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Evaluation of Superoxide Dismutase Isoforms Activity and Defense System-Related Proteins’ Expression in Ascochyta Blight-Infected Chickpea Using 2D Electrophoresis Technique

  • PLANT PHYSIOLOGY
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Abstract

Fungal diseases are crucial factors in reducing chickpea production. Ascochyta Blight is caused by the necrotrophic fungi Didymella rabiei and is one of the most destructive diseases in most world areas. Therefore, a completely randomized factorial design with five replications was applied to evaluate the effects of Ascochyta Blight disease fungi on the chickpea plant. The chlorophyll index, the activities of superoxide dismutase isoforms, and evolutionary analyses were performed to get further insights. Also, 2D electrophoresis of chickpea leaf proteins, gene ontology, and protein-protein interactions analysis was performed. The results did not show any significant effect of A. rabiei infection on the wet weight of chickpea seedlings. Chlorophyll index levels significantly decreased with A. rabiei infection in both chickpea lines. Electrophoretic analysis of superoxide dismutase on 8% polyacrylamide gel revealed three isoforms. The activities of superoxide dismutase isoforms significantly increased with A. rabiei disease. Identification of proteins was performed according to their isoelectric points and approximate molecular weights. Leaf proteome analysis of chickpea lines showed that the expression of eight reproducible spots changed significantly under A. rabiei disease condition. Candidate proteins were components of defense and regulation systems. High expression of Dual specificity protein, Peptide methionine sulfoxide reductase B2, and chloroplastic phosphatase 1B (the proteins involved in the defense system) reveals their essential functions under A. rabiei infection. Increased activities of superoxide dismutase enzymes and proteins involved in the defense system can reduce A. rabiei infection effects on chickpea seedlings.

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Notes

  1. b-ZIP Transcription factor TGACGTCA Motif-Binding Prote-in.

REFERENCES

  1. Bagheban, F., Mohraminajad, S., Lotfi, R., Bandehhagh, A., and Karbalaei, H., Study of catalase activity and photosynthetic efficiency of maize lines under Fusarium contamination (Fusarium verticillioides), J. Appl. Res. Plant Prot., 2019, vol. 8, pp. 13–23.https://doi.org/10.1002/elps.1150080203

    Article  Google Scholar 

  2. Blum, H., Beier, H., and Gross, H.J., Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels, Electrophoresis, 1987, vol. 8, pp. 93–99. https://doi.org/10.1002/elps.1150080203

    Article  CAS  Google Scholar 

  3. Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 1976, vol. 72, pp. 248–254. https://doi.org/10.1006/abio.1976.9999

    Article  CAS  PubMed  Google Scholar 

  4. Chen, Z., Silva, H., and Klessig, D.F., Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid, Science, 1993, vol. 262, pp. 1883–1886. https://doi.org/10.1126/science.8266079

    Article  CAS  PubMed  Google Scholar 

  5. Chen, W., Coyne, C., Peever, T., and Muehlbauer, F., Characterization of chickpea differentials for pathogenicity assay of ascochyta blight and identification of chickpea accessions resistant to Didymella rabiei, Plant Pathol., 2004, vol. 53, pp. 759–769. https://doi.org/10.1111/j.1365-3059.2004.01103.x

    Article  Google Scholar 

  6. Chen, Y.-Y., Li, M.-Y., Wu, X.-J., Huang, Y., Ma, J., and Xiong, A.-S., Genome-wide analysis of basic helix–loop–helix family transcription factors and their role in responses to abiotic stress in carrot, Mol. Breed., 2015, vol. 35, pp. 1–12. https://doi.org/10.1007/s11032-015-0319-0

    Article  CAS  Google Scholar 

  7. Chivasa, S., Tomé, D.F., Hamilton, J.M., and Slabas, A.R., Proteomic analysis of extracellular ATP-regulated proteins identifies ATP synthase beta-subunit as a novel plant cell death regulator, Mol. Cell Proteomics, 2011, vol. 10, p. M110.003905. https://doi.org/10.1074/mcp.M110.003905

  8. Damerval, C., Zivy, M., and Granier, F., Two-Dimensional Electrophoresis in Plant Biology, Laboratoire de génétique des systèmes végétaux, 1988.

