Transcriptional profiling of watermelon during its incompatible interaction with Fusarium oxysporum f. sp. niveum

Article

Abstract

Transcriptome profiling of watermelon during its incompatible interactions with Fusarium oxysporum f.sp. niveum (FON) was performed using an Agilent custom microarray, which contains 15,000 probes representing approximately 8,200 watermelon genes. A total of 24, 275, 596, 598, and 592 genes showed significant differential expression in FON-infected plant roots, as compared with mock-inoculated roots, at 0.5, 1, 3, 5 and 8 days post inoculation (dpi), respectively. Bioinformatics analysis of these differentially expressed genes revealed that during the incompatible interaction between watermelon and FON, the expression of a number of pathogenesis-related (PR) genes, transcription factors, signalling/regulatory genes, and cell wall modification genes, was significantly induced. A number of genes for transporter proteins such as aquaporins were down-regulated, indicating that transporter proteins might contribute to the development of wilt symptoms after FON infection. In the incompatible interaction, most genes involved in biosynthesis of jasmonic acid (JA) were expressed stronger and more sustained than those in a compatible interaction in FON-infected tissues. Similarly, genes associated with shikimate-phenylpropanoid-lignin biosynthesis were also induced during the incompatible interaction, but expression of these genes were not changed or repressed in the compatible interaction. Those results demonstrate that JA biosynthesis and shikimate-phenylpropanoid-lignin pathways might play important roles in watermelon against FON infection and thus provides new insights in understanding the molecular basis and signalling network in watermelon plants in response to FON infection. We also performed confocal imaging of watermelon roots infected with the green fluorescent protein (GFP)-tagged FON1 to revealed histological characteristics of the infection.

Keywords

Watermelon Fusarium oxysporum Incompatible interaction Microarrary GFP 

Notes

Acknowledgments

This research was supported by National High Technology Research and Development Program 863 (No.2010AA101907), National Natural Science Foundation of China (No.30972015), the earmarked fund for Modern Agro-industry Technology Research System (No.CARS-26), National Public Benefit (Agricultural) Research Foundation of China (No.20090349-07), the Major Research Plan of Nature Science Foundation of Beijing (No.5100001), China International Science and Technology Cooperation Project (No.2010DFA54310), and 948 Ministry of Agriculture project (No.2008-Z42).

Supplementary material

10658_2011_9833_MOESM1_ESM.doc (81 kb)
Table S1 (DOC 81 kb)

