Login Register Cart 0
Generic placeholder image

Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Selective Activation of Chloroplast psbD Light-Responsive Promoter and psaA/B Promoter in Transplastomic Tobacco Plants Overexpressing Arabidopsis Sigma Factor AtSIG5

Author(s): Mikio Nozoe, Yuichi Tsunoyama, Yoko Ishizaki, Yoichi Nakahira and Takashi Shiina*

Volume 27, Issue 2, 2020

Page: [168 - 175] Pages: 8

DOI: 10.2174/0929866526666191014130605

Price: $65

Abstract

Background: Plastid-encoded eubacterial-type RNA polymerase (PEP) plays a critical role in the transcription of photosynthesis genes in chloroplasts. Notably, some of the reaction center genes, including psaA, psaB, psbA, and psbD genes, are differentially transcribed by PEP in mature chloroplasts. However, the molecular mechanism of promoter selection in the reaction center gene transcription by PEP is not well understood.

Objective: Sigma factor proteins direct promoter selection by a core PEP in chloroplasts as well as bacteria. AtSIG5 is a unique chloroplast sigma factor essential for psbD light-responsive promoter (psbD LRP) activity. To analyze the role of AtSIG5 in chloroplast transcription in more detail, we assessed the effect of AtSIG5 hyper-expression on the transcription of plastid-encoded genes in chloroplast transgenic plants.

Results: The chloroplast transgenic tobacco (CpOX-AtSIG5) accumulates AtSIG5 protein at extremely high levels in chloroplasts. Due to the extremely high-level expression of recombinant AtSIG5, most PEP holoenzymes are most likely to include the recombinant AtSIG5 in the CpOXAtSIG5 chloroplasts. Thus, we can assess the promoter preference of AtSIG5 in vivo. The overexpression of AtSIG5 significantly increased the expression of psbD LRP transcripts encoding PSII reaction center D2 protein and psaA/B operon transcripts encoding PSI core proteins. Furthermore, run-on transcription analyses revealed that AtSIG5 preferentially recognizes the psaA/B promoter, as well as the psbD LRP. Moreover, we found that psbD LRP is constitutively active in CpOX-AtSIG5 plants irrespective of light and dark.

Conclusion: AtSIG5 probably plays a significant role in differential transcription of reaction center genes in mature chloroplasts.

Keywords: Chloroplast transformation, sigma factor, AtSIG5, photosynthesis reaction center protein, transcription, chloroplast transgenic plant.

