2 research outputs found

    Ethylene is Involved in Symptom Development and Ribosomal Stress of Tomato Plants upon Citrus Exocortis Viroid Infection

    Full text link
    [EN] Citrus exocortis viroid (CEVd) is known to cause different symptoms in citrus trees, and its mechanism of infection has been studied in tomato as an experimental host, producing ribosomal stress on these plants. Some of the symptoms caused by CEVd in tomato plants resemble those produced by the phytohormone ethylene. The present study is focused on elucidating the relationship between CEVd infection and ethylene on disease development. To this purpose, the ethylene insensitive Never ripe (Nr) tomato mutants were infected with CEVd, and several aspects such as susceptibility to infection, defensive response, ethylene biosynthesis and ribosomal stress were studied. Phenotypic characterization revealed higher susceptibility to CEVd in these mutants, which correlated with higher expression levels of both defense and ethylene biosynthesis genes, as well as the ribosomal stress marker SlNAC082. In addition, Northern blotting revealed compromised ribosome biogenesis in all CEVd infected plants, particularly in Nr mutants. Our results indicate a higher ethylene biosynthesis in Nr mutants and suggest an important role of this phytohormone in disease development and ribosomal stress caused by viroid infection.Vázquez Prol, F.; López-Gresa, MP.; Rodrigo Bravo, I.; Belles Albert, JM.; Lisón, P. (2020). Ethylene is Involved in Symptom Development and Ribosomal Stress of Tomato Plants upon Citrus Exocortis Viroid Infection. Plants. 9(5):1-15. https://doi.org/10.3390/plants9050582S11595Flores, R., Hernández, C., Alba, A. E. M. de, Daròs, J.-A., & Serio, F. D. (2005). Viroids and Viroid-Host Interactions. Annual Review of Phytopathology, 43(1), 117-139. doi:10.1146/annurev.phyto.43.040204.140243Adkar‐Purushothama, C. R., & Perreault, J. (2019). Current overview on viroid–host interactions. WIREs RNA, 11(2). doi:10.1002/wrna.1570Di Serio, F., Flores, R., Verhoeven, J. T. J., Li, S.-F., Pallás, V., Randles, J. W., … Owens, R. A. (2014). Current status of viroid taxonomy. Archives of Virology, 159(12), 3467-3478. doi:10.1007/s00705-014-2200-6Verhoeven, J. th. j., Jansen, C. C. C., Willemen, T. M., Kox, L. F. F., Owens, R. A., & Roenhorst, J. W. (2004). Natural infections of tomato by Citrus exocortis viroid, Columnea latent viroid, Potato spindle tuber viroid and Tomato chlorotic dwarf viroid. European Journal of Plant Pathology, 110(8), 823-831. doi:10.1007/s10658-004-2493-5López-Gresa, M. P., Lisón, P., Yenush, L., Conejero, V., Rodrigo, I., & Bellés, J. M. (2016). Salicylic Acid Is Involved in the Basal Resistance of Tomato Plants to Citrus Exocortis Viroid and Tomato Spotted Wilt Virus. PLOS ONE, 11(11), e0166938. doi:10.1371/journal.pone.0166938Wang, Y., Wu, J., Qiu, Y., Atta, S., Zhou, C., & Cao, M. (2019). Global Transcriptomic Analysis Reveals Insights into the Response of ‘Etrog’ Citron (Citrus medica L.) to Citrus Exocortis Viroid Infection. Viruses, 11(5), 453. doi:10.3390/v11050453Jia, C., Zhang, L., Liu, L., Wang, J., Li, C., & Wang, Q. (2013). Multiple phytohormone signalling pathways modulate