Identification and Expression Profiling of Two Saudi Arabia Catalase Genes from Wheat and Barley in Response to Abiotic and Hormonal Stresses

Antioxidants - Tập 11 Số 11 - Trang 2208
Mouna Ghorbel1,2, Malek Besbes Hlila1, Najla Haddaji1, Nouha Bouali1, Faïçal Brini2
1Biology Department, Faculty of Science, University of Hail, Ha'il 2440, Saudi Arabia
2Laboratory of Biotechnology and Plant Improvement, Center of Biotechnology of Sfax, Sfax 3018, Tunisia

Tóm tắt

Catalase is a crucial enzyme in antioxidant defense systems protecting eukaryotes from oxidative stress. These proteins are present in almost all living organisms and play important roles in controlling plant responses to biotic and abiotic stresses by catalyzing the decomposition of H2O2. Despite their importance, little is known about their expression in the majority of monocotyledonous species. Here, we isolated and characterized two novel catalase genes from Triticum turgidum and Hordeum vulgare, designated as TtCAT1 and HvCAT1, respectively. Phylogenetic analysis revealed that TtCAT1 and HvCAT1 presented 492 aa and shared an important identity with other catalase proteins belonging to subfamily 1. Using bioinformatic analysis, we predicted the 3D structure models of TtCAT1 and HvCAT1. Interestingly, analysis showed that the novel catalases harbor a peroxisomal targeting signal (PTS1) located at their C-terminus portion, as shown for other catalase proteins. In addition, this motif is responsible for the in silico peroxisomal localization of both proteins. Finally, RT-qPCR analysis showed that TtCAT1 and HvCAT1 are highly expressed in leaves in normal conditions but faintly in roots. Moreover, both genes are upregulated after the application of different stresses such as salt, osmotic, cold, heavy metal, and hormonal stresses. The positive responses of TtCAT1 and HvCAT1 to the various stimuli suggested that these proteins can help to protect both species against environmental stresses.

Từ khóa


Tài liệu tham khảo

Gechev, T., and Petrov, V. (2020). Reactive Oxygen Species and Abiotic Stress in Plants. Int. J. Mol. Sci., 21.

Choudhury, 2017, Reactive oxygen species, abiotic stress and stress combination, Plant J., 90, 856, 10.1111/tpj.13299

Apel, 2004, Reactive oxygen species: Metabolism, oxidative stress, and signal transduction, Annu. Rev. Plant Biol., 55, 373, 10.1146/annurev.arplant.55.031903.141701

Mittler, 2004, Reactive oxygen gene network of plants, Trends Plant Sci., 9, 490, 10.1016/j.tplants.2004.08.009

He, 2018, Epigallocatechin gallate is the most effective catechin against antioxidant stress via hydrogen peroxide and radical scavenging activity, Med. Sci. Monit., 24, 8198, 10.12659/MSM.911175

Su, Y., Guo, J., Ling, H., Chen, S., Wang, S., Xu, L., and Allan, A.C. (2014). Isolation of a Novel Peroxisomal Catalase Gene from Sugarcane, Which Is Responsive to Biotic and Abiotic Stresses. PLoS ONE, 9.

Feki, 2015, Multiple abiotic stress tolerance of the transformants yeast cells and the transgenic Arabidopsis plants expressing a novel durum wheat catalase, Plant Physiol. Biochem., 97, 420, 10.1016/j.plaphy.2015.10.034

Tounsi, 2019, Localization and expression analysis of a novel catalase from Triticum monococcum TmCAT1 involved in response to different environmental stresses, Plant Physiol. Biochem., 139, 366, 10.1016/j.plaphy.2019.03.039

Wang, J., Wang, Y., Gao, C., Jiang, L., and Guo, D. (2017). PPero, a computational model for plant PTS1 type peroxisomal protein prediction. PLoS ONE, 12.

Wang, W., Cheng, Y., Chen, D., Liu, D., Hu, M., Jie Dong, J., Zhang, X., Song, L., and Shen, F. (2019). The Catalase Gene Family in Cotton: Genome-Wide Characterization and Bioinformatics Analysis. Cells, 8.

Hu, 2012, Catalase and estradiol inhibit mitochondrial protein S-glutathionylation, Mol. Cell. Biochem., 367, 51, 10.1007/s11010-012-1318-7

Iwamoto, 2000, Differential diurnal expression of rice catalase genes: The 5′-flanking region of CatA is not sufficient for circadian control, Plant Sci., 151, 39, 10.1016/S0168-9452(99)00194-6

Zhang, Y., Zheng, L., Yun, L., Ji, L., Li, G., Ji, M., Shi, Y., and Zheng, X. (2022). Catalase (CAT) Gene Family in Wheat (Triticum aestivum L.): Evolution, Expression Pattern and Function Analysis. Int. J. Mol. Sci., 23.

