Abstract
The mycotoxigenic fungal species Fusarium graminearum is able to attack several important cereal crops, such as wheat and barley. By causing Fusarium Head Blight (FHB) disease, F. graminearum induces yield and quality losses and poses a public health concern due to in planta mycotoxin production. The molecular and physiological plant responses to FHB, and the cellular biochemical pathways used by F. graminearum to complete its infectious process remain still unknown. In this study, a proteomics approach, combining 2D-gel approach and mass spectrometry, has been used to determine the specific protein patterns associated with the development of the fungal infection during grain growth on susceptible wheat. Our results reveal that F. graminearum infection does not deeply alter the grain proteome and does not significantly disturb the first steps of grain ontogeny but impacts molecular changes during the grain filling stage (impact on starch synthesis and storage proteins). The differentially regulated proteins identified were mainly involved in stress and defence mechanisms, primary metabolism, and main cellular processes such as signalling and transport. Our survey suggests that F. graminearum could take advantage of putative susceptibility factors closely related to grain development processes and thus provide new insights into key molecular events controlling the susceptible response to FHB in wheat grains.
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References
Bai, G., & Shaner, G. (2004). Management and resistance in wheat and barley to fusarium head blight. Annual Review of Phytopathology, 42, 135–161.
Bottalico, A., & Perrone, G. (2002). Toxigenic Fusarium species and mycotoxins associated with head blight in small-grain cereals in Europe. European Journal of Plant Pathology, 108(7), 611–624.
Bradford, M. M. (1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254.
Buerstmayr, H., Steiner, B., Hartl, L., Griesser, M., Angerer, N., Lengauer, D., Miedaner, T., Schneider, B., & Lemmens, M. (2003). Molecular mapping of QTLs for Fusarium head blight resistance in spring wheat. II. resistance to fungal penetration and spread. Theoretical and Applied Genetics, 107, 503–508.
Buerstmayr, H., Ban, T., & Anderson, J. A. (2009). QTL mapping and marker-assisted selection for Fusarium head blight resistance in wheat: A review. Plant Breeding, 128(1), 1–26.
Cuthbert, P. A., Somers, D. J., Thomas, J., Cloutier, S., & Brulé-Babel, A. (2006). Fine mapping Fhb1, a major gene controlling fusarium head blight resistance in bread wheat (Triticum aestivum L.). Theoretical and Applied Genetics, 112(8), 1465–1472.
Ding, L., Xu, H., Yi, H., Yang, L., Kong, Z., Zhang, L., et al. (2011). Resistance to hemi-biotrophic F. graminearum infection is associated with coordinated and ordered expression of diverse defense signaling pathways. PloS One, 6(4), e19008.
Dornez, E., Croes, E., Gebruers, K., Carpentier, S., Swennen, R., Laukens, K., et al. (2010). 2-D DIGE reveals changes in wheat xylanase inhibitor protein families due to Fusarium graminearum DeltaTri5 infection and grain development. Proteomics, 10(12), 2303–2319.
Eckardt, N. A. (2002). Plant disease susceptibility genes? The Plant Cell, 14(9), 1983–1986.
Evers, T., & Millar, S. (2002). Cereal grain structure and development: Some implications for quality. Journal of Cereal Science, 36(3), 261–284.
Geddes, J., Eudes, F., Laroche, A., & Selinger, L. B. (2008). Differential expression of proteins in response to the interaction between the pathogen Fusarium graminearum and its host, Hordeum vulgare. Proteomics, 8(3), 545–554.
Giménez, M. J., Pistón, F., & Atienza, S. G. (2011). Identification of suitable reference genes for normalization of qPCR data in comparative transcriptomics analyses in the Triticeae. Planta, 233(1), 163–173.
González-Lamothe, R., El Oirdi, M., Brisson, N., & Bouarab, K. (2012). The conjugated auxin indole-3-acetic acid-aspartic acid promotes plant disease development. The Plant Cell, 24(2), 762–777.
Goswami, R. S., & Kistler, H. C. (2004). Heading for disaster: Fusarium graminearum on cereal crops. Molecular Plant Pathology, 5(6), 515–525.
Gottwald, S., Samans, B., Lück, S., & Friedt, W. (2012). Jasmonate and ethylene dependent defence gene expression and suppression of fungal virulence factors: Two essential mechanisms of Fusarium head blight resistance in wheat? BMC Genomics, 13, 369.
