Identification and analysis of superoxide dismutase (SOD) family genes in oat (Avena sativa L.) and their potential role in abiotic stress responses
Mouna Ghorbel A , Ikram Zribi B , Ahmad Alghamidi
A C , Khalil Mseddi D and Faiçal Brini B *
A
B
C
D
Abstract
Superoxide dismutase (SOD) enzymes form the first line of plant protection against reactive oxygen species (ROS) accumulation in cells. In this study, we recognised 14 AvSOD genes in the hexaploid oat (Avena sativa) genome, including nine AvCSDs, three AvFSDs, and two AvMSDs. Phylogenetic analysis revealed that AvSOD genes from oat and different other monocotyledonous and dicotyledonous plant species were clustered into two different groups based on the metallic binding domain. The predicted 3D protein structures revealed comparable conserved AvSOD protein configuration within groups. Interestingly, different hormonal and light-responsive cis-elements were identified in the promoters of AvSOD genes. Gene ontology annotation results validate the AvSODs role such as response to contrasting stress stimuli (ozone, light intensity, UV-B, metallic stress…), metal-ion binding activities, cellular oxidant detoxification activity, and different other cellular components. Expression profiling by real time quantitative PCR showed that 12 genes (AvCSD1, AvCSD2, AvCSD3, AvCSD4, AvCSD5, AvCSD6, AvCSD7, AvFSD1, AvFSD2, AvFSD3, AvMSD1, and AvMSD2) were strongly upregulated in response to different hormones (abscisic acid and salicylic acid) and/or abiotic stress (salinity, cold, and drought) treatments. Our data provides more knowledge of SOD genes in plants and information for advanced functional analyses of this antioxidant gene family in oat.
Keywords: abiotic stress, antioxidant enzymes, Avena sativa L., bioinformatic analysis, expression profile, phytohormones, ROSs, superoxide dismutase.
References
Aleem M, Aleem S, Sharif I, et al. (2022) Characterization of SOD and GPX gene families in the soybeans in response to drought and salinity stresses. Antioxidants 11(3), 460.
| Crossref | Google Scholar | PubMed |
Aury J-M, Jaillon O, Duret L, et al. (2006) Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444, 171-178.
| Crossref | Google Scholar | PubMed |
Bai J, Yan W, Wang Y, et al. (2018) Screening oat genotypes for tolerance to salinity and alkalinity. Frontiers in Plant Science 9, 1302.
| Crossref | Google Scholar | PubMed |
Bailey JA, Yavor AM, Massa HF, et al. (2001) Segmental duplications: organization and impact within the current human genome project assembly. Genome Research 11, 1005-1017.
| Crossref | Google Scholar | PubMed |
Bailey TL, Boden M, Buske FA, et al. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Research 37, W202-W208.
| Crossref | Google Scholar | PubMed |
Bustin SA, Benes V, Garson JA, et al. (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55(4), 611-622.
| Crossref | Google Scholar | PubMed |
Butt MS, Tahir-Nadeem M, Khan MKI, et al. (2008) Oat: unique among the cereals. European Journal of Nutrition 47, 68-79.
| Crossref | Google Scholar |
Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biology 4(1), 10.
| Crossref | Google Scholar |
Case AJ (2017) On the origin of superoxide dismutase: an evolutionary perspective of superoxide-mediated redox signaling. Antioxidants 6(4), 82.
| Crossref | Google Scholar |
Chao J, Li Z, Sun Y, et al. (2021) MG2C: a user-friendly online tool for drawing genetic maps. Molecular Horticulture 1, 16.
| Crossref | Google Scholar |
Chen C, Chen H, Zhang Y, et al. (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Molecular Plant 13(8), 1194-1202.
| Crossref | Google Scholar | PubMed |
Dehury B, Sarma K, Sarmah R, et al. (2013) In silico analyses of superoxide dismutases (SODs) of rice (Oryza sativa L.). Journal of Plant Biochemistry and Biotechnology 22, 150-156.
| Crossref | Google Scholar |
Dupont CL, Neupane K, Shearer J, Palenik B (2008) Diversity, function and evolution of genes coding for putative Ni-containing superoxide dismutases. Environmental Microbiology 10(7), 1831-1843.
| Crossref | Google Scholar | PubMed |
Dupont CL, Buck KN, Palenik B, Barbeau K (2010) Nickel utilization in phytoplankton assemblages from contrasting oceanic regimes. Deep Sea Research Part I: Oceanographic Research Papers 57(4), 553-566.