Raza, A., Su, W., Gao, A., Mehmood, S., Hussain, M., Nie, W., Lv, Y., Zou, X., and Zhang, X. (2021). Catalase (CAT) Gene Family in Rapeseed (Brassica napus L.): Genome-Wide Analysis, Identification, and Expression Pattern in Response to Multiple Hormones and Abiotic Stress Conditions. Int. J. Mol. Sci., 22.

Md, 2020, Response of catalase to drought in barley (Hordeum vulgare L.) seedlings and its purification, Afr. J. Biotechnol., 19, 478, 10.5897/AJB2020.17169

Giri, 2017, Nano-encapsulation of dietary phytoconstituent capsaicin on emulsome: Evaluation of anticancer activity through the measurement of liver oxidative stress in rats, Anti-Cancer Agents Med. Chem., 17, 1669

Zimmermann, 2006, Senescence-specific regulation of catalases in Arabidopsis thaliana (L.) Heynh, Plant Cell Environ., 29, 1049, 10.1111/j.1365-3040.2005.01459.x

Du, 2008, Comprehensive functional analysis of the catalase gene family in Arabidopsis thaliana, J. Integr. Plant Biol., 50, 1318, 10.1111/j.1744-7909.2008.00741.x

Kumar, 2016, MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets, Mol. Biol. Evol., 33, 1870, 10.1093/molbev/msw054

Geourjon, 1995, SOPMA: Significant improvements in protein secondary structure prediction by consensus prediction from multiple alignements, CABIOS, 11, 681

Reynolds, 2018, EzMol: A web server wizard for the rapid visualisation and image production of protein and nucleic acid structures, J. Mol. Biol., 430, 2244, 10.1016/j.jmb.2018.01.013

Dimmer, 2012, The UniProt-GO Annotation database in 2011, Nucl. Acids Res., 40, 565, 10.1093/nar/gkr1048

Wilson, 2009, SUPERFAMILY—Sophisticated comparative genomics, data mining, visualization and phylogeny, Nucl. Acids Res., 37, D380, 10.1093/nar/gkn762

Kiefer, 2009, The SWISS-MODEL Repository and associated resources, Nucl. Acids Res., 37, D387, 10.1093/nar/gkn750

Yap, 2000, Calmodulin target database, J. Struct. Funct. Genom., 1, 8, 10.1023/A:1011320027914

Pandit, S.B., Bhadra, R., Gowri, V., Balaji, S., Anand, B., and Srinivasan, N. (2004). SUPFAM: A database of sequence superfamilies of protein domains. BMC Bioinform., 5.

Kopp, 2004, The SWISS-MODEL Repository of annotated three-dimensional protein structure homology models, Nucl. Acids Res., 32, 230, 10.1093/nar/gkh008

Yu, C.S., Cheng, C.W., Su, W.C., Chang, K.C., Huang, S.W., Hwang, J.K., and Lu, C.H. (2014). CELLO2GO: A Web Server for Protein subCELlular LOcalization Prediction with Functional Gene Ontology Annotation. PLoS ONE, 9.

Horton, 2007, WoLF PSORT: Protein localization predictor, Nucl. Acids Res., 35, W585, 10.1093/nar/gkm259

Chang, 2013, EuLoc: A web-server for accurately predict protein subcellular localization in eukaryotes by incorporating various features of sequence segmentsinto the general form of Chou’s PseAAC, J. Comput.-Aided Mol. Des., 27, 91, 10.1007/s10822-012-9628-0

Livak, 2001, Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method, Methods, 25, 402, 10.1006/meth.2001.1262

Sedmak, 1977, A rapid, sensitive, and versatile assay for protein using Coomassie brilliant blue G250, Anal. Biochem., 79, 544, 10.1016/0003-2697(77)90428-6

Ashraf, 2008, Relative membrane permeability and activities of some antioxidant enzymes as the key determinants of salt tolerance in canola (Brassica napus L.), Environ. Exp. Bot., 63, 266, 10.1016/j.envexpbot.2007.11.008

Hao, 2006, The role of salicylic acid and carrot embryogenic callus extracts in somatic embryogenesis of naked oat (Avena nuda), Plant Cell Tissue Organ Cult., 85, 109, 10.1007/s11240-005-9052-4

Frugoli, 1996, Catalase is encoded by a multigene family in Arabidopsis thaliana (L.) Heynh, Plant Physiol., 112, 327, 10.1104/pp.112.1.327

Anisimova, O.K., Shchennikova, A.V., Kochieva, E.Z., and Filyushin, M.A. (2021). Pathogenesis-RelatedGenes of PR1, PR2, PR4 and PR5 Families Are Involved in the Response to Fusarium Infection in Garlic (Allium sativum L.). Int. J. Mol. Sci., 22.

