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Salinity stress reveals three types of RNA editing sites in mitochondrial Nad7 gene of wild barley both in silico and in qRT-PCR experiments

Abstract

Cellular respiration is an important process performed by mitochondria. Nad complex is the major complex involved in this process and one of the main subunits in this complex is the nad7 (nad dehydrogenase subunit 7). In Hordeum vulgare subsp. spontaneum, four nad7 cDNAs are described at 500 mM salinity, 0 h, or control (GenBank accession no. MW433884), after 2 h (GenBank accession no. MW433885), after 12 h (GenBank accession no. MW433886) and after 24 h (GenBank accession no. MW433887). Twenty six RNA editing sites were revealed in positions: C44, C45, C77, C83, C99, C137, C224, C244, C251, C383, C445, U488, C491, U525, C578, C679, C698, C724, C734, C739, C836, C926, C1088, C1103, C1119, and C1124. These alterations represent three types of editing: C to U, U to C and the very rare type U to G with a differential rate depending on exposure times. Two and twelve hours are shown as the maximum editing rate. However, RNA editing disturbance over 24 h was observed, possibly due to the activation of the machinery for programmed cell death. In addition, RNA editing has been found to optimize codon bias by altering the nucleotides without modifying the amino acids. Small kernel 1 pentatricopeptide repeat protein (Smk1) characterization in wild barley has assisted to explaining the behavior of C836 editing under salt stress. The behavior of nad7 editing under stress may lead to a discrepancy between the editing of RNA and the control of cellular respiration.

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References

  • Affenzeller MJ, Dareshouri A, Andosch A et al (2009) Salt stress-induced cell death in the unicellular green alga Micrasterias denticulata. J Exp Bot 60:939–954

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bahieldin A, Atef A, Sabir JS, Gadalla NO, Edris S, Alzohairy AM, Radhwan NA, Baeshen MN, Ramadan AM, Eissa HF, Hassan SM, Baeshen NA, Abuzinadah O, Al-Kordy MA, El-Domyati FM, Jansen RK (2015) RNA-Seq analysis of the wild barley (H. spontaneum) leaf transcriptome under salt stress. C R Biol 338(5):285–297

    PubMed  Google Scholar 

  • Bentolila S, Heller WP, Sun T, Babina AM, Friso G, Wijk KJ, Hanson MR (2012) RIP1, a member of an Arabidopsis protein family, interacts with the protein RARE1 and broadly affects RNA editing. Proc Natl Acad Sci USA 109:E1453–E1461

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Chu D, Wei L (2019) The chloroplast and mitochondrial C-to-U RNA editing in Arabidopsis thaliana shows signals of adaptation. Plant Direct 3(9):e00169

    CAS  PubMed  PubMed Central  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 Mol Biol 97(3):215–231

    CAS  PubMed  Google Scholar 

  • Farre JC, Aknin C, Araya A, Castandet B (2012) RNA editinin mitochondrial trans-introns is required for splicing. PLoS ONE 7

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fujii S, Bond CS, Small ID (2011) Selection patterns on restorer like genes reveal a conflict between nuclear and mitochondrial genomes throughout angiosperm evolution. Proc Natl Acad Sci USA 108:1723–1728

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guo W, Grewe F, Fan W, Young GJ, Knoop V, Palmer JD, Mower JP (2016) Ginkgo and Welwitschia mitogenomes reveal extreme contrasts in gymnosperm mitochondrial evolution. Mol Biol Evol 33(6):1448–1460

    CAS  PubMed  Google Scholar 

  • Hajrah NH, Obaid AY, Atef A, Ramadan AM, Arasappan D, Nelson CA, Edris S, Mutwakil MZ, Alhebshi A, Gadalla NO, Makki RM, Al-Kordy MA, El-Domyati FM, Sabir JSM, Khiyami MA, Hall N, Bahieldin A, Jansen RK (2017) Transcriptomic analysis of salt stress responsive genes in Rhazya stricta. PLoS ONE 12(5):e0177589

    PubMed  PubMed Central  Google Scholar 

  • Hammani K, Giege P (2014) RNA metabolism in plant mitochondria. Trends Plant Sci 19(6):380–389

    CAS  PubMed  Google Scholar 

  • He P, Xiao G, Liu H, Zhang L, Zhao L, Tang M, Huang S, An Y, Yu J (2018) Two pivotal RNA editing sites in the mitochondrial atp1mRNA are required for ATP synthase to produce sufficient ATP for cotton fiber cell elongation. New Phytol 218(1):167–182

    CAS  PubMed  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):824

    PubMed  PubMed Central  Google Scholar 

  • Hoagland DR, Arnon D (1950) The water-culture method for growing plants without soil. Calif Agric Expt Stn Circ 347:1–32

