Skip to main content
Log in

Moss PPR-SMR protein PpPPR_64 influences the expression of a psaA-psaB-rps14 gene cluster and processing of the 23S–4.5S rRNA precursor in chloroplasts

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Key message

Moss PPR-SMR protein PpPPR_64 is a pTAC2 homolog but is functionally distinct from pTAC2. PpPPR_64 is required for psaA gene expression and its function may have evolved in mosses.

Abstract

The pentatricopeptide repeat (PPR) proteins are key regulatory factors responsible for the control of plant organellar gene expression. A small subset of PPR proteins possess a C-terminal small MutS-related (SMR) domain and have diverse roles in plant organellar biogenesis. However, the function of PPR-SMR proteins is not fully understood. Here, we report the function of PPR-SMR protein PpPPR_64 in the moss Physcomitrium patens. Phylogenetic analysis indicated that PpPPR_64 belongs to the same clade as the Arabidopsis PPR-SMR protein pTAC2. PpPPR_64 knockout (KO) mutants grew autotrophically but with reduced protonemata growth and the poor formation of photosystems’ antenna complexes. Quantitative reverse transcription-polymerase chain reaction and RNA gel blot hybridization analyses revealed a significant reduction in transcript levels of the psaA-psaB-rps14 gene cluster but no alteration to transcript levels of most photosynthesis- and non-photosynthesis-related genes. In addition, RNA processing of 23S–4.5S rRNA precursor was impaired in the PpPPR_64 KO mutants. This suggests that PpPPR_64 is specifically involved in the expression level of the psaA-psaB-rps14 gene and in processing of the 23S–4.5S rRNA precursor. Our results indicate that PpPPR_64 is functionally distinct from pTAC2 and is a novel PPR-SMR protein required for proper chloroplast biogenesis in P. patens.

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

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

Similar content being viewed by others

References

  • Barkan A, Small I (2014) Pentatricopeptide repeat proteins in plants. Annu Rev Plant Biol 65:415–442

    CAS  PubMed  Google Scholar 

  • Brochier C, Philippe H, Moreira D (2000) The evolutionary history of ribosomal protein RpS14: horizontal gene transfer at the heart of the ribosome. Trend Genet 16:529–533

    CAS  Google Scholar 

  • Cheng S, Gutmann B, Zhong X, Ye Y, Fisher MF, Bai F, Castleden I, Song Y, Song B, Huang J, Liu X, Xu X, Lim BL, Bond CS, Yiu SM, Small I (2016) Redefining the structural motifs that determine RNA binding and RNA editing by pentatricopeptide repeat proteins in land plants. Plant J 85:532–547

    CAS  PubMed  Google Scholar 

  • Colcombet J, Lopez-Obando M, Heurtevin L, Bernard C, Martin K, Berthomé R, Lurin C (2013) Systematic study of subcellular localization of Arabidopsis PPR proteins confirms a massive targeting to organelles. RNA Biol 10:1557–1575

    PubMed  PubMed Central  Google Scholar 

  • Ebihara T, Matsuda T, Sugita C, Ichinose M, Yamamoto H, Shikanai T, Sugita M (2019) The P-class pentatricopeptide repeat protein PpPPR_21 is needed for accumulation of the psbI-ycf12 dicistronic mRNA in Physcomitrella chloroplasts. Plant J 97:1120–1131

    CAS  PubMed  Google Scholar 

  • Gerke P, Szövényi P, Neubauer A, Lenz H, Gutmann B, McDowell R, Small I, Schallenberg-Rüdinger M, Knoop V (2020) Towards a plant model for enigmatic U-to-C RNA editing: the organelle genomes, transcriptomes, editomes and candidate RNA editing factors in the hornwort Anthoceros agrestis. New Phytol 225:1974–1992

    CAS  PubMed  Google Scholar 

  • Goto S, Kawaguchi Y, Sugita C, Ichinose M, Sugita M (2016) P-class pentatricopeptide repeat protein PTSF1 is required for splicing of the plastid pre-tRNAIle in Physcomitrella patens. Plant J 86:493–503

    CAS  PubMed  Google Scholar 

  • Granneman S, Baserga SJ (2005) Crosstalk in gene expression: coupling and co-regulation of rDNA transcription, pre-ribosome assembly and pre-rRNA processing. Curr Opin Cell Biol 17:281–286

    CAS  PubMed  Google Scholar 

  • Gray MW (1989) The evolutionary origins of organelles. Trends Genet 5:294–299

    CAS  PubMed  Google Scholar 

  • Hein A, Polsakiewicz M, Knoop V (2016) Frequent chloroplast RNA editing in early-branching flowering plants: pilot studies on angiosperm-wide coexistence of editing sites and their nuclear specificity factors. BMC Evol Biol 16:23