References

  1. Amaral, D. O. J., Lima, M. M. A., Resende, L. V., & Silva, M. V. (2008). Differential gene expression induced by salicylic acid and Fusarium oxysporum f. sp. lycopersici infection, in tomato. Pesquisa Agropecuária Brasileira, 43, 1017–1023.CrossRefGoogle Scholar
  2. Baldo, A., Norelli, J. L., Farrell, R. E., Jr., Bassett, C. L., Aldwinckle, H. S., & Malnoy, M. (2010). Identification of genes differentially expressed during interaction of resistant and susceptible apple cultivars (Malus × domestica) with Erwinia amylovora. BMC Plant Biology, 10, 1.PubMedCrossRefGoogle Scholar
  3. Berrocal-Lobo, M., Molina, A., & Solano, R. (2002). Constitutive expression of Ethylene Response Factor1 in Arabidopsis confers resistance to several necrotrophic fungi. The Plant Journal, 29, 23–32.PubMedCrossRefGoogle Scholar
  4. Bieri, S., Potrykus, I., & Fütterer, J. (2003). Effects of combined expression of antifungal barley seed proteins in transgenic wheat on powdery mildew infection. Molecular Breeding, 11, 37–48.CrossRefGoogle Scholar
  5. Bolstad, B. M., Irizarry, R. A., Åstrand, M., & Speed, T. P. (2003). A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics, 19, 185–193.PubMedCrossRefGoogle Scholar
  6. Chang, P. F. L., Hsu, C. C., Lin, Y. H., Chen, K. S., Huang, J. W., & Liou, T. D. (2008). Histopathology comparison and phenylalanine ammonia lyase (PAL) gene expressions in Fusarium wilt infected watermelons. Australian Journal Agriculture Research, 59, 1146–1155.CrossRefGoogle Scholar
  7. Cheong, Y. H., Kim, C. Y., Chun, H. J., Moon, B. C., Park, H. C., Kim, J. K., et al. (2000). Molecular cloning of a soybean class III beta-1, 3-glucanase gene that is regulated both developmentally and in response to pathogen infection. Plant Science, 154, 71–81.PubMedCrossRefGoogle Scholar
  8. Cosgrove, D. J. (2000). Loosening of plant cell walls by expansins. Nature, 407, 321–326.PubMedCrossRefGoogle Scholar
  9. Creelman, R. A., & Mullet, J. E. (1995). Jasmonic acid distribution and action in plants: Regulation during development and response to biotic and abiotic stress. PANS, 92, 4114–4419.CrossRefGoogle Scholar
  10. Ding, X., Cao, Y., Huang, L., Zhao, J., Xu, C., Li, X., et al. (2008). Activation of the indole-3-acetic acid-amido synthetase GH3-8 suppresses expansin expression and promotes salicylate-and jasmonate-indepent basal immunity in race. The Plant Cell, 20, 228–240.PubMedCrossRefGoogle Scholar
  11. Dowd, C., Wilson, I. W., & McFadden, H. (2004). Gene expression profile changes in cotton root and hypocotyl tissues in response to infection with Fusarium oxysporum f.sp.vasinfectum. Molecular Plant-Microbe Interactions, 17, 654–667.PubMedCrossRefGoogle Scholar
  12. Fujimoto, S. Y., Ohta, M., Usui, A., Shinshi, H., & Ohme-Takagi, M. (2000). Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box–mediated gene expression. The Plant Cell, 12, 393–404.PubMedCrossRefGoogle Scholar
  13. Glazebrook, J. (2001). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology, 43, 205–222.CrossRefGoogle Scholar
  14. Gupta, S., Chakraborti, D., Sengupta, A., Basu, D., & Das, S. (2010). Primary metabolism of chickpea is the initial target of wound inducing early sensed Fusarium oxysporum f. sp. ciceri race1. PloS One, 5, e9030.PubMedCrossRefGoogle Scholar
  15. Huang, Z., Zhang, Z., Zhang, X., Zhang, H., Huang, D., & Huang, R. (2004). Tomato TERF1 modulates ethylene response and enhances osmotic stress tolerance by activating expression of downstream genes. FEBS Letter, 573, 110–116.CrossRefGoogle Scholar
  16. Martyn, R. D., & Netzer, D. (1991). Resistance to races 0, 1 and 2 of Fusarium wilt of watermelon in Citrullus sp. PI296341 FR. Hortscience, 26, 429–432.Google Scholar
  17. Pandey, S. P., & Somssich, I. E. (2009). The role of WRKY transcription factors in plant immunity. Plant Physiology, 150, 1648–1655.PubMedCrossRefGoogle Scholar
  18. Rinaldi, C., Kohler, A., Frey, P., Duchaussoy, F., Ningre, N., Couloux, A., et al. (2007). Transcript profiling of poplar leaves upon infection with compatible and incompatible strains of the foliar rust Melampsora larici-populina. Plant Physiology, 144, 347–366.PubMedCrossRefGoogle Scholar
  19. Sade, N., Vinocur, B. J., Diber, A., Shatil, A., Ronen, G., Nissan, H., et al. (2009). Improving plant stress tolerance and yield production: is the tonoplast aquaporin SlTIP2: A key to isohydric to anisohydric conversion. The New Phytologist, 181, 651–661.PubMedCrossRefGoogle Scholar