  9. Dangl, J.L., Dietrich, R.A., and Richberg, M.H., Death don’t have no mercy: cell death programs in plant-microbe interactions, Plant Cell, 1996, vol. 8, p. 1793. https://doi.org/10.1105%2Ftpc.8.10.1793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Danon, A., Rotari, V.I., Gordon, A., Mailhac, N., and Gallois, P., Ultraviolet-C overexposure induces programmed cell death in Arabidopsis, which is mediated by caspase-like activities and which can be suppressed by caspase inhibitors, p35 and Defender against apoptotic death, J. Biol. Chem., 2004, vol. 279, pp. 779–787. https://doi.org/10.1074/jbc.M304468200

    Article  CAS  PubMed  Google Scholar 

  11. Ding, C., Gao, J., Zhang, S., Jiang, N., Su, D., Huang, X., and Zhang, Z., The basic/helix-loop-helix transcription factor family gene RcbHLH112 is a susceptibility gene in gray mould resistance of rose (Rosa chinensis), Int. J. Mol. Sci., 2023, vol. 24. https://doi.org/10.3390/ijms242216305

  12. Farahani, S., Maleki, M., Ford, R., Mehrabi, R., Kanouni, H., Kema, G.H.J., Naji, A.M., and Talebi, R., Genome-wide association mapping for isolate-specific resistance to Ascochyta rabiei in chickpea (Cicer arietinum L.), Physiol. Mol. Plant Pathol., 2022, vol. 121, p. 101883. https://doi.org/10.1016/j.pmpp.2022.101883

    Article  CAS  Google Scholar 

  13. Foresto, E., Carezzano, M.E., Giordano, W., and Bogino, P., Ascochyta blight in chickpea: an update, J. Fungi (Basel), 2023, vol. 9. https://doi.org/10.3390/jof9020203

  14. Ge, Y., Cai, Y.M., Bonneau, L., Rotari, V., Danon, A., McKenzie, E.A., McLellan, H., Mach, L., and Gallois, P., Inhibition of cathepsin B by caspase-3 inhibitors blocks programmed cell death in Arabidopsis, Cell Death Differ., 20163, vol. 23, pp. 1493–1501. https://doi.org/10.1038/cdd.2016.34

  15. Gilroy, E.M., Hein, I., Van Der Hoorn, R., Boevink, P.C., Venter, E., McLellan, H., Kaffarnik, F., Hrubikova, K., Shaw, J., Holeva, M., et al., Involvement of cathepsin B in the plant disease resistance hypersensitive response, Plant J., 2007, vol. 52, pp. 1–13. https://doi.org/10.1111/j.1365-313X.2007.03226.x

    Article  CAS  PubMed  Google Scholar 

  16. Gupta, S., Dong, Y., Dijkwel, P.P., Mueller-Roeber, B., and Gechev, T.S., Genome-wide analysis of ROS antioxidant genes in resurrection species suggest an involvement of distinct ROS detoxification systems during desiccation, Int. J. Mol. Sci., 20193, vol. 20, p. 3101. https://doi.org/10.3390/ijms20123101

  17. Heang, D. and Sassa, H., Antagonistic actions of HLH/bHLH proteins are involved in grain length and weight in rice, PLoS One, 2012, vol. 7, p. e31325. https://doi.org/10.1371/journal.pone.0031325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Houssin, C., Eynard, N., Shechter, E., and Ghazi, A.J.B.e.B.A.-B., Effect of osmotic pressure on membrane energy-linked functions in Escherichia coli, Biochim. Biophys. Acta, Bioenerg., 1991, vol. 1056, pp. 76–84. https://doi.org/10.1016/S0005-2728(05)80075-1