    PubMed  PubMed Central  Google Scholar 

  • Hein A, Brenner S, Knoop V (2019) Multifarious evolutionary path- ways of a nuclear RNA editing factor: disjunctions in co-evolution of DOT4 and its chloroplast target rpoC1eU488SL. Genome Biol Evol 11:798–813

    CAS  PubMed  PubMed Central  Google Scholar 

  • Herrmann RG, Westohoff P, Link G (1992) Biogenesis of plastids in higher plants. In: Herrmann RG (ed) Plant gene research, vol 6. Springer, New York, pp 275–349

    Google Scholar 

  • Hess WR, Börner T (1999) Organellar RNA polymerases of higher plants. Int Rev Cytol 190:1–59

    CAS  PubMed  Google Scholar 

  • Ichinose M, Sugita C, Yagi Y, Nakamura T, Sugita M (2013) 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

    CAS  PubMed  Google Scholar 

  • Ito A, Sugita C, Ichinose M, Kato Y, Yamamoto H, Shikanai T, Sugita M (2018) An evolutionarily conserved P-subfamily pentatricopeptide repeat protein is required to splice the plastid ndhA transcript in the moss Physcomitrella patens and Arabidopsis thaliana. Plant J 94:638–648

    CAS  PubMed  Google Scholar 

  • Jiang T, Zhang J, Rong L, Feng Y, Wang Q, Song Q, Zhang L, Ouyang M (2018) ECD1 functions as an RNA-editing trans-factor of rps14-149 in plastids and is required for early chloroplast development in seedlings. J Exp Bot 69:3037–3051

    CAS  PubMed  PubMed Central  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 chloroplast of Arabidopsis. Plant Mol Biol 55:595–606

    CAS  PubMed  Google Scholar 

  • Leaver CJ, Ingle J (1971) The molecular integrity of chloroplast ribosomal ribonucleic acid. Biochem J 123:235–243

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Yu F, Rodermel S (2010) An Arabidopsis pentatricopeptide repeat protein, SUPPRESSOR OF VARIEGATION7, is required for FtsH-mediated chloroplast biogenesis. Plant Physiol 154:1588–1601

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu S, Melonek J, Boykin LM, Small I, Howell KA (2013) PPR-SMRs. Ancient proteins with enigmatic function. RNA Biol 10:1501–1510

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maliga P (1998) Two plastid RNA polymerases of higher plants: an evolving story. Trends Plant Sci 3:4–6

    Google Scholar 

  • Manavski N, Schmid L, Meurer J (2018) RNA-stabilization factors in chloroplasts of vascular plants. Essays Biochem 62:51–64

    PubMed  PubMed Central  Google Scholar 

  • Meurer J, Plücken H, Kowallik KV, Westhoff P (1998) A nuclear-encoded protein of prokaryotic origin is essential for the stability of photosystem II in Arabidopsis thaliana. EMBO J 17:5286–5297

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nishiyama T, Hiwatashi Y, Sakakibara K, Kato M, Hasebe M (2000) Tagged mutagenesis and gene-trap in the moss, Physcomitrella patens by shuttle mutagenesis. DNA Res 7:9–17

    CAS  PubMed  Google Scholar 

  • Pfalz J, Liere K, Kandlbinder A, Dietz K, Oelmüller R (2006) pTAC2, -6, and -12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell 18:176–197

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rensing SA, Goffinet B, Meyberg R, Wu SZ, Bezanilla M (2020) The moss Physcomitrium (Physcomitrella) patens: a model organism for non-seed plants. Plant Cell 32:1361–1376

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rüdinger M, Szövényi P, Rensing SASA, Knoop V (2011) Assigning DYW-type PPR proteins to RNA editing sites in the funariid mosses Physcomitrella patens and Funaria hygrometrica. Plant J 67:370–380

    PubMed  Google Scholar 

  • Schmitz-Linneweber C, Small I (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 13:663–670

    CAS  PubMed  Google Scholar 

  • Shimizu H, Peng L, Myouga F, Motohashi R, Shinozaki K, Shikanai T (2008) CRR23/NdhL is a subunit of the chloroplast NAD(P)H dehydrogenase complex in Arabidopsis. Plant Cell Physiol 49:835–842

    CAS  PubMed  Google Scholar 

  • Small I, Peeters N (2000) The PPR motif—a TPR-related motif prevalent in plant organelle. Trend Biochem Sci 25:46–47