susceptibility of tomato plants to Alternaria alternata f. sp. lycopersici. Journal of Experimental Botany, 64(2), 637-650. doi:10.1093/jxb/ers360Van Loon, L. C., Geraats, B. P. J., & Linthorst, H. J. M. (2006). Ethylene as a modulator of disease resistance in plants. Trends in Plant Science, 11(4), 184-191. doi:10.1016/j.tplants.2006.02.005Bellés, J. M., & Conejero, V. (1989). Ethylene Mediation of the Viroid-Like Syndrome Induced by Ag+Ions inGynura aurantiacaDC Plants. Journal of Phytopathology, 124(4), 275-284. doi:10.1111/j.1439-0434.1989.tb04924.xDubois, M., Van den Broeck, L., & Inzé, D. (2018). The Pivotal Role of Ethylene in Plant Growth. Trends in Plant Science, 23(4), 311-323. doi:10.1016/j.tplants.2018.01.003Yang, S. F., & Hoffman, N. E. (1984). Ethylene Biosynthesis and its Regulation in Higher Plants. Annual Review of Plant Physiology, 35(1), 155-189. doi:10.1146/annurev.pp.35.060184.001103Wang, K. L.-C., Li, H., & Ecker, J. R. (2002). Ethylene Biosynthesis and Signaling Networks. The Plant Cell, 14(suppl 1), S131-S151. doi:10.1105/tpc.001768Han, L., Li, G.-J., Yang, K.-Y., Mao, G., Wang, R., Liu, Y., & Zhang, S. (2010). Mitogen-activated protein kinase 3 and 6 regulate Botrytis cinerea-induced ethylene production in Arabidopsis. The Plant Journal, no-no. doi:10.1111/j.1365-313x.2010.04318.xBellés, J. M., Granell, A., Durán-vila, N., & Conejero, V. (1989). ACC Synthesis as the Activated Step Responsible for the Rise of Ethylene Production Accompanying Citrus Exocortis Viroid Infection in Tomato Plants. Journal of Phytopathology, 125(3), 198-208. doi:10.1111/j.1439-0434.1989.tb01061.xBellés, J. M., Vera, P., Durán-Vila, N., & Conejero, V. (1989). Ethylene production in tomato cultures infected with citrus exocortis viroid (CEV). Canadian Journal of Plant Pathology, 11(3), 256-262. doi:10.1080/07060668909501109Bellés, J. M., & Conejero, V. (1989). Evolution of Ethylene Production, ACC and Conjugated ACC Levels Accompanying Symptom Development in Tomato and Gynura aurantiaca DC Leaves Infected with Citrus Exocortis Viroid (CEV). Journal of Phytopathology, 127(1), 81-85. doi:10.1111/j.1439-0434.1989.tb04506.xBellés, J. M., & Conejero, V. (1991). Suppression by Citrus Exocortis Viroid Infection of the Naturally Occurring Inhibitor of the Conversion of 1-aminocyclopropane-1-carboxylic Acid to Ethylene by Tomato Microsomes. Journal of Phytopathology, 132(3), 245-250. doi:10.1111/j.1439-0434.1991.tb00117.xJu, C., Yoon, G. M., Shemansky, J. M., Lin, D. Y., Ying, Z. I., Chang, J., … Chang, C. (2012). CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis. Proceedings of the National Academy of Sciences, 109(47), 19486-19491. doi:10.1073/pnas.1214848109Aloni, R., Wolf, A., Feigenbaum, P., Avni, A., & Klee, H. J. (1998). The Never ripe Mutant Provides Evidence That Tumor-Induced Ethylene Controls the Morphogenesis ofAgrobacterium tumefaciens-Induced Crown Galls on Tomato Stems1,2. Plant Physiology, 117(3), 841-849. doi:10.1104/pp.117.3.841Klee, H. J. (2004). Ethylene Signal Transduction. Moving beyond Arabidopsis. Plant Physiology, 135(2), 660-667. doi:10.1104/pp.104.040998Chen, Y., Rofidal, V., Hem, S., Gil, J., Nosarzewska, J., Berger, N., … Chervin, C. (2019). Targeted