ارزیابی واکنش مورفولوژیکی و مولکولی چند رقم توتون در مقابل باکتری عامل آتشک توتون Pseudomonas syringae pv. tabaci

نوع مقاله : مقاله پژوهشی

نویسندگان

1 گروه بیمارشی شناسی گیاهی، دانشگده کشاورزی، دانشگاه آزاد اسلامی واحد ورامین-پیشوا، ورامین، تهران، ایران

2 گروه گیاهپزشکی، دانشگده علوم زراعی، دانشگاه علوم کشاورزی و منابع طبیعی ساری، ساری، ایران

3 گروه گیاهپزشکی، دانشکده علوم زراعی، دانشگاه علوم کشاورزی و منابع طبیعی ساری، ساری، ایران

چکیده

هدف: یکی از بزرگترین چالش‌های جامعه بشری مسئله امنیت و سلامت غذای است. مدیریت شیمیایی آفات و بیماری‌های گیاهی منتج به افزایش میزان آلوده کننده‌های زیست محیطی شده است. لذا یافتن روشی جایگزین جهت مقابله با بیماری‌ها امری ضروری به نظر می‌رسد. در این راستا ژن‌های مسئول مقاومت در گیاهان نسبت به عوامل بیماری‌زا ، منابع ژنتیکی با ارزشی هستند که می‌توان از آن‌ها در جهت مدیریت بیماری‌های گیاهی استفاده کرد. در این تحقیق با هدف آنالیز بیان چند ژن کنترل کننده مقاومت و حساسیت در ارقام با درجات مختلف حساسیت در برابر باکتری Pseudomonas syringae pv.tabaci (Pst) عامل سوختگی وحشی توتون استفاده شد. 
مواد و روش‌ها: در ابتدا شش رقم توتون تهیه و کشت شدند و پس از هفت هفته، گیاهچه‌ها به باکتری Pst آلوده شدند سپس بر اساس میزان قطر بافت نکروزه و آزمون میزان رشد و تکثیر  باکتری انجام گرفت در نتیجه، ارقام مقاوم و حساس شناسایی شده و برای مراحل بعدی انتخاب و کشت شدند. جهت تعیین الگوی بیان ژنهای دخیل در مقاومت از برگ های گیاهچه های هفت هفته ای  در ساعات مختلف پس از تلقیح (صفر، 12، 24، 48، 72) نمونه برداری شده و RNA کل از آن ها استخراج شد. سپس از روی نمونه های RNA رشته مکمل DNA (cDNA) سنتز شد پروفایل ژن‌های WRKY، PAL، PR1، PR2 و PR5 مورد بررسی با تکنیک  qPCR انجام گردید.
نتایج: بر اساس نتایج قطر بافت نکروزه و آزمون میزان رشد و تکثیر باکتری، رقم Basma به عنوان رقم مقاوم و رقم White Burley به عنوان رقم حساس شناخته شدند. بررسی فعالیت بیان ژن‌های مسئول بروز مقاومت WRKY، PAL، PR1، PR2 و PR5 در رقم مقاوم Basma نسبت به رقم حساس White Burley پس از مایه زنی به طور قابل ملاحظه ای افزایش یافت.
نتیجه‌گیری: یافته‌های این مطالعه نشان داد که این ژن‌ها نقش مهمی در پاسخ‌های دفاعی گیاه ایفا می‌کنند و در مکانیسم‌های مقاومت و حساسیت گیاه توتون در تعامل با باکتری Pst نقش دارند و می‌توانند به‌عنوان اهدافی مناسب برای تولید گیاهان تراریخته مقاوم به بیماری‌ها مورد استفاده قرار گیرند. با این حال نیازمند انجام مطالعات تکمیلی و دقیق‌تر است.

