Abstract
Tunisia is one of the main producers of durum wheat, the most consumed cereal in Tunisia and represents a trademark of several local dishes such as couscous and bulgur. Nonetheless and despite its leading stand in the local consumption and commercial share, a scarcity in Tunisian durum wheat production has long been a major problem obstructing the fulfilment of the increasing local demand. Septoria tritici blotch (STB) caused by Zymoseptoria tritici (Z. tritici) is one of the most common and detrimental foliar disease on durum wheat in Tunisia causing considerable yield losses. To-date and despite the damaging effects of STB on durum wheat, limited sources of resistance to Z. tritici have been identified. In this present study, we assessed necrosis and pycnidia development of a collection of 304 Tunisian durum wheat landraces representative of 11 landrace populations and artificially inoculated with Z. tritici at the seedling stage under controlled conditions and at the adult plant stage under field conditions. Based on necrosis and pycnidia scores, a hierarchical classification analysis clustered the durum wheat landraces into three phenotypic classes of response to Z. tritici, namely resistant, intermediate and susceptible genotypes. While resistant plants represented the most frequent class at the seedling stage, susceptible phenotypes were more frequent at the adult plant stage. Nevertheless, a heat map correlation study showed that resistant landraces with low-percentages of necrosis and pycnidia at seedling and adult plant stages represented the dominant group within the tested collection. Moreover, the assessed frequencies per landrace populations of the resistant, the intermediate and the susceptible accessions to Z. tritici infection at the adult plant stage for pycnidia development has shown that the landrace populations Badri, Jneh Khotifa (JK), Mekki and Taganrog were the highest resistant accessions, in contrast to the landrace populations Biskri, Mahmoudi, Azizi and Biada where susceptible genotypes were predominant. Mahmoudi and Azizi represented the most variable landrace populations encompassing the three phenotypic classes. Our results highlight that Tunisian durum wheat landraces may harbour variable and stable sources of resistance to Z. tritici at seedling and adult plant stages, which would represent a good basis for further investigation and deployment in breeding programs to enhance STB resistance.
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References
Addinsoft, S. (2010). XLSTAT software, version 9.0. Addinsoft, Paris, France.
Adhikari, T. B., Anderson, J. M., & Goodwin, S. B. (2003). Identification and molecular mapping of a gene in wheat conferring resistance to Mycosphaerella graminicola. Phytopathology, 93, 1158–1164.
Adhikari, T. B., Cavaletto, J. R., Dubcovsky, J., Gieco, J. O., Schlatter, A. R., & Goodwin, S. B. (2004). Molecular mapping of the Stb4 Gene for resistance to Septoria tritici blotch in wheat. Phytopathology, 94, 1198–1206.
Aouini, L. (2018). Durum wheat and septoria tritici blotch: Genes and prospects for breeding. PhD dissertation Wageningen University, https://library.wur.nl/WebQuery/wurpubs/fulltext/443719.
Arraiano, L. S., Worland, A. J., Ellerbrook, C., & Brown, J. K. (2001). Chromosomal location of a gene for resistance to septoria tritici blotch (Mycosphaerella graminicola) in the hexaploid wheat ‘synthetic 6x’. Theoretical and Applied Genetics, 103, 758–764.
Baloch, F. S., Alsaleh, A., Shahid, M. Q., Çiftçi, V., de Miera, L. E. S., Aasim, M., Nadeem, M. A., Aktaş, H., Özkan, H., & Hatipoğlu, R. (2017). A whole genome DArTseq and SNP analysis for genetic diversity assessment in durum wheat from central fertile crescent. PLoS One, 12, e0167821.
Bansal,U. K., Kazi, A. G., Singh, B., Hare, R. A., & Bariana, H. S. (2014). Mapping of durable stripe rust resistance in a durum wheat cultivar Wollaroi. Molecular breeding, 33(1), 51–59.