Gunnaiah, R., Kushalappa, A. C., Duggavathi, R., Fox, S., & Somers, D. J. (2012). Integrated metabolo-proteomic approach to decipher the mechanisms by which wheat QTL (Fhb1) contributes to resistance against Fusarium graminearum. PloS One, 7(7), e40695.
Hamzehzarghani, H., Kushalappa, A. C., Dion, Y., Rioux, S., Comeau, A., Yaylayan, V., & Mather, D. E. (2005). Metabolic profiling and factor analysis to discriminate quantitative resistance in wheat cultivars against fusarium head blight. Physiological and Molecular Plant Pathology, 66(4), 119–133.
Hubert, D. A., Tornero, P., Belkhadir, Y., Krishna, P., Takahashi, A., Shirasu, K., & Dangl, J. L. (2003). Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. The EMBO Journal, 22(21), 5679–5689.
Ilgen, P., Hadeler, B., Maier, F. J., & Schäfer, W. (2009). Developing kernel and rachis node induce the trichothecene pathway of Fusarium graminearum during wheat head infection. Molecular Plant-Microbe Interactions, 22(8), 899–908. doi:10.1094/MPMI-22-8-0899.
Jansen, C., von Wettstein, D., Schäfer, W., Kogel, K.-H., Felk, A., & Maier, F. J. (2005). Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proceedings of the National Academy of Sciences of the United States of America, 102(46), 16892–16897. doi:10.1073/pnas.0508467102.
Jubault, M., Lariagon, C., Taconnat, L., Renou, J.-P., Gravot, A., Delourme, R., & Manzanares-Dauleux, M. J. (2013). Partial resistance to clubroot in Arabidopsis is based on changes in the host primary metabolism and targeted cell division and expansion capacity. Functional & Integrative Genomics, 13(2), 191–205.
Jurado, M., Vázquez, C., Patiño, B., & González-Jaén, M. T. (2005). PCR detection assays for the trichothecene-producing species Fusarium graminearum, Fusarium culmorum, Fusarium poae, Fusarium equiseti and Fusarium sporotrichioides. Systematic and Applied Microbiology, 28(6), 562–568.
Kang, G.-Z., Wang, Y.-H., Guo, T.-C., Zhu, Y.-J., & Guan, C.-Y. (2006). Key enzymes in starch synthesis in plants. Zhongguo Yi Chuan Xue Hui Bian Ji, 28(1), 110–116.
Kugler, K. G., Siegwart, G., Nussbaumer, T., Ametz, C., Spannagl, M., Steiner, B., et al. (2013). Quantitative trait loci-dependent analysis of a gene co-expression network associated with Fusarium head blight resistance in bread wheat (Triticum aestivum L.). BMC Genomics, 14, 728.
Lawrence Bogorad, E. J. G. (1983). [17] Cloning and physical mapping of maize plastid genes. Methods in Enzymology, 97, 524–554. doi:10.1016/0076-6879(83)97160-4.
Li, S., Ji, R., Dudler, R., Yong, M., Deng, Q., Wang, Z., & Hu, D. (2013). Wheat gene TaS3 contributes to powdery mildew susceptibility. Plant Cell Reports. doi:10.1007/s00299-013-1501-7.
Ma, H., Bai, G., Gill, G., & Hart, L. (2006). Deletion of a chromosome arm altered wheat resistance to fusarium head blight and deoxynivalenol accumulation in chinese spring. Plant Disease, 90, 1545–1549.
Mesterházy, A. (1995). Types and components of resistance to Fusarium head blight of wheat. Plant Breeding, 114(5), 377–386.
Miller, J. D., Young, J. C., & Sampson, D. R. (1985). Deoxynivalenol and Fusarium head blight resistance in spring cereals. Journal of Phytopathology, 113(4), 359–367.
Nadaud, I., Girousse, C., Debiton, C., Chambon, C., Bouzidi, M. F., Martre, P., & Branlard, G. (2010). Proteomic and morphological analysis of early stages of wheat grain development. Proteomics, 10(16), 2901–2910.
Pathuri, I. P., Reitberger, I. E., Hückelhoven, R., & Proels, R. K. (2011). Alcohol dehydrogenase 1 of barley modulates susceptibility to the parasitic fungus Blumeria graminis f.sp. hordei. Journal of Experimental Botany, 62(10), 3449–3457.