کلیدواژه‌ها


عنوان مقاله [English]

Evaluation of the morphological and molecular response of several tobacco cultivars to the tobacco fire blight pathogen Pseudomonas syringae pv. tabaci

نویسندگان [English]

  • Amin Zoroofian 1
  • Milad Habibi Daronkolaei 2
  • Valiollah Babaeizad 3
1 Department of Plant Pathology, Faculty of Agriculture, Islamic Azad University OF Tehran Varamin Pishva Branch, Varamin, Iran
2 Department of Plant Protection, Agronomy Science, Sari Agricultural Sciences and Natural Resources University, Sari, Iran
3 Department of Plant Protection, Sari Agricultural Sciences and Natural Resources University, Sari. Iran
چکیده [English]

Objective
One of the most significant challenges facing human society today is food safety and security. The chemical management of plant pests and diseases has led to an increase in environmental pollutants. Therefore, it is essential to find alternative methods for combating these diseases. In this context, genes that confer resistance to pathogens represent valuable genetic resources for managing plant diseases. This study aimed to analyze the expression of several genes that regulate resistance and sensitivity in cultivars with varying degrees of susceptibility to the bacterium Pseudomonas syringae pv. tabaci (Pst), the causative agent of wild tobacco blight.
Materials and methods
Initially, six tobacco cultivars were prepared and cultivated. After seven weeks, the seedlings were inoculated with Pst bacteria. Based on the diameter of the necrotic tissue and the assessment of bacterial growth and proliferation, resistant and susceptible cultivars were identified and selected for subsequent stages of cultivation. To determine the expression patterns of genes involved in resistance, leaves from the seven-week-old seedlings were sampled at various time points post-inoculation (0, 12, 24, 48, and 72 hours), and total RNA was extracted from these samples. Subsequently, complementary DNA (cDNA) was synthesized from the RNA. The expression profiles of the WRKY, PAL, PR1, PR2, and PR5 genes were analyzed using the qPCR technique.
Results
Based on the results of the necrotic tissue diameter and bacterial growth and proliferation tests, the Basma cultivar was identified as resistant, while the White Burley cultivar was classified as susceptible. The examination of gene expression activity for resistance-related genes, including WRKY, PAL, PR1, PR2, and PR5, revealed a significant increase in expression in the resistant Basma cultivar compared to the susceptible White Burley cultivar following inoculation.
Conclusions
The findings of this study indicate that certain genes play a crucial role in plant defense responses. These genes are involved in the mechanisms of resistance and sensitivity of tobacco plants in their interactions with Pst bacteria. They genes may serve as promising targets for the development of transgenic plants that exhibit resistance to diseases. However, further detailed and complementary studies are necessary.

کلیدواژه‌ها [English]

