Transcriptional Response of Defensive and Regulatory Genes Involved in Tomato Plant Hormone Signaling Pathways against Fusarium Wilt

Document Type : Original research paper

Authors

1 Department of Plant Production and Genetics, Faculty of Agriculture, Agricultural Sciences and Natural Resources University of Khuzestan, Mollasani, Iran

2 Department of Plant Protection, Faculty of Agriculture, Agricultural Sciences and Natural Resources University of Khuzestan, Mollasani, Khuzestan, Iran

Abstract

Fusarium wilt caused by the fungus Fusarium oxysporum f. sp. lycopersici (FOL) is one of the major devastating diseases of tomato plants throughout the world. There is no information on the molecular response of tomato line, Early Urbana-Y to FOL. The present study was performed to study the line response to FOL using phytopathological (disease severity and shoot fresh weight) as well as molecular methodologies. The transcription of several genes responsive to jasmonic acid (JA; Pin2), salicylic acid (SA; Chi3, Chi9 and PR1), the regulatory genes responsive to the signaling hormone JA (MYC2 and WRKY33) and ethylene (ET; ERF1) were studied by qRT-PCR technique at different time points after FOL inoculation (6-96 hour after inoculation). Disease symptoms development and reduced shoot fresh weight of the inoculated plants despite up-regulation of SA-dependent defense genes at different time points after pathogen infection indicated that SA signaling pathway is involved in the susceptibility of the Early Urbana-Y line to FOL. In contrast, JA and ET pathway genes were not strongly induced in response to the pathogen suggesting the involvement of JA/ET-mediated defense responses in reducing disease susceptibility. However, to gain a better understanding of enhanced resistance to fusarium wilt, more detailed molecular mechanisms underlying susceptibility of Early Urbana-Y line to FOL need to be further investigated in the future.

