Skip to main content
SpringerLink
Log in

OsCRS2 encoding a peptidyl-tRNA hydrolase protein is essential for chloroplast development in rice

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Chloroplasts are identified as important organelles for photosynthesis, biosynthesis, and storage of metabolites. So far, the molecular regulatory mechanism of chloroplast development remains to be unclear. The chloroplast RNA splicing 2 (CRS2) protein was determined to play a key role in chloroplast development as they affect the splicing of chloroplast gene introns in maize. However, the functions of OsCRS2 in rice chloroplast development have rarely been studied. In this study, oscrs2-1 and oscrs2-2 mutants were obtained to gene function research using the CRISPR/Cas9 gene editing technology. Both of the mutants displayed an albino seedling phenotype. The OsCRS2 is located in the chloroplast, and is highly expressed in green tissues. OsCRS2 could affect group I and seven group II introns splicing and participate in chloroplast rRNA biogenesis. RNA sequencing analysis indicated that both nuclear-encoded photosynthesis and chloroplast development-related genes expression were significantly reduced in the oscrs2-1 mutant. To conclude, these results suggested that OsCRS2 is necessary for early chloroplast development in rice.

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

References

  • Asakura Y, Barkan A (2006) Arabidopsis orthologs of maize chloroplast splicing factors promote splicing of orthologous and species-specific group II introns. Plant Physiol 142(4):1656–1663

    Article  CAS  Google Scholar 

  • Asakura Y, Barkan A (2007) A CRM domain protein functions dually in group I and group II intron splicing in land plant chloroplasts. Plant Cell 19(12):3864–3875

    Article  CAS  Google Scholar 

  • Asakura Y, Bayraktar OA, Barkan A (2008) Two CRM protein subfamilies cooperate in the splicing of group IIB introns in chloroplasts. RNA 14(11):2319–2332

    Article  CAS  Google Scholar 

  • Barkan A, Goldschmidt-Clermont M (2000) Participation of nuclear genes in chloroplast gene expression. Biochimie 82(6–7):559–572

    Article  CAS  Google Scholar 

  • Beick S, Schmitz-Linneweber C, Williams-Carrier R, Jensen B, Barkan A (2008) The pentatricopeptide repeat protein PPR5 stabilizes a specific tRNA precursor in maize chloroplasts. Mol Cell Biol 28(17):5337–5347

    Article  CAS  Google Scholar 

  • Bose J, Munns R, Shabala S, Gilliham M, Pogson B, Tyerman SD (2015) Insights into chloroplast biogenesis and development. Biochim Biophys Acta 47(9):1017–1024

    Google Scholar 

  • Chateigner-Boutin AL, des Francs-Small CC, Delannoy E, Kahlau S, Tanz SK, de Longevialle AF, Fujii S, Small I (2011) OTP70 is a pentatricopeptide repeat protein of the E subgroup involved in splicing of the plastid transcript rpoC1. Plant J 65(4):532–542

    Article  CAS  Google Scholar 

  • Daras G, Rigas S, Alatzas A, Samiotaki M, Chatzopoulos D, Tsitsekian D, Papadaki V, Templalexis D, Banilas G, Athanasiadou AM, Kostourou V, Panayotou G, Hatzopoulos P (2019) LEFKOTHEA regulates nuclear and chloroplast mRNA splicing in plants. Dev Cell 50(6):767–779

    Article  CAS  Google Scholar 

  • de Longevialle AF, Small ID, Lurin C (2010) Nuclearly encoded splicing factors implicated in RNA splicing in higher plant organelles. Mol Plant 3(4):691–705

    Article  Google Scholar 

  • Gong X, Jiang Q, Xu J, Zhang J, Teng S, Lin D, Dong Y (2013) Disruption of the rice plastid ribosomal protein s20 leads to chloroplast developmental defects and seedling lethality. Genes Genomes Genet 23(10):1769–1777

    Google Scholar 

  • Gothandam KM, Kim ES, Cho H, Chung YY (2005) OsPPR1, a pentatricopeptide repeat protein of rice is essential for the chloroplast biogenesis. Plant Mol Biol 58(3):421–433

    Article  CAS  Google Scholar 

  • Hiei Y, Komari T (2008) Agrobacterium-mediated transformation of rice using immature embryos or calli induced from mature seed. Nat Protoc 3(5):824–834

    Article  CAS  Google Scholar 

  • Jenkins BD, Barkan A (2001) Recruitment of a peptidyl-tRNA hydrolase as a facilitator of group II intron splicing in chloroplasts. EMBO J 20(4):872–879

    Article  CAS  Google Scholar 

  • Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:480–484

    Article  Google Scholar 

  • Kirchhoff H (2019) Chloroplast ultrastructure in plants. New Phytol 223(2):565–574

    Article  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Liu C, Zhu H, Xing Y, Tan J, Chen X, Zhang J, Peng H, Xie Q, Zhang Z (2016) Albino leaf 2 is involved in the splicing of chloroplast group I and II introns in rice. J Exp Bot 67(18):5339–5347