  • Chemical management
  • Resistance Cultivar
  • Resistance genes
  • Sensitive cultivar
  • Transgenic plants
Abbruscato, P., Nepusz, T., Mizzi, L., Del Corvo, M., Morandini, P., Fumasoni, I., Michel, C., Paccanaro, A., Guiderdoni, E., Schaffrath, U., & MOREL, J.B. (2012). OsWRKY22, a monocot WRKY gene, plays a role in the resistance response to blast. Molecular plant pathology, 13(8), 828-841. https://doi.org/10.1111/j.1364-3703.2012.00795.x
Ali, S., Ganai, B.A., Kamili, A.N., Bhat, A.A., Mir, Z.A., Bhat, J.A., Tyagi, A., Islam, S.T., Mushtaq, M., Yadav, P., & Rawat, S. (2018). Pathogenesis-related proteins and peptides as promising tools for engineering plants with multiple stress tolerance. Microbiological research, 212, 29-37. https://doi.org/10.1016/j.micres.2018.04.008
Ali, S., Mir, Z.A., Bhat, J.A., Tyagi, A., Chandrashekar, N., Yadav, P., Rawat, S., Sultana, M., & Grover, A. (2018). Isolation and characterization of systemic acquired resistance marker gene PR1 and its promoter from Brassica juncea. 3 Biotech, 8(1), 10. https://doi.org/10.1007/s13205-017-1027-8
Arabi, E., Jawhar, M., Al-daoude, A., Al-Shehadah, E., Shoaib, A., & Imad, M. (2019). Differential expression of defense-related genes in susceptible versus resistant barley genotypes challenged with Pyrenophora teres. Mycopath, 15(2).
Basavand, E., & Khodaygan, P. (2020). Common water-plantain, a new host of Pseudomonas viridiflava in rice fields in Iran. Journal of Plant Pathology, 102(3), 913-913. https://doi.org/10.1007/s42161-020-00491-9
Batchvarova, R., Nikolaeva, V., Slavov, S., Bossolova, S., Valkov, V., Atanassova, S., Guelemerov, S., Atanassov, A., & Anzai, H. (1998). Transgenic tobacco cultivars resistant to Pseudomonas syringae pv. tabaci. Theoretical and Applied Genetics, 97(5), 986-989. https://doi.org/10.1007/s001220050981
Bundalovic-Torma, C., Lonjon, F., Desveaux, D., & Guttman, D. S. (2022). Diversity, evolution, and function of Pseudomonas syringae effectoromes. Annual Review of Phytopathology, 60(1), 211-236. https://doi.org/10.1146/annurev-phyto-021621-121935
Cech, R., Zaller, J. G., Lyssimachou, A., Clausing, P., Hertoge, K., & Linhart, C. (2023). Pesticide drift mitigation measures appear to reduce contamination of non-agricultural areas, but hazards to humans and the environment remain. Science of the Total Environment, 854, 158814. https://doi.org/10.1016/j.scitotenv.2022.158814
Chen, X., Li, C., Wang, H., & Guo, Z. (2019). WRKY transcription factors: evolution, binding, and action. Phytopathology research, 1(1), 1-15. https://doi.org/10.1186/s42483-019-0022-x
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. https://doi.org/10.1105/tpc.114.131185
Cheng, D. D., Zhang, Z. S., Sun, X. B., Zhao, M., Sun, G. Y., & Chow, W. S. (2016). Photoinhibition and photoinhibition-like damage to the photosynthetic apparatus in tobacco leaves induced by pseudomonas syringae pv. Tabaci under light and dark conditions. BMC Plant Biology, 16(1), 29. https://doi.org/10.1186/s12870-016-0723-6
Cheng, D.D., Liu, M.J., Sun, X.B., Zhao, M., Chow, W.S., Sun, G.Y., Zhang, Z.S., & Hu, Y.B. (2016). Light suppresses bacterial population through the accumulation of hydrogen peroxide in tobacco leaves infected with Pseudomonas syringae pv. tabaci. Frontiers in Plant Science, 7, 512. https://doi.org/10.3389/fpls.2016.00512
Chien, P. S., Nam, H. G., & Chen, Y. R. (2015). A salt-regulated peptide derived from the CAP superfamily protein negatively regulates salt-stress tolerance in Arabidopsis. Journal of experimental botany, 66(17), 5301-5313. https://doi.org/10.1093/jxb/erv263
Cutt, J. R., Harpster, M. H., Dixon, D. C., Carr, J. P., Dunsmuir, P., & Klessig, D. F. (1989). Disease response to tobacco mosaic virus in transgenic tobacco plants that constitutively express the pathogenesis-related PR1b gene. Virology, 173(1), 89-97. https://doi.org/10.1016/0042-6822(89)90224-9