    Article  CAS  Google Scholar 

  19. Hu, X., Yang, L., Ren, M., Liu, L., Fu, J., and Cui, H., TGA factors promote plant root growth by modulating redox homeostasis or response, J. Integr. Plant Biol., 2022, vol. 64, pp. 1543–1559. https://doi.org/10.1111/jipb.13310

    Article  CAS  PubMed  Google Scholar 

  20. Hu, D., Guo, Q., Zhang, Y., and Chen, F., Maize methionine sulfoxide reductase genes ZmMSRA2 and ZmMSRA5.1 involved in the tolerance to osmotic or salinity stress in Arabidopsis and maize, Plant Mol. Biol. Rep., 2023, vol. 41, pp. 118–133. https://doi.org/10.1007/s11105-022-01354-6

    Article  CAS  Google Scholar 

  21. Ishidoh, K.-i., Kinoshita, H., Ihara, F., and Nihira, T., Efficient and versatile transformation systems in entomopathogenic fungus Lecanicillium species, Curr. Genet., 2014, vol. 60, pp. 99–108. https://doi.org/10.1007/s00294-013-0399-5

    Article  CAS  PubMed  Google Scholar 

  22. Jia, Z.-C., Das, D., Zhang, Y., Fernie, A.R., Liu, Y.-G., Chen, M., and Zhang, J., Plant serine/arginine-rich proteins: versatile players in RNA processing, Planta, 2023, vol. 257, p. 109. https://doi.org/10.1007/s00425-023-04132-0

    Article  CAS  PubMed  Google Scholar 

  23. Jiang, N., Wang, L., Lan, Y., Liu, H., Zhang, X., He, W., Wu, M., Yan, H., and Xiang, Y., Genome-wide identification of the Carya illinoinensis bZIP transcription factor and the potential function of S1-bZIPs in abiotic stresses, Tree Genet. Genomes, 2023, vol. 19, p. 47. https://doi.org/10.1007/s11295-023-01622-w

    Article  CAS  Google Scholar 

  24. Jukanti, A.K., Gaur, P.M., Gowda, C., and Chibbar, R.N., Nutritional quality and health benefits of chickpea (Cicer arietinum L.): a review, Br. J. Nutr., 2012, vol. 108, pp. S11–S26. https://doi.org/10.1017/S0007114512000797

    Article  CAS  PubMed  Google Scholar 

  25. Kasote, D.M., Katyare, S.S., Hegde, M.V., and Bae, H., Significance of antioxidant potential of plants and its relevance to therapeutic applications, Int. J. Biol. Sci., 2015, vol. 11, pp. 982–991. https://doi.org/10.7150/ijbs.12096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Kaur, K., Grewal, S.K., Singh, S., Rani, U., and Bhardwaj, R.D., Timing and intensity of upregulated defensive enzymes is a key factor determining resistance in chickpea to Ascochyta rabiei, Physiol. Mol. Plant Pathol., 2021, vol. 114, p. 101645. https://doi.org/10.1016/j.pmpp.2021.101645

    Article  CAS  Google Scholar 

  27. Kavousi, H.R., Marashi, H., and Bagheri, A., Expression of phenylpropanoid pathway genes in chickpea defense against race 3 of Ascochyta rabiei, Plant Pathol. J., 2009, vol. 8.

  28. Khaledi, N., Taheri, P., and Falahati-Rastegar, M., Evaluation of resistance and the role of some defense responses in wheat cultivars to Fusarium head blight, J. Plant Prot. Res., 2017, vol. 57. https://doi.org/10.1515/jppr-2017-0054

  29. Kosová, K., Vítámvás, P., Urban, M.O., and Prášil, I.T., Plant proteome responses to salinity stress–comparison of glycophytes and halophytes, Funct. Plant Biol., 2013, vol. 40, pp. 775–786. https://doi.org/10.1071/FP12375

