Function of PPR Proteins in Plastid Gene Expression

Overview

Journal RNA Biol

Specialty Molecular Biology

Date 2013 Jun 18

PMID 23771106

Citations 26

Authors

Toshiharu Shikanai

Sota Fujii

Affiliations

Soon will be listed here.

Abstract

PPR proteins form a huge family in flowering plants and are involved in RNA maturation in plastids and mitochondria. These proteins are sequence-specific RNA-binding proteins that recruit the machinery of RNA processing. We summarize progress in the research on the functional mechanisms of divergent RNA maturation and on the mechanism by which RNA sequences are recognized. We further focus on two topics. RNA editing is an enigmatic process of RNA maturation in organelles, in which members of the PLS subfamily contribute to target site recognition. As the first topic, we speculate on why the PLS subfamily was selected by the RNA editing machinery. Second, we discuss how the regulation of plastid gene expression contributes to efficient photosynthesis. Although the molecular functions of PPR proteins have been studied extensively, information on the physiological significance of regulation by these proteins remains very limited.

Citing Articles

Dek570-1, a PPR-DYW protein, is required for maize seed and plant development via modulation of C-to-U RNA editing in mitochondria and chloroplasts.

Li W, Zhao M, Liu B, Liu Y, Deng J, Gu Y Planta. 2025; 261(4):64.

PMID: 39985592 DOI: 10.1007/s00425-025-04634-z.

encodes a DYW-type pentatricopeptide repeat protein involved in chloroplast RNA processing and regulated chloroplast development.

Xu M, Zhang X, Cao J, Liu J, He Y, Guan Q Mol Breed. 2024; 44(4):29.

PMID: 38549701 PMC: 10965880. DOI: 10.1007/s11032-024-01468-7.

Maize kernel development.

Dai D, Ma Z, Song R Mol Breed. 2023; 41(1):2.

PMID: 37309525 PMC: 10231577. DOI: 10.1007/s11032-020-01195-9.

Mechanisms governing codon usage bias and the implications for protein expression in the chloroplast of Chlamydomonas reinhardtii.

Fages-Lartaud M, Hundvin K, Hohmann-Marriott M Plant J. 2022; 112(4):919-945.

PMID: 36071273 PMC: 9828097. DOI: 10.1111/tpj.15970.

An overview of RNA splicing and functioning of splicing factors in land plant chloroplasts.

Wang X, Wang J, Li S, Lu C, Sui N RNA Biol. 2022; 19(1):897-907.

PMID: 35811474 PMC: 9275481. DOI: 10.1080/15476286.2022.2096801.

References

Yamazaki H, Tasaka M, Shikanai T . PPR motifs of the nucleus-encoded factor, PGR3, function in the selective and distinct steps of chloroplast gene expression in Arabidopsis. Plant J. 2004; 38(1):152-63. DOI: 10.1111/j.1365-313X.2004.02035.x. View

Delannoy E, Stanley W, Bond C, Small I . Pentatricopeptide repeat (PPR) proteins as sequence-specificity factors in post-transcriptional processes in organelles. Biochem Soc Trans. 2007; 35(Pt 6):1643-7. DOI: 10.1042/BST0351643. View

Svab Z, Maliga P . High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene. Proc Natl Acad Sci U S A. 1993; 90(3):913-7. PMC: 45780. DOI: 10.1073/pnas.90.3.913. View

Barkan A, Walker M, Nolasco M, Johnson D . A nuclear mutation in maize blocks the processing and translation of several chloroplast mRNAs and provides evidence for the differential translation of alternative mRNA forms. EMBO J. 1994; 13(13):3170-81. PMC: 395209. DOI: 10.1002/j.1460-2075.1994.tb06616.x. View

Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S . Breaking the code of DNA binding specificity of TAL-type III effectors. Science. 2009; 326(5959):1509-12. DOI: 10.1126/science.1178811. View

Kazama T, Toriyama K . A pentatricopeptide repeat-containing gene that promotes the processing of aberrant atp6 RNA of cytoplasmic male-sterile rice. FEBS Lett. 2003; 544(1-3):99-102. DOI: 10.1016/s0014-5793(03)00480-0. View

