Abstract
Tomato Cf genes confer resistance to the leaf mold pathogen Cladosporium fulvum. The Avr4/Cf-4- and Avr9/Cf-9-dependent hypersensitive responses (HRs) are distinct in cell death pattern, intensity, and sensitivity to environmental conditions. To understand the mechanism resulting in these differences, comparative transcript profiling for Avr4/Cf-4- and Avr9/Cf-9-dependent defence gene expression by cDNA-AFLP was performed previously. 367 ACE (Avr/Cf-elicited) transcript-derived fragments (TDFs) were identified, among which 189 were cloned and sequenced. In this study, we report another 89 ACE fragments. These ACE genes were associated with: defence, signal transduction, HR and cell death, transcriptional regulation, metabolism, protein synthesis, photosynthesis, membrane fusion, secretion and trafficking, miscellaneous biological processes, and genes with unknown function or with no significant similarity to known sequences. Among these sequences 43 (potentially encoding 36 types of proteins) were identified for the first time as genes differentially expressed during the development of Avr/Cf-dependent HR. Sequence and expression data from this study further support that transcription is reprogrammed to promote defence response and HR and repress photosynthesis in the Avr/Cf HR+ seedlings.
This is a preview of subscription content, log in via an institution to check access.
References
Albert, M., Belastegui-Macadam, X., & Kaldenhoff, R. (2006). An attack of the plant parasite Cuscuta reflexa induces the expression of attAGP, an attachment protein of the host tomato. Plant Journal, 48, 548–556.
Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J. H., Zhang, Z., Miller, W., et al. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25, 3389–3402.
Cai, X., Takken, F. L. W., Joosten, M. H. A. J., & De Wit, P. J. G. M. (2001). Specific recognition of AVR4 and AVR9 results in distinct patterns of hypersensitive cell death in tomato, but similar patterns of defence-related gene expression. Molecular Plant Pathology, 2, 77–86.
Chaves, I., Regalado, A. P., Chen, M., Ricardo, C. P., & Showalter, A. M. (2002). Programmed cell death induced by (b-D-galactosyl)3 Yariv reagent in Nicotiana tabacum BY-2 suspension-cultured cells. Physiologia Plantarum, 116, 548–553.
Collins, N. C., Thordal-Christensen, H., Lipka, V., Bau, S., Kombrink, E., Qui, J. L., et al. (2003). SNARE-protein-mediated disease resistance at the plant cell wall. Nature, 425, 973–007.
De Jong, C. F., Takken, F. L. W., Cai, X., De Wit, P. J. G. M., & Joosten, M. H. A. J. (2002). Attenuation of Cf-mediated defense responses at elevated temperatures correlates with a decrease in elicitor-binding sites. Molecular Plant-Microbe Interactions, 15, 1040–1049.
Durrant, W. E., Rowland, O., Piedras, P., Hammond-Kosack, K. E., & Jones, J. D. G. (2000). cDNA-AFLP reveals a striking overlap in race specific resistance and wound response gene expression profiles. Plant Cell, 12, 963–977.
Gabriëls, S. H. E. J., Takken, F. L. W., Vossen, J. H., de Jong, C. F., Liu, Q., Turk, S. C. H. J., et al. (2006). cDNA-AFLP combined with functional analysis reveals novel genes involved in the hypersensitive response. Molecular Plant-Microbe Interactions, 19, 567–576.
Gish, W. (1996–2006). http://blast.wustl.edu.
Gong, Z., Dong, C. -H., Lee, H., Zhu, J., Xiong, L., Gong, D., et al. (2005). A DEAD box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cell, 17, 256–267.
Heese, A., Ludwig, A. A., & Jones, J. D. G. (2005). Rapid phosphorylation of a syntaxin during the Avr9/Cf-9-race-specific signaling pathway. Plant Physiology, 138, 2406–2416.
Hong, W., Xu, Y. P., Zheng, Z., Cao, J. S., & Cai, X. Z. (2007). Comparative transcript profiling by cDNA-AFLP reveals similar patterns of Avr4/Cf-4- and Avr9/Cf-9-dependent defence gene expression. Molecular Plant Pathology, 8, 515–527.
Jacobsen, S. E., Running, M. P., & Meyerowitz, E. M. (1999). Disruption of an RNA helicase/RNAse III gene in Arabidopsis causes unregulated cell division in floral meristems. Development, 126, 5231–5243.
Jones, D. A., Thomas, C. M., Hammond-Kosack, K. E., Balint-Kurti, P. J., & Jones, J. D. G. (1994). Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science, 266, 789–793.
Joosten, M. H. A. J., Cozijnsen, T. J., & De Wit, P. J. G. M. (1994). Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene. Nature, 367, 384–386.
Joosten, M. H. A. J., & De Wit, P. J. G. M. (1999). The tomato-Cladosporium fulvum interaction: a versatile experimental system to study plant-pathogen interactions. Annual Review of Phytopathology, 37, 335–367.
Kalde, M., Nuhse, T. S., Findlay, K., & Peck, S. C. (2007). The syntaxin SYP132 contributes to plant resistance against bacteria and secretion of pathogenesis-related protein 1. Proceedings of the National Academy of Science of the USA, 104, 11850–11855.
