Skip to main content
Log in

OsPPR1, a pentatricopeptide repeat protein of rice is essential for the chloroplast biogenesis

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

In this paper, we report a novel pentatricopeptide repeat (PPR) protein gene in rice. PPR, a characteristic repeat motif consisted of tandem 35 amino acids, has been found in various biological systems including plant. Sequence analysis revealed that the gene designated OsPPR1 consisted of an open reading frame of 2433 nucleotides encoding 810 amino acids that include 11 PPR motifs. Blast search result indicated that the gene did not align with any of the characterized PPR genes in plant. The OsPPR1 gene was found to contain a putative chloroplast transit peptide in the N-terminal region, suggesting that the gene product targets to the chloroplast. Southern blot hybridization indicated that the OsPPR1 is the member of a gene family within the rice genome. Expression analysis and immunoblot analysis suggested that the OsPPR1 was accumulated mainly in rice leaf. Antisense transgenic strategy was used to suppress the expression of OsPPR1 and the resulted transgenic rice showed the typical phenotypes of chlorophyll-deficient mutants; albinism and lethality. Cytological observation using microscopy revealed that the antisense transgenic plant contained a significant defect in the chloroplast development. Taken together, the results suggest that the OsPPR1 is a nuclear gene of rice, encoding the PPR protein that might play a role in the chloroplast biogenesis. This is the first report on the PPR protein required for the chloroplast biogenesis in rice.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

cTP:

chloroplast transit peptide

ORF:

open reading frame

PPR:

pentatricopeptide repeat

RT-PCR:

reverse-transcriptase polymerase chain reaction

References

  • H. Akagi A. Nakamura Y. Yokozeki-Misono A. Inagaki H. Takahashi K. Mori T. Fujimura (2004) ArticleTitlePositional cloning of the rice Rf-1 gene, a restorer of BT-type cytoplasmic male sterility that encodes a mitochondria-targeting PPR protein Theor. Appl. Genet. 108 1449–1457

    Google Scholar 

  • S.F. Altschul W. Gish W. Miller E.W. Myers D.J. Lipman (1990) ArticleTitleBasic local alignment search tool J. Mol. Biol. 215 403–410

    Google Scholar 

  • G. An P.R. Ebert A. Mitra S.B. Ha (1988) Binary vector S.B. Gelvin R.A. Schilperoort (Eds) Plant Molecular Biology Manual EditionNumberA3 Kluwer Dordrecht, Netherlands 1–19

    Google Scholar 

  • D.I. Arnon (1949) ArticleTitleCopper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris Plant Physiol. 24 1–15

    Google Scholar 

  • S. Aubourg N. Boudet M. Kreis A. Lecharny (2000) ArticleTitleIn Arabidopsis thaliana, 1% of the genome codes for a novel protein family unique to plants Plant Mol. Biol. 42 603–613

    Google Scholar 

  • A. Bateman E. Birney L. Cerruti R. Durbin L. Etwiller S.R. Eddy S. Griffiths-Jones K.L. Howe M. Marshall E.L.L. Sonnhammer. (2002) ArticleTitleThe Pfam protein families database Nucleic Acids Res. 30 276–280

    Google Scholar 

  • S. Bentolila A.A. Alfonso M.R. Hanson (2002) ArticleTitleA pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants Proc Natl Acad. Sci. 99 10887–10892

    Google Scholar 

  • P.L. Bhalla N. Smith. (1998) ArticleTitleAgrobacterium tumefaciens-mediated transformation of cauliflower, Brassica oleracea var. botrytis. Mol Breeding 4 531–541

    Google Scholar 

  • G.G. Brown N. Formanova H. Jin R. Wargachuk C. Dendy P. Patil M. Laforest J. Zhang W.Y. Cheung B.S. Landry (2003) ArticleTitleThe radish Rfo restorer gene of Ogura cytoplasmic male sterility encodes a protein with multiple pentatricopeptide repeats Plant J. 35 262–272

    Google Scholar 

  • A.H. Christensen R.A. Sharrock P.H. Quail (1992) ArticleTitleMaize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation Plant Mol. Biol. 18 675–689

    Google Scholar 

  • G.M. Church W. Gilbert (1984) ArticleTitleGenomic sequencing Proc. Natl. Acad. Sci. 81 1991–1995

    Google Scholar 

  • J.W. Coffin R. Dhillon R.G. Ritzel F.E. Nargang (1997) ArticleTitleThe Neurospora crassa cya-5 nuclear gene encodes a protein with a region of homology to the Saccharomyces cerevisiae PET309 protein and is required in a post-transcriptional step for the expression of the mitochondrially encoded COXI protein Curr. Genet. 32 273–280

    Google Scholar 

  • S.L. Dellaporta J. Wood J.B. Hicks (1983) ArticleTitleA plant DNA minipreparation: version II Plant Mol. Biol. Rep. 1 19–21