Ben M’Barek, S. B., Karisto, P., Fakhfakh, M., Kouki, H., Mikaberidze, A., & Yahyaoui, A. (2019). Improved control of Septoria tritici blotch in durum wheat using cultivar mixtures. BioRxiv, 664078.
Berraies, S., Ammar, K., Salah Gharbi, M., Yahyaoui, A., & Rezgui, S. (2014). Quantitative inheritance of resistance to Septoria tritici blotch in durum wheat in Tunisia. Chilean Journal of Agricultural Research, 74, 35–40.
Borlaug, N.E. (2002). The green revolution revisited and the road ahead. Nobelprize.org.
Brown, J. K. (2015). Durable resistance of crops to disease: A Darwinian perspective. Annual Review of Phytopathology, 53, 513–539.
Brown, J. K., Kema, G. H. J., Forrer, H. R., Verstappen, E., Arraiano, L. S., Brading, P., Foster, E., Fried, P., & Jenny, E. (2001). Resistance of wheat cultivars and breeding lines to septoria tritici blotch caused by isolates of Mycosphaerella graminicola in field trials. Plant Pathology, 50, 325–338.
Brown, J. K., Chartrain, L., Lasserre-Zuber, P., & Saintenac, C. (2015). Genetics of resistance to Zymoseptoria tritici and applications to wheat breeding. Fungal Genetics and Biology, 79, 33–41.
Castro, A. J., Chen, X., Corey, A., Filichkina, T., Hayes, P. M., Mundt, C., Richardson, K., Sandoval-Islas, S., & Vivar, H. (2003). Pyramiding and validation of quantitative trait locus (QTL) alleles determining resistance to barley stripe rust. Crop Science, 43, 2234–2239.
Chakraborty, S., Tiedemann, A. V., & Teng, P. S. (2000). Climate change: Potential impact on plant diseases. Environmental Pollution, 108, 317–326.
Chartrain, L., Brading, P. A., Widdowson, J. P., & Brown, J. K. M. (2004). Partial resistance to Septoria tritici blotch (Mycosphaerella graminicola) in wheat cultivars Arina and Riband. Phytopathology, 94(5), 497–504.
Chartrain, L., Berry, S., & Brown, J. K. (2005). Resistance of wheat line Kavkaz-K4500 L. 6. A. 4 to Septoria tritici blotch controlled by isolate-specific resistance genes. Phytopathology, 95, 664–671.
Condorelli, G. E., Maccaferri, M., Newcomb, M., Andrade-Sanchez, P., White, J. W., French, A. N., Sciara, G., Ward, R., & Tuberosa, R. (2018). Comparative aerial and ground based high throughput Phenotyping for the Genetic dissection of NDVI as a proxy for drought adaptive traits in durum wheat. Frontiers in Plant Science, 9, 893.
Cowger, C., Hoffer, M. E., & Mundt, C. C. (2000). Specific adaptation by Mycosphaerella graminicola to a resistant wheat cultivar. Plant Pathology, 49.
El Felah, M., Gharbi, M. S., Ben Ghanem, H., Elloumi, M. (2015). Les Céréales en Tunisie entre Mythe et Réalité = Cereals in Tunisia between Myth and Reality. In: Annales de l'Inrat, 389 (3563), 1–17.
Fabricant, F. (1998). Rome’s glory is now Tunisia’s. New York Times.
FAO. 2017. Country fact sheet on food and agriculture policy trends. Socio-economic context and role of agriculture. Food and Agriculture Policy Decision Analysis (FAPDA). Rome: FAO. Available at http://www.fao.org/3/a-i7738e.pdf.
Faris, J. D. (2014). Wheat domestication: Key to agricultural revolutions past and future, in Genomics of Plant Genetic Resources, Vol. 1. Managing, Sequencing and Mining Genetic Resources, Tuberosa, R., Graner, A., Frison, E., Eds. (Springer, 2014), pp. 439–464
Fayaz, F., Sarbarzeh, M. A., Talebi, R., Azadi, A. (2019). Genetic Diversity and Molecular Characterization of Iranian Durum Wheat Landraces (Triticum turgidum durum (Desf.) Husn.) Using DArT Markers. Biochemical genetics, 57(1), 98-116.