| Crossref | Google Scholar |
Feng X, Lai Z, Lin Y, et al. (2015) Genome-wide identification and characterization of the superoxide dismutase gene family in Musa acuminata cv. Tianbaojiao (AAA group). BMC Genomics 16, 823.
| Crossref | Google Scholar |
Feng K, Yu J, Cheng Y, et al. (2016) The SOD gene family in tomato: identification, phylogenetic relationships, and expression patterns. Frontiers in Plant Science 7, 1279.
| Crossref | Google Scholar | PubMed |
Filiz E, Tombuloğlu H (2015) Genome-wide distribution of superoxide dismutase (SOD) gene families in Sorghum bicolor. Turkish Journal of Biology 39, 49-59.
| Crossref | Google Scholar |
Fisher CL, Cabelli DE, Tainer JA, et al. (1994) The role of arginine 143 in the electrostatics and mechanism of Cu, Zn superoxide dismutase: computational and experimental evaluation by mutational analysis. Proteins: Structure, Function, and Bioinformatics 19(1), 24-34.
| Crossref | Google Scholar |
Franssen SU, Gu J, Bergmann N, et al. (2011) Transcriptomic resilience to global warming in the seagrass Zostera marina, a marine foundation species. Proceedings of the National Academy of Sciences 108(48), 19276-19281.
| Crossref | Google Scholar |
Garg VK, Avashthi H, Tiwari A, et al. (2016) MFPPI – multi FASTA protparam interface. Bioinformation 12(2), 74-77.
| Crossref | Google Scholar | PubMed |
Gechev TS, Van Breusegem F, Stone JM, et al. (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28(11), 1091-1101.
| Crossref | Google Scholar | PubMed |
Geng A, Wang X, Wu L, et al. (2018) Silicon improves growth and alleviates oxidative stress in rice seedlings (Oryza sativa L.) by strengthening antioxidant defense and enhancing protein metabolism under arsanilic acid exposure. Ecotoxicology and Environmental Safety 158, 266-273.
| Crossref | Google Scholar | PubMed |
Geourjon C, Deleage G (1995) SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments. Bioinformatics 11(6), 681-684.
| Crossref | Google Scholar |
Ghorbel M, Zribi I, Chihaoui M, Alghamidi A, Mseddi K, Brini F (2023) Genome-wide investigation and expression analysis of the catalase gene family in oat plants (Avena sativa L.). Plants 12(21), 3694.
| Crossref | Google Scholar | PubMed |
Goyal M, Kaur N (2018) Low temperature induced oxidative stress tolerance in oats (Avena sativa L.) genotypes. Indian Journal of Plant Physiology 23, 316-324.
| Crossref | Google Scholar |
Guan Q, Liao X, He M, et al. (2017) Tolerance analysis of chloroplast OsCu/Zn-SOD overexpressing rice under NaCl and NaHCO3 stress. PLoS ONE 12(10), e0186052.
| Crossref | Google Scholar | PubMed |
Han L-M, Hua W-P, Cao X-Y, et al. (2020) Genome-wide identification and expression analysis of the superoxide dismutase (SOD) gene family in Salvia miltiorrhiza. Gene 742, 144603.
| Crossref | Google Scholar | PubMed |
Haskirli H, Yilmaz O, Ozgur R, et al. (2021) Melatonin mitigates UV-B stress via regulating oxidative stress response, cellular redox and alternative electron sinks in Arabidopsis thaliana. Phytochemistry 182, 112592.
| Crossref | Google Scholar | PubMed |
Huo C, He L, Yu T, Ji X, Li R, Zhu S, Zhang F, Xie H, Liu W (2022) The superoxide dismutase gene family in Nicotiana tabacum: genome-wide identification, characterization, expression profiling and functional analysis in response to heavy metal stress. Frontiers in Plant Sciences 13, 904105.
| Crossref | Google Scholar |
Jaillon O, Aury J-M, Brunet F, et al. (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431, 946-957.
| Crossref | Google Scholar | PubMed |
Janská A, Hodek J, Svoboda P, Zámečník J, Prášil IT, Vlasáková E, Milella L, Ovesná J (2013) The choice of reference gene set for assessing gene expression in barley (Hordeum vulgare L.) under low temperature and drought stress. Molecular Genetics and Genomics 288(11), 639-649.
| Crossref | Google Scholar |
Jiang W, Yang L, He Y, et al. (2019) Genome-wide identification and transcriptional expression analysis of superoxide dismutase (SOD) family in wheat (Triticum aestivum). PeerJ 7, e8062.
