Abstract
Background
Nad dehydrogenase complex in mtDNA has a significant role in cellular respiration. One of the largest subunits in the complex is subunit 5 (Nad5).
Methods and results
Four cDNAs of the Hordeum vulgare subsp. spontaneum nad5 gene have been characterized and subjected to four phases of 0.5 M salinity, at 0 h (control, accession no. MT235236), after 2 h (acc. no. MT235237), after 12 h (acc. no. MT235238) and after 24 h (acc. no. MT235239). Utilizing raw data from RNA-seq, ten RNA editing sites were reported. Seven sites have common editing from C to U in positions (C1490, C1859, C1895, C1900, C1901, C1916, C1918). A rare editing event U to C was detected in two positions (U1650 and U1652) and a novel editing event U to G was for the first time in positions nad5-U231. The highest editing level was shown in 2 and 12 h after salinity exposure. After 24 h, these edits were disrupted, possibly due to the launch of the programed cell death mechanism. However, the RNA editing in positions U1650, U1652 and U231 was fixed at all exposure times.
Conclusions
Although study clarified the role of salinity stress in nad5 RNA editing sites, the main achievements are first report of U to G RNA editing in plants at position U231 and first report of U to C editing in the nad5 gene at U1650 and U1652.
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Data availability
All data generated or analyzed during this study is included in this published article [and its supplementary information files].
References
Nishikura K (2006) Editor meets silencer: crosstalk between RNA editing and RNA interference. Nat Rev Mol Cell Biol 7(12):919–931
Farajollahi S, Maas S (2010) Molecular diversity through RNA editing: a balancing act. Trends Genet 26(5):221–230
Benne R, Van den Burg J, Brakenhoff JP, Sloof P, Van Boom JH, Tromp MC (1986) Major transcript of the frame shifted coxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell 46(6):819–826
Maris C, Masse J, Chester A, Navaratnam N, Allain FH (2005) Structure of the apoB mRNA stem-loop and its interaction with the C to U editing APOBEC1 complementary factor. RNA 11(2):173–186
Castandet B, Araya A (2011) RNA editing in plant organelles. Why make it easy? Biochemistry (Mosc) 76(8):924–931
Takenaka M, Jörg A, Burger M, Haag S (2019) RNA editing mutants as surrogates for mitochondrial SNP mutants. Plant Physiol Biochem 135:310–321
Ruwe H, Castandet B, Schmitz-Linneweber C, Stern DB (2013) Arabidopsis chloroplast quantitative editotype. FEBS Lett 587:1429–1433
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 Genet 9:e1003584
Licht K, Jantsch MF (2016) Rapid and dynamic transcriptome regulation by RNA editing and RNA modifications. J Cell Biol 213(1):15–22
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
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
Tseng CC, Lee CJ, Chung YT, Sung TY, Hsieh MH (2013) Differential regulation of Arabidopsis plastid gene expression and RNA editing in non-photosynthetic tissues. Plant Mol Biol 82(4–5):375–392
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
Wang C, Chen X, Li H, Song W (2007) RNA editing analysis of mitochondrial nad3/rps12 genes in cytoplasmic male sterility and male-fertile cauliflower (Brassica oleracea var. botrytis) by cDNA-SSCP. Bot Stud 48(1):13–23
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
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
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 137:53–61
Bahieldin A, Atef A, Sabir JS, Gadalla NO, Edris S, Alzohairy AM, Radhwan NA, Baeshen MN, Ramadan AM, Eissa HF et al (2015) RNA-seq analysis of the wild barley (H. spontaneum) leaf transcriptome under salt stress. C R Biol 338(5):285–297
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
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
Chen TC, Liu YC, Wang X, Wu CH, Huang CH, Chang CC (2017) Whole plastid transcriptomes reveal abundant RNA editing sites and differential editing status in Phalaenopsis aphrodite subsp. formosana. Bot Stud 58(1):38. https://doi.org/10.1186/s40529-017-0193-7
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
Rodrigues NF, Christoff AP, da Fonseca GC, Kulcheski FR, Margis R (2017) Unveiling chloroplast RNA editing events using next generation small RNA sequencing data. Front Plant Sci 8:1686
Tukey J (1949) Comparing individual means in the analysis of variance. Biometrics 5(2):99–114
Takenaka M, Zehrmann A, Verbitskiy D, Härtel B, Brennicke A (2013) RNA editing in plants and its evolution. Annu Rev Genet 47:335–352
Rania MM, Areej AS, Thana KK, Hani MA, Ahmed MR (2019) Single nucleotide polymorphism analysis in plastomes of eight Catharanthus roseus cultivars. Biotechnol Biotechnol Equip 33(1):419–428. https://doi.org/10.1080/13102818.2019.1579671
Schuster W, Hiesel R, Wissinger B, Brennicke A (1990) RNA editing in the cytochrome b locus of the higher plant Oenothera berteriana includes a U-to-C transition. Mol Cell Biol 10(5):2428–2431. https://doi.org/10.1128/mcb.10.5.2428
Hajrah NH, Obaid AY, Atef A, Ramadan AM, Arasappan D, Nelson CA, Edris S, Mutwakil MZ, Alhebshi A, Gadalla NO et al (2017) Transcriptomic analysis of salt stress responsive genes in Rhazya stricta. PLoS ONE 12(5):e0177589
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
Ramadan AM (2020) Salinity effects on nad3 gene RNA editing of wild barley mitochondria. Mol Biol Rep 47(5):3857–3865. https://doi.org/10.1007/s11033-020-05475-7
Ramadan AM (2014) RNA editing in Calotropis procera mitochondrial nadh-dehydrogenase subunit 3 gene. Egypt J Genet Cytol 43:353–364
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
Katsuhara M (1997) Apoptosis-like cell death in barley roots under salt stress. Plant Cell Physiol 38:1091–1093
Katsuhara M, Shibasaka M (2000) Cell death and growth recovery of barley after transient salt stress. J Plant Res 113:239–243
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
Li JY, Jiang AL, Zhang W (2007) Salt stress-induced programmed cell death in rice root tip cells. J Integr Biol 49:481–486
Li JY, Jiang AL, Chen HY, Wang Y, Wang Y, Zhang W (2007) Lanthanum prevents salt stress-induced programmed cell death in rice root tip cells by controlling early induction events. J Integr Biol 49:1024–1031
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
Acknowledgements
This project was funded by the Deanship of Scientific Research (DSR) at King Abdulaziz University, Jeddah, under Grant No. G- 91-130-1441. 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- 91-130-1441.
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Ramadan, A.M., Alnufaei, A.A., Khan, T.K. et al. 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, 6057–6064 (2021). https://doi.org/10.1007/s11033-021-06609-1
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DOI: https://doi.org/10.1007/s11033-021-06609-1