Ferjaoui, S., Sbei, A., Aouadi, N., & Hamza, S. (2011). Monogenic inheritance of resistance to septoria tritici blotch in durum wheat ‘Agili’. International Journal of Plant Breeding, 5, 17–20.
Ferjaoui, S., M’Barek, S., Bahri, B., Slimane, R., & Hamza, S. (2015). Identification of resistance sources to septoria tritici blotch in old Tunisian durum wheat germplasm appliad for the analysis of the Zymoseptoria tritici-durum wheat interaction. Journal of Plant Pathology, 97, 471–481.
Ghaffary, S. M. T. (2011). Efficacy and mapping of resistance to Mycosphaerella graminicola in wheat. PhD dissertation, Wageningen University, https://library.wur.nl/WebQuery/wurpubs/406468.
Ghaffary, S. M. T., Faris, J. D., Friesen, T. L., Visser, R. G., Van der Lee, T. A., Robert, O., & Kema, G. H. J. (2012). New broad-spectrum resistance to septoria tritici blotch derived from synthetic hexaploid wheat. Theoretical and Applied Genetics, 124, 125–142.
Gharbi, M., Deghais, M., Ben Amar, F. (2000). Breeding for resistance to Septoria tritici in durum wheat. Proceedings of Durum Wheat Conference, Zaragoza 2000, pp 397–401.
Goodwin, S. B., Ben M'Barek, S., Dhillon, B., Wittenberg, A. H. J., Crane, C. F., & Hane, J. K. (2011). Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genetics, 7(6), e1002070.
Hartmann, F. E., & Croll, D. (2017). Distinct trajectories of massive recent gene gains and losses in populations of a microbial eukaryotic pathogen. Molecular Biology and Evolution, 34, 2808–2822.
Jacobs,T.H, Parlevliet, J.E., eds, 1993. Durability of Disease Resistance. Dordrecht, the Netherlands: Kluwer Academic Publishers.
Kabbaj, H., Sall, A. T., Al-Abdallat, A., Geleta, M., Amri, A., Filali-Maltouf, A., Belkadi, B., Ortiz, R., & Bassi, F. M. (2017). Genetic diversity within a global panel of durum wheat (Triticum durum) landraces and modern germplasm reveals the history of alleles exchange. Frontiers in Plant Science, 8, 1277.
Kema, G. H. J., & Van Silfhout, C. H. (1997). Genetic variation for virulence and resistance in the wheat-Mycosphaerella graminicola pathosystem III. Comparative seedling and adult plant experiments. Phytopathology, 87, 266–272.
Kema, G. H. J., Annone, J., Sayoud, R., Van Silfhout, C., Van Ginkel, M., & De Bree, J. (1996a). Genetic variation for virulence and resistance in the wheat-Mycosphaerella graminicola pathosystem. I: Interactions between pathogen isolates and host cultivars. Phytopathology, 86, 200–212.
Kema, G. H. J., Sayoud, R., Annone, J., & Van Silfhout, C. (1996b). Genetic variation for virulence and resistance in the wheat-Mycosphaerella graminicola pathosystem. II: analysis of interactions between pathogen isolates and host cultivars. Phytopathology, 86, 213–220.
Kema, G. H. J., Gohari, A. M., Aouini, L., Gibriel, H. A., Ware, S. B., Van Den Bosch, F., Manning-Smith, R., Alonso-Chavez, V., Helps, J., & M’Barek, S. B. (2018). Stress and sexual reproduction affect the dynamics of the wheat pathogen effector AvrStb6 and strobilurin resistance. Nature Genetics, 50, 375.