Proteomics Allows Quantification of Ethylene Receptors and Reveals SlETR3 Accumulation in Never-Ripe Tomatoes. Frontiers in Plant Science, 10. doi:10.3389/fpls.2019.01054HU, X., NIE, X., SONG, Y., XIONG, X., & Tai, H. (2011). Ethylene is Involved but Plays a Limited Role in Tomato Chlorotic Dwarf Viroid-Induced Symptom Development in Tomato. Agricultural Sciences in China, 10(4), 544-552. doi:10.1016/s1671-2927(11)60035-7Dı́az, J., ten Have, A., & van Kan, J. A. L. (2002). The Role of Ethylene and Wound Signaling in Resistance of Tomato to Botrytis cinerea  . Plant Physiology, 129(3), 1341-1351. doi:10.1104/pp.001453Lund, S. T., Stall, R. E., & Klee, H. J. (1998). Ethylene Regulates the Susceptible Response to Pathogen Infection in Tomato. The Plant Cell, 10(3), 371-382. doi:10.1105/tpc.10.3.371Tsolakidou, M.-D., Pantelides, lakovos S., Tzima, A. K., Kang, S., Paplomatas, E. J., & Tsaltas, D. (2019). Disruption and Overexpression of the Gene Encoding ACC (1-Aminocyclopropane-1-Carboxylic Acid) Deaminase in Soil-Borne Fungal Pathogen Verticillium dahliae Revealed the Role of ACC as a Potential Regulator of Virulence and Plant Defense. Molecular Plant-Microbe Interactions®, 32(6), 639-653. doi:10.1094/mpmi-07-18-0203-rWięsyk, A., Iwanicka-Nowicka, R., Fogtman, A., Zagórski-Ostoja, W., & Góra-Sochacka, A. (2018). Time-Course Microarray Analysis Reveals Differences between Transcriptional Changes in Tomato Leaves Triggered by Mild and Severe Variants of Potato Spindle Tuber Viroid. Viruses, 10(5), 257. doi:10.3390/v10050257Eiras, M., Nohales, M. A., Kitajima, E. W., Flores, R., & Daròs, J. A. (2010). Ribosomal protein L5 and transcription factor IIIA from Arabidopsis thaliana bind in vitro specifically Potato spindle tuber viroid RNA. Archives of Virology, 156(3), 529-533. doi:10.1007/s00705-010-0867-xDubé, A., Bisaillon, M., & Perreault, J.-P. (2009). Identification of Proteins from Prunus persica That Interact with Peach Latent Mosaic Viroid. Journal of Virology, 83(23), 12057-12067. doi:10.1128/jvi.01151-09Lisón, P., Tárraga, S., López-Gresa, P., Saurí, A., Torres, C., Campos, L., … Rodrigo, I. (2013). A noncoding plant pathogen provokes both transcriptional and posttranscriptional alterations in tomato. PROTEOMICS, 13(5), 833-844. doi:10.1002/pmic.201200286Cottilli, P., Belda-Palazón, B., Adkar-Purushothama, C. R., Perreault, J.-P., Schleiff, E., Rodrigo, I., … Lisón, P. (2019). Citrus exocortis viroid causes ribosomal stress in tomato plants. Nucleic Acids Research, 47(16), 8649-8661. doi:10.1093/nar/gkz679Ohbayashi, I., Lin, C.-Y., Shinohara, N., Matsumura, Y., Machida, Y., Horiguchi, G., … Sugiyama, M. (2017). Evidence for a Role of ANAC082 as a Ribosomal Stress Response Mediator Leading to Growth Defects and Developmental Alterations in Arabidopsis. The Plant Cell, 29(10), 2644-2660. doi:10.1105/tpc.17.00255Mayer, C., & Grummt, I. (2005). Cellular Stress and Nucleolar Function. Cell Cycle, 4(8), 1036-1038. doi:10.4161/cc.4.8.1925Weis, B. L., Kovacevic, J., Missbach, S., & Schleiff, E. (2015). Plant-Specific Features of Ribosome Biogenesis. Trends in Plant Science, 20(11), 729-740. doi:10.1016/j.tplants.2015.07.003Palm, D., Streit, D., Shanmugam, T., Weis, B. L., Ruprecht, M., Simm, S., & Schleiff, E. (2018). Plant-specific