Dixon, E., Kennedy, B., Pearce, R., & Pfeufer, E. (2018). Occurrence of frogeye leaf spot, caused by Cercospora nicotianae, on greenhouse tobacco transplants in Kentucky. Plant Disease, 102(5), 1036. https://doi.org/10.1094/PDIS-10-17-1548-PDN
Dixon, R. A., Achnine, L., Kota, P., Liu, C. J., Reddy, M. S., & Wang, L. (2002). The phenylpropanoid pathway and plant defence—a genomics perspective. Molecular plant pathology, 3(5), 371-390. https://doi.org/10.1046/j.1364-3703.2002.00131.x
Dolatabadi, B., Ranjbar, G., Tohidfar, M., & Dehestani, A. (2014). Genetic transformation of Tomato with three pathogenesis-related protein genes for increased resistance to Fusarium oxysporum f. sp. lycopersici. Journal of Plant Molecular Breeding, 2(1), 1-11. https://doi.org/10.22058/jpmb.2014.8424
Drakhshan, A., SALARI, M., BABAEIZAD, V., PANJEHKEH, N., & Taheri, A. (2021). Study of biochemical and molecular changes of iranian rice cultivars in interaction with bacterial pathogen Xanthomonas oryzae pv. oryzae causes leaf blight disease.
Du, L., & Chen, Z. (2000). Identification of genes encoding receptor‐like protein kinases as possible targets of pathogen‐and salicylic acid‐induced WRKY DNA‐binding proteins in Arabidopsis. The Plant Journal, 24(6), 837-847. https://doi.org/10.1111/j.1365-313X.2000.00923.x
Duan, L., Liu, H., Li, X., Xiao, J., & Wang, S. (2014). Multiple phytohormones and phytoalexins are involved in disease resistance to Magnaporthe oryzae invaded from roots in rice. Physiologia plantarum, 152(3), 486-500. https://doi.org/10.1111/ppl.12192
Edwards, K., Cramer, C. L., Bolwell, G. P., Dixon, R. A., Schuch, W., & Lamb, C. J. (1985). Rapid transient induction of phenylalanine ammonia-lyase mRNA in elicitor-treated bean cells. Proceedings of the National Academy of Sciences, 82(20), 6731-6735. https://doi.org/10.1073/pnas.82.20.6731
Finkina, E., N. Melnikova, D., V. Bogdanov, I., & V. Ovchinnikova, T. (2017). Plant pathogenesis-related proteins PR-10 and PR-14 as components of innate immunity system and ubiquitous allergens. Current Medicinal Chemistry, 24(17), 1772-1787. https://doi.org/10.2174/0929867323666161026154111
Freeman, B., & Beattie, G. (2008). An overview of plant defenses against pathogens and herbivores.
Gao, L., Wang, S., Li, X. Y., Wei, X. J., Zhang, Y. J., Wang, H. Y., & Liu, D. Q. (2015). Expression and functional analysis of a pathogenesis-related protein 1 gene, TcLr19PR1, involved in wheat resistance against leaf rust fungus. Plant Molecular Biology Reporter, 33(4), 797-805. https://doi.org/10.1007/s11105-014-0790-5
Guo, Z., Xie, H., Wang, H., Huang, Y., Chen, Q., Xiang, L., Yu, Z. and Yang, X. (2020). Leaf spot caused by Didymella segeticola on tobacco in China. Plant Disease, 104(5), 1559. https://doi.org/10.1094/PDIS-11-19-2398-PDN
Gutiérrez-Barranquero, J. A., Cazorla, F. M., & De Vicente, A. (2019). Pseudomonas syringae pv. syringae associated with mango trees, a particular pathogen within the “hodgepodge” of the Pseudomonas syringae complex. Frontiers in Plant Science, 10, 570. https://doi.org/10.3389/fpls.2019.00570
He, J., Liu, Y., Yuan, D., Duan, M., Liu, Y., Shen, Z., Yang, C., Qiu, Z., Liu, D., Wen, P., & Huang, J. (2020). An R2R3 MYB transcription factor confers brown planthopper resistance by regulating the phenylalanine ammonia-lyase pathway in rice. Proceedings of the National Academy of Sciences, 117(1), 271-277. https://doi.org/10.1073/pnas.1902771116
He, L., Ding, L., Zhang, P., Li, B., Mu, W., & Liu, F. (2021). Impact of the equilibrium relationship between deposition and wettability behavior on the high‐efficiency utilization of pesticides. Pest Management Science, 77(5), 2485-2493. https://doi.org/10.1002/ps.6279
