Skip to main content
Log in

Effect of salinity on ccmfn gene RNA editing of mitochondria in wild barley and uncommon types of RNA editing

  • Original Article
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

The primary function of mitochondria is cellular respiration and energy production. Cytochrome C complex is an essential complex that transports electrons in the respiratory chain between complex III and complex IV. One of this complex’s main subunits is CcmFN, which is believed to be crucial for holocytochrome assembly. In wild-type plant Hordeum vulgare subsp. spontaneum, four ccmfn cDNAs are subjected to high salt stress (500 mM salinity), 0 h (or control) (GenBank accession no. ON764850), after 2 h (GenBank accession no. ON7648515), after 12 h (GenBank accession no. ON764852), and after 24 h (GenBank accession no. ON764853) and mtDNA of ccmfn gene (GenBank accession no. ON764854). Using raw data from RNA-seq, 47 sites with nucleotide and amino acid modifications were detected. There were ten different RNA editing types, with most of them are C to U. Unusual editing types in plants have also been found, such as A to C, C to A, A to G, A to U, T to A, T to C, C to G, G to C, and T to G. High levels of editing were observed in control as well as treatments of salinity stress. Amino acid changes were found in 43 sites; nearly all showed hydrophilic to hydrophilic alterations. Only C749 showed regulation under salinity stress.

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data Availability

All data generated or analyzed during this study are included in this published article [and its supplementary information files].

References

  • Bahieldin A, Atef A, Sabir JS, Gadalla NO, Edris S, Alzohairy AM, Radhwan NA, Baeshen MN, Ramadan AM, Eissa HF (2015) RNA-seq analysis of the wild barley (H. spontaneum) leaf transcriptome under salt stress. Comptes rendus biologies. 338(5):285–297

    PubMed  Google Scholar 

  • Benne R, Van den Burg J, Brakenhoff JP, Sloof P, Van Boom JH, Tromp MC (1986) Major transcript of the frameshifted coxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell. 46(6):819–826

    CAS  PubMed  Google Scholar 

  • Bentolila S, Oh J, Hanson MR, Bukowski R (2013) Comprehensive high-resolution analysis of the role of an arabidopsis gene family in RNA editing. PLoS genetics. 9(6):e1003584

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bi C, Lu N, Xu Y, He C, Lu Z (2020) Characterization and analysis of the mitochondrial genome of common bean (Phaseolus vulgaris) by comparative genomic approaches. Int J Molecular Sci 21(11):3778

    CAS  Google Scholar 

  • Brenner WG, Mader M, Müller NA, Hoenicka H, Schroeder H, Zorn I, Fladung M, Kersten B (2019) High level of conservation of mitochondrial RNA editing sites among four populus species G3. Genes Genomes Genetics. 9(3):709–717

    CAS  PubMed  PubMed Central  Google Scholar 

  • Castandet B, Araya A (2011) RNA editing in plant organelles Why make it easy? Biochemistry (Moscow) 76(8):924–931

    CAS  PubMed  Google Scholar 

  • Chen T-C, Liu Y-C, Wang X, Wu C-H, Huang C-H, Chang C-C (2017) Whole plastid transcriptomes reveal abundant RNA editing sites and differential editing status in Phalaenopsis aphrodite subsp formosana. Botanical Stud 58(1):1–14

    Google Scholar 

  • Edera AA, Gandini CL, Sanchez-Puerta MV (2018) Towards a comprehensive picture of C-to-U RNA editing sites in angiosperm mitochondria. Plant molecular biology. 97(3):215–231

    CAS  PubMed  Google Scholar 

  • Germain A, Hanson MR, Bentolila S (2015) High-throughput quantification of chloroplast RNA editing extent using multiplex RT-PCR mass spectrometry. The Plant J 83(3):546–554

    CAS  PubMed  Google Scholar 

  • Giegé P, Brennicke A (1999) RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs. Proc Nat Acad Sci 96(26):15324–15329

    PubMed  PubMed Central  Google Scholar 

  • Giegé P, Rayapuram N, Meyer EH, Grienenberger JM, Bonnard G (2004) Ccmfc involved in cytochrome c maturation is present in a large sized complex in wheat mitochondria. FEBS letters. 563(1–3):165–169

    PubMed  Google Scholar 

  • Giudice CL, Hernández I, Ceci LR, Pesole G, Picardi E (2019) RNA editing in plants: a comprehensive survey of bioinformatics tools and databases. Plant Physiol Biochem 137:53–61

    PubMed  Google Scholar 

  • Gray M (2003) Diversity and evolution of mitochondrial RNA editing systems. IUBMB life. 55(4–5):227–233

    CAS  PubMed  Google Scholar 

  • Hajrah NH, Obaid AY, Atef A, Ramadan AM, Arasappan D, Nelson CA, Edris S, Mutwakil MZ, Alhebshi A, Gadalla NO (2017) Transcriptomic analysis of salt stress responsive genes in Rhazya stricta. PloS one. 12(5):e0177589