    Article  CAS  Google Scholar 

  • Liu X, Lan J, Huang Y, Cao P, Zhou C, Ren Y, He N, Liu S, Tian Y, Nguyen T, Jiang L, Wan J (2018) WSL5, a pentatricopeptide repeat protein, is essential for chloroplast biogenesis in rice under cold stress. J Exp Bot 69(16):3949–3961

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆CT method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Ostersetzer O, Cooke AM, Watkins KP, Barkan A (2005) CRS1, a chloroplast group II intron splicing factor, promotes intron folding through specific interactions with two intron domains. Plant Cell 17(1):241–255

    Article  CAS  Google Scholar 

  • Ostheimer GJ, Williams-Carrier R, Belcher S, Osborne E, Gierke J, Barkan A (2003) Group II intron splicing factors derived by diversification of an ancient RNA-binding domain. EMBO J 22(15):3919–3929

    Article  CAS  Google Scholar 

  • Ostheimer GJ, Rojas M, Hadjivassiliou H, Barkan A (2006) Formation of the CRS2-CAF2 group II intron splicing complex is mediated by a 22-amino acid motif in the COOH-terminal region of CAF2. J Biol Chem 281(8):4732–4738

    Article  CAS  Google Scholar 

  • Robles P, Quesada V (2019) Transcriptional and post-transcriptional regulation of organellar gene expression (OGE) and its roles in plant salt tolerance. Int J Mol Sci 20(5):1056

    Article  CAS  Google Scholar 

  • Strand A, Asami T, Alonso J, Ecker JR, Chory J (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421(6918):79–83

    Article  CAS  Google Scholar 

  • Sun Y, Tian Y, Cheng S, Wang Y, Hao Y, Zhu J, Zhu X, Zhang Y, Yu M, Lei J, Bao X, Wu H, Wang Y, Wan J (2019) WSL6 encoding an Era-type GTP-binding protein is essential for chloroplast development in rice. Plant Mol Biol 100(6):635–645

    Article  CAS  Google Scholar 

  • Surpin M, Larkin RM, Chory J (2002) Signal transduction between the chloroplast and the nucleus. Plant Cell 14(Suppl):S327–S338

    Article  CAS  Google Scholar 

  • Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11(2):R14

    Article  Google Scholar 

  • Zhang Y, Su J, Duan S, Ao Y, Dai J, Liu J, Wang P, Li Y, Liu B, Feng D, Wang J, Wang H (2011) A highly efficient rice green tissue protoplast system for transient gene expression and studying light/chloroplast-related processes. Plant Methods 7(1):30

    Article  CAS  Google Scholar 

  • Zhang YY, Hao YY, Wang YH, Wang CM, Wang YL, Long WH, Wang D, Liu X, Jiang L, Wan JM (2017) Lethal albinic seedling, encoding a threonyl-tRNA synthetase, is involved in development of plastid protein synthesis system in rice. Plant Cell Rep 36(7):1053–1064

    Article  CAS  Google Scholar 

  • Zhang Q, Shen L, Wang Z, Hu G, Ren D, Hu J, Zhu L, Gao Z, Zhang G, Guo L, Zeng D, Qian Q (2019) OsCAF1, a CRM domain containing protein, influences chloroplast development. Int J Mol Sci 20(18):4386

    Article  CAS  Google Scholar 

  • Zhang Q, Shen L, Ren D, Hu J, Zhu L, Gao Z, Zhang G, Guo L, Zeng D, Qian Q (2020) Characterization of the CRM gene family and elucidating the function of OsCFM2 in rice. Biomolecules 10(2):327

    Article  CAS  Google Scholar 

  • Zheng H, Wang Z, Tian Y, Liu L, Lv F, Kong W, Bai W, Wang P, Wang C, Yu X, Liu X, Jiang L, Zhao Z, Wan J (2019) Rice albino 1, encoding a glycyl-tRNA synthetase, is involved in chloroplast development and establishment of the plastidic ribosome system in rice. Plant Physiol Biochem 139:495–503

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the ‘Collaborative Innovation Project’ of the Chinese Academy of Agricultural Sciences, the Central Public-interest Scientific Institution Basal Research Fund of China National Rice Research Institute (2017RG001-4), and the National Natural Science Foundation of China (31801333).

Author information

Author notes

  1. Qiang Zhang, Yaliang Wang and Lan Shen contributed equally to this study.

Authors and Affiliations

  1. State Key Lab of Rice Biology, China National Rice Research Institute, Hangzhou, 310006, China

    Qiang Zhang, Yaliang Wang, Lan Shen, Deyong Ren, Jiang Hu, Li Zhu, Guangheng Zhang, Longbiao Guo, Dali Zeng & Qian Qian

Authors
  1. Qiang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yaliang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lan Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Deyong Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jiang Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Li Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Guangheng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Longbiao Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Dali Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Qian Qian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Qian Qian.

Additional information

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Electronic supplementary material 1 (DOCX 377 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Q., Wang, Y., Shen, L. et al. OsCRS2 encoding a peptidyl-tRNA hydrolase protein is essential for chloroplast development in rice. Plant Growth Regul 92, 535–545 (2020). https://doi.org/10.1007/s10725-020-00655-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-020-00655-8

Keywords

Search

Navigation