« Previous Next »
Graphical Abstract

[1]
Hess, W.R.; Börner, T. Organellar RNA polymerases of higher plants. Int. Rev. Cytol., 1999, 190, 1-59.
[http://dx.doi.org/10.1016/S0074-7696(08)62145-2] [PMID: 10331238]
[2]
Ortelt, J.; Link, G. Plastid gene transcription: Promoters and RNA polymerases. Methods Mol. Biol., 2014, 1132, 47-72.
[http://dx.doi.org/10.1007/978-1-62703-995-6_3] [PMID: 24599846]
[3]
Pfannschmidt, T.; Blanvillain, R.; Merendino, L.; Courtois, F.; Chevalier, F.; Liebers, M.; Grübler, B.; Hommel, E.; Lerbs-Mache, S. Plastid RNA polymerases: Orchestration of enzymes with different evolutionary origins controls chloroplast biogenesis during the plant life cycle. J. Exp. Bot., 2015, 66(22), 6957-6973.
[http://dx.doi.org/10.1093/jxb/erv415] [PMID: 26355147]
[4]
Börner, T.; Aleynikova, A.Y.; Zubo, Y.O.; Kusnetsov, V.V. Chloroplast RNA polymerases: Role in chloroplast biogenesis. Biochim. Biophys. Acta, 2015, 1847(9), 761-769.
[http://dx.doi.org/10.1016/j.bbabio.2015.02.004] [PMID: 25680513]
[5]
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(11), 2215-2223.
[http://dx.doi.org/10.1271/bbb.68.2215] [PMID: 15564657]
[6]
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.
[http://dx.doi.org/10.1016/S0074-7696(05)44001-2] [PMID: 16157177]
[7]
Schweer, J.; Türkeri, H.; Kolpack, A.; Link, G. Role and regulation of plastid sigma factors and their functional interactors during chloroplast transcription - recent lessons from Arabidopsis thaliana. Eur. J. Cell Biol., 2010, 89(12), 940-946.
[http://dx.doi.org/10.1016/j.ejcb.2010.06.016] [PMID: 20701995]
[8]
Yagi, Y.; Shiina, T. Recent advances in the study of chloroplast gene expression and its evolution. Front. Plant Sci., 2014, 25, 5-61.
[http://dx.doi.org/10.3389/fpls.2014.00061]
[9]
Chi, W.; He, B.; Mao, J.; Jiang, J.; Zhang, L. Plastid sigma factors: Their individual functions and regulation in transcription. Biochim. Biophys. Acta, 2015, 1847(9), 770-778.
[http://dx.doi.org/10.1016/j.bbabio.2015.01.001] [PMID: 25596450]
[10]
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(10), 1034-1043.
[http://dx.doi.org/10.1093/pcp/pce155] [PMID: 11673617]
[11]
Privat, I.; Hakimi, M.A.; Buhot, L.; Favory, J.J.; Mache-Lerbs, S. Characterization of Arabidopsis plastid sigma-like transcription factors SIG1, SIG2 and SIG3. Plant Mol. Biol., 2003, 51(3), 385-399.
[http://dx.doi.org/10.1023/A:1022095017355] [PMID: 12602869]
[12]
Nagashima, A.; Hanaoka, M.; Shikanai, T.; Fujiwara, M.; Kanamaru, K.; Takahashi, H.; Tanaka, K. The multiple-stress responsive plastid sigma factor, SIG5, directs activation of the psbD Blue Light-Responsive Promoter (BLRP) in Arabidopsis thaliana. Plant Cell Phys; , 2004, 45, pp. 357-368.
[13]
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. USA, 2004, 101(9), 3304-3309.
[http://dx.doi.org/10.1073/pnas.0308362101] [PMID: 14976253]
[14]
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.
[http://dx.doi.org/10.1093/nar/gki908]
[15]
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(2), 133-144.
[http://dx.doi.org/10.1111/j.1365-313X.2005.02362.x] [PMID: 15807777]
[16]
Loschelder, H.; Schweer, J.; Link, B.; Link, G. Dual temporal role of plastid sigma factor 6 in Arabidopsis development. Plant Physiol., 2006, 142(2), 642-650.
[http://dx.doi.org/10.1104/pp.106.085878] [PMID: 16905663]
[17]
Hanaoka, M.; Kato, M.; Anma, M.; Tanaka, K. SIG1, a sigma factor for the chloroplast RNA polymerase, differently associates with multiple DNA regions in the chloroplast chromosomes in vivo. Int. J. Mol. Sci., 2012, 13(10), 12182-12194.
[http://dx.doi.org/10.3390/ijms131012182] [PMID: 23202891]
[18]
Shimmura, S.; Nozoe, M.; Kitora, S.; Kin, S.; Matsutani, S.; Ishizaki, Y.; Nakahira, Y.; Shiina, T. Comparative analysis of chloroplast psbD promoters in terrestrial plants. Front. Plant Sci., 2017, 13, 8-1186.
[http://dx.doi.org/10.3389/fpls.2017.01186]
[19]
Kim, M.; Mullet, J.E. Identification of a sequence-specific DNA binding factor required for transcription of the barley chloroplast blue light-responsive psbD-psbC promoter. Plant Cell, 1995, 7(9), 1445-1457.