| Crossref | Google Scholar | PubMed |
Jin H-D, Zheng C-Y, Hua B, Yu C-L, Li K-Y, Yu W-W (2022) Rooting anatomy and physiological enzyme activity of Torreya grandis cuttings. Acta Agriculturae Zhejiangensis 34(9), 1955-1966.
| Google Scholar |
Kamal N, Tsardakas Renhuldt N, Bentzer J, et al. (2022) The mosaic oat genome gives insights into a uniquely healthy cereal crop. Nature 606, 113-119.
| Crossref | Google Scholar | PubMed |
Khan WU, Khan LU, Chen D, Chen F (2023) Comparative analyses of superoxide dismutase (SOD) gene family and expression profiling under multiple abiotic stresses in water lilies. Horticulturae 9(7), 781.
| Crossref | Google Scholar |
Kliebenstein DJ, Monde R-A, Last RL (1998) Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiology 118(2), 637-650.
| Crossref | Google Scholar | PubMed |
Kurotani A, Tokmakov AA, Sato K-I, Stefanov VE, Yamada Y, Sakurai T (2019) Localization-specific distributions of protein pI in human proteome are governed by local pH and membrane charge. BMC Molecular and Cell Biology 20, 36.
| Crossref | Google Scholar |
Lescot M, Déhais P, Thijs G, et al. (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research 30(1), 325-327.
| Crossref | Google Scholar | PubMed |
Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Research 40(D1), D302-D305.
| Crossref | Google Scholar | PubMed |
Li J, Zhang Z, Vang S, Yu J, Wong GK-S, Wang J (2009) Correlation between Ka/Ks and Ks is related to substitution model and evolutionary lineage. Journal of Molecular Evolution 68, 414-423.
| Crossref | Google Scholar | PubMed |
Liu L, Gallagher J, Arevalo ED, et al. (2021) Enhancing grain-yield-related traits by CRISPR–Cas9 promoter editing of maize CLE genes. Nature Plants 7, 287-294.
| Crossref | Google Scholar | PubMed |
Lu S, Wang J, Chitsaz F, et al. (2020) CDD/SPARCLE: the conserved domain database in 2020. Nucleic Acids Research 48(D1), D265-D268.
| Crossref | Google Scholar | PubMed |
Matés JM (2000) Effects of antioxidant enzymes in the molecular control of reactive oxygen species toxicology. Toxicology 153(1–3), 83-104.
| Crossref | Google Scholar | PubMed |
Nath K, Kumar S, Poudyal RS, Yang YN, Timilsina R, Park YS, Nath J, Chauhan PS, Pant B, Lee C-H (2014) Developmental stage-dependent differential gene expression of superoxide dismutase isoenzymes and their localization and physical interaction network in rice (Oryza sativa L.). Genes and Genomics 36, 45-55.
| Crossref | Google Scholar |
Negi NP, Shrivastava DC, Sharma V, Sarin NB (2015) Overexpression of CuZnSOD from Arachis hypogaea alleviates salinity and drought stress in tobacco. Plant Cell Reports 34, 1109-1126.
| Crossref | Google Scholar | PubMed |
Nekrutenko A, Makova KD, Li W-H (2002) The KA/KS ratio test for assessing the protein-coding potential of genomic regions: an empirical and simulation study. Genome Research 12(1), 198-202.
| Crossref | Google Scholar | PubMed |
Omasits U, Ahrens CH, Müller S, Wollscheid B (2014) Protter: interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics 30(6), 884-886.
| Crossref | Google Scholar | PubMed |
Paysan-Lafosse T, Blum M, Chuguransky S, et al. (2023) InterPro in 2022. Nucleic Acids Research 51(D1), D418-D427.
| Crossref | Google Scholar | PubMed |
Pilon M, Ravet K, Tapken W (2011) The biogenesis and physiological function of chloroplast superoxide dismutases. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1807(8), 989-998.
| Crossref | Google Scholar | PubMed |
Potter SC, Luciani A, Eddy SR, et al. (2018) HMMER web server: 2018 update. Nucleic Acids Research 46(W1), W200-W204.
| Crossref | Google Scholar | PubMed |
Prates LL, Yu P (2017) Recent research on inherent molecular structure, physiochemical properties, and bio-functions of food and feed-type Avena sativa oats and processing-induced changes revealed with molecular microspectroscopic techniques. Applied Spectroscopy Reviews 52, 850-867.