Heydari Nezhad, A. M., Baba Zad, V. A., & Rahimian, H. A. (2016). Studying PR2 and PAL genes involvement in rice resistance against Acidovorax avenae subsp. Avenae. Agricultural Biotechnology Journal, 7(4), 67-82. https://doi.org/10.22103/jab.2016.1391
Hockett, K. L., Burch, A. Y., & Lindow, S. E. (2013). Thermo-regulation of genes mediating motility and plant interactions in Pseudomonas syringae. PLoS One, 8(3), e59850. https://doi.org/10.1371/journal.pone.0059850
Huang, J., Yao, C., Sun, Y., Ji, Q., & Deng, X. (2022). Virulence-related regulatory network of Pseudomonas syringae. Computational and structural biotechnology journal, 20, 6259-6270. https://doi.org/10.1016/j.csbj.2022.11.011
Hussain, M.M., Saeed, A., Shakeel, M., Rauf, A., Jan, F., Gul, S., Mohibullah, M., Munir, M., Khan, I., & Yasin, M. (2023). Dynamics of lead tolerance in Tobacco (Nicotiana tabacum L.) genotypes. SABRAO J. Breed. Genet, 55(4), 1321-1331. http://doi.org/10.54910/sabrao2023.55.4.25
Jain, D., & Khurana, J. P. (2018). Role of pathogenesis-related (PR) proteins in plant defense mechanism. In Molecular aspects of plant-pathogen interaction (pp. 265-281). Singapore: Springer Singapore. https://doi.org/10.1007/978-981-10-7371-7_12
Jiang LiangYu, J.L., Wu JunJiang, W.J., Fan SuJie, F.S., Li WenBin, L.W., Dong LiDong, D.L., Cheng Qun, C.Q., Xu PengFei, X.P., & Zhang ShuZhen, Z.S. (2015). Isolation and characterization of a novel pathogenesis-related protein gene (GmPRP) with induced expression in soybean (Glycine max) during infection with Phytophthora sojae. https://doi.org/10.1371/journal.pone.0129932
Jiang, J., Ma, S., Ye, N., Jiang, M., Cao, J., & Zhang, J. (2017). WRKY transcription factors in plant responses to stresses. Journal of integrative plant biology, 59(2), 86-101. https://doi.org/10.1111/jipb.12513
Kim, D. S., & Hwang, B. K. (2014). An important role of the pepper phenylalanine ammonia-lyase gene (PAL1) in salicylic acid-dependent signalling of the defence response to microbial pathogens. Journal of experimental botany, 65(9), 2295-2306. https://doi.org/10.1093/jxb/eru109
Kitajima, S., & Sato, F. (1999). Plant pathogenesis-related proteins: molecular mechanisms of gene expression and protein function. The journal of biochemistry, 125(1), 1-8.
Kusajima, M., Yasuda, M., Kawashima, A., Nojiri, H., Yamane, H., Nakajima, M., Akutsu, K., & Nakashita, H. (2010). Suppressive effect of abscisic acid on systemic acquired resistance in tobacco plants. Journal of General Plant Pathology, 76(2), 161-167. https://doi.org/10.1007/s10327-010-0218-5
Lai, Z., Li, Y., Wang, F., Cheng, Y., Fan, B., Yu, J. Q., & Chen, Z. (2011). Arabidopsis sigma factor binding proteins are activators of the WRKY33 transcription factor in plant defense. The Plant Cell, 23(10), 3824-3841. https://doi.org/10.1105/tpc.111.090571
Lammoglia, S. K., Kennedy, M. C., Barriuso, E., Alletto, L., Justes, E., Munier-Jolain, N., & Mamy, L. (2017). Assessing human health risks from pesticide use in conventional and innovative cropping systems with the BROWSE model. Environment International, 105, 66-78. https://doi.org/10.1016/j.envint.2017.04.012
Lee, J. S., Cha, J. Y., & Baik, H. S. (2011). Plant cell contact-dependent virulence regulation of hrp genes in Pseudomonas syringae pv. tabaci 11528. 생명과학회지, 21(2), 227-234.
Li, J., Brader, G., & Palva, E. T. (2004). The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. The Plant Cell, 16(2), 319-331. https://doi.org/10.1105/tpc.016980
Li, P., Lu, Y. J., Chen, H., & Day, B. (2020). The lifecycle of the plant immune system. Critical reviews in plant sciences, 39(1), 72-100. https://doi.org/10.1080/07352689.2020.1757829
Lincoln, J. E., Sanchez, J. P., Zumstein, K., & Gilchrist, D. G. (2018). Plant and animal PR1 family members inhibit programmed cell death and suppress bacterial pathogens in plant tissues. Molecular Plant Pathology, 19(9), 2111-2123. https://doi.org/10.1111/mpp.12685