    Google Scholar 

  • Huh GH, Damsz B, Matsumoto TK, Reddy MP, Rus AM, Ibeas JI, Narasimhan ML, Bressan RA, Hasegawa PM (2002) Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. Plant J 29:649–659

    CAS  PubMed  Google Scholar 

  • Ishii S, 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 4:1601

    PubMed  Google Scholar 

  • Junjie Y, Yao Y, Hong S, Yang Y, Shen C, Zhang Q, Zhang D, Zou T, Yin Ping (2019) Delineation of pentatricopeptide repeat codes for target RNA prediction. Nucleic Acid Res 47(7):3728–3738. https://doi.org/10.1093/nar/gkz075

    Article  CAS  Google Scholar 

  • Katsuhara M, Shibasaka M (2000) Cell death and growth recovery of barley after transient salt stress. J Plant Res 113:239–243

    CAS  Google Scholar 

  • Kim S-R, Yang J-I, Moon S, Ryu C-H, An K, Kim K-M, Yim J, An G (2009) Rice OGR1 encodes a pentatricopeptide repeat-DYW proteinand is essential for RNA editing in mitochondria. Plant J 59:738–749

    CAS  PubMed  Google Scholar 

  • Knie N, Grewe F, Fischer S, Knoop V (2016) Reverse U-to-C editing exceeds C-to-U RNA editing in some ferns–a monilophyte-wide comparison of chloroplast and mitochondrial RNA editing suggests independent evolution of the two processes in both organelles. BMC Evol Biol 16:134

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kurihara-Yonemoto S, Kubo T (2010) Increased accumulation of introncontaining transcripts in rice mitochondria caused by low temperature: is cold-sensitive RNA editing implicated? Curr Genet 56:529–541. https://doi.org/10.1007/s00294-010-0320-4

    Article  CAS  PubMed  Google Scholar 

  • Li JY, Jiang AL, Chen HY, Wang Y, Wang Y, Zhang W (2007a) Lanthanum prevents salt stress-induced programmed cell death in rice root tip cells by controlling early induction events. J Integr Biol 49:1024–1031

    CAS  Google Scholar 

  • Li JY, Jiang AL, Zhang W (2007b) Salt stress-induced programmed cell death in rice root tip cells. J Integr Biol 49:481–486

    CAS  Google Scholar 

  • Li XJ, Zhang YF, Hou M, Sun F, Shen Y, Xiu ZH, Wang X, Chen ZL, Sun SS, Small I, Tan BC (2014) Small kernel 1 encodes a pentatricopeptide repeat protein required for mitochondrial nad7 transcript editing and seed development in maize (Zea mays) and rice (Oryza sativa). Plant J J79(5):797–809. https://doi.org/10.1111/tpj.12584

    Article  CAS  Google Scholar 

  • Licht K, Jantsch MF (2016) Rapid and dynamic transcriptome regulation by RNA editing and RNA modifications. J Cell Biol 213(1):15–22

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lin J, Wang Y, Wang G (2005) Salt stress-induced programmed cell death via Ca2+-mediated mitochondrial permeability transition in tobacco protoplasts. Plant Growth Regul 45:243–250

    CAS  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) Method. Methods 25(4):402–408

    CAS  PubMed  Google Scholar 

  • Lo Giudice C, Hernández I, Ceci LR, Pesole G, Picardi E (2019) RNA editing in plants: a comprehensive survey of bioinformatics tools and databases. Plant Physiol Biochem 137:53–56

    CAS  PubMed  Google Scholar 

  • Luyen TV, Toshifumi T (2017) C-to-U editing and site-directed RNA editing for the correction of genetic mutations. Biosci Trends 11(3):243–253

    Google Scholar 

  • Nakajima Y, Mulligan RM (2001) Heat stress results in incomplete Cto-U editing of maize chloroplast mRNAs and correlates with changes in chloroplast transcription rate. Curr Genet 40:209–213. https://doi.org/10.1007/s002940100249

    Article  CAS  PubMed  Google Scholar 

  • O’Toole N, Hattori M, Andres C, Iida K, Lurin C, Schmitz-Linneweber C, Sugita M, Small I (2008) On the expansion of the pentatricopeptide repeat gene family in plants. Mol Biol Evol 25:1120–1128

    PubMed  Google Scholar 

  • Picardi E, D’Erchia AM, Gallo A, Montalvo A, Pesole G (2014) Uncovering RNA editing sites in long non-coding RNAs. Front Bioeng Biotechnol 2:64

    PubMed  PubMed Central  Google Scholar 

  • Ramadan AM (2020a) Salinity effects on nad3 gene RNA editing of wild barley mitochondria. Mol Biol Rep 47(5):3857–3865. https://doi.org/10.1007/s11033-020-05475