Kidane, Y. G., Hailemariam, B. N., Mengistu, D. K., Fadda, C., Pè, M. E., & Dell'Acqua, M. (2017). Genome-wide association study of Septoria tritici blotch resistance in Ethiopian durum wheat landraces. Frontiers in Plant Science, 8, 1586.
Latiri, K., Lhomme, J. P., Annabi, M., & Setter, T. L. (2010). Wheat production in Tunisia: Progress, inter-annual variability and relation to rainfall. European Journal of Agronomy, 33, 33–42.
Lopes, M. S., El-Basyoni, I., Baenziger, P. S., Singh, S., Royo, C., Ozbek, K., Aktas, H., Ozer, E., Ozdemir, F., & Manickavelu, A. (2015). Exploiting genetic diversity from landraces in wheat breeding for adaptation to climate change. Journal of Experimental Botany, 66(12), 3477–3486.
Luck, J., Spackman, M., Freeman, A., Tre˛ bicki, P., Griffiths, W., Finlay, K., & Chakraborty, S. (2011). Climate change and diseases of food crops. Plant Pathology, 60, 113–121.
Ma, H., Singh, R., & Mujeeb-Kazi, A. (1995). Resistance to stripe rust in Triticum turgidum, T. tauschii and their synthetic hexaploids. Euphytica, 82, 117–124.
Madden, L.V., Hughes G., Van den Bosch, F. (2007). The study of plant disease epidemics. APS, St Paul, MN.
Marzario, S., Logozzo, G., David, J., Zeuli, P., & Gioia, T. (2018). Molecular genotyping (SSR) and agronomic phenotyping for utilization of durum wheat (Triticum durum Desf.) ex situ collection from southern Italy: A combined approach including pedigreed varieties. Genes, 9(10), 465.
McCartney, C., Brûlé-Babel, A., Lamari, L., & Somers, D. (2003). Chromosomal location of a race-specific resistance gene to Mycosphaerella graminicola in the spring wheat ST6. Theoretical and Applied Genetics, 107, 1181–1186.
McDonald, B. A., & Mundt, C. C. (2016). How knowledge of pathogen population biology informs management of Septoria tritici blotch. Phytopathology, 106, 948–955.
McDonald, B. A., & Stukenbrock, E. H. (2016). Rapid emergence of pathogens in agro-ecosystems: Global threats to agricultural sustainability and food security. Philosophical Transactions of the Royal Society, B: Biological Sciences, 371(1709), 20160026.
Medini, M., & Hamza, S. (2008). Pathotype and molecular characterisation of Mycosphaerella graminicola isolates collected from Tunisia, Algeria and Canada. Journal of Plant Pathology, 90, 65–73.
Medini, M., Ferjaoui, S., Bahri, B., Mhiri, W., Hattab, S., & Hamza, S. (2014). Bulk segregant analysis and marker-trait association reveal common AFLP markers for resistance to septoria leaf blotch in Tunisian old durum wheat. Biotechnologie, Agronomie, Société et Environnement, 18(1), 3.
Meile, L., Croll, D., Brunner, P. C., Plissonneau, C., Hartmann, F. E., McDonald, B. A., & Sánchez-Vallet, A. (2018). A fungal avirulence factor encoded in a highly plastic genomic region triggers partial resistance to septoria tritici blotch. New Phytologist, 219, 1048–1061.
Mundt, C. C. (2014). Durable resistance: A key to sustainable management of pathogens and pests. Infection, Genetics and Evolution, 27, 446–455.
Mundt, C. C., Cowger, C., & Garrett, K. A. (2002). Relevance of integrated disease management to resistance durability. Euphytica, 124, 245–252.
Nefzaoui, A., Ketata, H., Elmourid, M. (2012). Agricultural technological and institutional innovations for enhanced adaptation to environmental change in North Africa, p 29. Available from https://www.intechopen.com.
Nelson,R., Wiesner-Hanks, T.,Wisser, R., Balint-Kurti, P. (2018). Navigating complexity to breed disease-resistant crops. Nature Reviews Genetics, 19(1), 21–33.
