerase involved in redox-regulated organellar gene expression. Plant Physiol. 2001, 127:1044-1052.
3. Baginsky S., Tiller K., Link G. Transcription factor phosphorylation by a protein kinase associated with chloroplast RNA polymerase from mustard (Sinapis alba). Plant Mol. Biol. 1997, 34:181-189.
4. Baginsky S., Tiller K., Pfannschmidt T., Link G. PTK, the chloroplast RNA polymerase-associated protein kinase from mustard (Sinapis alba), mediates redox control of plastid in vitro transcription. Plant Mol. Biol. 1999, 39:1013-1023.
5. Baginsky S., Link G. Redox regulation of chloroplast gene expression. Photoprotection, Photoinhibition, Gene Regulation, and Environment Springer 2005, 269-287. Dordrecht, The Netherlands. B. Demmig-Adams, W.I. Adams, A.K. Mattoo (Eds.).
6. Benayoun B.A., Veitia R.A. A post-translational modification code for transcription factors: sorting through a sea of signals. Trends Cell Biol. 2009, 19:189-197.
7. Bollenbach T.J., Sharwood R.E., Gutierrez R., Lerbs-Mache S., Stern D.B. The RNA-binding proteins CSP41a and CSP41b may regulate transcription and translation of chloroplast-encoded RNAs in Arabidopsis. Plant Mol. Biol. 2009, 69:541-552.
8. Bülow S., Link G. DNA-binding proteins of the transcriptionally active chromosome from mustard (Sinapis alba L.) chloroplasts. Curr. Genet. 1987, 12:157-159.
9. Bülow S., Link G. Sigma-like activity from mustard (Sinapis alba L.) chloroplasts conferring DNA-binding and transcription specificity to E. coli core RNA polymerase. Plant Mol. Biol. 1988, 10:349-357.
10. Burgess R.R., Travers A.A., Dunn J.J., Bautz E.K.F. Factor stimulating transcription by RNA polymerase. Nature 1969, 221:43-46.
11. Cahoon A.B., Stern D.B. Plastid transcription: a menage à trois. Trends Plant Sci. 2001, 6:45-46.
12. Chang C.C., Sheen J., Bligny M., Niwa Y., Lerbs-Mache S., Stern D.B. Functional analysis of two maize cDNAs encoding T7-like RNA polymerases. Plant Cell 1999, 11:911-926.
13. Coll N.S., Danon A., Meurer J., Cho W.K., Apel K. Characterization of soldat8, a suppressor of singlet oxygen-induced cell death in Arabidopsis seedlings. Plant Cell Physiol. 2009, 50:707-718.
14. DeLano W.L. The PyMOL Molecular Graphics System 2002, DeLano Scientific, Palo Alto, CA, USA. http://www.pymol.org/.
15. Favory J.J., Kobayashi M., Tanaka K., Peltier G., Kreis M., Valay J.G., Lerbs-Mache S. Specific function of a plastid sigma factor for ndhF gene transcription. Nucleic Acids Res. 2005, 33:5991-5999.
16. Fujiwara M., Nagashima A., Kanamaru K., Tanaka K., Takahashi H. Three new nuclear genes, sigD, sigE and sigF, encoding putative plastid RNA polymerase sigma factors in Arabidopsis thaliana. FEBS Lett. 2000, 481:47-52.
17. Gray M.W., Lang B.F. Transcription in chloroplasts and mitochondria: a tale of two polymerases. Trends Microbiol. 1998, 6:1-3.
18. Gruber T.M., Gross C.A. Multiple sigma subunits and the partitioning of bacterial transcription space. Annu. Rev. Microbiol. 2003, 57:441-466.
19. Hakimi M.A., Privat I., Valay J.G., Lerbs-Mache S. Evolutionary conservation of C-terminal domains of primary sigma(70)-type transcription factors between plants and bacteria. J. Biol. Chem. 2000, 275:9215-9221.
20. Hallick R.B., Lipper C., Richards O.C., Rutter W.J. Isolation of a transcriptionally active chromosome from chloroplasts of Euglena gracilis. Biochemistry 1976, 15:3039-3045.
21. Hanaoka M., Kanamaru K., Takahashi H., Tanaka K. 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. 2003, 31:7090-7098.