    Google Scholar 

  • S. Deslorie H. Gherbi W. Laloui (2003) ArticleTitleIdentification of the fertility restoration locus, Rfo, in radish as a member of the pentatricopeptide-repeat protein family EMBO Rep. 4 1–7

    Google Scholar 

  • O. Emanuelsson H. Nielsen G. Heijne Particlevon (1999) ArticleTitleChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites Protein Sci. 8 978–984

    Google Scholar 

  • D.G. Fisk M.B. Walker A. Barkan (1999) ArticleTitleMolecular cloning of the maize gene crp1 reveals similarity between regulators of mitochondrial and chloroplast gene expression EMBO J. 18 2621–2630

    Google Scholar 

  • A. Hoekema P.R. Hirsch P.J.J. Hooykaas R.A. Schilperoort (1983) ArticleTitleA binary vector strategy based on separation of vir- and T-region of the Agrobacterium tumefaciens Ti-plasmid Nature 303 179–181

    Google Scholar 

  • J.S. Jeon Y.Y Chung S. Lee G.H. Yi B.G. Oh G. An (1999) ArticleTitleIsolation and characterization of an anther-specific gene, RA8, from rice (Oryza sativa) Plant Mol. Biol. 39 35–44

    Google Scholar 

  • J.B. Jin Y.A. Kim S.J. Kim S.H. Lee D.H. Kim G.-W. Cheong I. Hwang (2001) ArticleTitleA new dynamin-like protein, ADL6, is involved in trafficking from the trans-Golgi network to the central vacuole in Arabidopsis Plant Cell 13 1511–1525

    Google Scholar 

  • K.H. Jung J. Hur C.H. Ryu Y. Choi Y.Y. Chung A. Miyao H. Hirochika G. An (2003) ArticleTitleCharacterization of a rice chlorophyll-deficient mutant using the T-DNA gene-trap system Plant Cell Physiol. 44 463–472

    Google Scholar 

  • H.-G. Kang J.-S. Jeon S. Lee G. An (1998) ArticleTitleIdentification of class B and class C floral organ identity genes from rice plants Plant Mol. Biol. 38 1021–1029

    Google Scholar 

  • T. Kazama K. Toriyama (2003) ArticleTitleA pentatricopeptide repeat-containing gene that promotes the processing of aberrant atp6 RNA of cytoplasmic male-sterile rice FEBS Lett. 544 99–102

    Google Scholar 

  • C. Kim D.H. Jeong G. An (2000) ArticleTitleMolecular cloning and characterization of OsLRK1 encoding a putative receptor-like protein kinase from Oryza sativa Plant Sci. 152 17–26

    Google Scholar 

  • N. Koizuka R. Imai H. Fujimoto T. Hayakawa Y. Kimura J. Kohno-Murase T. S. Sakai Kawasaki J. Imamura (2003) ArticleTitleGenetic characterization of a pentatricopeptide repeat protein gene, orf687, that restores fertility in the cytoplasmic male-sterile Kosena radish Plant J. 34 407–415

    Google Scholar 

  • T. Komori S. Ohta N. Murai Y. Takakura Y. Kuraya S. Suzuki Y. Hiei H. Imaseki N. Nitta (2004) ArticleTitleMap-based cloning of a fertility restorer gene, Rf-1, in rice (Oryza sativa L.) Plant J. 37 315–325

    Google Scholar 

  • S. Lahmy F. Barneche J. Derancourt W. Filipowicz M. Delseny M. Echeverria (2000) ArticleTitleA chloroplastic RNA-binding protein is a new member of the PPR family FEBS Lett. 480 255–260

    Google Scholar 

  • S. Lee J.S. Jeon K.H. Jung G. An (1999) ArticleTitleBinary vectors for efficient transformation of rice J. Plant Biol. 42 310–316

    Google Scholar 

  • C. Lurin C. Andres S. Aubourg M. Bellaoui F. Bitton C. Bruyere M. Caboche C. Debast J. Gualberto B. Hoffmann A. Lecharny M.L. Ret M.L. Martin-Magniette H. Mireau N. Peeters J.P. Renou B. Szurek L. Taconnat I. Small (2004) ArticleTitleGenome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis Plant Cell 16 2089–2103

    Google Scholar 

  • G.M. Manthey J.E. McEwen (1995) ArticleTitleThe product of the nuclear gene PET309 is required for translation of mature mRNA and stability or production of intron-containing RNAs derived from the mitochondrial COX1 locus of Saccharomyces cerevisiae EMBO J. 14 4031–4043

    Google Scholar 

  • G.M. Manthey B.D. Przybyla-Zawislak J.E. McEwen (1998) ArticleTitleThe Saccharomyces cerevisiae Pet309 protein is embedded in the mitochondrial inner membrane Eur. J. Biochem. 255 156–161