ribosome biogenesis factors in Arabidopsis thaliana with essential function in rRNA processing. Nucleic Acids Research, 47(4), 1880-1895. doi:10.1093/nar/gky1261Christoffersen, R. E., & Laties, G. G. (1982). Ethylene regulation of gene expression in carrots. Proceedings of the National Academy of Sciences, 79(13), 4060-4063. doi:10.1073/pnas.79.13.4060Marei, N., & Romani, R. (1971). Ethylene-stimulated Synthesis of Ribosomes, Ribonucleic Acid, and Protein in Developing Fig Fruits. Plant Physiology, 48(6), 806-808. doi:10.1104/pp.48.6.806Spiers, J., Brady, C., Grierson, D., & Lee, E. (1984). Changes in Ribosome Organization and Messenger RNA Abundance in Ripening Tomato Fruits. Functional Plant Biology, 11(3), 225. doi:10.1071/pp9840225Merchante, C., Brumos, J., Yun, J., Hu, Q., Spencer, K. R., Enríquez, P., … Alonso, J. M. (2015). Gene-Specific Translation Regulation Mediated by the Hormone-Signaling Molecule EIN2. Cell, 163(3), 684-697. doi:10.1016/j.cell.2015.09.036Tornero, P., Rodrigo, I., Conejero, V., & Vera, P. (1993). Nucleotide Sequence of a cDNA Encoding a Pathogenesis-Related Protein, P1-p14, from Tomato (Lycopersicon esculentum). Plant Physiology, 102(1), 325-325. doi:10.1104/pp.102.1.325Granell, A., Bellés, J. M., & Conejero, V. (1987). Induction of pathogenesis-related proteins in tomato by citrus exocortis viroid, silver ion and ethephon. Physiological and Molecular Plant Pathology, 31(1), 83-90. doi:10.1016/0885-5765(87)90008-7Mehari, Z. H., Elad, Y., Rav-David, D., Graber, E. R., & Meller Harel, Y. (2015). Induced systemic resistance in tomato (Solanum lycopersicum) against Botrytis cinerea by biochar amendment involves jasmonic acid signaling. Plant and Soil, 395(1-2), 31-44. doi:10.1007/s11104-015-2445-1Nakatsuka, A., Murachi, S., Okunishi, H., Shiomi, S., Nakano, R., Kubo, Y., & Inaba, A. (1998). Differential Expression and Internal Feedback Regulation of 1-Aminocyclopropane-1-Carboxylate Synthase, 1-Aminocyclopropane-1-Carboxylate Oxidase, and Ethylene Receptor Genes in Tomato Fruit during Development and Ripening. Plant Physiology, 118(4), 1295-1305. doi:10.1104/pp.118.4.1295Katsarou, K., Wu, Y., Zhang, R., Bonar, N., Morris, J., Hedley, P. E., … Hornyik, C. (2016). Insight on Genes Affecting Tuber Development in Potato upon Potato spindle tuber viroid (PSTVd) Infection. PLOS ONE, 11(3), e0150711. doi:10.1371/journal.pone.0150711Bellés, J. M., Carbonell, J., & Conejero, V. (1991). Polyamines in Plants Infected by Citrus Exocortis Viroid or Treated with Silver Ions and Ethephon. Plant Physiology, 96(4), 1053-1059. doi:10.1104/pp.96.4.1053O’Donnell, P. J., Jones, J. B., Antoine, F. R., Ciardi, J., & Klee, H. J. (2001). Ethylene-dependent salicylic acid regulates an expanded cell death response to a plant pathogen. The Plant Journal, 25(3), 315-323. doi:10.1046/j.1365-313x.2001.00968.xGómez, G., Martínez, G., & Pallás, V. (2008). Viroid-Induced Symptoms in Nicotiana benthamiana Plants Are Dependent on RDR6 Activity  . Plant Physiology, 148(1), 414-423. doi:10.1104/pp.108.120808Li, G., Meng, X., Wang, R., Mao, G., Han, L., Liu, Y., & Zhang, S. (2012). Dual-Level Regulation of ACC Synthase