Karim, S., Holmström, K.–O., Mandal, A., Dahl, P., Hohmann, S., Brader, G., et al. (2007). AtPTR3, a wound-induced peptide transporter needed for defence against virulent bacterial pathogens in Arabidopsis. Planta, 225, 1431–1445.
Langlois-Meurinne, M., Gachon, C. M. M., & Saindrenan, P. (2005). Pathogen-responsive expression of glycosyltransferase genes UGT73B3 and UGT73B5 is necessary for resistance to Pseudomonas syringae pv. tomato in Arabidopsis. Plant Physiology, 139, 1890–1901.
Lorsch, J. R. (2002). RNA chaperones exist and DEAD box proteins get a life. Cell, 109, 797–800.
Nobuta, K., Okrent, R. A., Stoutemyer, M., Rodibaugh, N., Kempema, L., Wildermuth, M. C., et al. (2007). The GH3 acyl adenylase family member PBS3 regulates salicylic acid-dependent defense responses in Arabidopsis. Plant Physiology, 144, 1144–1156.
Park, W., Li, J., Song, R., Messing, J., & Chen, X. (2002). CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Current Biology, 12, 1484–1495.
Sanderfoot, A. A., Pilgrim, M., Adam, L., & Raikhel, N. V. (2001). Disruption of individual members of Arabidopsis syntaxin gene families indicates each has essential functions. Plant Cell, 13, 659–666.
Stacey, G., Koh, S., Granger, C., & Becker, J. M. (2002). Peptide transport in plants. Trends in Plant Science, 7, 257–263.
Tang, D., Simonich, M. T., & Innes, R. W. (2007). Mutations in LACS2, a long-chain acyl-coenzyme A synthetase, enhance susceptibility to avirulent Pseudomonas syringae but confer resistance to Botrytis cinerea in Arabidopsis. Plant Physiology, 144, 1093–1103.
Thomas, C. M., Jones, D. A., Parniske, M., Harrison, K., Balint-Kurti, P. J., Hatzixanthis, K., et al. (1997). Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell, 9, 2209–2224.
Thomas, C. M., Tang, S., Hammond-Kosack, K., & Jones, J. D. G. (2000). Comparison of the hypersensitive response induced by the Cf-4 and Cf-9 genes in Nicotiana spp. Molecular Plant-Microbe Interactions, 13, 465–469.
Van den Ackerveken, G. F. J. M., Van Kan, J. A. L., & De Wit, P. J. G. M. (1992). Molecular analysis of the avirulence gene avr9 of the fungal tomato pathogen Cladosporium fulvum fully supports the gene-for-gene hypothesis. Plant Journal, 2, 359–366.
Van der Hoorn, R. A., Laurent, F., Roth, R., & De Wit, P. J. G. M. (2000). Agroinfiltration is a versatile tool that facilitates comparative analyses of Avr9/Cf-9-induced and Avr4/Cf-4-induced necrosis. Molecular Plant-Microbe Interactions, 13, 439–446.
Wang, C., Cai, X., & Xu, Y. (2006). Molecular mechanism of interaction between tomato and leaf mold pathogen Cladosporium fulvum. Acta Phytopathologica Sinica, 36, 385–391.
Wang, C., Cai, X., & Zheng, Z. (2005). High humidity represses Cf-4/Avr4- and Cf-9/Avr9-dependent hypersensitive cell death and defense gene expression. Planta, 222, 947–956.
Yang, H., Li, Y., & Hua, J. (2006). The C2 domain protein BAP1 negatively regulates defense responses in Arabidopsis. Plant Journal, 48, 238–248.
Yang, H., Yang, S., Li, Y., & Hua, J. (2007). The Arabidopsis BAP1 and BAP2 genes are general inhibitors of programmed cell death. Plant Physiology, 145, 135–146.
Zhang, Z. G., Feechan, A., Pedersen, C., Newman, M. A., Qiu, J. L., Olesen, K. L., et al. (2007). A SNARE-protein has opposing functions in penetration resistance and defence signalling pathways. Plant Journal, 49, 302–312.
Acknowledgements
We are grateful to Dr. Matthieu Joosten (Wageningen University, The Netherlands) for providing sequences of the ART fragments. This work was financially supported by the National Basic Research Programme of China (grant No. 2006CB101903), the Fok Ying Tong Education Foundation (grant No. 101032), and the National Natural Science Foundation of China (grant nos. 30070492, 30671352).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Table 1
List of newly cloned tomato ACE fragments isolated using cDNA-AFLP (DOC 270 kb)
Supplementary Table 2
Functional overlaps between the ACRE, ART and ACE genes (DOC 55.5 kb)
Rights and permissions
About this article
Cite this article
Zhu, JW., Xu, YP., Zhang, ZX. et al. Transcript profiling for Avr4/Cf-4- and Avr9/Cf-9-dependent defence gene expression. Eur J Plant Pathol 122, 307–314 (2008). https://doi.org/10.1007/s10658-008-9294-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-008-9294-1