Photosynthetica 2018, 56(1):62-66 | DOI: 10.1007/s11099-017-0755-7

Chloroplast ribonucleoprotein-like proteins of the moss Physcomitrella patens are not involved in RNA stability and RNA editing

H. Uchiyama1, M. Ichinose1,2, M. Sugita1,*
1 Center for Gene Research, Nagoya University, Chikusa-ku, Nagoya, Japan
2 Institute of Transformative Bio-Molecules, Nagoya University, Chikusa-ku, Nagoya, Japan

Many RNA recognition motif (RRM)-containing proteins are known to exist in chloroplasts. Major members of the RRM protein family, which are chloroplast ribonucleoproteins (cpRNPs), have been investigated in seed plants, including tobacco and Arabidopsis thaliana, but never in early land plants, such as bryophytes. In this study, we surveyed RRM proteins encoded in the moss Physcomitrella patens genome and predicted 25 putative chloroplast RRM proteins. Among them, two RRM-containing proteins, PpRBP2a and PpRBP2b, resembled cpRNPs and were thus referred to as cpRNP-like proteins. However, knockout mutants of either one or two PpRBP2 genes exhibited a wild type-like phenotype. Unlike Arabidopsis cpRNPs, the levels of mRNA accumulation in chloroplasts were not affected in the PpRBP2 knockout mutants. In addition, the efficiency of RNA editing was also not altered in the mutants. This suggests that PpRBP2a and 2b may be functionally distinct from Arabidopsis cpRNPs.

Keywords: pentatricopeptide repeat protein; photosynthesis gene; posttranscriptional regulation; RNA-binding protein; RNA processing

Received: April 29, 2017; Accepted: July 17, 2017; Published: March 1, 2018Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Uchiyama, H., Ichinose, M., & Sugita, M. (2018). Chloroplast ribonucleoprotein-like proteins of the moss Physcomitrella patens are not involved in RNA stability and RNA editing. Photosynthetica56(1), 62-66. doi: 10.1007/s11099-017-0755-7.
Download citation

