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 and Cell Physiology

Volumn 54, Issue 10, 2013, Pages 1736-1748

  Kanazawa, Takehiko ^a,d   Ishizaki, Kimitsune ^b,e   Kohchi, Takayuki ^b   Hanaoka, Mitsumasa ^a   Tanaka, Kan ^a,c  

^a CHIBA UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e KOBE UNIVERSITY   (Japan)

Author keywords

Light dark response; Liverwort; Marchantia polymorpha; Plastid sigma factor; Plastid encoded plastid RNA polymerase; Stress response

Indexed keywords

ISOPROTEIN; MANNITOL; PHOTOPROTEIN; SIGMA FACTOR; VEGETABLE PROTEIN;

ADAPTATION; AMINO ACID SEQUENCE; ARTICLE; CELL NUCLEUS; CLASSIFICATION; COLD; DRUG EFFECT; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; LIGHT; LIGHT/DARK RESPONSE; LIVERWORT; MARCHANTIA; MARCHANTIA POLYMORPHA; METABOLISM; MOLECULAR GENETICS; NORTHERN BLOTTING; PHYLOGENY; PHYSIOLOGICAL STRESS; PLANT; PLASTID; PLASTID SIGMA FACTOR; PLASTID-ENCODED PLASTID RNA POLYMERASE; RADIATION EXPOSURE; SEQUENCE HOMOLOGY; STRESS; TIME; TRANSGENIC PLANT;

LIGHT/DARK RESPONSE; LIVERWORT; MARCHANTIA POLYMORPHA; PLASTID SIGMA FACTOR; PLASTID-ENCODED PLASTID RNA POLYMERASE; STRESS RESPONSE;

ADAPTATION, PHYSIOLOGICAL; AMINO ACID SEQUENCE; BLOTTING, NORTHERN; CELL NUCLEUS; COLD TEMPERATURE; GENE EXPRESSION REGULATION, PLANT; LIGHT; LUMINESCENT PROTEINS; MANNITOL; MARCHANTIA; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT PROTEINS; PLANTS; PLANTS, GENETICALLY MODIFIED; PLASTIDS; PROTEIN ISOFORMS; SEQUENCE HOMOLOGY, AMINO ACID; SIGMA FACTOR; STRESS, PHYSIOLOGICAL; TIME FACTORS;

EID: 84885945353     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pct119     Document Type: Article

References (63)