Newton, A. C., Johnson, S. N., & Gregory, P. J. (2011). Implications of climate change for diseases, crop yields and food security. Euphytica, 179, 3–18.
Oliveira, H. R., Campana, M. G., Jones, H., Hunt, H. V., Leigh, F., Redhouse, D. I., Lister, D. L., & Jones, M. K. (2012). Tetraploid wheat landraces in the Mediterranean basin: Taxonomy, evolution and genetic diversity. PLoS One, 7(5), e37063.
Orton, E. S., Deller, S., & Brown, J. K. (2011). Mycosphaerella graminicola: from genomics to disease control. Molecular Plant Pathology, 12, 413–424.
Parlevliet, J.E. (1993). What is durable resistance, a general outline. In: Th. Jacobs,T.H. and Parlevliet J.E. (Eds.), Durability of Disease Resistance, pp. 23–39. Kluwer Academic Publishers, Dordrecht, The Netherlands.
Sadok, W., Schoppach, R., Ghanem, M. E., Zucca, C., & Sinclair, T. R. (2019). Wheat drought-tolerance to enhance food security in Tunisia, birthplace of the Arab spring. European Journal of Agronomy, 107, 1–9.
Sánchez-Vallet, A., Fouché, S., Fudal, I., Hartmann, F. E., Soyer, J. L., Tellier, A., & Croll, D. (2018). The genome biology of effector gene evolution in filamentous plant pathogens. Annual Review of Phytopathology, 56, 21–40.
Smale, M. (1997). The green revolution and wheat genetic diversity: Some unfounded assumptions. World Development, 25(8), 1257–1269.
Soriano, J. M., Villegas, D., Aranzana, M. J., del Moral, L. F. G., & Royo, C. (2016). Genetic structure of modern durum wheat cultivars and Mediterranean landraces matches with their agronomic performance. PLoS One, 11(8), e0160983.
Soriano, J. M., Villegas, D., Sorrells, M. E., & Royo, C. (2018). Durum wheat landraces from east and west regions of the Mediterranean Basin are genetically distinct for yield components and phenology. Frontiers in Plant Science, 9, 80.
Taher, K., Graf, S., Fakhfakh, M. M., Salah, H. B., Yahyaoui, A., Rezgui, S., Nasraoui, B., & Stammler, G. (2014). Sensitivity of Zymoseptoria tritici isolates from Tunisia to Pyraclostrobin, Fluxapyroxad, Epoxiconazole, Metconazole, Prochloraz and Tebuconazole. Journal of Phytopathology, 162, 442–448.
R Development Core Team (2013). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Zadoks, J. C., Chang, T. T., & Konzak, C. F. (1974). A decimal code for the growth stages of cereals. Weed Research, 14, 415–421.
Zhong, Z., Marcel, T. C., Hartmann, F. E., Ma, X., Plissonneau, C., Zala, M., Ducasse, A., Confais, J., Compain, J., & Lapalu, N. (2017). A small secreted protein in Zymoseptoria tritici is responsible for avirulence on wheat cultivars carrying the Stb6 resistance gene. New Phytologist, 214(2), 619–631.
Acknowledgements
We are thankful to Zied Hammami and Hanen Sbei for their help with statistical analysis, Martin Willigsecker and Béatrice Beauzoone from INRA Bioger for their help in setting-up the seedling assays. The research was supported by the federated project untitled “Identification of durum wheat resistant genotypes to biotic and drougth stress and their valorization for sustainable agriculture” acronym RESIDUR, supported by IRESA under the Tunisian Ministry of Agriculture.
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Ouaja, M., Aouini, L., Bahri, B. et al. Identification of valuable sources of resistance to Zymoseptoria tritici in the Tunisian durum wheat landraces. Eur J Plant Pathol 156, 647–661 (2020). https://doi.org/10.1007/s10658-019-01914-9
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DOI: https://doi.org/10.1007/s10658-019-01914-9