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Expression of HSP90, PR1, and AGO2a During the Defensive Response of Tomato Cultivars to Tomato Brown Rugose Fruit Virus
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Golbanoo Azizpour    , Ahmad Rohibakhsh , Davoud Koolivand * , Shahrokh Ghovvati |
| Department of Plant Protection, Faculty of Agriculture, University of Zanjan, Zanjan, Iran, , koolivand@znu.ac.ir |
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Abstract: (695 Views) |
Tomato brown rugose fruit virus (ToBRFV; Tobamovirus fructirugosum) is an emerging and highly destructive pathogen threatening tomato production worldwide. This study investigated the expression patterns of three key defense-related genes: HSP90, PR1, and AGO2a in two tomato cultivars exhibiting contrasting levels of tolerance to ToBRFV infection. Four-leaf–stage plants were mechanically inoculated with a verified viral isolate, and systemic leaf samples were collected at 7, 14, and 21 days post-inoculation (dpi). Total RNA was extracted, viral presence was confirmed using specific primers, and gene expression was quantified by real-time PCR. In the tolerant cultivar, all three genes were significantly upregulated following infection. HSP90 and PR1 displayed a sustained and consistent increase across all sampling times, while AGO2a showed a marked induction at 14 dpi, reaching levels significantly higher than those in the susceptible cultivar (P < 0.0001). These expression profiles indicate the activation of stable and effective defense pathways in the tolerant cultivar. By contrast, the susceptible cultivar exhibited minimal or even decreased expression of these genes, particularly PR1, suggesting ineffective induction of antiviral defenses. The coordinated upregulation of HSP90, PR1, and AGO2a in the tolerant cultivar highlights their complementary roles in disease mitigation: HSP90 likely stabilizes defense-related proteins, PR1 serves as a marker of salicylic acid–mediated signaling, and AGO2a contributes directly to viral suppression through RNA silencing. Overall, these findings underscore the importance of rapid and sustained activation of defense genes in conferring tolerance to ToBRFV and provide a molecular basis for breeding strategies, genetic improvement, and the identification of molecular markers for resistant tomato cultivars.
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| Keywords: disease resistance, heat shock protein (HSP90), disease susceptibility, gene silencing, PR genes, gene expression responses |
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Full-Text [PDF 735 kb]
(112 Downloads)
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Type of Study: Research |
Subject:
Microrganisms and Viruses
Received: 2025/09/21 | Accepted: 2025/10/23 | Published: 2025/10/28
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| References |