1. Ashby, M.K., Houmard, J. and Mullineaux, C.W. (2002) The ycf27 genes from cyanobacteria and eukaryotic algae: distribution and implications for chloroplast evolution. FEMS Microbiol. Lett. 214: 25-30. (Pubitemid 35245518)
2. Bowman, J.L., Floyd, S.K. and Sakakibara, K. (2007) Green genes-comparative genomics of the green branch of life. Cell 129: 229-234. (Pubitemid 46574980)
3. Chiyoda, S., Linley, P.J., Yamato, K.T., Fukuzawa, H., Yokota, A. and Kohchi, T. (2007) Simple and efficient plastid transformation system for the liverwort Marchantia polymorpha L. suspensionculture cells. Transgenic Res. 16: 41-49. (Pubitemid 46058751)
4. Chiyoda, S., Ishizaki, K., Kataoka, H., Yamato, K.T. and Kohchi, T. (2008) Direct transformation of the liverwort Marchantia polymorpha L. by particle bombardment using immature thalli developing from spores. Plant Cell Rep. 27: 1467-1473.
5. Christopher, D.A., Kim, M. and Mullet, J.E. (1992) A novel lightregulated promoter is conserved in cereal and dicot chloroplasts. Plant Cell 4: 785-798.
6. Curtis, M.D. and Grossniklaus, U. (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133: 462-469. (Pubitemid 37325657)
7. Dat, J., Vandenabeele, S., Vranová, E., Van Montagu, M., Inzé, D. and Van Breusegem, F. (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol. Life Sci. 57: 779-795. (Pubitemid 30392035)
8. Enami, K., Ozawa, T., Motohashi, N., Nakamura, M., Tanaka, K. and Hanaoka, M. (2011) Plastid-to-nucleus retrograde signals are essential for the expression of nuclear starch biosynthesis genes during amyloplast differentiation in tobacco BY-2 cultured cells. Plant Physiol. 157: 518-530.
9. Favory, J.-J., Kobayashi, M., Tanaka, K., Peltier, G., Kreis, M., Valay, J.-G. et al. (2005) Specific function of a plastid sigma factor for ndhF gene transcription. Nucleic Acids Res. 33: 5991-5999. (Pubitemid 41742618)
10. Fujiwara, M., Nagashima, A., Kanamaru, K., Tanaka, K. and Takahashi, H. (2000) Three new nuclear genes, sigD, sigE and sigF, encoding putative plastid RNA polymerase s factors in Aarabidopsis thaliana. FEBS Lett. 481: 47-52. (Pubitemid 30662375)
11. Gadjev, I., Vanderauwera, S., Gechev, T.S., Laloi, C., Minkov, I.N., Shulaev, V. et al. (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol. 141: 436-445. (Pubitemid 43974538)
12. Gamborg, O.L., Miller, R.A. and Ojima, K. (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp. Cell Res. 50: 151-158.
13. Griesbeck, O., Baird, G.S., Campbell, R.E., Zacharias, D.A. and Tsien, R.Y. (2001) Reducing the environmental sensitivity of yellow fluorescent protein. J. Biol. Chem. 276: 29188-29194.
14. Hajdukiewicz, P., Svab, Z. and Maliga, P. (1994) The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25: 989-994. (Pubitemid 2152867)
15. Hanaoka, M., Kanamaru, K., Fujiwara, M., Takahashi, H. and Tanaka, K. (2005) Glutamyl-tRNA mediates a switch in RNA polymerase use during chloroplast biogenesis. EMBO Rep. 6: 545-550. (Pubitemid 40973963)
16. Hanaoka, M., Kato, M., Anma, M. and Tanaka, K. (2012) In vivo monitoring of transcription regulation by SIG1, an essential sigma factor for chloroplast RNA polymerase in Arabidopsis thaliana. Int. J. Mol. Sci. 13: 12182-12194.
17. Hanaoka, M. and Tanaka, K. (2008) Dynamics of RpaB-promoter interaction during high light stress, revealed by chromatin immunoprecipitation (ChIP) analysis in Synechococcus elongatus PCC 7942. Plant J. 56: 327-335.
18. Hara, K., Morita, M., Takahashi, R., Sugita, M., Kato, S. and Aoki, S. (2001a) Characterization of two genes, Sig1 and Sig2, encoding distinct plastid s factors in the moss Physcomitrella patens: phylogenetic relationships to plastid s factors in higher plants. FEBS Lett. 499: 87-91. (Pubitemid 32539327)
19. Hara, K., Sugita, M. and Aoki, S. (2001b) Cloning and characterization of the cDNA for a plastid s factor from the moss Physcomitrella patens. Biochim. Biophys. Acta 1517: 302-306. (Pubitemid 32126530)
20. Hirooka, S., Hanaoka, M., Enami, K., Kanazawa, T., Sone, T., Imoto, Y. et al. (2012) Nuclear-encoded plastid sigma factor SIG6 exclusively contributes to chloroplast differentiation in plastid differentiation of Arabidopsis thaliana. Cytologia 77: 73-82.
21. Ichikawa, K., Shimizu, A., Okada, R., Satbhai, S.B. and Aoki, S. (2008) The plastid sigma factor SIG5 is involved in the diurnal regulation of the chloroplast gene psbD in the moss Physcomitrella patens. FEBS Lett. 582: 405-409.