22. Hedtke B., Börner T., Weihe A. Mitochondrial and chloroplast phage-type RNA polymerases in Arabidopsis. Science 1997, 277:809-811.
23. Hedtke B., Börner T., Weihe A. One RNA polymerase serving two genomes. EMBO Rep. 2000, 1:435-440.
24. Hedtke B., Legen J., Weihe A., Herrmann R.G., Börner T. Six active phage-type RNA polymerase genes in Nicotiana tabacum. Plant J. 2002, 30:625-637.
25. Helmann J.D. RNA polymerase: a nexus of gene regulation. Methods 2009, 47:1-5.
26. Hess W.R., Börner T. Organellar RNA polymerases of higher plants. Int. Rev. Cytol. 1999, 190:1-59.
27. Homann A., Link G. 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. 2003, 270:1288-1300.
28. Ishikawa M., Fujiwara M., Sonoike K., Sato N. Orthogenomics of photosynthetic organisms: bioinformatic and experimental analysis of chloroplast proteins of endosymbiont origin in Arabidopsis and their counterparts in Synechocystis. Plant Cell Physiol. 2009, 50:773-788.
29. Ishizaki Y., Tsunoyama Y., Hatano K., Ando K., Kato K., Shinmyo A., Kobori M., Takeba G., Nakahira Y., Shiina T. A nuclear-encoded sigma factor Arabidopsis SIG6, recognizes sigma-70 type chloroplast promoters and regulates early chloroplast development in cotyledons. Plant J. 2005, 42:133-144.
30. Jeong S.Y., Peffer N., Meier I. Phosphorylation by protein kinase CKII modulates the DNA-binding activity of a chloroplast nucleoid-associated protein. Planta 2004, 219:298-302.
31. Kanamaru K., Fujiwara M., Seki M., Katagiri T., Nakamura M., Mochizuki N., Nagatani A., Shinozaki K., Tanaka K., Takahashi H. Plastidic RNA polymerase sigma factors in Arabidopsis. Plant Cell Physiol. 1999, 40:832-842.
32. Kanamaru K., Nagashima A., Fujiwara M., Shimada H., Shirano Y., Nakabayashi K., Shibata D., Tanaka K., Takahashi H. An Arabidopsis sigma factor (SIG2)-dependent expression of plastid-encoded tRNAs in chloroplasts. Plant Cell Physiol. 2001, 42:1034-1043.
33. Kanamaru K., Tanaka K. Roles of chloroplast RNA polymerase sigma factors in chloroplast development and stress response in higher plants. Biosci. Biotechnol. Biochem. 2004, 68:2215-2223.
34. Kestermann M., Neukirchen S., Kloppstech K., Link G. Sequence and expression characteristics of a nuclear-encoded chloroplast sigma factor from mustard (Sinapis alba). Nucleic Acids Res. 1998, 26:2747-2753.
35. Kobayashi Y., Dokiya Y., Sugita M. 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. 2001, 289:1106-1113.
36. Kornberg R.D. The molecular basis of eukaryotic transcription. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:12955-12961.
37. Koussevitzky S., Nott A., Mockler T.C., Hong F., Sachetto-Martins G., Surpin M., Lim I.J., Mittler R., Chory J. Signals from chloroplasts converge to regulate nuclear gene expression. Science 2007, 316:715-719.
38. Kubota Y., Miyao A., Hirochika H., Tozawa Y., Yasuda H., Tsunoyama Y., Niwa Y., Imamura S., Shirai M., Asayama M. 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. 2007, 48:186-192.
39. Lerbs S., Bräutigam E., Mache R. DNA-dependent RNA polymerase of spinach chloroplasts: characterization of sigma-like and alpha-like polypeptides. Mol. Gen. Genet. 1988, 211:459-464.
40. Lerbs-Mache S. 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. U.S.A. 1993, 90:5509-5513.
41. Link G. Redox regulation of chloroplast transcription. Antioxid. Redox Signal. 2003, 5:79-88.
42. Liu B., Troxler R.F. 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. 1996, 93:3313-3318.
43. Loschelder H., Homann A., Ogrzewalla K., Link G. Proteomics-based sequence analysis of plant gene expression - the chloroplast transcription apparatus. Phytochemistry 2004, 65:1785-1793.
44. Loschelder H., Schweer J., Link B., Link G. Dual temporal role of plastid sigma factor 6 in Arabidopsis development. Plant Physiol. 2006, 142:642-650.
