Skip to main content
SpringerLink
Log in

Arabidopsis BPG2: a phytochrome-regulated gene whose protein product binds to plastid ribosomal RNAs

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

BPG2 (Brz-insensitive pale green 2) is a dark-repressible and light-inducible gene that is required for the greening process in Arabidopsis. Light pulse experiments suggested that light-regulated gene expression of BPG2 is mediated by phytochrome. The T-DNA insertion mutant bpg2-2 exhibited a reduced level of chlorophyll and carotenoid pigmentation in the plastids. Measurements of time resolved chlorophyll fluorescence and of fluorescence emission at 77 K indicated defective photosystem II and altered photosystem I functions in bpg2 mutants. Kinetic analysis of chlorophyll fluorescence induction suggested that the reduction of the primary acceptor (QA) is impaired in bpg2. The observed alterations resulted in reduced photosynthetic efficiency as measured by the electron transfer rate. BPG2 protein is localized in the plastid stroma fraction. Co-immunoprecipitation of a formaldehyde cross-linked RNA–protein complex indicated that BPG2 protein binds with specificity to chloroplast 16S and 23S ribosomal RNAs. The direct physical interaction with the plastid rRNAs supports an emerging model whereby BPG2 provides light-regulated ribosomal RNA processing functions, which are rate limiting for development of the plastid and its photosynthetic apparatus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

BPG2:

Brz-insensitive pale green 2

Brz:

Brassinazole

CaMV:

Cauliflower mosaic virus

ETR:

Electron transfer rate

LHC:

Light-harvesting complex

PSI:

Photosystem I

PSII:

Photosystem II

YFP:

Yellow fluorescence protein

References

  • Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

    Article  PubMed  Google Scholar 

  • Anand B, Verma SK, Prakash B (2006) Structural stabilization of GTP-binding domains in circularly permuted GTPases: implications for RNA binding. Nucleic Acids Res 34:2196–2205

    Article  PubMed  CAS  Google Scholar 

  • Bellaoui M, Gruissem W (2004) Altered expression of the Arabidopsis ortholog of DCL affects normal plant development. Planta 219:819–826

    Article  PubMed  CAS  Google Scholar 

  • Bellaoui M, Keddie JS, Gruissem W (2003) DCL is a plant-specific protein required for plastid ribosomal RNA processing and embryo development. Plant Mol Biol 53:531–543

    Article  PubMed  CAS  Google Scholar 

  • Bisanz C, Bégot L, Carol P, Perez P, Bligny M, Pesey H, Gallois JL, Lerbs-Mache S, Mache R (2003) The Arabidopsis nuclear DAL gene encodes a chloroplast protein which is required for the maturation of the plastid ribosomal RNAs and is essential for chloroplast differentiation. Plant Mol Biol 51:651–663

    Article  PubMed  CAS  Google Scholar 

  • Bollenbach TJ, Lange H, Gutierrez R, Erhardt M, Stern DB, Gagliardi D (2005) RNR1, a 3′–5′ exoribonuclease belonging to the RNR superfamily, catalyzes 3′ maturation of chloroplast ribosomal RNAs in Arabidopsis thaliana. Nucleic Acids Res 33:2751–2763

    Article  PubMed  CAS  Google Scholar 

  • Brown T (2001) Dot and slot blotting of DNA. In: Current protocols in molecular biology 2:Unit 2.9B

  • Connolly K, Culver G (2009) Deconstructing ribosome construction. Trends Biochem Sci 34:256–263

    Article  PubMed  CAS  Google Scholar 

  • Daigle DM, Brown ED (2004) Studies of the interaction of Escherichia coli YjeQ with the ribosome in vitro. J Bacteriol 186:1381–1387

    Article  PubMed  CAS  Google Scholar 

  • Franklin KA, Quail PH (2010) Phytochrome functions in Arabidopsis development. J Exp Bot 61(1):11–24

    Article  PubMed  CAS  Google Scholar 

  • Franklin KA, Larner VS, Whitelam GC (2005) The signal transducing photoreceptors of plants. Int J Dev Biol 49:653–664

    Article  PubMed  CAS  Google Scholar 

  • Ghanotakis DF, Tsiotsis G, Bricker TM (1999) Polypeptides of PS II: structure and function. In: Singhal GS, Renger G, Sopory SK, Irrgang KD, Govindjee   (eds) Concepts in photobiology: photosynthesis and photomorphogenesis. Narosa, New Delhi, pp 264–291

    Google Scholar 

  • Gilmore AM, Yamamoto HY (1991) Resolution of lutein and zeaxanthin using a non-endcapped, lightly carbon-loaded C18 high-performance liquid chromatographic column. J Chromatogr A 543:137–145

    Article  CAS  Google Scholar 

  • Giuliano G, Pichersky E, Malik VS, Timko MP, Scolnik PA, Cashmore AR (1988) An evolutionarily conserved protein binding sequence upstream of a plant light-regulated gene. Proc Natl Acad Sci USA 85:7089–7093