22. Ichikawa, K., Sugita, M., Imaizumi, T., Wada, M. and Aoki, S. (2004) 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: 4285-4298.
23. Ishizaki, K., Chiyoda, S., Yamato, K.T. and Kohchi, T. (2008) Agrobacterium-mediated transformation of the haploid liverwort Marchantia polymorpha L., an emerging model for plant biology. Plant Cell Physiol. 49: 1084-1091. (Pubitemid 351989696)
24. Ishizaki, K., Johzuka-Hisatomi, Y., Ishida, S., Iida, S. and Kohchi, T. (2013) Homologous recombination-mediated gene targeting in the liverwort Marchantia polymorpha L. Sci. Rep. 3: 1532.
25. Ishizaki, K., Nonomura, M., Kato, H., Yamato, K.T. and Kohchi, T. (2012) Visualization of auxin-mediated transcriptional activation using a common auxin-responsive reporter system in the liverwort Marchantia polymorpha. J. Plant Res. 125: 643-651.
26. Ishizaki, Y., Tsunoyama, Y., Hatano, K., Ando, K., Kato, K., Shinmyo, A. et al. (2005) A nuclear-encoded sigma factor, Arabidopsis SIG6, recognizes sigma-70 type chloroplast promoters and regulates early chloroplast development in cotyledons. Plant J. 42: 133-144. (Pubitemid 40589377)
27. Isono, K., Shimizu, M., Yoshimoto, K., Niwa, Y., Satoh, K., Yokota, A. et al. (1997) Leaf-specifically expressed genes for polypeptides destined for chloroplasts with domains of s70 factors of bacterial RNA polymerases in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 94: 14948-14953.
28. Jaspers, P. and Kangasjärvi, J. (2010) Reactive oxygen species in abiotic stress signaling. Physiol. Plant. 138: 405-413.
29. Jefferson, R.A., Kavanagh, T.A. and Bevan, M.W. (1987) GUS fusions: b-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6: 3901-3907.
30. Kanamaru, K., Nagashima, A., Fujiwara, M., Shimada, H., Shirano, Y., Nakabayashi, K. et al. (2001) An Arabidopsis sigma factor (SIG2)-dependent expression of plastid-encoded tRNAs in chloroplasts. Plant Cell Physiol. 42: 1034-1043. (Pubitemid 33037870)
31. Kappel, A.D. and van Waasbergen, L.G. (2007) The response regulator RpaB binds the high light regulatory 1 sequence upstream of the high-light-inducible hliB gene from the cyanobacterium Synechocystis PCC 6803. Arch. Microbiol. 187: 337-342. (Pubitemid 46452217)
32. Kasai, K., Kawagishi-Kobayashi, M., Teraishi, M., Ito, Y., Ochi, K., Wakasa, K. et al. (2004) Differential expression of three plastidial sigma factors, OsSIG1, OsSIG2A, and OsSIG2B, during leaf development in rice. Biosci. Biotechnol. Biochem. 68: 973-977. (Pubitemid 39251479)
33. Kestermann, M., Neukirchen, S., Kloppstech, K. and Link, G. (1998) Sequence and expression characteristics of a nuclear-encoded chloroplast sigma factor from mustard (Sinapis alba). Nucleic Acids Res. 26: 2747-2753. (Pubitemid 28297392)
34. Kubota, Y., Miyao, A., Hirochika, H., Tozawa, Y., Yasuda, H., Tsunoyama, Y. et al. (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: 186-192. (Pubitemid 46181133)
35. Kubota, A., Ishizaki, K., Hosaka, M. and Kohchi, T. (2013) Efficient Agrobacterium-mediated transformation of the liverwort Marchantia polymorpha using regenerating thalli. Biosci. Biotechnol. Biochem. 77: 167-172.
36. Kuchka, M.R., Goldschmidt-Clermont, M., van Dillewijn, J. and Rochaix, J.D. (1989) Mutation at the Chlamydomonas nuclear NAC2 locus specifically affects stability of the chloroplast psbD transcript encoding polypeptide D2 of PS II. Cell 58: 869-876.
37. Lahiri, S.D., Yao, J., McCumbers, C. and Allison, L.A. (1999) Tissuespecific and light-dependent expression within a family of nuclear-encoded sigma-like factors from Zea mays. Mol. Cell Biol. Res. Commun. 1: 14-20. (Pubitemid 129532287)
38. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H. et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948. (Pubitemid 350162903)
39. 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: 235-249.
40. Liu, B. and Troxler, R.F. (1996) Molecular characterization of a positively photoregulated nuclear gene for a chloroplast RNA polymerase s factor in Cyanidium caldarium. Proc. Natl Acad. Sci. USA 93: 3313-3318. (Pubitemid 26125616)
41. Møller, S.G., Kim, Y.S., Kunkel, T. and Chua, N.H. (2003) PP7 is a positive regulator of blue light signaling in Arabidopsis. Plant Cell 15: 1111-1119. (Pubitemid 36579971)