    Article  CAS  PubMed  Google Scholar 

  • Ramadan AM (2020b) Light/heat effects on RNA editing in chloroplast NADH-plastoquinone oxidoreductase subunit 2 (ndhB) gene of Calotropis (Calotropis procera). J Genet Eng Biotechnol 18:49. https://doi.org/10.1186/s43141-020-00064-4

    Article  PubMed  PubMed Central  Google Scholar 

  • Rieder LE, Savva YA, Reyna MA, Chang YJ, Dorsky JS, Rezaei A, Reenan RA (2015) Dynamic response of RNA editing to temperature in Drosophila. BMC Biol 13:1

    PubMed  PubMed Central  Google Scholar 

  • Riemondy KA, Gillen AE, White EA, Bogren LK, Hesselberth JR, Martin SL (2018) Dynamic temperature-sensitive A-to-I RNA editing in the brain of a heterothermic mammal during hibernation. RNA 24:1481–1495

    CAS  PubMed  PubMed Central  Google Scholar 

  • Slugina MA, Shchennikova AV, Kochieva EZ (2019) Differences in the sucrose synthase gene SUS1 expression pattern between Solanum lycopersicum and wild tomato species. Theor Exp Plant Physiol 31:455–462. https://doi.org/10.1007/s40626-019-00158-6

    Article  CAS  Google Scholar 

  • Rodrigues NF, Fonseca D, Kulcheski GC, Margis R (2017a) Salt stress affects mRNA editing in soybean chloroplasts. Genet Mol Biol 40:200–208

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rodrigues NF, Christoff AP, Fonseca D, Kulcheski GC, Margis R (2017b) Unveiling chloroplast RNA editing events using next generation small RNA sequencing data. Front Plant Sci 8:1686

    PubMed  PubMed Central  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 Biochim Pol 48(3):711–717

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Sun T, Bentolila S, Hanson MR (2016) The unexpected diversity of plant organelle RNA editosomes. Trends Plant Sci 21(11):962–973

    CAS  PubMed  Google Scholar 

  • Toda T, Fujii S, Noguchi K, Kazama T, Toriyama K (2012) Rice MPR25 encodes a pentatricopeptide repeat protein and is essential for RNA editing of nad5 transcripts in mitochondria. Plant J 72:450–460

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Wang M, Cui L, Feng K, Deng P, Du X, Wan F, Song W, 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 

  • Xiao H, Zhang Q, Qin X, Xu Y, Ni C, Huang J, Zhu L, Zhong F, Liu W, Yao G, Zhu Y, Hu J (2018) Rice PPS1 encodes a DYW motif-containing pentatricopeptide repeat protein required for five consecutive RNA-editing sites of nad3 in mitochondria. New Phytol 220:878–892

    CAS  PubMed  Google Scholar 

  • Xiong J, Tao T, Luo Z, Yan S, Liu Y, Yu X, Liu G, Xia H, Luo L (2017) RNA editing responses to oxidative stress between a wild abortive type male-sterile line and its maintainer line. Front Plant Sci 8:2023. https://doi.org/10.3389/fpls.2017.02023

    Article  PubMed  PubMed Central  Google Scholar 

  • Yap A, Kindgren P, Colas des Francs-Small C, Kazama T, Tanz SK, Toriyama K, Small I (2015) AEF1/MPR25 is implicated in RNA editingof plastid atpF and mitochondrial nad5 and also promotes atpF splicingin Arabidopsis and rice. Plant J 81:661–669

    CAS  PubMed  Google Scholar 

  • Yuan H, Liu D (2012) Functional disruption of the pentatricopeptide protein SLG1affects mitochondrial RNA editing, plant development, and responses to abiotic stresses in Arabidopsis. Plant J 70:432–444

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors acknowledge the Saudi Basic Industries Corporation (SABIC) and the Deanship of Scientific Research (DSR) at King Abdulaziz University, Jeddah, for technical and financial support.

Funding

This project was funded by the Deanship of Scientific Research (DSR) at King Abdulaziz University, Jeddah, under grant no S-86-130-1440.

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Research ideas and experimental design were achieved by (AMR). Material preparation, data collection and analysis were performed by (OAMS). The first draft of the manuscript was written by (AMA) and all the authors commented on the previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Ahmed M. Ramadan.

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Ramadan, A.M., Said, O.A.M. & Abushady, A.M. Salinity stress reveals three types of RNA editing sites in mitochondrial Nad7 gene of wild barley both in silico and in qRT-PCR experiments. Theor. Exp. Plant Physiol. 34, 13–22 (2022). https://doi.org/10.1007/s40626-021-00225-x

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  • DOI: https://doi.org/10.1007/s40626-021-00225-x

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