| Crossref | Google Scholar |
Qiao X, Li Q, Yin H, et al. (2019) Gene duplication and evolution in recurring polyploidization–diploidization cycles in plants. Genome Biology 20, 38.
| Crossref | Google Scholar |
Rafique MU, Nahid N, Azeem F, et al. (2023) Genome wide analysis for the identification and characterization of superoxide-dismutase gene family in Rosa chinensis ascertains the role of salinity-responsive RcMSD1 protein and its interaction with peroxyl radical. Plant Stress 10, 100218.
| Crossref | Google Scholar |
Ramsey J, Ramsey TS (2014) Ecological studies of polyploidy in the 100 years following its discovery. Philosophical Transactions of the Royal Society B: Biological Sciences 369, 20130352.
| Crossref | Google Scholar |
Razali N, Mat Junit S, Ariffin A, et al. (2015) Polyphenols from the extract and fraction of T. indica seeds protected HepG2 cells against oxidative stress. BMC Complementary and Alternative Medicine 15, 438.
| Crossref | Google Scholar |
Sarkar O, Li Y, Anand-Srivastava MB (2017a) Nitric oxide attenuates overexpression of Giα proteins in vascular smooth muscle cells from SHR: role of ROS and ROS-mediated signaling. PLoS ONE 12, e0179301.
| Crossref | Google Scholar |
Sarkar T, Mogili T, Sivaprasad V (2017b) Improvement of abiotic stress adaptive traits in mulberry (Morus spp.): an update on biotechnological interventions. 3 Biotech 7(3), 214.
| Google Scholar |
Silver N, Best S, Jiang J, Thein SL (2006) Selection of housekeeping genes for gene expression studies in human reticulocytes using real-time PCR. BMC Molecular Biology 7, 33.
| Crossref | Google Scholar | PubMed |
Song J, Zeng L, Chen R, Wang Y, Zhou Y (2018) In silico identification and expression analysis of superoxide dismutase (SOD) gene family in Medicago truncatula. 3Biotech 8, 348.
| Crossref | Google Scholar |
Su W, Raza A, Gao A, et al. (2021) Genome-wide analysis and expression profile of superoxide dismutase (SOD) gene family in rapeseed (Brassica napus L.) under different hormones and abiotic stress conditions. Antioxidants 10(8), 1182.
| Crossref | Google Scholar | PubMed |
Sunkar R, Kapoor A, Zhu J-K (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. The Plant Cell 18(8), 2051-2065.
| Crossref | Google Scholar | PubMed |
Tajti J, Pál M, Janda T (2021) Validation of reference genes for studying different abiotic stresses in oat (Avena sativa L.) by RT-qPCR. Plants 10, 1272.
| Crossref | Google Scholar |
Teufel F, Almagro Armenteros JJ, Johansen AR, et al. (2022) SignalP 6.0 predicts all five types of signal peptides using protein language models. Nature Biotechnology 40, 1023-1025.
| Crossref | Google Scholar | PubMed |
Törönen P, Holm L (2022) PANNZER—a practical tool for protein function prediction. Protein Science 31(1), 118-128.
| Crossref | Google Scholar | PubMed |
Tounsi S, Jemli S, Feki K, et al. (2023) Superoxide dismutase (SOD) family in durum wheat: promising candidates for improving crop resilience. Protoplasma 260(1), 145-158.
| Crossref | Google Scholar |
Tyagi S, Sharma S, Taneja M, et al. (2017) Superoxide dismutases in bread wheat (Triticum aestivum L.): comprehensive characterization and expression analysis during development and, biotic and abiotic stresses. Agri Gene 6, 1-13.
| Crossref | Google Scholar |
Verma D, Lakhanpal N, Singh K (2019) Genome-wide identification and characterization of abiotic-stress responsive SOD (superoxide dismutase) gene family in Brassica juncea and B. rapa. BMC Genomics 20, 227.
| Crossref | Google Scholar |
Wang B, Song FB (2006) Response and adaptability of Oat to saline-alkali stress. Ecol Environ 15, 625.
| Google Scholar |
Wang N-J, Lee C-C, Cheng C-S, et al. (2012) Construction and analysis of a plant non-specific lipid transfer protein database (nsLTPDB). BMC Genomics 13 S9.
| Crossref | Google Scholar |
Wang W, Xia M, Chen J, et al. (2016) Data set for phylogenetic tree and RAMPAGE Ramachandran plot analysis of SODs in Gossypium raimondii and G. arboreum. Data in Brief 9, 345-348.