42. Nakahira, Y., Baba, K., Yoneda, A., Shiina, T. and Toyoshima, Y. (1998) Circadian-regulated transcription of the psbD light-responsive promoter in wheat chloroplasts. Plant Physiol. 118: 1079-1088. (Pubitemid 128653034)
43. Nagashima, A., Hanaoka, M., Shikanai, T., Fujiwara, M., Kanamaru, K., Takahashi, H. et al. (2004) 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: 357-368. (Pubitemid 38592362)
44. Niwa, Y., Hirano, T., Yoshimoto, K., Shimizu, M. and Kobayashi, H. (1999) Non-invasive quantitative detection and applications of non-toxic, S65T-type green fluorescent protein in living plants. Plant J. 18: 455-463.
45. Noordally, Z.B., Ishii, K., Atkins, K.A., Wetherill, S.J., Kusakina, J., Walton, E.J. et al. (2013) Circadian control of chloroplast transcription by a nuclear-encoded timing signal. Science 339: 1316-1319.
46. Ohyama, K., Fukuzawa, H., Kohchi, T., Shirai, H., Sano, T., Sano, S. et al. (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322: 572-574. (Pubitemid 16049213)
47. Onda, Y., Yagi, Y., Saito, Y., Takenaka, N. and 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: 968-978.
48. Patron, N.J. and Waller, R.F. (2007) Transit peptide diversity and divergence: a global analysis of plastid targeting signals. Bioessays 29: 1048-1058. (Pubitemid 47522845)
49. Pitzschke, A., Djamei, A., Bitton, F. and Hirt, H. (2009) A major role of the MEKK1-MKK1/2-MPK4 pathway in ROS signalling. Mol. Plant 2: 120-137.
50. Qiu, Y.L., Li, L., Wang, B., Chen, Z., Knoop, V., Groth-Malonek, M. et al. (2006) The deepest divergences in land plants inferred from phylogenomic evidence. Proc. Natl Acad. Sci. USA 103: 15511-15516. (Pubitemid 44625623)
51. Saitou, N. and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
52. Schwarz, C., Elles, I., Kortmann, J., Piotrowski, M. and Nickelsen, J. (2007) Synthesis of the D2 protein of photosystem II in Chlamydomonas is controlled by a high molecular mass complex containing the RNA stabilization factor Nac2 and the translational activator RBP40. Plant Cell 19: 3627-3639.
53. Shimmura, S., Nozoe, M. and Shiina, T. (2008) Evolution of the light responsive psbD promoter in chloroplast. In Photosynthesis. Energy from the Sun: 14th International Congress on Photosynthesis. Edited by Allen, J.F., Gantt, E., Golbeck, J.H. and Osmond, B. pp. 1194-1197.
54. Springer, Berlin. Shinozaki, K., Ohme, M., Tanaka, M., Wakasugi, T., Hayashida, N., Matsubayashi, T. et al. (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J. 5: 2043-2049.
55. Tanaka, K., Oikawa, K., Ohta, N., Kuroiwa, H., Kuroiwa, T. and Takahashi, H. (1996) Nuclear encoding of a chloroplast RNA polymerase sigma subunit in a red alga. Science 272: 1932-1935. (Pubitemid 26234503)
56. Tanaka, K., Tozawa, Y., Mochizuki, N., Shinozaki, K., Nagatani, A., Wakasa, K. et al. (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: 309-313. (Pubitemid 27353290)
57. Tan, S. and Troxler, R.F. (1999) Characterization of two chloroplast RNA polymerase sigma factors from Zea mays: photoregulation and differential expression. Proc. Natl Acad. Sci. USA 96: 5316-5321. (Pubitemid 29214580)
58. Tougane, K., Komatsu, K., Bhyan, S.B., Sakata, Y., Ishizaki, K., Yamato, K.T. et al. (2010) Evolutionarily conserved regulatory mechanisms of abscisic acid signaling in land plants: characterization of ABSCISIC ACID INSENSITIVE1-like type 2C protein phosphatase in the liverwort Marchantia polymorpha. Plant Physiol. 152: 1529-1543.
59. Toyoshima, Y., Onda, Y., Shiina, T. and Nakahira, Y. (2005) Plastid transcription in higher plants. Crit. Rev. Plant Sci. 24: 59-81. (Pubitemid 40307601)
60. Tozawa, Y., Tanaka, K., Takahashi, H. and Wakasa, K. (1998) Nuclear encoding of a plastid s factor in rice and its tissue-and lightdependent expression. Nucleic Acids Res. 26: 415-419. (Pubitemid 28291562)
61. Tsunoyama, Y., Ishizaki, Y., Morikawa, K., Kobori, M., Nakahira, Y., Takeba, G. et al. (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: 3304-3309. (Pubitemid 38327776)
62. Tsunoyama, Y., Morikawa, K., Shiina, T. and Toyoshima, Y. (2002) Blue light specific and differential expression of a plastid s factor, Sig5 in Arabidopsis thaliana. FEBS Lett. 516: 225-228. (Pubitemid 34311966)
63. Vanderauwera, S., Zimmermann, P., Rombauts, S., Vandenabeele, S., Langebartels, C., Gruissem, W. et al. (2005) Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiol. 139: 806-821. (Pubitemid 43907108)