Lindgren, P. B. (1997). The role of hrp genes during plant-bacterial interactions. Annual review of phytopathology, 35(1), 129-152. https://doi.org/10.1146/annurev.phyto.35.1.129
Liu, Y., Liu, L., Yang, S., Zeng, Q., He, Z., & Liu, Y. (2019a). Cloning, characterization and expression of the phenylalanine Ammonia-Lyase gene (PaPAL) from spruce Picea asperata. Forests, 10(8), 613. https://doi.org/10.3390/f10080613
Liu, Y., Liu, Q., Tang, Y., & Ding, W. (2019b). NtPR1a regulates resistance to Ralstonia solanacearum in Nicotiana tabacum via activating the defense-related genes. Biochemical and Biophysical Research Communications, 508(3), 940-945. https://doi.org/10.1016/j.bbrc.2018.12.017
Liu, Y., Wang, L., Cai, G., Jiang, S., Sun, L., & Li, D. (2013). Response of tobacco to the Pseudomonas syringae pv. tomato DC3000 is mainly dependent on salicylic acid signaling pathway. FEMS microbiology letters, 344(1), 77-85. https://doi.org/10.1111/1574-6968.12157
Maher, E. A., Bate, N. J., Ni, W., Elkind, Y., Dixon, R. A., & Lamb, C. J. (1994). Increased disease susceptibility of transgenic tobacco plants with suppressed levels of preformed phenylpropanoid products. Proceedings of the National Academy of Sciences, 91(16), 7802-7806. https://doi.org/10.1073/pnas.91.16.7802
Mao, G., Meng, X., Liu, Y., Zheng, Z., Chen, Z., & Zhang, S. (2011). Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. The Plant Cell, 23(4), 1639-1653. https://doi.org/10.1105/tpc.111.084996
Marpu, S., Kolailat, S.S., Korir, D., Kamras, B.L., Chaturvedi, R., Joseph, A., Smith, C.M., Palma, M.C., Shah, J., & Omary, M.A. (2017). Photochemical formation of chitosan-stabilized near-infrared-absorbing silver Nanoworms: A “Green” synthetic strategy and activity on Gram-negative pathogenic bacteria. Journal of Colloid and Interface Science, 507, 437-452. https://doi.org/10.1016/j.jcis.2017.08.009
Maschietto, V., Lanubile, A., De Leonardis, S., Marocco, A., & Paciolla, C. (2016). Constitutive expression of pathogenesis-related proteins and antioxydant enzyme activities triggers maize resistance towards Fusarium verticillioides. Journal of Plant Physiology, 200, 53-61. https://doi.org/10.1016/j.jplph.2016.06.006
Mauch-Mani, B., & Slusarenko, A. J. (1996). Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica. The Plant Cell, 8(2), 203-212. https://doi.org/10.1105/tpc.8.2.203
Meijer, H. J., Schoina, C., Wang, S., Bouwmeester, K., Hua, C., & Govers, F. (2019). Phytophthora infestans small phospholipase D‐like proteins elicit plant cell death and promote virulence. Molecular Plant Pathology, 20(2), 180-193. https://doi.org/10.1111/mpp.12746
Mhlongo, M. I., Piater, L. A., Madala, N. E., Labuschagne, N., & Dubery, I. A. (2018). The chemistry of plant–microbe interactions in the rhizosphere and the potential for metabolomics to reveal signaling related to defense priming and induced systemic resistance. Frontiers in plant science, 9, 112. https://doi.org/10.3389/fpls.2018.00112
Moralejo, F. J., Cardoza, R. E., Gutierrez, S., & Martin, J. F. (1999). Thaumatin production in Aspergillus awamori by use of expression cassettes with strong fungal promoters and high gene dosage. Applied and Environmental Microbiology, 65(3), 1168-1174. https://doi.org/10.1128/AEM.65.3.1168-1174.1999
Musa-Khalifani, K., Darvishzadeh, R., & Abrinbana, M. (2021). Resistance against Sclerotinia basal stem rot pathogens in sunflower. Tropical Plant Pathology, 46(6), 651-663. https://doi.org/10.1007/s40858-021-00463-z
Nguyen, Q. M., Iswanto, A. B. B., Son, G. H., & Kim, S. H. (2021). Recent advances in effector-triggered immunity in plants: new pieces in the puzzle create a different paradigm. International Journal of Molecular Sciences, 22(9), 4709. https://doi.org/10.3390/ijms22094709
Nishad, R., Ahmed, T., Rahman, V. J., & Kareem, A. (2020). Modulation of plant defense system in response to microbial interactions. Frontiers in Microbiology, 11, 1298. https://doi.org/10.3389/fmicb.2020.01298