Pavan, S., Jacobsen, E., Visser, R. G. F., & Bai, Y. (2010). Loss of susceptibility as a novel breeding strategy for durable and broad-spectrum resistance. Molecular Breeding: New Strategies In Plant Improvement, 25(1), 1–12.
Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 29(9), e45.
Rabilloud, T. (2002). Two-dimensional gel electrophoresis in proteomics: old, old fashioned, but it still climbs up the mountains. Proteomics, 2(1), 3–10.
Rogers, S. O., & Bendich, A. J. (1994). Extraction of total cellular DNA from plants, algae and fungi. In S. B. Gelvin & R. A. Schilperoort (Eds.), Plant molecular biology manual (pp. 183–190). Netherlands: Springer.
Schroeder, H. W. (1963). Factors affecting resistance of wheat to scab caused by Gibberella zeae (Schw.) Petch. doi:oclc/17921162
Tasleem-Tahir, A., Nadaud, I., Chambon, C., & Branlard, G. (2012). Expression profiling of starchy endosperm metabolic proteins at 21 stages of wheat grain development. Journal of Proteome Research, 11(5), 2754–2773.
Wang, K. K., Posner, A., & Hajimohammadreza, I. (1996). Total protein extraction from cultured cells for use in electrophoresis and western blotting. BioTechniques, 20(4), 662–668.
Xiao, J., Jin, X., Jia, X., Wang, H., Cao, A., Zhao, W., et al. (2013). Transcriptome-based discovery of pathways and genes related to resistance against Fusarium head blight in wheat landrace Wangshuibai. BMC Genomics, 14, 197.
Yang, F., Jensen, J. D., Spliid, N. H., Svensson, B., Jacobsen, S., Jørgensen, L. N., et al. (2010a). Investigation of the effect of nitrogen on severity of Fusarium head blight in barley. Journal of Proteomics, 73(4), 743–752.
Yang, F., Jensen, J. D., Svensson, B., Jørgensen, H. J. L., Collinge, D. B., & Finnie, C. (2010b). Analysis of early events in the interaction between Fusarium graminearum and the susceptible barley (Hordeum vulgare) cultivar Scarlett. Proteomics, 10(21), 3748–3755.
Yang, F., Jensen, J. D., Svensson, B., Jørgensen, H. J. L., Collinge, D. B., & Finnie, C. (2012). Secretomics identifies Fusarium graminearum proteins involved in the interaction with barley and wheat. Molecular Plant Pathology, 13(5), 445–453.
Yang, F., Jacobsen, S., Jørgensen, H. J. L., Collinge, D. B., Svensson, B., & Finnie, C. (2013). Fusarium graminearum and its interactions with cereal heads: Studies in the proteomics Era. Frontiers in Plant Science, 4, 37.
Zantinge, K. K. (2010). Comparison of barley seed proteomic profiles associated with fusarium head blight reaction. Canadian Journal of Plant Pathology, 32(4), 496–512.
Zhang, X., Fu, J., Hiromasa, Y., Pan, H., & Bai, G. (2013). Differentially expressed proteins associated with fusarium head blight resistance in wheat. PloS One, 8(12), e82079.
Zhou, W. C., Kolb, F. L., Bai, G. H., Domier, L. L., & Yao, J. B. (2002). Effect of individual Sumai 3 chromosomes on resistance to scab spread within spikes and deoxynivalenol accumulation within kernels in wheat. Hereditas, 137(2), 81–89.
Zhou, W., Kolb, F. L., & Riechers, D. E. (2005). Identification of proteins induced or upregulated by Fusarium head blight infection in the spikes of hexaploid wheat (Triticum aestivum). Genome, 48(5), 770–780. doi:10.1139/g05-041.
Acknowledgments
We thank members of the Experimental Unit INRA 1375 PHACC (INRA Center of Clermont-Theix, France) for plants production, Christophe Chambon and Didier Viala from PFEM (INRA Center of Clermont-Theix, France) for mass spectrometry analyses. This study is part of CC PhD work, funded by the French National Institute for Agronomic Research (INRA).
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Chetouhi, C., Bonhomme, L., Lecomte, P. et al. A proteomics survey on wheat susceptibility to Fusarium head blight during grain development. Eur J Plant Pathol 141, 407–418 (2015). https://doi.org/10.1007/s10658-014-0552-0
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DOI: https://doi.org/10.1007/s10658-014-0552-0