    CAS  PubMed  Google Scholar 

  • Stern DB, Goldschmidt-Clermont M, Hanson MR (2010) Chloroplast RNA metabolism. Ann Rev Plant Biol 61:125–155

    CAS  Google Scholar 

  • Strittmatter G, Kössel H (1984) Cotranscription and processing of 23S, 4.5S and 5S rRNA in chloroplasts from Zea mays. Nucleic Acids Res 12:7633–7647

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sugita M, Sugiura M (1996) Regulation of gene expression in chloroplasts of higher plants. Plant Mol Biol 32:315–326

    CAS  PubMed  Google Scholar 

  • Sugita M, Ichinose M, Ide M, Sugita C (2013) Architecture of the PPR gene family in the moss Physcomitrella patens. RNA Biol 10:1439–1445

    PubMed  PubMed Central  Google Scholar 

  • Sugiura C, Kobayashi Y, Aoki S, Sugita C, Sugita M (2003) Complete chloroplast DNA sequence of the moss Physcomitrella patens: evidence for the loss and relocation of rpoA from the chloroplast to the nucleus. Nucleic Acids Res 31:5324–5331

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tasaki E, Hattori M, Sugita M (2010) The moss pentatricopeptide repeat protein with a DYW domain is responsible for RNA editing of mitochondrial ccmFc transcript. Plant J 62:560–570

    CAS  PubMed  Google Scholar 

  • Uchida M, Ohtani S, Ichinose M, Sugita C, Sugita M (2011) The PPR-DYW proteins are required for RNA editing of rps14, cox1 and nad5 transcripts in Physcomitrella patens mitochondria. FEBS Lett 585:2367–2371

    CAS  PubMed  Google Scholar 

  • Waltz F, Nguyen T, Arrivé M, Bochler A, Chicher J, Hammann P, Kuhn L, Quadrado M, Mireau H, Hashem Y, Giegé P (2019) Small is big in Arabidopsis mitochondrial ribosome. Nature Plants 5:106–117. https://doi.org/10.1038/s41477-018-0339-y

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Liu H, Zhai G, Wang L, Shao J, Tao Y (2016) OspTAC2 encodes a pentatricopeptide repeat protein and regulates rice chloroplast development. J Genet Genom 43:601–608

    Google Scholar 

  • Wu W, Liu S, Ruwe H, Zhang D, Melonek J, Zhu Y, Hu X, Gusewski S, Yin P, Small I, Howell KA, Huang J (2016) SOT1, a pentatricopeptide repeat protein with a small MutS-related domain, is required for correct processing of plastid 23S–4.5S rRNA precursors in Arabidopsis thaliana. Plant J 85:607–621

    CAS  PubMed  Google Scholar 

  • Yagi Y, Hayashi S, Kobayashi K, Hirayama T, Nakamura T (2013) Elucidation of the RNA recognition code for pentatricopeptide repeat proteins involved in organelle RNA editing in plants. PLoS ONE 8:e57286

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Lu C (2019) The enigmatic roles of PPR-SMR proteins in plants. Adv Sci 6:1900361

    Google Scholar 

  • Zhou W, Lu Q, Li Q, Wang L, Ding S, Zhang A, Wen X, Zhang L, Lu C (2017) PPR-SMR protein SOT1 has RNA endonuclease activity. Proc Natl Acad Sci USA 114:E1554

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zoschke R, Watkins KP, Miranda RG, Barkan A (2016) The PPR-SMR protein PPR 53 enhances the stability and translation of specific chloroplast RNAs in maize. Plant J 85:594–606

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Yasuhiro Kawaguchi and Taiga Yamada for contribution in part to this work and Setsuyuki Aoki for helpful advice and discussion. We also thank Fumihiko Sato (Kyoto University), Amane Makino (Tohoku University) and Toru Hisabori (Tokyo Institute of Technology) for providing us antibodies.

Funding

This research was funded by The Japan Society for the Promotion of Science (JSPS KAKENHI Grant Nos. JP17K08195, JP20K05957 to MS; JP18K14435 to MI).

Author information

Authors and Affiliations

Authors

Contributions

CS and MS conceived and designed the experiments. AT, CS and MI performed most of the experiments and analyzed data. MS wrote the manuscript. All authors edited and approved the manuscript.

Corresponding author

Correspondence to Mamoru Sugita.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Takahashi, A., Sugita, C., Ichinose, M. et al. Moss PPR-SMR protein PpPPR_64 influences the expression of a psaA-psaB-rps14 gene cluster and processing of the 23S–4.5S rRNA precursor in chloroplasts. Plant Mol Biol 107, 417–429 (2021). https://doi.org/10.1007/s11103-020-01090-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-020-01090-z

Keywords

Navigation