  20. Smyth, G. K. (2004). Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Statistical Applications in Genetics and Molecular Biology, 3(1), Article 3.Google Scholar
  21. Stephens, A. E., Gardiner, D. M., White, R. G., Munn, A. L., & Manners, J. M. (2008). Phases of infection and gene expression of Fusarium graminearum during crown rot disease of wheat. Molecular Plant-Microbe Interactions, 21, 1571–1581.PubMedCrossRefGoogle Scholar
  22. Sugimoto, K., Takeda, S., & Hirochika, H. (2000). MYB-related transcription factor NtMYB2 induced by wounding and elicitors is a regulator of the tobacco retrotransposon Tto1 and defense-related genes. The Plant Cell, 12, 2511–2527.PubMedCrossRefGoogle Scholar
  23. Swiader, M., Proñczuk, M., & Niemirowicz-Szczytt, K. (2002). Resistance of polish lines and hybrids of watermelon [citrullus lanatus (thunb.) matsum et nakai] to Fusarium oxysporum at the seedling stage. Journal of Applied Genetics, 43, 161–170.PubMedGoogle Scholar
  24. Uppalapati, S. R., Marek, S. M., Lee, H. K., Nakashima, J., Tang, Y., Sledge, M. K., et al. (2009). Global gene expression profiling during Medicago truncatula–Phymatotrichopsis omnivore interaction reveals a role for jasmonic acid, ethylene, and the flavonoid pathway in disease development. Molecular Plant-Microbe Interactions, 22, 7–17.PubMedCrossRefGoogle Scholar
  25. Vissenberg, K., Martinez-Vilchez, I. M., Verbelen, J. P., Miller, J. G., & Fry, S. C. (2000). In vivo colocalization of xyloglucan endotransglycosylase activity and its donor substrate in the elongation zone of Arabidopsis roots. The Plant Cell, 12, 1229–1237.PubMedCrossRefGoogle Scholar
  26. Wang, J., Guo, C., Zhang, Z., He, Y., & Li, W. (2002). Biochemical and physiological changes of different watermelon cultivars infected by Fusarium oxysporum. Scientia Agricultura Sinica, 35, 1343–1348.Google Scholar
  27. Wang, X., Liu, W., Chen, X., Tang, C., Dong, Y., Ma, J., et al. (2010). Differential gene expression in incompatible interaction between wheat and stripe rust fungus revealed by cDNA-AFLP and comparison to compatible interaction. BMC Plant Biology, 10, 9.PubMedCrossRefGoogle Scholar
  28. Wasternack, C. (2007). Jasmonates: An update on biosynthesis, signal transduction and action in plant stress response, growth and development. Annals of Botany, 100, 681–697.PubMedCrossRefGoogle Scholar
  29. Whetten, R., & Sederoff, R. (1995). Lignin biosynthesis. The Plant Cell, 25, 1001–1013.CrossRefGoogle Scholar
  30. Wu, H., Luo, J., Raza, W., Liu, Y., Gu, M., Chen, G., et al. (2010). Effect of exogenously added ferulic acid on in vitro Fusarium oxysporum f.sp. niveum. Scientia Horticulturae, 124, 448–453.CrossRefGoogle Scholar
  31. Xu, Y., Wang, Y., Ge, X., Song, F., & Zheng, Z. (2000). The relation between the induced constriction resistance and changes in activities of related enzymes in watermelon seedlings after infection by Fusarium oxysporum f. sp. niveum. Journal of Fruit Science, 17, 123–127.Google Scholar
  32. Xu, Y., Guo, S., Zhang, H., Gong, G., Mao, A., & Geng, L. (2008). Construction of watermelon SSH cDNA libraries induced by Fusarium oxysporum and analysis of expressed sequence tags. In M. Pitrat (Ed.), (Paper presented at Cucurbitaceae 2008, Proceedings of the IXth EUCARPIA meeting on genetics and breeding of Cucurbitaceae. INRA, Avignon , France).Google Scholar
  33. Zhang, Z., Zhang, J., Wang, Y., & Zheng, X. (2005). Molecular detection of Fusarium oxysporum f. sp. niveum and Mycosphaerella melonis in infected plant tissues and soil. FEMS Microbiology Letter, 249, 39–47.CrossRefGoogle Scholar
  34. Zhou, X. G., & Everts, K. L. (2010). Race 3, a new and highly virulent race of Fusarium oxysporum f. sp. niveum causing fusarium wilt in watermelon. Plant Disease, 94, 92–98.CrossRefGoogle Scholar
  35. Zhou, X., & Wu, F. (2009). Differentially expressed transcripts from cucumber (Cucumis sativus L.) root upon inoculation with Fusarium oxysporum f. sp. cucumerinum Owen. Physiology Molecular Plant Pathology, 10, 005.Google Scholar

Copyright information

© KNPV 2011

Authors and Affiliations

  1. 1.National Engineering Research Center for VegetablesBeijing People’s Republic of China
  2. 2.Hebei Agricultural UniversityBaodingChina
  3. 3.Department of Plant Protection, College of Agriculture and BiotechnologyZhejiang UniversityHangzhouChina
  4. 4.Boyce Thompson InstituteCornell UniversityIthacaUSA
  5. 5.USDA Robert Holley Center for Agriculture and HealthIthacaUSA

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