1. Alazem, M., & Lin, N. S. (2017). Antiviral roles of abscisic acid in plants. Frontiers in plant science, 8, 1760. doi:10.3389/fpls.2017.01760 [ DOI:10.3389/fpls.2017.01760] [ PMID] [ PMCID] 2. Amorim, L. L., da Fonseca Dos Santos, R., Neto, J. P. B., Guida-Santos, M., Crovella, S., & Benko-Iseppon, A. M. (2017). Transcription factors involved in plant resistance to pathogens. Current Protein & Peptide Science, 18(4), 335-351. doi:10.2174/1389203717666160619185308 [ DOI:10.2174/1389203717666160619185308] [ PMID] 3. Asadi Jaefari, S., Maleki, M., & Gholamnejad, J. (2022). The Effect of Salicylic Acid and Jasmonic Acid on Disease Symptoms and Defense Genes Expression in a Greenhouse Cucumber Infected with CMV. Genetic Engineering and Biosafety Journal, 10 (2), 206-224. doi: 20.1001.1.25885073.1400.10.2.7.9 4. Asghari, N., Koolivand, D., & Eini, O. 2020. Differential expression of HSP90 ,AGO1 and AGO4 genes in tomato infected by Cucumber mosaic virus. Crop Biotechnology, 9 (4), 31-42: doi: 10.30473/CB.2020.53550.1811 5. Bayer Vegetables. (2019). Tomato Brown Rugose Fruit Virus. Available at: https://www.vegetables.bayer.com/nz/en-nz/resources/growing-tips/cultivation-insights/tomato-brown-rugose-fruit-virus.html). 6. Breen, S., Williams, S. J., Outram, M., Kobe, B., & Solomon, P. S. (2017). Emerging insights into the functions of pathogenesis-related protein 1. Trends in plant science, 22(10), 871-879. doi: 10.1016/j.tplants.2017.06.013 [ DOI:10.1016/j.tplants.2017.06.013] [ PMID] [ PMCID] 7. Campos, M. D., Felix, M. D. R., Patanita, M., Materatski, P., Albuquerque, A., Ribeiro, J. A., & Varanda, C. (2022). Defense strategies: The role of transcription factors in tomato-pathogen interaction. Biology, 11(2), 235. doi: 10.3390/biology11020235 [ DOI:10.3390/biology11020235] [ PMID] [ PMCID] 8. Carbonell, A., & Daròs, J. A. (2017). Artificial microRNAs and synthetic trans‐acting small interfering RNAs interfere with viroid infection. Molecular Plant Pathology, 18(5), 746-753. doi: 10.1111/mpp.12529 [ DOI:10.1111/mpp.12529] [ PMID] [ PMCID] 9. Chen, Y. L., Lee, C. Y., Cheng, K. T., Chang, W. H., Huang, R. N., Nam, H. G., & Chen, Y. R. (2014). Quantitative peptidomics study reveals that a wound-induced peptide from PR-1 regulates immune signaling in tomato. The Plant Cell, 26(10), 4135-4148. doi: 10.1105/tpc.114.131185 [ DOI:10.1105/tpc.114.131185] [ PMID] [ PMCID] 10. Chen, Y. L., Lin, F. W., Cheng, K. T., Chang, C. H., Hung, S. C., Efferth, T., & Chen, Y. R. (2023). XCP1 cleaves Pathogenesis-related protein 1 into CAPE9 for systemic immunity in Arabidopsis. Nature Communications, 14(1), 4697. doi: 10.1038/s41467-023-40406-7 [ DOI:10.1038/s41467-023-40406-7] [ PMID] [ PMCID] 11. EPPO Global Database. (2025). Tobamovirus fructirugosum (TOBRFV). [Online]. (Available at: https://gd.eppo.int/taxon/TOBRFV/datasheet). 12. Esmaeilzadeh, F., & Koolivand, D. (2022a). First report of tomato brown rugose fruit virus infecting bell pepper in Iran. Journal of Plant Pathology, 104(2), 893-893. doi: 10.1007/s42161-022-01094-2 [ DOI:10.1007/s42161-022-01094-2] 13. Esmaeilzadeh, F., & Koolivand, D. (2022b). Occurrence of tomato brown rugose fruit virus in tomato in Iran. Journal of Plant Pathology, 104(1), 457-457. doi: 10.1007/s42161-021-01009-7 [ DOI:10.1007/s42161-021-01009-7] 14. Esmaeilzadeh, F., Santosa, A. I., Çelik, A., & Koolivand, D. (2023). Revealing an Iranian Isolate of Tomato Brown Rugose Fruit Virus: Complete Genome Analysis and Mechanical Transmission. Microorganisms, 11(10), 2434. doi: 10.3390/microorganisms11102434 [ DOI:10.3390/microorganisms11102434] [ PMID] [ PMCID] 15. Gamir, J., Darwiche, R., Van't Hof, P., Choudhary, V., Stumpe, M., Schneiter, R., & Mauch, F. (2017). The sterol‐binding activity of PATHOGENESIS‐RELATED PROTEIN 1 reveals the mode of action of