Oh, S. K., Baek, K. H., Park, J. M., Yi, S. Y., Yu, S. H., & Choi, D. (2008). Capsicum annuum WRKY protein CaWRKY1 is a negative regulator of pathogen defense. New Phytologist, 177(4). https://doi.org/10.1111/j.1469-8137.2007.02310.x
Peng, X., Hu, Y., Tang, X., Zhou, P., Deng, X., Wang, H., & Guo, Z. (2012). Constitutive expression of rice WRKY30 gene increases the endogenous jasmonic acid accumulation, PR gene expression and resistance to fungal pathogens in rice. Planta, 236(5), 1485-1498. https://doi.org/10.1007/s00425-012-1698-7
Phukan, U. J., Jeena, G. S., & Shukla, R. K. (2016). WRKY transcription factors: molecular regulation and stress responses in plants. Frontiers in plant science, 7, 760. https://doi.org/10.3389/fpls.2016.00760
Reichert, A. I., He, X. Z., & Dixon, R. A. (2009). Phenylalanine ammonia-lyase (PAL) from tobacco (Nicotiana tabacum): characterization of the four tobacco PAL genes and active heterotetrameric enzymes. Biochemical Journal, 424(2), 233-242. https://doi.org/10.1042/BJ20090620
Riviere, M. P., Marais, A., Ponchet, M., Willats, W., & Galiana, E. (2008). Silencing of acidic pathogenesis-related PR-1 genes increases extracellular β-(1→ 3)-glucanase activity at the onset of tobacco defence reactions. Journal of experimental botany, 59(6), 1225-1239. https://doi.org/10.1093/jxb/ern044
Santén, K., Marttila, S., Liljeroth, E., & Bryngelsson, T. (2005). Immunocytochemical localization of the pathogenesis-related PR-1 protein in barley leaves after infection by Bipolaris sorokiniana. Physiological and molecular plant pathology, 66(1-2), 45-54. https://doi.org/10.1016/j.pmpp.2005.04.006
Sheikh, A. H., Eschen-Lippold, L., Pecher, P., Hoehenwarter, W., Sinha, A. K., Scheel, D., & Lee, J. (2016). Regulation of WRKY46 transcription factor function by mitogen-activated protein kinases in Arabidopsis thaliana. Frontiers in Plant Science, 7, 61. https://doi.org/10.3389/fpls.2016.00061
Shi, Y.L., Sheng, Y.Y., Cai, Z.Y., Yang, R., Li, Q.S., Li, X.M., Li, D., Guo, X.Y., Lu, J.L., Ye, J.H., & Wang, K.R. (2019). Involvement of salicylic acid in anthracnose infection in tea plants revealed by transcriptome profiling. International Journal of Molecular Sciences, 20(10), 2439. https://doi.org/10.3390/ijms20102439
Shimono, M., Koga, H., Akagi, A.Y.A., Hayashi, N., Goto, S., Sawada, M., Kurihara, T., Matsushita, A., Sugano, S., JIANG, C.J., & Kaku, H. (2012). Rice WRKY45 plays important roles in fungal and bacterial disease resistance. Molecular plant pathology, 13(1), 83-94. https://doi.org/10.1111/j.1364-3703.2011.00732.x
Showmy, K. S., & Yusuf, A. (2020). Characterization of disease resistance in nine traditional rice (Oryza sativa L.) cultivars and expression of chennellu PR1 gene in response to Xanthomonas oryzae pv. Oryzae. Indian Phytopathology, 73(2), 281-291. https://doi.org/10.1007/s42360-020-00220-3
Song, F., & Goodman, R. M. (2001). Molecular biology of disease resistance in rice. Physiological and Molecular Plant Pathology, 59(1), 1-11. https://doi.org/10.1006/pmpp.2001.0353
Souza, T. P., Dias, R. O., & Silva-Filho, M. C. (2017). Defense-related proteins involved in sugarcane responses to biotic stress. Genetics and Molecular Biology, 40(1 suppl 1), 360-372. https://doi.org/10.1590/1678-4685-GMB-2016-0057
Stintzi, A., Heitz, T., Prasad, V., Wiedemann-Merdinoglu, S., Kauffmann, S., Geoffroy, P., Legrand, M., & Fritig, B. (1993). Plant ‘pathogenesis-related’proteins and their role in defense against pathogens. Biochimie, 75(8), 687-706. https://doi.org/10.1016/0300-9084(93)90100-7
Taguchi, F., Suzuki, T., Inagaki, Y., Toyoda, K., Shiraishi, T., & Ichinose, Y. (2010). The siderophore pyoverdine of Pseudomonas syringae pv. tabaci 6605 is an intrinsic virulence factor in host tobacco infection. Journal of Bacteriology, 192(1), 117-126. https://doi.org/10.1128/jb.00689-
