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.
This is a preview of subscription content, access via your institution.





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
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
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
Castandet B, Araya A (2011) RNA editing in plant organelles. Why make it easy? Biochemistry 76(8):924–931
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
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
Farre JC, Aknin C, Araya A, Castandet B (2012) RNA editinin mitochondrial trans-introns is required for splicing. PLoS ONE 7
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
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
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
Hammani K, Giege P (2014) RNA metabolism in plant mitochondria. Trends Plant Sci 19(6):380–389
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
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
Hoagland DR, Arnon D (1950) The water-culture method for growing plants without soil. Calif Agric Expt Stn Circ 347:1–32
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
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
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
Katsuhara M, Shibasaka M (2000) Cell death and growth recovery of barley after transient salt stress. J Plant Res 113:239–243
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
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
Kotera E, Tasaka M, Shikanai T (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature 433:326–330
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
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
Li JY, Jiang AL, Zhang W (2007b) Salt stress-induced programmed cell death in rice root tip cells. J Integr Biol 49:481–486
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
Licht K, Jantsch MF (2016) Rapid and dynamic transcriptome regulation by RNA editing and RNA modifications. J Cell Biol 213(1):15–22
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
Liu S, Melonek J, Boykin LM, Small I, Howell KA (2013) Ancient proteins with enigmatic functions PPR-SMRs. RNA Biol 10:1501–1510
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
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
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
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
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
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
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
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
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
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
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
Rodrigues NF, Fonseca D, Kulcheski GC, Margis R (2017a) Salt stress affects mRNA editing in soybean chloroplasts. Genet Mol Biol 40:200–208
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
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
Ruwe H, Castandet B, Schmitz-Linneweber C, Stern DB (2013) Arabidopsis chloroplast quantitative editotype. FEBS Lett 587:1429–1433
Sun T, Bentolila S, Hanson MR (2016) The unexpected diversity of plant organelle RNA editosomes. Trends Plant Sci 21(11):962–973
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
Tukey J (1949) “Comparing individual means in the analysis of variance.” Biometrics 5(2):99–114
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
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
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
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
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
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.
Author information
Authors and Affiliations
Contributions
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.
Corresponding author
Ethics declarations
Conflict of interest
The author declares that there is no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by the author.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40626-021-00225-x