    Article  CAS  Google Scholar 

  30. Kufel, J., Diachenko, N., and Golisz, A., Alternative splicing as a key player in the fine-tuning of the immunity response in Arabidopsis, Mol. Plant Pathol., 2022, vol. 23, pp. 1226–1238. https://doi.org/10.1111/mpp.13228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Kumar, R., Tiwari, R.K., Jeevalatha, A., Siddappa, S., Shah, M.A., Sharma, S., Sagar, V., Kumar, M., and Chakrabarti, S.K., Potato apical leaf curl disease: current status and perspectives on a disease caused by tomato leaf curl New Delhi virus, J. Plant Dis. Prot., 2021, vol. 128, pp. 897–911. https://doi.org/10.1007/s41348-021-00463-w

    Article  Google Scholar 

  32. Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K., MEGA X: molecular evolutionary genetics analysis across computing platforms, Mol. Biol. Evol., 2018, vol. 35, pp. 1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Ladizinsky, G. and Adler, A., The origin of chickpea Cicer arietinum L., Euphytica, 1976, vol. 25, pp. 211–217. https://doi.org/10.1007/BF00041547

    Article  Google Scholar 

  34. Laugier, E., Tarrago, L., Vieira Dos Santos, C., Eymery, F., Havaux, M., and Rey, P., Arabidopsis thaliana plastidial methionine sulfoxide reductases B, MSRBs, account for most leaf peptide MSR activity and are essential for growth under environmental constraints through a role in the preservation of photosystem antennae, Plant J., 2010, vol. 61, pp. 271–282. https://doi.org/10.1111/j.1365-313X.2009.04053.x

    Article  CAS  PubMed  Google Scholar 

  35. Liu, W., Zhao, C., Liu, L., Huang, D., Ma, C., Li, R., and Huang, L., Genome-wide identification of the TGA gene family in kiwifruit (Actinidia chinensis spp.) and revealing its roles in response to Pseudomonas syringae pv. actinidiae (Psa) infection, Int. J. Biol. Macromol., 2022, vol. 222, pp. 101–113. https://doi.org/10.1016/j.ijbiomac.2022.09.154

    Article  CAS  PubMed  Google Scholar 

  36. Luo, Z., Hu, X., Wu, Z., Liu, X., Wu, C., and Zeng, Q., Identification and expression profiling of TGA transcription factor genes in sugarcane reveals the roles in response to Sporisorium scitamineum infection, Agriculture, 2022, vol. 12. https://doi.org/10.3390/agriculture12101644

  37. Makonya, G.M., Ogola, J.B.O., Gabier, H., Rafudeen, M.S., Muasya, A.M., Crespo, O., Maseko, S., Valentine, A.J., Ottosen, C.-O., Rosenqvist, E., and Chimphango, S.B.M., Proteome changes and associated physiological roles in chickpea (Cicer arietinum) tolerance to heat stress under field conditions, Funct. Plant Biol., 2022, vol. 49, pp. 13–24.

    Article  CAS  Google Scholar 

  38. Mi, H., Ebert, D., Muruganujan, A., Mills, C., Albou, L.-P., Mushayamaha, T., and Thomas, P.D., PANTHER version 16: a revised family classification, tree-based classification tool, enhancer regions and extensive API, Nucleic Acids Res., 2021, vol. 49, pp. D394–D403. https://doi.org/10.1093/nar/gkaa1106

    Article  CAS  PubMed  Google Scholar 

  39. Moharramnejad, S. and Valizadeh, M., A key response of grain yield and superoxide dismutase in maize (Zea mays L.) to water deficit stress, J. Plant Physiol. Breed., 2019, vol. 9, pp. 77–84.