Activity by MPK3/MPK6 Cascade and Its Downstream WRKY Transcription Factor during Ethylene Induction in Arabidopsis. PLoS Genetics, 8(6), e1002767. doi:10.1371/journal.pgen.1002767Berrocal-Lobo, M., Molina, A., & Solano, R. (2002). Constitutive expression ofETHYLENE-RESPONSE-FACTOR1inArabidopsisconfers resistance to several necrotrophic fungi. The Plant Journal, 29(1), 23-32. doi:10.1046/j.1365-313x.2002.01191.xChowdhury, S., Basu, A., & Kundu, S. (2017). Biotrophy-necrotrophy switch in pathogen evoke differential response in resistant and susceptible sesame involving multiple signaling pathways at different phases. Scientific Reports, 7(1). doi:10.1038/s41598-017-17248-7Shin, S., Lv, J., Fazio, G., Mazzola, M., & Zhu, Y. (2014). Transcriptional regulation of ethylene and jasmonate mediated defense response in apple (Malus domestica) root during Pythium ultimum infection. Horticulture Research, 1(1). doi:10.1038/hortres.2014.53Glazebrook, J. (2005). Contrasting Mechanisms of Defense Against Biotrophic and Necrotrophic Pathogens. Annual Review of Phytopathology, 43(1), 205-227. doi:10.1146/annurev.phyto.43.040204.135923McDowell, J. M., & Dangl, J. L. (2000). Signal transduction in the plant immune response. Trends in Biochemical Sciences, 25(2), 79-82. doi:10.1016/s0968-0004(99)01532-7Heck, S., Grau, T., Buchala, A., Metraux, J.-P., & Nawrath, C. (2003). Genetic evidence that expression of NahG modifies defence pathways independent of salicylic acid biosynthesis in the Arabidopsis-Pseudomonas syringae pv. tomato interaction. The Plant Journal, 36(3), 342-352. doi:10.1046/j.1365-313x.2003.01881.xConejero, V., & Granell, A. (1986). Stimulation of a viroid-like syndrome and the impairment of viroid infection in Gynura aurantiaca plants by treatment with silver ions. Physiological and Molecular Plant Pathology, 29(3), 317-323. doi:10.1016/s0048-4059(86)80048-0Yan, S., & Dong, X. (2014). Perception of the plant immune signal salicylic acid. Current Opinion in Plant Biology, 20, 64-68. doi:10.1016/j.pbi.2014.04.006Fu, Z. Q., Yan, S., Saleh, A., Wang, W., Ruble, J., Oka, N., … Dong, X. (2012). NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature, 486(7402), 228-232. doi:10.1038/nature11162Schott-Verdugo, S., Müller, L., Classen, E., Gohlke, H., & Groth, G. (2019). Structural Model of the ETR1 Ethylene Receptor Transmembrane Sensor Domain. Scientific Reports, 9(1). doi:10.1038/s41598-019-45189-wClark, D. G., Gubrium, E. K., Barrett, J. E., Nell, T. A., & Klee, H. J. (1999). Root Formation in Ethylene-Insensitive Plants. Plant Physiology, 121(1), 53-60. doi:10.1104/pp.121.1.53Rodrı́guez, F. I., Esch, J. J., Hall, A. E., Binder, B. M., Schaller, G. E., & Bleecker, A. B. (1999). A Copper Cofactor for the Ethylene Receptor ETR1 from Arabidopsis. Science, 283(5404), 996-998. doi:10.1126/science.283.5404.996Schaller, G. E., Ladd, A. N., Lanahan, M. B., Spanbauer, J. M., & Bleecker, A. B. (1995). The Ethylene Response Mediator ETR1 from Arabidopsis Forms a Disulfide-linked Dimer. Journal of Biological Chemistry, 270(21), 12526-12530. doi:10.1074/jbc.270.21.12526Gao, Z., & Schaller, G. E. (2009). The role of receptor interactions in regulating ethylene signal transduction. Plant Signaling & Behavior, 4(12), 1152-1153. doi:10.4161/psb.4.12.9943Gao, Z., Wen, C.