45. Lund O., Nielsen M., Lundegaard C., Worning P. CPHmodels 2.0: a computer program to extract 3D models. CASP5 Conference, Abstract A102 2002, http://www.cbs.dtu.dk/services/CPHmodels/.
46. Lysenko E.A. Plant sigma factors and their role in plastid transcription. Plant Cell Rep. 2007, 26:845-859.
47. Maliga P. Two plastid RNA polymerases of higher plants: an evolving story. Trends Plant Sci. 1998, 3:4-6.
48. Morikawa K., Shiina T., Murakami S., Toyoshima Y. Novel nuclear-encoded proteins interacting with a plastid sigma factor Sig1, in Arabidopsis thaliana. FEBS Lett. 2002, 514:300-304.
49. Nagashima A., Hanaoka M., Motohashi R., Seki M., Shinozaki K., Kanamaru K., Takahashi H., Tanaka K. DNA microarray analysis of plastid gene expression in an Arabidopsis mutant deficient in a plastid transcription factor, SIG2. Biosci. Biotechnol. Biochem. 2004, 68:694-704.
50. Narusaka M., Kawai K., Izawa N., Seki M., Shinozaki K., Seo S., Kobayashi M., Shiraishi T., Narusaka Y. 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. 2008, 74:345-354.
51. Niefind K., Guerra B., Pinna L.A., Issinger O.G., Schomburg D. Crystal structure of the catalytic subunit of protein kinase CK2 from Zea mays at 2.1Å resolution. EMBO J. 1998, 17:2451-2462.
52. Ogrzewalla K., Piotrowski M., Reinbothe S., Link G. The plastid transcription kinase from mustard (Sinapis alba L.). A nuclear-encoded CK2-type chloroplast enzyme with redox-sensitive function. Eur. J. Biochem. 2002, 269:3329-3337.
53. Onda Y., Yagi Y., Saito Y., Takenaka N., Toyoshima Y. 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. 2008, 55:968-978.
54. Pfalz J., Liere K., Kandlbinder A., Dietz K.J., Oelmuller R. pTAC2, -6, and -12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell 2006, 18:176-197.
55. Pfannschmidt T., Link G. Separation of two classes of plastid DNA-dependent RNA polymerases that are differentially expressed in mustard (Sinapis alba L.) seedlings. Plant Mol. Biol. 1994, 25:69-81.
56. Pfannschmidt T., Link G. 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. 1997, 257:35-44.
57. Pfannschmidt T., Ogrzewalla K., Baginsky S., Sickmann A., Meyer H.E., Link G. The multisubunit chloroplast RNA polymerase A from mustard (Sinapis alba L.) Integration of a prokaryotic core into a larger complex with organelle-specific functions. Eur. J. Biochem. 2000, 267:253-261.
58. Privat I., Hakimi M.A., Buhot L., Favory J.-J., Lerbs-Mache S. Characterization of Arabidopsis plastid sigma-like transcription factors SIG1, SIG2 and SIG3. Plant Mol. Biol. 2003, 51:385-399.
59. Puthiyaveetil S., Kavanagh T.A., Cain P., Sullivan J.A., Newell C.A., Gray J.C., Robinson C., van der Giezen M., Rogers M.B., Allen J.F. The ancestral symbiont sensor kinase CSK links photosynthesis with gene expression in chloroplasts. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:10061-10066.
60. Ream T.S., Haag J.R., Wierzbicki A.T., Nicora C.D., Norbeck A.D., Zhu J.K., Hagen G., Guilfoyle T.J., Pasa-Tolic L., Pikaard C.S. Subunit compositions of the RNA-silencing enzymes Pol IV and Pol V reveal their origins as specialized forms of RNA polymerase II. Mol. Cell 2009, 33:192-203.
61. Reiland S., Messerli G., Baerenfaller K., Gerrits B., Endler A., Grossmann J., Gruissem W., Baginsky S. Large-scale Arabidopsis phosphoproteome profiling reveals novel chloroplast kinase substrates and phosphorylation networks. Plant Physiol. 2009, 150:889-903.
62. Richter U., Kiessling J., Hedtke B., Decker E., Reski R., rner T., Weihe A. Two RpoT genes of Physcomitrella patens encode phage-type RNA polymerases with dual targeting to mitochondria and plastids. Gene 2002, 290:95-105.