    Google Scholar 

  40. Mohsenzadeh Golfazani, M., Taghvaei, M.M., Samizadeh Lahiji, H., Ashery, S., and Raza, A., Investigation of proteins’ interaction network and the expression pattern of genes involved in the ABA biogenesis and antioxidant system under methanol spray in drought-stressed rapeseed, 3 Biotech, 2022, vol. 12, p. 217. https://doi.org/10.1007/s13205-022-03290-4

  41. Mostafaie, A., Theoretical and Practical Guide Protein Electrophoresis in Gel, Press yadavaran, 2003.

  42. Nalçacı, N., Kafadar, F.N., Özkan, A., Turan, A., Başbuğa, S., Anay, A., Mart, D., Öğut, E., Sarpkaya, K., Atik, O., and Can, C., Epiphytotics of chickpea Ascochyta blight in Turkey as influenced by climatic factors, J. Plant Dis. Prot., 2021, vol. 128, pp. 1121–1128. https://doi.org/10.1007/s41348-021-00458-7

    Article  CAS  Google Scholar 

  43. Negash Tufa, E., Distribution of Ascochyta Blight (Didymella rabiei) and Evaluation of Chickpea (Cicer rietinum L.) Varieties to the Disease in East Shewa, Central Ethiopia, Haramaya University, 2021.

    Google Scholar 

  44. Nizam, S., Singh, K., and Verma, P.K., Expression of the fluorescent proteins DsRed and EGFP to visualize early events of colonization of the chickpea blight fungus Ascochyta rabiei, Curr. Genet., 2010, vol. 56, pp. 391–399. https://doi.org/10.1007/s00294-010-0305-3

    Article  CAS  PubMed  Google Scholar 

  45. Noshi, M., Mori, D., Tanabe, N., Maruta, T., and Shigeoka, S., Arabidopsis clade IV TGA transcription factors, TGA10 and TGA9, are involved in ROS-mediated responses to bacterial PAMP flg22, Plant Sci., 2016, vol. 252, pp. 12–21. https://doi.org/10.1016/j.plantsci.2016.06.019

    Article  CAS  PubMed  Google Scholar 

  46. Pandey, A.K. and Basandrai, A.K., Will Macrophomina phaseolina spread in legumes due to climate change? A critical review of current knowledge, J. Plant Dis. Prot., 2021, vol. 128, pp. 9–18. https://doi.org/10.1007/s41348-020-00374-2

    Article  Google Scholar 

  47. Pasandideh Arjmand, M., Samizadeh Lahiji, H., Mohsenzadeh Golfazani, M., and Biglouei, M.H., Evaluation of protein’s interaction and the regulatory network of some drought-responsive genes in Canola under drought and re-watering conditions, Physiol. Mol. Biol. Plants, 2023, vol. 29, pp. 1085–1102. https://doi.org/10.1007/s12298-023-01345-1

    Article  CAS  PubMed  Google Scholar 

  48. Rossignol, M., Peltier, J.B., Mock, H.P., Matros, A., Maldonado, A.M., and Jorrín, J.V., Plant proteome analysis: a 2004–2006 update, Proteomics, 2006, vol. 6, pp. 5529–5548. https://doi.org/10.1002/pmic.200600260

    Article  CAS  PubMed  Google Scholar 

  49. Sanjog, T.T., Feroz, K., and Suman, P.S.K., Cathepsin B-like protease from chili pepper revealed by “in silico” approach, Plant Omics, 2016. https://doi.org/10.3316/informit.027795688541121

  50. Shah, J.A., Iqbal, A., Mahmood, M.T., Aslam, M., Abbas, M., and Ahmad, I., Screening of elite chickpea germplasm against Ascochyta blight under controlled conditions, Pak. J. Agric. Res., 2021, vol. 34, pp. 774–780. https://doi.org/10.17582/journal.pjar/2021/34.4.774.780

    Article  Google Scholar 

  51. Singh, R., Kumar, K., Purayannur, S., Chen, W., and Verma, P.K., Ascochyta rabiei: a threat to global chickpea production, Mol. Plant Pathol., 2022, vol. 23, pp. 1241–1261. https://doi.org/10.1111/mpp.13235