| Crossref | Google Scholar | PubMed |
Wang J, Wang Y, Gao C, et al. (2017a) PPero, a computational model for plant PTS1 type peroxisomal protein prediction. PLoS ONE 12, e0168912.
| Crossref | Google Scholar |
Wang W, Zhang X, Deng F, et al. (2017b) Genome-wide characterization and expression analyses of superoxide dismutase (SOD) genes in Gossypium hirsutum. BMC Genomics 18, 376.
| Crossref | Google Scholar |
Wang Y, Deng C, Ai P, Cui XA, Zhang Z (2021) ALM1, encoding a Fe-superoxide dismutase, is critical for rice chloroplast biogenesis and drought stress response. The Crop Journal 9(5), 1018-1029.
| Crossref | Google Scholar |
Wang J, Song Y, Wang Z, et al. (2024) RNA sequencing analysis and verification of paeonia ostii ‘Fengdan’ CuZn superoxide dismutase (PoSOD) genes in root development. Plants 13, 421.
| Crossref | Google Scholar | PubMed |
Wolfe KH, Shields DC (1997) Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387, 708-713.
| Crossref | Google Scholar | PubMed |
Xiao ZF, Sheng PJ, Xu YF, Peng Y, Jiang R, Zheng BJ, Li F (2022) Changes in relevant oxidase activities and carbohydrates during the rooting process of micro-cuttage of Cinnamomum camphora ct. Linalool. Journal of Yibin University 22, 62-66.
| Google Scholar |
Yadav S, Gill SS, Passricha N, et al. (2019) Genome-wide analysis and transcriptional expression pattern-assessment of superoxide dismutase (SOD) in rice and Arabidopsis under abiotic stresses. Plant Gene 17, 100165.
| Crossref | Google Scholar |
Yan J-J, Zhang L, Wang R-Q, et al. (2016) The sequence characteristics and expression models reveal superoxide dismutase involved in cold response and fruiting body development in Volvariella volvacea. International Journal of Molecular Sciences 17, 34.
| Crossref | Google Scholar |
Yang J, Roy A, Zhang Y (2012) BioLiP: a semi-manually curated database for biologically relevant ligand–protein interactions. Nucleic Acids Research 41(D1), D1096-D1103.
| Crossref | Google Scholar | PubMed |
Yang H, Zhang Q, Zhong S, et al. (2023) Genome-wide identification of superoxide dismutase and expression in response to fruit development and biological stress in Akebia trifoliata: a bioinformatics study. Antioxidants 12(3), 726.
| Crossref | Google Scholar | PubMed |
Yates AD, Allen J, Amode RM, et al. (2022) Ensembl Genomes 2022: an expanding genome resource for non-vertebrates. Nucleic Acids Research 50(D1), D996-D1003.
| Crossref | Google Scholar | PubMed |
Zhang W, Fan J, Tan Q, Zhao M, Zhou T, Cao F (2017) The effects of exogenous hormones on rooting process and the activities of key enzymes of Malus hupehensis stem cuttings. PLoS ONE 12, e0172320.
| Crossref | Google Scholar | PubMed |
Zhang S, Li C, Ren H, et al. (2020) BAK1 mediates light intensity to phosphorylate and activate catalases to regulate plant growth and development. International Journal of Molecular Sciences 21(4), 1437.
| Crossref | Google Scholar | PubMed |
Zhang X, Zhang L, Chen Y, et al. (2021a) Genome-wide identification of the SOD gene family and expression analysis under drought and salt stress in barley. Plant Growth Regul 94, 49-60.
| Crossref | Google Scholar |
Zhang R-R, Wang Y-H, Li T, et al. (2021b) Effects of simulated drought stress on carotenoid contents and expression of related genes in carrot taproots. Protoplasma 258, 379-390.
| Crossref | Google Scholar |
Zhang J, Pu D, Yang C, Wang P, Zhao Y, Zhou Q (2025) Differences in salinity tolerance in Avena sativa and Avena nuda. Agronomy 15(3), 594.
| Crossref | Google Scholar |
Zhou X, Wang M, Yang L, Wang W, Zhang Y, Liu L, Chai J, Liu H, Zhao G (2024) Comparative physiological and transcriptomic analyses of oat (Avena sativa) seedlings under salt stress reveal salt tolerance mechanisms. Plants 13, 2238.
| Crossref | Google Scholar | PubMed |