    PubMed  PubMed Central  Google Scholar 

  • Handa H (2003) The complete nucleotide sequence and RNA editing content of the mitochondrial genome of rapeseed (Brassica napus L.): comparative analysis of the mitochondrial genomes of rapeseed and Arabidopsis thaliana. Nucleic acids Res 31(20):5907–5916

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hisano H, Tsujimura M, Yoshida H, Terachi T, Sato K (2016) Mitochondrial genome sequences from wild and cultivated barley (Hordeum vulgare). BMC genomics 17(1):1–12

    Google Scholar 

  • Ichinose M, Sugita M (2017) RNA editing and its molecular mechanism in plant organelles. Genes 8(1):5

    Google Scholar 

  • Kim B, Kim K, Yang T-J, Kim S (2016) Completion of the mitochondrial genome sequence of onion (Allium cepa L.) containing the CMS-S male-sterile cytoplasm and identification of an independent event of the ccmf n gene split. Curr Genet 62(4):873–885

    CAS  PubMed  Google Scholar 

  • Kotera E, Tasaka M, Shikanai T (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature. 433(7023):326–330

    CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method (2001). Methods 25(4):402-8. https://doi.org/10.1006/meth.2001.1262

  • Meng Y, Chen D, Jin Y, Mao C, Wu P, Chen M (2010) RNA editing of nuclear transcripts in Arabidopsis thaliana. BMC genomics 11(4):1–7

    Google Scholar 

  • Ramadan AM (2020) Salinity effects on nad3 gene RNA editing of wild barley mitochondria. Mol Biol Rep 47(5):3857–3865

    CAS  PubMed  Google Scholar 

  • Ramadan AM, Alnufaei AA, Khan TK, Ali HM, Eissa HF, Hassan SM (2021) The first report of RNA U to C or G editing in the mitochondrial NADH dehydrogenase subunit 5 (NAD5) transcript of wild barley. Mol Biol Rep 48(8):6057–6064

    CAS  PubMed  Google Scholar 

  • Rayapuram N, Hagenmuller J, Grienenberger J-M, Giegé P, Bonnard G (2007) Atccma interacts with atccmb to form a novel mitochondrial ABC transporter involved in cytochrome c maturation in arabidopsis. J Biol Chem 282(29):21015–21023

    CAS  PubMed  Google Scholar 

  • Rayapuram N, Hagenmuller J, Grienenberger JM, Bonnard G, Giegé P (2008) The three mitochondrial encoded ccmf proteins form a complex that interacts with CCMH and c-type apocytochromes in arabidopsis. J Biol Chem 283(37):25200–25208

    CAS  PubMed  Google Scholar 

  • Rurek M, Szklarczyk M, Adamczyk N, Michalik B, Augustyniak H (2001) Differences in editing of mitochondrial NAD3 transcripts from CMS and fertile carrots. Acta Biochimica Polonica. 48(3):711–717

    CAS  PubMed  Google Scholar 

  • Ruwe H, Castandet B, Schmitz-Linneweber C, Stern DB (2013) Arabidopsis chloroplast quantitative editotype. FEBS letters. 587(9):1429–1433

    CAS  PubMed  Google Scholar 

  • Sabir JS, Arasappan D, Bahieldin A, Abo-Aba S, Bafeel S, Zari TA, Edris S, Shokry AM, Gadalla NO, Ramadan AM, Atef A, Al-Kordy MA, El-Domyati FM, Jansen RK (2014) Whole mitochondrial and plastid genome SNP analysis of nine date palm cultivars reveals plastid heteroplasmy and close phylogenetic relationships among cultivars. PLoS One 9(4):e94158

    PubMed  PubMed Central  Google Scholar 

  • Sechet J, Roux C, Plessis A, Effroy D, Frey A, Perreau F, Biniek C, Krieger-Liszkay A, Macherel D, North HM (2015) The ABA-deficiency suppressor locus HAS2 encodes the PPR protein LOI1/MEF11 involved in mitochondrial RNA editing. Molecular Plant 8(4):644–656

    CAS  PubMed  Google Scholar 

  • Si Ishii, Suzuki S, Norden-Krichmar TM, Tenney A, Chain PS, Scholz MB, Nealson KH, Bretschger O (2013) A novel metatranscriptomic approach to identify gene expression dynamics during extracellular electron transfer. Nat Commun 4(1):1–10

    Google Scholar 

  • Sun F, Wang X, Bonnard G, Shen Y, Xiu Z, Li X, Gao D, Zhang Z, Tan BC (2015) Empty pericarp7 encodes a mitochondrial E–subgroup pentatricopeptide repeat protein that is required for ccm FN editing, mitochondrial function and seed development in maize. The Plant J 84(2):283–295

    CAS  PubMed  Google Scholar 

  • Sun Y, Law Y-S, Cheng S, Lim BL (2017) RNA editing of cytochrome c maturation transcripts is responsive to the energy status of leaf cells in Arabidopsis thaliana. Mitochondrion. 35:23–34

    CAS  PubMed  Google Scholar 

  • Szandar K, Krawczyk K, Myszczyński K, Ślipiko M, Sawicki J, Szczecińska M (2022) Breaking the limits-multichromosomal structure of an early eudicot pulsatilla patens mitogenome reveals extensive RNA-editing, longest repeats and chloroplast derived regions among sequenced land plant mitogenomes. BMC Plant Biol 22(1):1–15