    Article  PubMed  CAS  Google Scholar 

  • Green PJ, Kay SA, Chua N-H (1987) Sequence-specific interactions of a pea nuclear factor with light-responsive elements upstream of the rbcS-3A gene. EMBO J 6:2543–2549

    PubMed  CAS  Google Scholar 

  • Hajdukiewicz P, Svab Z, Maliga P (1994) The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol Biol 25:989–994

    Article  PubMed  CAS  Google Scholar 

  • Haldrup A, Simpson DJ, Scheller HV (2000) Down-regulation of the PSI-F subunit of photosystem I (PSI) in Arabidopsis thaliana. The PSI-F subunit is essential for photoautotrophic growth and contributes to antenna function. J Biol Chem 275:31211–31218

    Article  PubMed  CAS  Google Scholar 

  • Himeno H, Hanawa-Suetsugu K, Kimura T, Takagi K, Sugiyama W, Shirata S, Mikami T, Odagiri F, Osanai Y, Watanabe D, Goto S, Kalachnyuk L, Ushida C, Muto A (2004) A novel GTPase activated by the small subunit of ribosome. Nucleic Acids Res 32:5303–5309

    Article  PubMed  CAS  Google Scholar 

  • Kim BH, von Arnim AG (2006) The early dark-response in Arabidopsis thaliana revealed by cDNA microarray analysis. Plant Mol Biol 60:321–342

    Article  PubMed  CAS  Google Scholar 

  • Kishine M, Takabayashi A, Munekage Y, Shikanai T, Endo T, Sato F (2004) Ribosomal RNA processing and an RNase R family member in chloroplasts of Arabidopsis. Plant Mol Biol 55:595–606

    Article  PubMed  CAS  Google Scholar 

  • Kleffmann T, von Zychlinski A, Russenberger D, Hirsch-Hoffmann M, Gehrig P, Gruissem W, Baginsky S (2007) Proteome dynamics during plastid differentiation in rice. Plant Physiol 143:912–923

    Article  PubMed  CAS  Google Scholar 

  • Komatsu T, Kawaide H, Saito C, Yamagami A, Shimada S, Nakazawa M, Matsui M, Nakano A, Tsujimoto M, Natsume M, Abe H, Asami T, Nakano T (2010) The chloroplast protein BPG2 functions in brassinosteroid-mediated post-transcriptional accumulation of chloroplast rRNA. Plant J 61:409–422

    Article  PubMed  CAS  Google Scholar 

  • Krause GH (1991) Chlorophyll fluorescence and photosynthesis—the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349

    Article  CAS  Google Scholar 

  • Kusnetsov V, Herrmann RG, Kulaeva ON, Oelmuller R (1998) Cytokinin stimulates and abscisic acid inhibits greening of etiolated Lupinus luteus cotyledons by affecting the expression of the light-sensitive protochlorophyllide oxidoreductase. Mol Gen Genet 259:21–28

    PubMed  CAS  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigment of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Luo XM, Lin WH, Zhu S, Zhu JY, Sun Y, Fan XY, Cheng M, Hao Y, Oh E, Tian M, Liu L, Zhang M, Xie Q, Chong K, Wang ZY (2010) Integration of light- and brassinosteroid-signaling pathways by a GATA transcription factor in Arabidopsis. Dev Cell 19:872–883

    Article  PubMed  CAS  Google Scholar 

  • Ma L, Li J, Qu L, Hager J, Chen Z, Zhao H, Deng XW (2001) Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell 13:2589–2607

    PubMed  CAS  Google Scholar 

  • Mantoura RFC, Llewellyn CA (1983) The rapid-determination of algal chlorophyll and carotenoid pigments and their breakdown products in natural waters by reverse-phase high-performance liquid chromatography. Anal Chim Acta 151:297–314

    Article  CAS  Google Scholar 

  • Martínez-García JF, Huq E, Quail PH (2000) Direct targeting of light signals to a promoter element-bound transcription factor. Science 288:859–863

    Article  PubMed  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  PubMed  CAS  Google Scholar 

  • Motohashi R, Yamazaki T, Myouga F, Ito T, Ito K, Satou M, Kobayashi M, Nagata N, Yoshida S, Nagashima A, Tanaka K, Takahashi S, Shinozaki K (2007) Chloroplast ribosome release factor 1 (AtcpRF1) is essential for chloroplast development. Plant Mol Biol 64:481–497

    Article  PubMed  CAS  Google Scholar 

  • Nagata N, Min YK, Nakano T, Asami T, Yoshida S (2000) Treatment of dark-grown Arabidopsis thaliana with a brassinosteroid-biosynthesis inhibitor, brassinazole, induces some characteristics of light-grown plants. Planta 211:781–790