    Google Scholar 

  • D. McElroy R.I.S. Brettell (1994) ArticleTitleForeign gene expression in transgenic cereals Trend Biotechnol. 12 62–68

    Google Scholar 

  • K. Meierhoff S. Felder T. Nalamura N. Bechtold G. Schuster (2003) ArticleTitleHCF152, an Arabidopsis RNA binding pentatricopeptide repeat protein involved in the processing of chloroplast psbB-psbT-psbH-petB-PetD RNAs Plant Cell 15 1480–1495

    Google Scholar 

  • K. Miyoshi Y. Ito A. Serizwa N. Kurata (2003) ArticleTitleOsHAP3 genes regulate chloroplast biogenesis in rice Plant J. 3 532–540

    Google Scholar 

  • T. Nakamura K. Meierhoff P. Westhoff G. Schuster (2003) ArticleTitleRNA-binding properties of HCF152, an Arabidopsis PPR protein involved in the processing of chloroplast RNA Eur. J. Biochem. 270 4070–4081

    Google Scholar 

  • T. Nakamura G. Schuster M. Sugiura M. Sugita (2004) ArticleTitleChloroplast RNA-binding and pentatricopeptide repeat proteins Biochem Soc Trans. 32 571–574

    Google Scholar 

  • H. Nielsen J. Engelbrecht S. Brunak G. Heijne Particlevon (1997) ArticleTitleIdentification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites Prot. Eng. 10 1–6

    Google Scholar 

  • T. Oguchi K. Sage-Ono H. Kamada M. Ono (2004) ArticleTitleGenomic structure of a novel Arabidopsis clock-controlled gene AtC401, which encodes a pentatricopeptide repeat protein Gene 330 29–37

    Google Scholar 

  • K.A. Pyke (1999) ArticleTitlePlastid division and development Plant Cell 11 549–556

    Google Scholar 

  • J. Sambrook E. Fritsch T. Maniatis (1989) Molecular cloning: A laboratory manual EditionNumber2 Cold spring Harbor Laboratory Press Cold Spring Harbor, New York

    Google Scholar 

  • I.D. Small N. Peeters (2000) ArticleTitleThe PPR motif – a TPR-related motif prevalent in plant organellar proteins Trends Biochem. Sci. 25 46–47

    Google Scholar 

  • D.B. Stern M.R. Hanson A. Barkan (2004) ArticleTitleGenetics and genomics of chloroplast biogenesis: maize as a model system Trends Plant Sci. 9 293–301

    Google Scholar 

  • Y. Tada M. Nakase T. Adachi R. Nakamura H. Shimada M. Takahashi T. Fujimura T. Matsuda (1996) ArticleTitleReduction of 14–16 kDa allergenic proteins in transgenic rice plants by antisense gene FEBS Lett. 391 341–345

    Google Scholar 

  • N. Tsuchiya H. Fukuda T. Sugimura M. Nagao H. Nakagama (2002) ArticleTitleLRP130, a protein containing nine pentatricopeptide repeat motifs, interacts with a single-stranded cytosine-rich sequence of mouse hyper variable minisatellite Pc-1 Eur. J. Biochem. 269 2927–2933

    Google Scholar 

  • I.M. Meer ParticleVan der M.E. Stam A.J. Tunen Particlevan J.N. Mol A.R. Stuitje (1992) ArticleTitleAntisense inhibition of flavonoid biosynthesis in Petunia anthers results in male sterility Plant Cell 4 253–262

    Google Scholar 

  • P.M. Williams A. Barkan (2003) ArticleTitleA chloroplast-localized PPR protein required for plastid ribosome accumulation Plant J. 36 675–686

    Google Scholar 

  • H. Xu R.B. Knox P.E. Taylor M.B. Singh (1995) ArticleTitleBcp1, a gene required for male fertility in Arabidopsis Proc. Natl. Acad. Sci. 92 2106–2110

    Google Scholar 

  • H. Yamazaki M. Tasaka T. Shikanai (2004) ArticleTitlePPR motifs of the nucleus-encoded factor, PGR3, function in the selective and distinct steps of chloroplast gene expression in Arabidopsis. Plant J 38 152–163

    Google Scholar 

  • S. Yehudai-Resheff M. Hirsh G. Schuster (2001) ArticleTitlePolynucleotide phosphorylase functions as both an exonuclease and a poly(A) polymerase in spinach chloroplasts Mol. Cell. Biol. 21 5408–5416

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yong-Yoon Chung.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gothandam, K.M., Kim, ES., Cho, H. et al. OsPPR1, a pentatricopeptide repeat protein of rice is essential for the chloroplast biogenesis. Plant Mol Biol 58, 421–433 (2005). https://doi.org/10.1007/s11103-005-5702-5

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-005-5702-5

Key words:

Navigation