-K., Binder, B. M., Chen, Y.-F., Chang, J., Chiang, Y.-H., … Schaller, G. E. (2008). Heteromeric Interactions among Ethylene Receptors Mediate Signaling in Arabidopsis. Journal of Biological Chemistry, 283(35), 23801-23810. doi:10.1074/jbc.m800641200Grefen, C., Städele, K., Růžička, K., Obrdlik, P., Harter, K., & Horák, J. (2008). Subcellular Localization and In Vivo Interactions of the Arabidopsis thaliana Ethylene Receptor Family Members. Molecular Plant, 1(2), 308-320. doi:10.1093/mp/ssm015Kim, H. J., Park, J.-H., Kim, J., Kim, J. J., Hong, S., Kim, J., … Hwang, D. (2018). Time-evolving genetic networks reveal a NAC troika that negatively regulates leaf senescence in Arabidopsis. Proceedings of the National Academy of Sciences, 115(21), E4930-E4939. doi:10.1073/pnas.1721523115Semancik, J. S., Roistacher, C. N., Rivera-Bustamante, R., & Duran-Vila, N. (1988). Citrus Cachexia Viroid, a New Viroid of Citrus: Relationship to Viroids of the Exocortis Disease Complex. Journal of General Virology, 69(12), 3059-3068. doi:10.1099/0022-1317-69-12-3059Campos, L., Granell, P., Tárraga, S., López-Gresa, P., Conejero, V., Bellés, J. M., … Lisón, P. (2014). Salicylic acid and gentisic acid induce RNA silencing-related genes and plant resistance to RNA pathogens. Plant Physiology and Biochemistry, 77, 35-43. doi:10.1016/j.plaphy.2014.01.016Adkar-Purushothama, C. R., Brosseau, C., Giguère, T., Sano, T., Moffett, P., & Perreault, J.-P. (2015). Small RNA Derived from the Virulence Modulating Region of the Potato spindle tuber viroid Silences callose synthase Genes of Tomato Plants. The Plant Cell, 27(8), 2178-2194. doi:10.1105/tpc.15.00523LAEMMLI, U. K. (1970). Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4. Nature, 227(5259), 680-685. doi:10.1038/227680a

    Ethylene is involved in symptom development and ribosomal stress of tomato plants upon citrus exocortis viroid infection

    Get PDF
    Citrus exocortis viroid (CEVd) is known to cause different symptoms in citrus trees, and its mechanism of infection has been studied in tomato as an experimental host, producing ribosomal stress on these plants. Some of the symptoms caused by CEVd in tomato plants resemble those produced by the phytohormone ethylene. The present study is focused on elucidating the relationship between CEVd infection and ethylene on disease development. To this purpose, the ethylene insensitive Never ripe (Nr) tomato mutants were infected with CEVd, and several aspects such as susceptibility to infection, defensive response, ethylene biosynthesis and ribosomal stress were studied. Phenotypic characterization revealed higher susceptibility to CEVd in these mutants, which correlated with higher expression levels of both defense and ethylene biosynthesis genes, as well as the ribosomal stress marker SlNAC082. In addition, Northern blotting revealed compromised ribosome biogenesis in all CEVd infected plants, particularly in Nr mutants. Our results indicate a higher ethylene biosynthesis in Nr mutants and suggest an important role of this phytohormone in disease development and ribosomal stress caused by viroid infection
    corecore