[PMID: 8589628]
[20]
Nakahira, Y.; Baba, K.; Yoneda, A.; Shiina, T.; Toyoshima, Y. Circadian-regulated transcription of the psbD light-responsive promoter in wheat chloroplasts. Plant Physiol., 1998, 118(3), 1079-1088.
[http://dx.doi.org/10.1104/pp.118.3.1079] [PMID: 9808753]
[21]
Svab, Z.; Hajdukiewicz, P.; Maliga, P. Stable transformation of plastids in higher plants. Proc. Natl. Acad. Sci. USA, 1990, 87(21), 8526-8530.
[http://dx.doi.org/10.1073/pnas.87.21.8526] [PMID: 11607112]
[22]
Hayashi, K.; Shiina, T.; Ishii, N.; Iwai, K.; Ishizaki, Y.; Morikawa, K.; Toyoshima, Y. A role of the -35 element in the initiation of transcription at psbA promoter in tobacco plastids. Plant Cell Physiol., 2003, 44(3), 334-341.
[http://dx.doi.org/10.1093/pcp/pcg041] [PMID: 12668780]
[23]
Svab, Z.; Maliga, P. High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene. Proc. Natl. Acad. Sci. USA, 1993, 90(3), 913-917.
[http://dx.doi.org/10.1073/pnas.90.3.913] [PMID: 8381537]
[24]
Legen, J.; Kemp, S.; Krause, K.; Profanter, B.; Herrmann, R.G.; Maier, R.M. Comparative analysis of plastid transcription profiles of entire plastid chromosomes from tobacco attributed to wild-type and PEP-deficient transcription machineries. Plant J., 2002, 31(2), 171-188.
[http://dx.doi.org/10.1046/j.1365-313X.2002.01349.x] [PMID: 12121447]
[25]
Asayama, M. Regulatory system for light-responsive gene expression in photosynthesizing bacteria: Cis-elements and trans-acting factors in transcription and post-transcription. Biosci. Biotechnol. Biochem., 2006, 70(3), 565-573.
[http://dx.doi.org/10.1271/bbb.70.565] [PMID: 16556970]
[26]
Shiina, T.; Allison, L.; Maliga, P. rbcL Transcript levels in tobacco plastids are independent of light: Reduced dark transcription rate is compensated by increased mRNA stability. Plant Cell, 1998, 10(10), 1713-1722.
[http://dx.doi.org/10.1105/tpc.10.10.1713] [PMID: 9761797]
[27]
Maliga, P. Progress towards commercialization of plastid transformation technology. Trends Biotechnol., 2003, 21(1), 20-28.
[http://dx.doi.org/10.1016/S0167-7799(02)00007-0] [PMID: 12480347]
[28]
Ruf, S.; Kössel, H.; Bock, R. Targeted inactivation of a tobacco intron-containing open reading frame reveals a novel chloroplast-encoded photosystem I-related gene. J. Cell Biol., 1997, 139(1), 95-102.
[http://dx.doi.org/10.1083/jcb.139.1.95] [PMID: 9314531]
[29]
Hager, M.; Biehler, K.; Illerhaus, J.; Ruf, S.; Bock, R. Targeted inactivation of the smallest plastid genome-encoded open reading frame reveals a novel and essential subunit of the cytochrome b(6)f complex. EMBO J., 1999, 18(21), 5834-5842.
[http://dx.doi.org/10.1093/emboj/18.21.5834] [PMID: 10545095]
[30]
Hager, M.; Hermann, M.; Biehler, K.; Krieger-Liszkay, A.; Bock, R. Lack of the small plastid-encoded PsbJ polypeptide results in a defective water-splitting apparatus of photosystem II, reduced photosystem I levels, and hypersensitivity to light. J. Biol. Chem., 2002, 277(16), 14031-14039.
[http://dx.doi.org/10.1074/jbc.M112053200] [PMID: 11827973]
[31]
Tsunoyama, Y.; Morikawa, K.; Shiina, T.; Toyoshima, Y. Blue light specific and differential expression of a plastid σ factor, Sig5 in Arabidopsis thaliana. FEBS Lett., 2002, 516(1-3), 225-228.
[http://dx.doi.org/10.1016/S0014-5793(02)02538-3] [PMID: 11959137]
[32]
Pfannschmidt, T.; Nilsson, A.; Tullberg, A.; Link, G.; Allen, J.F. Direct transcriptional control of the chloroplast genes psbA and psaAB adjusts photosynthesis to light energy distribution in plants. IUBMB Life, 1999, 48(3), 271-276.
[http://dx.doi.org/10.1080/713803507] [PMID: 10690637]
[33]
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(6), 968-978.
[http://dx.doi.org/10.1111/j.1365-313X.2008.03567.x] [PMID: 18532976]
[34]
Noordally, Z.B.; Ishii, K.; Atkins, K.A.; Wetherill, S.J.; Kusakina, J.; Walton, E.J.; Kato, M.; Azuma, M.; Tanaka, K.; Hanaoka, M.; Dodd, A.N. Circadian control of chloroplast transcription by a nuclear-encoded timing signal. Science, 2013, 339(6125), 1316-1319.