    Article  PubMed  PubMed Central  Google Scholar 

  52. Sowders, J.M. and Tanaka, K., A histochemical reporter system to study extracellular ATP response in plants, Front. Plant Sci., 2023, vol. 14, p. 1183335. https://doi.org/10.3389/fpls.2023.1183335

    Article  PubMed  PubMed Central  Google Scholar 

  53. Su, W., Raza, A., Gao, A., Jia, Z., Zhang, Y., Hussain, M.A., Mehmood, S.S., Cheng, Y., Lv, Y., and Zou, X., 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, 2021, vol. 10, p. 1182. https://doi.org/10.3390/antiox10081182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Szklarczyk, D., Gable, A.L., Lyon, D., Junge, A., Wyder, S., Huerta-Cepas, J., Simonovic, M., Doncheva, N.T., Morris, J.H., and Bork, P., STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets, Nucleic Acids Res., 2019, vol. 47, pp. D607–D613. https://doi.org/10.1093/nar/gky1131

    Article  CAS  PubMed  Google Scholar 

  55. Taghvaei, M.M., Lahiji, H.S., and Golfazani, M.M., Evaluation of expression changes, proteins interaction network, and microRNAs targeting catalase and superoxide dismutase genes under cold stress in rapeseed (Brassica napus L.), OCL, 2022, vol, 29.https://doi.org/10.1051/ocl/2021051

  56. Thakur, R., Sharma, S., Devi, R., Sirari, A., Tiwari, R.K., Lal, M.K., and Kumar, R., Exploring the molecular basis of resistance to Botrytis cinerea in chickpea genotypes through biochemical and morphological markers, PeerJ, 2023, vol. 11, p. e15560. https://doi.org/10.7717/peerj.15560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Thompson, J.D., Higgins, D.G., and Gibson, T.J., CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice, Nucleic Acids Res., 1994, vol. 22, pp. 4673–4680. https://doi.org/10.1093/nar/22.22.4673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Tivoli, B. and Banniza, S., Comparison of the epidemiology of ascochyta blights on grain legumes, in Ascochyta Blights of Grain Legumes, Springer, 2007, pp. 59–76. https://doi.org/10.1007/978-1-4020-6065-6_7

  59. Vilela, B., Pagès, M., and Lumbreras, V., Regulation of MAPK signaling and cell death by MAPK phosphatase MKP2, Plant Signal. Behav., 2010, vol. 5, pp. 1497–1500. https://doi.org/10.4161/psb.5.11.13645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Wang, F., Lin, R., Feng, J., Qiu, D., Chen, W., and Xu, S., Wheat bHLH transcription factor gene, TabHLH060, enhances susceptibility of transgenic Arabidopsis thaliana to Pseudomonas syringae, Physiol. Mol. Plant Pathol., 2015a, vol. 90, pp. 123–130. https://doi.org/10.1016/j.pmpp.2015.04.007

    Article  CAS  Google Scholar 

  61. Wang, J., Hu, Z., Zhao, T., Yang, Y., Chen, T., Yang, M., Yu, W., and Zhang, B., Genome-wide analysis of bHLH transcription factor and involvement in the infection by yellow leaf curl virus in tomato (Solanum lycopersicum), BMC Genomics, 2015b, vol. 16, p. 39. https://doi.org/10.1186/s12864-015-1249-2

    Article  PubMed  PubMed Central  Google Scholar 

  62. Wang, G., Fu, X., Zhao, W., Zhang, M., and Chen, F., Ectopic expression of maize plastidic methionine sulfoxide reductase ZmMSRB1 enhances salinity stress tolerance in Arabidopsis thaliana, Plant Mol. Biol. Rep., 2022, vol. 40, pp. 284–295. https://doi.org/10.1007/s11105-021-01320-8

    Article  CAS  Google Scholar 

  63. Wen, J., Jiang, F., Liu, M., Zhou, R., Sun, M., Shi, X., Zhu, Z., and Wu, Z., Identification and expression analysis of cathepsin B-like protease 2 genes in tomato at abiotic stresses especially at high temperature, Sci. Hortic., 2021, vol. 277, p. 109799. https://doi.org/10.1016/j.scienta.2020.109799