AlHudaib, K.A., Alanazi, N.A., Ghorbel, M., El-Ganainy, S.M., and Brini, F. (2022). Isolation and Characterization of a Novel Pathogenesis-Related Protein-1 Gene (AvPR-1) with Induced Expression in Oat (Avena sativa L.) during Abiotic and Hormonal Stresses. Plants, 11.

Chen, 2012, Expression of a cloned sweet potato catalase SPCAT1 alleviates ethephon-mediated leaf senescence and H2O2 elevation, J. Plant Physiol., 169, 86, 10.1016/j.jplph.2011.08.002

Ghorbel, M., Feki, K., Tounsi, S., Haddaji, N., Hanin, M., and Brini, F. (2022). The Activity of the Durum Wheat (Triticum durum L.) Catalase 1 (TdCAT1) Is Modulated by Calmodulin. Antioxidants, 11.

Purev, 2010, Isolation of a novel catalase (Cat1) gene from Panax ginseng and analysis of the response of this gene to various stresses, Plant Physiol. Biochem., 48, 451, 10.1016/j.plaphy.2010.02.005

Loewen, 2015, Unprecedented access of phenolic substrates to the heme active site of a catalase: Substrate binding and peroxidase-like reactivity of Bacillus pumilus catalase monitored by X-ray crystallography and EPR spectroscopy, Proteins Struct. Funct. Bioinform., 83, 853, 10.1002/prot.24777

Yang, 2002, Hydrogen peroxide homeostasis: Activation of plant catalase by calcium/calmodulin, Proc. Natl. Acad. Sci. USA, 99, 4097, 10.1073/pnas.052564899

Arsova, 2012, Current status of the plant phosphorylation site database PhosPhAt and its use as a resource for molecular plant physiology, Front. Plant Sci., 3, 132, 10.3389/fpls.2012.00132

Ghorbel, M., Feki, K., Tounsi, S., Bouali, N., Besbes, M., and Brini, F. (2022). The Putative Auto-Inhibitory Domain of Durum Wheat Catalase (TdCAT1) Positively Regulates Bacteria Cells in Response to Different Stress Conditions. Antioxidants, 11.

Willekens, 1994, Differential expression of catalase genes in Nicotiana plumbaginifolia (L.), Proc. Natl. Acad. Sci. USA, 91, 10450, 10.1073/pnas.91.22.10450

Mhamdi, 2010, Catalase function in plants: A focus on Arabidopsis mutants as stress-mimic models, J. Exp. Bot., 61, 4197, 10.1093/jxb/erq282

Joo, 2014, Rice CatA, CatB, and CatC are involved in environmental stress response, root growth, and photorespiration, respectively, J. Plant Biol., 57, 375, 10.1007/s12374-014-0383-8

Bouthiba, 2008, Varietal differences in the response of durum wheat (Triticum turgidum L. var. durum) to irrigation strategies in a semi-arid region of Algeria, Irrig. Sci., 26, 239, 10.1007/s00271-007-0089-5

Tyagi, 2021, Molecular characterization revealed the role of catalases under abiotic and arsenic stress in bread wheat (Triticum aestivum L.), J. Hazard. Mater., 403, 123585, 10.1016/j.jhazmat.2020.123585

Sooch, 2014, Recent insights into microbial catalases: Isolation, production and purification, Biotechnol. Adv., 32, 1429, 10.1016/j.biotechadv.2014.09.003

Oshima, 2008, Plant catalase is imported into peroxisomes by Pex5p but is distinct from typical PTS1 import, Plant. Cell Physiol., 49, 671, 10.1093/pcp/pcn038

Fujikawa, 2018, Effect of mutation of C-terminal and heme binding region of Arabidopsis catalaseon the import to peroxisomes, Biosci. Biotechnol. Biochem., 83, 322, 10.1080/09168451.2018.1530094

Kaur, 2011, Defining the plant peroxisomal proteome: From Arabidopsis to rice, Front. Plant Sci., 2, 103, 10.3389/fpls.2011.00103

Seth, 2018, A multiplex enzymatic machinery for cellular protein S-nitrosylation, Mol. Cell, 69, 451, 10.1016/j.molcel.2017.12.025

Chen, 2020, Transnitrosylation mediated by the non-canonical catalase ROG1 regulates nitric oxide signaling in plants, Dev. Cell, 53, 444, 10.1016/j.devcel.2020.03.020

Pande, 2022, Phytohormonal Regulation Through Protein S-Nitrosylation Under Stress, Front. Plant Sci., 13, 865542, 10.3389/fpls.2022.865542

Rodríguez-Ruiz, M., González-Gordo, S., Cañas, A., Campos, M.J., Paradela, A., Corpas, F.J., and Palma, J.M. (2019). Sweet Pepper (Capsicum annuum L.) Fruits Contain an Atypical Peroxisomal Catalase That Is Modulated by Reactive Oxygen and Nitrogen Species. Antioxydants, 8.