Taguchi, F., Yamamoto, M., Ohnishi-Kameyama, M., Iwaki, M., Yoshida, M., Ishii, T., Konishi, T., & Ichinose, Y. (2010). Defects in flagellin glycosylation affect the virulence of Pseudomonas syringae pv. tabaci 6605. Microbiology, 156(1), 72-80. https://doi.org/10.1099/mic.0.030700-0
Tanaka, N., Che, F. S., Watanabe, N., Fujiwara, S., Takayama, S., & Isogai, A. (2003). Flagellin from an incompatible strain of Acidovorax avenae mediates H2O2 generation accompanying hypersensitive cell death and expression of PAL, Cht-1, and PBZ1, but not of Lox in rice. Molecular plant-microbe interactions, 16(5), 422-428. https://doi.org/10.1094/MPMI.2003.16.5.422
Tunsagool, P., Jutidamrongphan, W., Phaonakrop, N., Jaresitthikunchai, J., Roytrakul, S., & Leelasuphakul, W. (2019). Insights into stress responses in mandarins triggered by Bacillus subtilis cyclic lipopeptides and exogenous plant hormones upon Penicillium digitatum infection. Plant cell reports, 38(5), 559-575. https://doi.org/10.1007/s00299-019-02386-1
van Verk, M. C., Neeleman, L., Bol, J. F., & Linthorst, H. J. (2010). Tobacco Transcription Factors NtWRKY12 and TGA2. 2 Interact in vitro and in vivo and Activate PR-1a Gene Expression.
Vicente, J. G., & Holub, E. B. (2013). Xanthomonas campestris pv. campestris (cause of black rot of crucifers) in the genomic era is still a worldwide threat to brassica crops. Molecular plant pathology, 14(1), 2-18. https://doi.org/10.1111/j.1364-3703.2012.00833.x
Vidhyasekaran, P. (2002). Bacterial disease resistance in plants. Haworth Press, Inc., 10 Alice Street Binghamton NY 13904-1580 USA. 466, 466.
Vigers, A. J., Roberts, W. K., & Selitrennikoff, C. P. (1991). A new family of plant antifungal proteins. Mol Plant Microbe Interact, 4(4), 315-323.
Wang, H., Hao, J., Chen, X., Hao, Z., Wang, X., Lou, Y., Peng, Y., & Guo, Z. (2007). Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants. Plant molecular biology, 65(6), 799-815. https://doi.org/10.1007/s11103-007-9244-x
Xing, L., Zhi, Q., Hu, X., Liu, L., Xu, H., Zhou, T., Yin, H., Yi, Z., & Li, J. (2022). Influence of association network properties and ecological assembly of the foliar fugal community on crop quality. Frontiers in microbiology, 13, 783923. https://doi.org/10.3389/fmicb.2022.783923
Yang, J., Wang, G. Q., Zhou, Q., Lu, W., Ma, J. Q., & Huang, J. H. (2019). Transcriptomic and proteomic response of Manihot esculenta to Tetranychus urticae infestation at different densities. Experimental and Applied Acarology, 78(2), 273-293. https://doi.org/10.1007/s10493-019-00387-z
Yang, X., Gu, X., Ding, J., Yao, L., Gao, X., Zhang, M., Meng, Q., Wei, S., & Fu, J. (2022). Gene expression analysis of resistant and susceptible rice cultivars to sheath blight after inoculation with Rhizoctonia solani. BMC genomics, 23(1), 278. https://doi.org/10.1186/s12864-022-08524-6
Yuan, M., Ngou, B. P. M., Ding, P., & Xin, X. F. (2021). PTI-ETI crosstalk: an integrative view of plant immunity. Current opinion in plant biology, 62, 102030. https://doi.org/10.1016/j.pbi.2021.102030
Zheng, Z., Qamar, S. A., Chen, Z., & Mengiste, T. (2006). Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. The Plant Journal, 48(4), 592-605. https://doi.org/10.1111/j.1365-313X.2006.02901.x
Zhou, X., Liao, H., Chern, M., Yin, J., Chen, Y., Wang, J., Zhu, X., Chen, Z., Yuan, C., Zhao, W., & Wang, J. (2018). Loss of function of a rice TPR-domain RNA-binding protein confers broad-spectrum disease resistance. Proceedings of the National Academy of Sciences, 115(12), 3174-3179. https://doi.org/10.1073/pnas.1705927115
Zribi, I., Ghorbel, M., & Brini, F. (2021). Pathogenesis related proteins (PRs): From cellular mechanisms to plant defense. Current Protein and Peptide Science, 22(5), 396-412. https://doi.org/10.2174/1389203721999201231212736