    Google Scholar 

  • Tac HA, Koroglu M, Sezerman U (2021) RDDSVM: accurate prediction of A-to-I RNA editing sites from sequence using support vector machines. Funct Integr Genomics 21:633–643. https://doi.org/10.1007/s10142-021-00805-9

    Article  CAS  PubMed  Google Scholar 

  • Takenaka M, Verbitskiy D, van der Merwe JA, Zehrmann A, Brennicke A (2008) The process of RNA editing in plant mitochondria. Mitochondrion. 8(1):35–46

    CAS  PubMed  Google Scholar 

  • Takenaka M, Zehrmann A, Verbitskiy D, Härtel B, Brennicke A (2013) RNA editing in plants and its evolution. Annu Rev Genet 47:335–352

    CAS  PubMed  Google Scholar 

  • Tan Z-J, Chen S-J (2011) Salt contribution to RNA tertiary structure folding stability. Biophysical Journal 101(1):176–187

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tseng C-C, Lee C-J, Chung Y-T, Sung T-Y, Hsieh M-H (2013) Differential regulation of arabidopsis plastid gene expression and RNA editing in non-photosynthetic tissues. Plant Mol Biol 82(4):375–392

    CAS  PubMed  Google Scholar 

  • Tukey J (1949) Comparing individual means in the analysis of variance". Biometrics 5(2):99–114

    CAS  PubMed  Google Scholar 

  • Unseld M, Marienfeld JR, Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet 15(1):57–61

    CAS  PubMed  Google Scholar 

  • Wang M, Cui L, Feng K, Deng P, Du X, Wan F, Weining S, Nie X (2015) Comparative analysis of Asteraceae chloroplast genomes: structural organization, RNA editing and evolution. Plant Mol Biol Rep 33(5):1526–1538

    CAS  Google Scholar 

  • Wintz H, Hanson MR (1991) A termination codon is created by RNA editing in the petunia mitochondrial ATP9 gene transcript. Curr Genet 19(1):61–64

    CAS  PubMed  Google Scholar 

  • Wu B, Chen H, Shao J, Zhang H, Wu K, Liu C (2017) Identification of symmetrical RNA editing events in the mitochondria of Salvia miltiorrhiza by strand-specific RNA sequencing. Sci Rep 7(1):1–11

    Google Scholar 

  • Xiao H, Zhang Q, Qin X, Xu Y, Ni C, Huang J, Zhu L, Zhong F, Liu W, Yao G (2018) Rice PPS 1 encodes a DYW motif-containing pentatricopeptide repeat protein required for five consecutive RNA-editing sites of nad3 in mitochondria. New Phytologist. 220(3):878–892

    CAS  PubMed  Google Scholar 

  • Yang J, Cui Y, Zhang X, Yang Z, Lai J, Song W, Liang J, Li X (2022) Maize PPR278 functions in mitochondrial RNA splicing and editing. Int J Mol Sci 23(6):3035

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan H, Liu D (2012) Functional disruption of the pentatricopeptide protein SLG1 affects mitochondrial RNA editing, plant development, and responses to abiotic stresses in arabidopsis. The Plant J 70(3):432–444

    CAS  PubMed  Google Scholar 

  • Zhang A, Jiang X, Zhang F et al (2020) Dynamic response of RNA editing to temperature in grape by RNA deep sequencing. Funct Integr Genomics 20:421–432. https://doi.org/10.1007/s10142-019-00727-7

    Article  CAS  PubMed  Google Scholar 

  • Zheng P, Wang D, Huang Y, Chen H, Du H, Tu J (2020) Detection and analysis of C-to-U RNA editing in rice mitochondria-encoded ORFs. Plants. 9(10):1277

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic acids Research. 31(13):3406–3415

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This project was funded by the Deanship of Scientific Research (DSR) at King Abdulaziz University, Jeddah, under grant no. G: 51-130-1440. The authors, therefore, acknowledge and thank DSR’s technical and financial support.

Funding

This project was funded by the Deanship of Scientific Research (DSR) at King Abdulaziz University, Jeddah, under grant no. G: 51-130-1440.

Author information

Authors and Affiliations

Authors

Contributions

A.M.R. contributed to the study’s conception and design. A.A.A. prepared material and data collection. T.K. performed analysis. S.M.H. and S.F. wrote the first draft of the manuscript, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Ahmed Ramadan or Afnan A. Alnufaei.

Ethics declarations

Ethics approval and consent to participate

This article does not contain any studies with human participants or animals performed by the authors.

Consent for publication

All the authors have consent for publication.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's note

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

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ramadan, A., Alnufaei, A.A., Fiaz, S. et al. Effect of salinity on ccmfn gene RNA editing of mitochondria in wild barley and uncommon types of RNA editing. Funct Integr Genomics 23, 50 (2023). https://doi.org/10.1007/s10142-023-00978-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10142-023-00978-5

Keywords

Navigation