    Article  PubMed  CAS  Google Scholar 

  • Park YJ, Cho HK, Jung HJ, Ahn CS, Kang H, Pai HS (2011) PRBP plays a role in plastid ribosomal RNA maturation and chloroplast biogenesis in Nicotiana benthamiana. Planta 233:1073–1085

    Article  PubMed  CAS  Google Scholar 

  • Pokorska B, Romanowska E (2007) Photoinhibition and D1 protein degradation in mesophyll and agranal bundle sheath thylakoids of maize. Funct Plant Biol 34:844–852

    Article  CAS  Google Scholar 

  • Rensink WA, Pilon M, Weisbeek P (1998) Domains of a transit sequence required for in vivo import in Arabidopsis chloroplasts. Plant Physiol 118:691–699

    Article  PubMed  CAS  Google Scholar 

  • Schreiber U (1997) Chlorophyll fluorescence and photosynthetic energy conversion: Simple introductory experiments with the TEACHING-PAM Chlorophyll Fluorometer. Heinz Walz GmbH

  • Schult K, Meierhoff K, Paradies S, Töller T, Wolff P, Westhoff P (2007) The nuclear-encoded factor HCF173 is involved in the initiation of translation of the psbA mRNA in Arabidopsis thaliana. Plant Cell 19:1329–1346

    Article  PubMed  CAS  Google Scholar 

  • Scott NS, Nair H, Smillie RM (1971) The effect of red irradiation on plastid ribosomal RNA synthesis in dark-grown pea seedlings. Plant Physiol 47:385–388

    Article  PubMed  CAS  Google Scholar 

  • Stöckel J, Oelmüller R (2004) A novel protein for photosystem I biogenesis. J Biol Chem 279:10243–10251

    Article  PubMed  Google Scholar 

  • Strasser R, Srivastava A, Tsimili-Michael M (2000) The fluorescent transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanism, regulation and adaptation. Taylor and Francis, London, pp 443–480

    Google Scholar 

  • Subramanian C, Woo J, Cai X, Xu X, Servick S, Johnson CH, Nebenfuhr A, von Arnim AG (2006) A suite of tools and application notes for in vivo protein interaction assays using bioluminescence resonance energy transfer (BRET). Plant J 48:138–152

    Article  PubMed  CAS  Google Scholar 

  • Terzi LC, Simpson GG (2009) Arabidopsis RNA immunoprecipitation. Plant J 59:163–168

    Article  PubMed  CAS  Google Scholar 

  • Thien W, Schopfer P (1975) Control by phytochrome of cytoplasmic and plastid rRNA accumulation in cotyledons of mustard seedlings in the absence of photosynthesis. Plant Physiol 56:660–664

    Article  PubMed  CAS  Google Scholar 

  • Uicker WC, Schaefer L, Koenigsknecht M, Britton RA (2007) The essential GTPase YqeH is required for proper ribosome assembly in Bacillus subtilis. J Bacteriol 189:2926–2929

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Goodman HM, Jansson S (1997) Antisense inhibition of the photosystem I antenna protein Lhca4 in Arabidopsis thaliana. Plant Physiol 115:1525–1531

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Plastid-targeted YFP or CFP fused to the plastid transit peptide of rbcS were kindly provided by Andreas Nebenführ. We also thank John Dunlap for technical assistance in confocal microscopy and Charles Murphy for help with mass spectrometry. This work was supported by the Division of Chemical Sciences, Geosciences, and Biosciences, Office of Basic Energy Sciences of the U.S. Department of Energy through grant DE-FG02-96ER20223 (BK and AGV). PM and AW gratefully acknowledge the support from the Ministry of Science and Higher Education (MNISzW) of the Republic of Poland (grant N 303 498 438) for Figs. 5b, 7 and 8.

Author information

Authors and Affiliations

  1. Department of Natural Sciences, Albany State University, 504 College Drive, Albany, GA, 31705, USA

    Byung-Hoon Kim

  2. Department of Biochemistry, Cellular and Molecular Biology, University of Tennessee, Knoxville, TN, 37996, USA

    Byung-Hoon Kim & Albrecht G. von Arnim

  3. Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, ul. Gronostajowa 7, 30-387, Krakow, Poland

    Przemyslaw Malec & Andrzej Waloszek

  4. Graduate Program in Genome Science and Technology, University of Tennessee, Knoxville, TN, 37996, USA

    Albrecht G. von Arnim

Authors
  1. Byung-Hoon Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Przemyslaw Malec
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andrzej Waloszek
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Albrecht G. von Arnim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Byung-Hoon Kim.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kim, BH., Malec, P., Waloszek, A. et al. Arabidopsis BPG2: a phytochrome-regulated gene whose protein product binds to plastid ribosomal RNAs. Planta 236, 677–690 (2012). https://doi.org/10.1007/s00425-012-1638-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-012-1638-6

Keywords

Search

Navigation