    Article  CAS  Google Scholar 

  64. Xin, J., Li, C., Ning, K., Qin, Y., Shang, J.-X., and Sun, Y., AtPFA-DSP3, an atypical dual-specificity protein tyrosine phosphatase, affects salt stress response by modulating MPK3 and MPK6 activity, Plant, Cell Environ., 2021, vol. 44, pp. 1534–1548. https://doi.org/10.1111/pce.14002

    Article  CAS  PubMed  Google Scholar 

  65. Xu, R., Zhou, J., Zheng, E., Yang, Y., Li, D., Chen, Y., Yan, C., Chen, J., and Wang, X., Systemic acquired resistance plays a major role in bacterial blight resistance in a progeny of somatic hybrids of cultivated rice (Oryza sativa L.) and wild rice (Oryza meyeriana L.), J. Plant Dis. Prot., 2023, vol. 128, pp. 1023–1040. https://doi.org/10.1007/s41348-021-00457-8

    Article  CAS  Google Scholar 

  66. Xu, S., Zhang, Z., Jing, B., Gannon, P., Ding, J., Xu, F., Li, X., and Zhang, Y., Transportin-SR is required for proper splicing of resistance genes and plant immunity, PLoS Genet., 2011, vol. 7, p. e1002159. https://doi.org/10.1371/journal.pgen.1002159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Yasuda, M., Ishikawa, A., Jikumaru, Y., Seki, M., Umezawa, T., Asami, T., Maruyama-Nakashita, A., Kudo, T., Shinozaki, K., and Yoshida, S., Antagonistic interaction between systemic acquired resistance and the abscisic acid–mediated abiotic stress response in Arabidopsis, Plant Cell, 2008, vol. 20, pp. 1678–1692. https://doi.org/10.1105/tpc.107.054296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Zhu, J., Ding, P., Li, Q., Gao, Y., Chen, F., and Xia, G., Molecular characterization and expression profile of methionine sulfoxide reductase gene family in maize (Zea mays) under abiotic stresses, Gene, 2021, vol. 562, pp. 159–168. https://doi.org/10.1016/j.gene.2015.02.066

    Article  CAS  Google Scholar 

  69. Zuo, Z.-F., Lee, H.-Y., and Kang, H.-G., Basic helix-loop-helix transcription factors: regulators for plant growth development and abiotic stress responses, Int. J. Mol. Sci., 2023, vol. 24. https://doi.org/10.3390/ijms24021419

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This work was supported by ongoing institutional funding. No additional grants to carry out or direct this particular research were obtained.

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Authors and Affiliations

  1. Department of Agricultural Biotechnology, Faculty of Agricultural Sciences, University of Guilan, Rasht, Iran

    Y. Shafiei, M. Mohsenzadeh Golfazani, M. M. Taghvaei & H. Samizadeh Lahiji

  2. Medical Biology Research Center, Kermanshah University of Medical Sciences, Kermanshah, Iran

    A. Mostafaie

  3. College of Agriculture, Fujian Agriculture and Forestry University (FAFU), 350002, Fuzhou, Fujian, China

    A. Raza

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M.M.G, planned and designed the study, drafted the manuscript, and participated in all the experiments. Y.S. and M.M.T. participated in all experiments and data analysis. H.S.L. and A.M. and A.R. participated in study design and supervised the study. All authors participated in revising and finalizing the manuscript.

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Correspondence to M. Mohsenzadeh Golfazani.

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Shafiei, Y., Golfazani, M.M., Mostafaie, A. et al. Evaluation of Superoxide Dismutase Isoforms Activity and Defense System-Related Proteins’ Expression in Ascochyta Blight-Infected Chickpea Using 2D Electrophoresis Technique. Biol Bull Russ Acad Sci (2024). https://doi.org/10.1134/S1062359023603336

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