63. Salinas P., Fuentes D., Vidal E., Jordana X., Echeverria M., Holuigue L. An extensive survey of CK2 alpha and beta subunits in Arabidopsis: multiple isoforms exhibit differential subcellular localization. Plant Cell Physiol. 2006, 47:1295-1308.
64. Sato N., Albrieux C., Joyard J., Douce R., Kuroiwa T. Detection and characterization of a plastid envelope DNA-binding protein which may anchor plastid nucleoids. EMBO J. 1993, 12:555-561.
65. Schliebner I., Pribil M., Zuhlke J., Dietzmann A., Leister D. A survey of chloroplast protein kinases and phosphatases in Arabidopsis thaliana. Curr. Genomics 2008, 9:184-190.
66. Schweer J., Loschelder H., Link G. A promoter switch that can rescue a plant sigma factor mutant. FEBS Lett. 2006, 580:6617-6622.
67. Schweer J., Geimer S., Meurer J., Link G. Arabidopsis mutants carrying chimeric sigma factor genes reveal regulatory determinants for plastid gene expression. Plant Cell Physiol. 2009, 50:1382-1386.
68. Schweer J. Plant sigma factors come of age: flexible transcription factor network for regulated plastid gene expression. Endocytobiosis Cell Res. 2010, 20:1-20.
69. Schweer J., Türkeri H., Link B., Link G. AtSIG6, a plastid sigma factor from Arabidopsis, reveals functional impact of cpCK2 phosphorylation. Plant J. 2010, 62:192-202.
70. Shiina T., Tsunoyama Y., Nakahira Y., Khan M.S. Plastid RNA polymerases, promoters, and transcription regulators in higher plants. Int. Rev. Cytol. 2005, 244:1-68.
71. 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. Chloroplast development in Arabidopsis thaliana requires the nuclear-encoded transcription factor Sigma B. FEBS Lett. 2000, 485:178-182.
72. Steiner S., Dietzel L., Schroter Y., Fey V., Wagner R., Pfannschmidt T. The role of phosphorylation in redox regulation of photosynthesis genes psaA and psbA during Photosynthetic acclimation of mustard. Mol. Plant 2009, 2:416-429.
73. Sugita M., Sugiura M. Regulation of gene expression in chloroplasts of higher plants. Plant Mol. Biol. 1996, 32:315-326.
74. Suzuki J.Y., Ytterberg A.J., Beardslee T.A., Allison L.A., Wijk K.J., Maliga P. Affinity purification of the tobacco plastid RNA polymerase and in vitro reconstitution of the holoenzyme. Plant J. 2004, 40:164-172.
75. Tanaka K., Oikawa K., Ohta N., Kuroiwa H., Kuroiwa T., Takahashi H. Nuclear encoding of a chloroplast RNA polymerase sigma subunit in a red alga. Science 1996, 272:1932-1935.
76. Tanaka K., Tozawa Y., Mochizuki N., Shinozaki K., Nagatani A., Wakasa K., Takahashi H. 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. 1997, 413:309-313.
77. Tiller K., Link G. Phosphorylation and dephosphorylation affect functional characteristics of chloroplast and etioplast transcription systems from mustard (Sinapis alba L.). EMBO J. 1993, 12:1745-1753.
78. Tsunoyama Y., Ishizaki Y., Morikawa K., Kobori M., Nakahira Y., Takeba G., Toyoshima Y., Shiina T. 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. 2004, 101:3304-3309.
79. Xie Y.D., Li W., Guo D., Dong J., Zhang Q., Fu Y., Ren D., Peng M., Xia Y. The Arabidopsis gene sigma factor-binding protein 1 plays a role in the salicylate- and jasmonate-mediated defence responses. Plant Cell Environ. 2010, (EPub ahead of print). 10.1111/j.1365-3040.2009.02109.x.
80. Yao J.L., Roy-Chowdhury S., Allison L.A. AtSig5 is an essential nucleus-encoded Arabidopsis sigma-like factor. Plant Physiol. 2003, 132:739-747.
81. Zghidi W., Merendino L., Cottet A., Mache R., Lerbs-Mache S. Nucleus-encoded plastid sigma factor SIG3 transcribes specifically the psbN gene in plastids. Nucleic Acids Res. 2007, 35:455-464.