Supplementary files

Download filephs-201801-0005_S1.pdf

File size: 258.94 kB

Download filephs-201801-0005_S2.pdf

File size: 1.07 MB

Download filephs-201801-0005_S3.pdf

File size: 319.04 kB

References

  1. Allen J.F., de Paula W.B.M., Puthiyaveetil S. et al: A structural phylogenetic map for chloroplast photosynthesis.-Trends Plant Sci. 16: 645-655, 2011. Go to original source...
  2. Amme S., Matros A., Schlesier B. et al.: Proteome analysis of cold stress response in Arabidopsis thaliana using DIGEtechnology.-J. Exp. Bot. 57: 1537-1546, 2006. Go to original source...
  3. Belostotsky D.A.: Unexpected complexity of poly(A)-binding protein gene families in flowering plants: Three conserved lineages that are at least 200 million years old and possible auto- and cross-regulation.-Genetics 163: 311-319, 2003.
  4. del Campo E.M.: Post-transcriptional control of chloroplast gene expression.-Gene Reg. Syst. Biol. 3: 31-47, 2009.
  5. Fesenko I., Seredina A., Arapidi G. et al.: The Physcomitrella patens chloroplast proteome changes in response to protoplastation.-Front. Plant Sci. 7: 1661, 2016.
  6. Goto S., Kawaguchi Y., Sugita C. et al.: P-class pentatricopeptide repeat protein PTSF1 is required for splicing of the plastid pretRNAIle in Physcomitrella patens.-Plant J. 86: 493-503, 2016. Go to original source...
  7. Hirose T., Sugiura M.: Involvement of a site-specific trans-acting factor and a common RNA-binding protein in the editing of chloroplast mRNAs: development of a chloroplast in vitro RNA editing system.-EMBO J. 20: 1144-1152, 2001. Go to original source...
  8. Ichinose M., Sugita C., Yagi Y. et al.: Two DYW subclass PPR proteins are involved in RNA editing of ccmFc and atp9 transcripts in the moss Physcomitrella patens: First complete set of PPR editing factors in plant mitochondria.-Plant Cell Physiol. 54: 1907-1916, 2013.
  9. Kupsch C., Ruwe H., Gusewski S. et al.: Arabidopsis chloroplast RNA binding proteins CP31A and CP29A associate with large transcript pools and confer cold stress tolerance by influencing multiple chloroplast RNA processing steps.-Plant Cell 24: 4266-4280, 2012. Go to original source...
  10. Li Y., Sugiura M.: Three distinct ribonucleoproteins from tobacco chloroplasts: each contains a unique amino terminal acidic domain and two ribonucleoprotein consensus motifs.-EMBO J. 9: 3059-3066, 1990. Go to original source...
  11. Maris C., Dominguez C., Allain F.H.T.: The RNA recognition motif, a plastic RNA-binding platform to regulate posttranscriptional gene expression.-FEBS J. 272: 2118-2131, 2005.
  12. Miyata Y., Sugita M.: Tissue- and stage-specific RNA editing of rps14 transcripts in moss (Physcomitrella patens) chloroplasts.-J. Plant Physiol. 161: 113-115, 2004. Go to original source...
  13. Mueller S.J., Lang D., Hoernstein S.N.W. et al.: Quantitative analysis of the mitochondrial and plastid proteomes of the moss Physcomitrella patens reveals protein macrocompartmentation and microcompartmentation.-Plant Physiol. 164: 2081-2095, 2014. Go to original source...
  14. Nagai K., Oubridge C., Jessen T.H. et al.: Crystal structure of the RNA-binding domain of the U1 small nuclear ribonucleoprotein A.-Nature 348: 515-520, 1990. Go to original source...
  15. Nakamura T., Ohta M., Sugiura M. et al.: Chloroplast ribonucleoproteins are associated with both mRNAs and intron-containing precursor tRNAs.-FEBS Lett. 460: 437-441, 1999. Go to original source...
  16. Nakamura T., Ohta M., Sugiura M. et al.: Chloroplast ribonucleoproteins function as a stabilizing factor of ribosomefree mRNAs in the stroma.-J. Biol. Chem. 276: 147-152, 2001. Go to original source...
  17. Nickelsen J.: Chloroplast RNA-binding proteins.-Curr. Genet. 43: 392-399, 2003. Go to original source...
  18. Pribat A., Blaby I.K., Lara-Núñez A. et al: A 5-formyltetrahydrofolate cycloligase paralog from all domains of life: comparative genomic and experimental evidence for a cryptic role in thiamin metabolism.-Funct. Integr. Genomic. 11: 467-478, 2011. Go to original source...
  19. Ruwe H., Kupsch C., Teubner M. et al.: The RNA-recognition motif in chloroplasts.-J. Plant Physiol. 168: 1361-1371, 2011. Go to original source...
  20. Sarhadi E., Mahfoozi S., Hosseini S.A. et al.: Cold acclimation proteome analysis reveals close link between the up-regulation of low-temperature associated proteins and vernalization fulfillment.-J. Proteome Res. 9: 5658-5667, 2010. Go to original source...
  21. Schuster G., Gruissem W.: Chloroplast mRNA 3' end processing requires a nuclear-encoded RNA-binding protein.-EMBO J. 10: 1493-1502, 1991. Go to original source...
  22. Stern D., Goldschmidt-Clermont M., Hanson M.R.: Chloroplast RNA metabolism.-Annu. Rev. Plant Biol. 61: 125-155, 2010. Go to original source...
  23. Sugita M., Ichinose M., Ide M. et al.: Architecture of the PPR gene family in the moss Physcomitrella patens.-RNA Biol. 10: 1439-1445, 2013. Go to original source...
  24. Sun T., Germain A., Giloteaux L. et al.: An RNA recognition motif-containing protein is required for plastid RNA editing in Arabidopsis and maize.-P. Natl. Acad. Sci. USA 110: E1169-E1178, 2013. Go to original source...
  25. Teubner M., Fuß J., Kühn K. et al.: The RNA recognition motif protein CP33A is a global ligand of chloroplast mRNAs and is essential for plastid biogenesis and plant development.-Plant J. 89: 472-485, 2017. Go to original source...
  26. Tillich M., Hardel S.L., Kupsch C. et al.: Chloroplast ribonucleoprotein CP31A is required for editing and stability of specific chloroplast mRNAs.-P. Natl. Acad. Sci. USA 106: 6002-6007, 2009. Go to original source...
  27. Tillich M., Beick S., Schmitz-Linneweber C.: Chloroplast RNAbinding proteins. Repair and regulation of chloroplast transcripts.-RNA Biol. 7: 172-178, 2010. Go to original source...
  28. Wang S., Bai G., Wang S. et al.: Chloroplast RNA-binding protein RBD1 promotes chilling tolerance through 23S rRNA processing in Arabidopsis.-PLoS Genet. 12: e1006027, 2016. Go to original source...