Keywords

[1] Darvishnia, D. and Dehghani, A. 2015. Diseases of vegetable crops in Iran and their integrated management. Sarva Publications.
[2] De Silva, N., Lumyong, S., Hyde, K., Bulgakov, T., Phillips, A. and Yan, J. 2016. Mycosphere essays 9: defining biotrophs and hemibiotrophs. Mycosphere, 7(5): 545-559.
[3] McGrath, D. J., Gillespie, D. and Vawdrey, L. 1987. Inheritance of resistance to Fusarium oxysporum f. sp. lycopersici races 2 and 3 in Lycopersicon pennellii. Aust J Agr Res, 38(4): 729-733.‏
[4] Ausubel, F.M. 2005. Are innate immune signaling pathways in plants and animals conserved? Nat Immunol, 6: 973–979.
[5] Boudsocq, M., Willmann, M.R., McCormack, M., Lee, H., Shan, L., He, P., Bush J., Cheng, S.H., Sheen, J. 2010. Differential innate immune signalling via Ca2+ sensor protein kinases. Nature, 464: 418–422.
[6] Van der Ent, S., Van Wees, S. C. and Pieterse, C. M. 2009. Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochem, 70: 1581–1588.
[7] Shah, J. and Zeier, J. 2013. Long‐distance communication and signal amplification in systemic acquired resistance. Front. Plant Sci, 4:30.
[8] Liu, P. P., von Dahl, C. C. and Klessig, D. F. 2011. The extent to which methyl salicylate is required for signaling systemic acquired resistance is dependent on exposure to light after infection. Plant Physiol, 157: 2216–2226.
[9] Mou, Z., Fan, W. and Dong, X. 2003. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell, 113: 935–944.
[10] Wasternack, C. and Hause, B. 2013. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann. Bot, 111(6): 1021-1058.
[11] Shakeel, S. N., Wang, X., Binder, B. M. and Schaller, G. E. 2013. Mechanisms of signal transduction by ethylene: overlapping and non-overlapping signalling roles in a receptor family. AoB plants, 5: 1-15
[12] Gutterson, N. and Reuber, T.L. 2004. Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol, 7: 465–471.
[13] Van Loon, L.C., Rep, M. and Pieterse, C. 2006. Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol, 44(1): 135-162.
[14] Ebrahim, S., Usha, K. and Singh, B. 2011. Pathogenesis related (PR) proteins in plant defense mechanism. Sci Against Microb Pathog, 2(3): 1043-1054.
[15] Delaney, T., Friedrich, L. and Ryals, J. 1995. Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc Natl Acad Sci U S A, 92(14): 6602-6606.
[16] Datta, S. K. and Muthukrishnan, S. 1999. Pathogenesis-related proteins in plants: Proteinase Inhibitors in Plant–Microbe and Plant–Insect Interactions, Acid-free paper, United States of America.
[17] Vidhyasekaran, P. 2007. Fungal pathogenesis in plants and crops: molecular biology and host defense mechanisms, 2nd edn. Tamil Nadu Agricultural University Coimbatore, India.
[18] Koornneef, A. and Pieterse, C. M. 2008. Cross talk in defense signaling. Plant Physiol, 146(3): 839-844.‏
[19] Li, C. Y., Deng, G. M., Yang, J., Viljoen, A., Jin, Y., Kuang, R. B., Zuo, C. W., Lv, Z. C., Yang, Q. S., Sheng, O., Wei, Y. R., Hu, C. H., Dong, T. and Yi G. J. 2012. Transcriptome profiling of resistant and susceptible Cavendish banana roots following inoculation with Fusarium oxysporum f. sp. cubense tropical race 4. BMC Genom, 13: 374.
[20] O’Donnell, P.J., Calvert, C., Atzorn, R., Wasternack, C., Leyser, H.M.O. and Bowles, D.J. 1996. Ethylene as a signal mediating the wound response of tomato plants. Science, 274(5294):1914–1917.
[21] Lawton, K. A., Potter, S. L., Uknes, S. and Ryals, J. 1994. Acquired resistance signal transduction in Arabidopsis is ethylene independent. Plant Cell, 6(5): 581-588.
[22] Husaini, A. M., Sakina, A. and Cambay, S. R. 2018. Host-Pathogen interaction in Fusarium oxysporum infections: Where do we stand? Mol Plant Microbe Interact, 31(9): 889-898.
[23] Takahashi, H., Nakaho, K., Ishihara, T., Ando, S., Wada, T., Kanayama, Y., Asano, S., Yoshida, S., Tsushima, S. and Hyakumachi, M. 2014. Transcriptional profile of tomato roots exhibiting Bacillus thuringiensis-induced resistance to Ralstonia solanacearum. Plant Cell Rep, 33(1): 99-110.
[24] Davari, B., Limoee, M., Khodavaisy, S., Zamini, G. and Izadi, S. 2015. Toxicity of entomopathogenic fungi, Beauveria bassiana and Lecanicillium muscarium against a field-collected strain of the German cockroach Blattella germanica (L.) (Dictyoptera: Blattellidae). Trop. Biomed, 32(3): 463-470.
[25] Anitha, A. and Rabeeth, M. 2009. Control of Fusarium wilt of tomato by bioformulation of Streptomyces griseus in green house condition. Afr J Basic Appl Sci, 27 : 9-14.