an antimicrobial protein. The Plant Journal, 89(3), 502-509. doi: 10.1111/tpj.13398 [ DOI:10.1111/tpj.13398] [ PMID] 16. Ghorbani, A., Rostami, M., Seifi, S., & Izadpanah, K. (2021). First report of Tomato brown rugose fruit virus in greenhouse tomato in Iran. New Disease Reports, 44(2), e12040. doi: 10.1002/ndr2.12040 [ DOI:10.1002/ndr2.12040] 17. Ghorbel, M., Brini, F., Sharma, A., & Landi, M. (2021). Role of jasmonic acid in plants: the molecular point of view. Plant Cell Reports, 40(8), 1471-1494. doi: 10.1007/s00299-021-02687-4 [ DOI:10.1007/s00299-021-02687-4] [ PMID] 18. Li, Y., Li, S., Bi, D., Cheng, Y. T., Li, X., & Zhang, Y. (2010). SRFR1 negatively regulates plant NB-LRR resistance protein accumulation to prevent autoimmunity. PLoS Pathogens, 6(9), e1001111. doi: 10.1371/journal.ppat.1001111 [ DOI:10.1371/journal.ppat.1001111] [ PMID] [ PMCID] 19. Ludman, M., Szalai, G., Janda, T., & Fátyol, K. (2023). Hierarchical contribution of Argonaute proteins to antiviral protection. Journal of Experimental Botany, 74(21), 6760-6772. doi: 10.1093/jxb/erad327 [ DOI:10.1093/jxb/erad327] [ PMID] [ PMCID] 20. Luria, N., Smith, E., Reingold, V., Bekelman, I., Lapidot, M., Levin, I., ... & Dombrovsky, A. (2017). A new Israeli Tobamovirus isolate infects tomato plants harboring Tm-22 resistance genes. PloS one, 12(1), e0170429. doi: 10.1371/journal.pone.0170429 [ DOI:10.1371/journal.pone.0170429] [ PMID] [ PMCID] 21. Panno, S., Caruso, A. G., & Davino, S. (2019). First report of tomato brown rugose fruit virus on tomato crops in Italy. Plant Disease, 103(6), 1443-1443. doi: 10.1094/PDIS-12-18-2254-PDN [ DOI:10.1094/PDIS-12-18-2254-PDN] 22. PlantwisePlus Knowledge Bank. (2023). Tomato brown rugose fruit virus. [Online]. (Available at: https://plantwiseplusknowledgebank.org/doi/full/10.1079/pwkb.species.88757522). 23. Pumplin, N., & Voinnet, O. (2013). RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nature Reviews Microbiology, 11(11), 745-760. doi:10.1038/nrmicro3120 [ DOI:10.1038/nrmicro3120] [ PMID] 24. Ramakers, C., Ruijter, J. M., Deprez, R. H. L., & Moorman, A. F. (2003). Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience letters, 339(1), 62-66. doi: 10.1016/S0304-3940(02)01423-4 [ DOI:10.1016/S0304-3940(02)01423-4] [ PMID] [ PMCID] 25. Salem, N., Mansour, A., Ciuffo, M., Falk, B. W., & Turina, M. (2016). A new tobamovirus infecting tomato crops in Jordan. Archives of virology, 161(2), 503-506. doi: 10.1007/s00705-015-2677-7 [ DOI:10.1007/s00705-015-2677-7] [ PMID] 26. Van Loon, L. C., Rep, M., & Pieterse, C. M. (2006). Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol., 44(1), 135-162. doi: 10.1146/annurev.phyto.44.070505.143425 [ DOI:10.1146/annurev.phyto.44.070505.143425] [ PMID] [ PMCID] 27. Wang, K., Zhang, X., Goatley, M., & Ervin, E. (2014). Heat shock proteins in relation to heat stress tolerance of creeping bentgrass at different N levels. PLoS One, 9(7), e102914. doi:10.1371/journal.pone.0102914.g001 [ DOI:10.1371/journal.pone.0102914.g001] |
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Azizpour G, Rohibakhsh A, Koolivand D, Ghovvati S. Expression of HSP90, PR1, and AGO2a During the Defensive Response of Tomato Cultivars to Tomato Brown Rugose Fruit Virus. gebsj 2025; 14 (1) :36-47 URL: http://gebsj.ir/article-1-528-en.html
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