[http://dx.doi.org/10.1126/science.1230397] [PMID: 23493713]
[35]
Yamburenko, M.V.; Zubo, Y.O.; Börner, T. Abscisic acid affects transcription of chloroplast genes via protein phosphatase 2C-dependent activation of nuclear genes: Repression by guanosine-3′-5′-bisdiphosphate and activation by sigma factor 5. Plant J., 2015, 82(6), 1030-1041.
[http://dx.doi.org/10.1111/tpj.12876] [PMID: 25976841]
[36]
Belbin, F.E.; Noordally, Z.B.; Wetherill, S.J.; Atkins, K.A.; Franklin, K.A.; Dodd, A.N. Integration of light and circadian signals that regulate chloroplast transcription by a nuclear-encoded sigma factor. New Phytol., 2017, 213(2), 727-738.
[http://dx.doi.org/10.1111/nph.14176] [PMID: 27716936]
[37]
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(24), 7090-7098.
[http://dx.doi.org/10.1093/nar/gkg935] [PMID: 14654684]
[38]
Oh, S.; Montgomery, B.L. Phytochrome-induced SIG2 expression contributes to photoregulation of phytochrome signalling and photomorphogenesis in Arabidopsis thaliana. J. Exp. Bot., 2013, 64(18), 5457-5472.
[http://dx.doi.org/10.1093/jxb/ert308] [PMID: 24078666]
[39]
Ichikawa, K.; Shimizu, A.; Okada, R.; Satbhai, S.B.; Aoki, S. The plastid sigma factor SIG5 is involved in the diurnal regulation of the chloroplast gene psbD in the moss Physcomitrella patens. FEBS Lett., 2008, 582(3), 405-409.
[http://dx.doi.org/10.1016/j.febslet.2007.12.034] [PMID: 18174028]
[40]
Kanazawa, T.; Ishizaki, K.; Kohchi, T.; Hanaoka, M.; Tanaka, K. Characterization of four nuclear-encoded plastid RNA polymerase sigma factor genes in the liverwort Marchantia polymorpha: Blue-light- and multiple stress-responsive SIG5 was acquired early in the emergence of terrestrial plants. Plant Cell Physiol., 2013, 54(10), 1736-1748.
[http://dx.doi.org/10.1093/pcp/pct119] [PMID: 23975891]
[41]
Thum, K.E.; Kim, M.; Christopher, D.A.; Mullet, J.E. Cryptochrome 1, cryptochrome 2, and phytochrome a co-activate the chloroplast psbD blue light-responsive promoter. Plant Cell, 2001, 13(12), 2747-2760.
[PMID: 11752385]
[42]
Chun, L.; Kawakami, A.; Christopher, D.A.; Phytochrome, A. Phytochrome A mediates blue light and UV-A-dependent chloroplast gene transcription in green leaves. Plant Physiol., 2001, 125(4), 1957-1966.
[http://dx.doi.org/10.1104/pp.125.4.1957] [PMID: 11299375]
[43]
Küchler, M.; Decker, S.; Hörmann, F.; Soll, J.; Heins, L. Protein import into chloroplasts involves redox-regulated proteins. EMBO J., 2002, 21(22), 6136-6145.
[http://dx.doi.org/10.1093/emboj/cdf621] [PMID: 12426385]
[44]
Stengel, A.; Benz, P.; Balsera, M.; Soll, J.; Bölter, B. TIC62 redox-regulated translocon composition and dynamics. J. Biol. Chem., 2008, 283(11), 6656-6667.
[http://dx.doi.org/10.1074/jbc.M706719200] [PMID: 18180301]
[45]
Järvi, S.; Suorsa, M.; Aro, E. Photosystem II repair in plant chloroplasts - Regulation, assisting proteins and shared components with photosystem II biogenesis. Biochim. Biophys. Acta, 1847, 2015, 900-909.
[http://dx.doi.org/10.1016/j.bbabio.2015.01.006] [PMID: 25615587]
[46]
Armbruster, U.; Zühlke, J.; Rengstl, B.; Kreller, R.; Makarenko, E.; Rühle, T.; Schünemann, D.; Jahns, P.; Weisshaar, B.; Nickelsen, J.; Leister, D. The Arabidopsis thylakoid protein PAM68 is required for efficient D1 biogenesis and photosystem II assembly. Plant Cell, 2010, 22(10), 3439-3460.
[http://dx.doi.org/10.1105/tpc.110.077453] [PMID: 20923938]
[47]
Zhang, D.; Zhou, G.; Liu, B.; Kong, Y.; Chen, N.; Qiu, Q.; Yin, H.; An, J.; Zhang, F.; Chen, F. HCF243 encodes a chloroplast-localized protein involved in the D1 protein stability of the arabidopsis photosystem II complex. Plant Physiol., 2011, 157(2), 608-619.
[http://dx.doi.org/10.1104/pp.111.183301] [PMID: 21862668]
[48]
Tzinas, G.; Argyroudi-Akoyunoglou, J. Chloramphenicol-induced stabilization of light-harvesting complexes in thylakoids during development. FEBS Lett., 1988, 229, 135-141.
[http://dx.doi.org/10.1016/0014-5793(88)80813-5]

Rights & Permissions Print Cite
Article Metrics
32
5
© 2024 Bentham Science Publishers | Privacy Policy