[26] Schmittgen, T.D. and Livak, K.J. 2008. Analyzing real-time PCR data by the comparative CT method. Nature Protoc, 3: 1101-1108
[27] Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res, 29(9): e45-e45.
[28] Koornneef, A., Pieterse, C.M. 2008. Cross talk in defense signaling. Plant Physiol, 146: 839–844.
[29] Glazebrook, J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol, 43: 205–227
[30] Dong, X. 2004. NPR1, all things considered. Curr Opin Plant Biol, 7: 547–552
[31] Vlot, A.C., Dempsey, D.A. and Klessig, D.F. 2009. Salicylic Acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol, 47: 177–206
[32] Aimé, S., Cordier, C., Alabouvette, C. and Olivain C. 2008. Comparative analysis of PR gene expression in tomato inoculated with virulent Fusarium oxysporum f. sp. lycopersici and the biocontrol strain F. oxysporum Fo47. Physiol Mol Plant Pathol, 73(1): 9-15.‏
[33] Schlumbaum, A., Mauch, F., Vögeli, U. and Boller, T. 1986. Plant chitinases are potent inhibitors of fungal growth. Nature, 324(6095): 365.‏
[34] Shibuya, N. and Minami, E. 2001. Oligosaccharide signalling for defence responses in plant. Physiol. Mol. Plant Pathol, 59(5): 223-233.‏
[35] Brogue, K., Chet, I., Holliday, M., Cressman, R., Biddle, P., Knowlton, S. and Broglie, R. 1991. Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science, 254(5035): 1194-1197.‏
[36] Epple, P., Apel, K. and Bohlmann, H. 1997. Overexpression of an endogenous thionin enhances resistance of Arabidopsis against Fusarium oxysporum. Plant Cell, 9: 509-520.
[37] Cao, H., Bowling, S. A., Gordon, A. S. and Dong, X. 1994. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell, 6:1583–1592.
[38] Roetschi, A., Si-Ammour, A., Belbahri, L., Mauch, F. and Mauch-Mani, B. 2001. Characterization of an Arabidopsis-Phytophthora pathosystem: resistance requires a functional PAD2 gene and is independent of salicylic acid, ethylene and jasmonic acid signaling. Plant J, 28: 293–305.
[39] Fan, W. and Dong, X. 2002. In vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid–mediated gene activation in Arabidopsis. Plant Cell, 14(6): 1377-1389.‏
[40] Berrocal-Lobo, M. and Molina, A. 2004. Ethylene response factor 1 mediates Arabidopsis resistance to the soilborne fungus Fusarium oxysporum. Mol Plant Microbe Interact, 17(7):763-770.‏
[41] Spoel, S.H., Koornneef, A., Claessens, S.M. et al. 2003. NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell, 15: 760–770.
[42] Leon-Reyes, A., van der Does, D., de Lange, E.S., Delker, C., Wasternack, C., van Wees, S.C., Ritsema, T. and Pieterse, C.M. 2010. Salicylate-mediated suppression of jasmonate-responsive gene expression in Arabidopsis is targeted downstream of the jasmonate biosynthesis pathway. Planta, 232: 1423–1432.
[43] Hernández-Aparicio, F., Lisón, P., Rodrigo, I., Bellés, J.M. and López-Gresa, M.P. 2021. Signaling in the tomato immunity against Fusarium oxysporum. Molecules, 26: 1818.
[44] Morid, B., and Hajmansoor, S. 2017. Assessment of tomato genotypes resistance to verticillium and fusarium wilt diseases using molecular markers. JMW, 10: 80-93.
[45] Bari, R. and Jones, J.D.G. 2009. Role of plant hormones in plant defence responses. Plant Mol. Biol, 69: 473–488.
[46] El Oirdi, M., Abd El Rahman, T., Rigano, L., El Hadrami, A., Rodriguez, M.C., Daayf, F., Vojnov, A. and Bouarab, K. 2011. Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato. Plant Cell, 23: 2405–2421.
[47] Swarupa, V., Ravishankar, K.V., and Rekha, A. 2014. Plant defense response against Fusarium oxysporum and strategies to develop tolerant genotypes in banana. Planta, 239: 735-751.
[48] Edgar, C.I., McGrath, K.C., Dombrecht, B., Manners, J.M., McLean, D.J., Schenk, P.M.P., and Kazan, K. 2006. Salicylic acid mediates resistance to the vascular wilt pathogen in the model host Arabidopsis thaliana. Australas. Plant Pathol, 356: 581-591.
[49] Makandar, R., Nalam, V.J., Lee, H., Trick, H.N., Dong, Y., and Shah, J. 2012. Salicylic acid regulates basal resistance to fusarium head blight in wheat. Mol. Plant Microbe Interact, 25: 431-439.
[50] Mandal, S., Mitra, A., and Mallick, N. 2008. Biochemical characterization of oxidative burst during interaction between Solanum lycopersicum and Fusarium oxysporum f. sp. lycopersici. Physiol. Mol. Plant Pathol, 72: 56-61.
 
Volume 8, Issue 1
June 2020
Pages 48-56
  • Receive Date: 05 April 2021
  • Revise Date: 13 October 2021
  • Accept Date: 03 November 2021
  • First Publish Date: 03 November 2021