Chateigner-Boutin A, Ramos-Vega M, Guevara-Garcia A, Andres C, Gutierrez-Nava M, Cantero A . CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts. Plant J. 2008; 56(4):590-602. DOI: 10.1111/j.1365-313X.2008.03634.x. View

Wang Z, Zou Y, Li X, Zhang Q, Chen L, Wu H . Cytoplasmic male sterility of rice with boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell. 2006; 18(3):676-87. PMC: 1383642. DOI: 10.1105/tpc.105.038240. View

Hauler A, Jonietz C, Stoll B, Stoll K, Braun H, Binder S . RNA Processing Factor 5 is required for efficient 5' cleavage at a processing site conserved in RNAs of three different mitochondrial genes in Arabidopsis thaliana. Plant J. 2013; 74(4):593-604. DOI: 10.1111/tpj.12143. View

10.

Williams-Carrier R, Kroeger T, Barkan A . Sequence-specific binding of a chloroplast pentatricopeptide repeat protein to its native group II intron ligand. RNA. 2008; 14(9):1930-41. PMC: 2525963. DOI: 10.1261/rna.1077708. View

11.

Barkan A, Goldschmidt-Clermont M . Participation of nuclear genes in chloroplast gene expression. Biochimie. 2000; 82(6-7):559-72. DOI: 10.1016/s0300-9084(00)00602-7. View

12.

Tsudzuki T, Wakasugi T, Sugiura M . Comparative analysis of RNA editing sites in higher plant chloroplasts. J Mol Evol. 2001; 53(4-5):327-32. DOI: 10.1007/s002390010222. View

13.

Cai W, Okuda K, Peng L, Shikanai T . PROTON GRADIENT REGULATION 3 recognizes multiple targets with limited similarity and mediates translation and RNA stabilization in plastids. Plant J. 2011; 67(2):318-27. DOI: 10.1111/j.1365-313X.2011.04593.x. View

14.

Makino A, Shimada T, Takumi S, Kaneko K, Matsuoka M, Shimamoto K . Does Decrease in Ribulose-1,5-Bisphosphate Carboxylase by Antisense RbcS Lead to a Higher N-Use Efficiency of Photosynthesis under Conditions of Saturating CO2 and Light in Rice Plants?. Plant Physiol. 1997; 114(2):483-491. PMC: 158328. DOI: 10.1104/pp.114.2.483. View

15.

Schmitz-Linneweber C, Williams-Carrier R, Barkan A . RNA immunoprecipitation and microarray analysis show a chloroplast Pentatricopeptide repeat protein to be associated with the 5' region of mRNAs whose translation it activates. Plant Cell. 2005; 17(10):2791-804. PMC: 1242273. DOI: 10.1105/tpc.105.034454. View

16.

Hanaoka M, Kanamaru K, Fujiwara M, Takahashi H, Tanaka K . Glutamyl-tRNA mediates a switch in RNA polymerase use during chloroplast biogenesis. EMBO Rep. 2005; 6(6):545-50. PMC: 1369087. DOI: 10.1038/sj.embor.7400411. View

17.

Maier U, Bozarth A, Funk H, Zauner S, Rensing S, Schmitz-Linneweber C . Complex chloroplast RNA metabolism: just debugging the genetic programme?. BMC Biol. 2008; 6:36. PMC: 2553071. DOI: 10.1186/1741-7007-6-36. View

18.

Sun T, Germain A, Giloteaux L, Hammani K, Barkan A, Hanson M . An RNA recognition motif-containing protein is required for plastid RNA editing in Arabidopsis and maize. Proc Natl Acad Sci U S A. 2013; 110(12):E1169-78. PMC: 3607000. DOI: 10.1073/pnas.1220162110. View

19.

Small I, Peeters N . The PPR motif - a TPR-related motif prevalent in plant organellar proteins. Trends Biochem Sci. 2000; 25(2):46-7. DOI: 10.1016/s0968-0004(99)01520-0. View

20.

Okuda K, Habata Y, Kobayashi Y, Shikanai T . Amino acid sequence variations in Nicotiana CRR4 orthologs determine the species-specific efficiency of RNA editing in plastids. Nucleic Acids Res. 2008; 36(19):6155-64. PMC: 2577327. DOI: 10.1093/nar/gkn629. View