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Genetic diversity of Australian Fusarium pseudograminearum populations causing crown rot in wheat

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Abstract

Fusarium crown rot (FCR) caused by the fungus Fusarium pseudograminearum (Fp) is an important disease of wheat that reduces yield and grain quality in many countries, including Australia. In this study, we investigated mating type idiomorph composition, putative chemotype and population genotypic structure of 98 Fp isolates from Western Australia (WA) and the eastern Australian states of New South Wales, Victoria and South Australia. Our results revealed the expected 1:1 mating type ratio for isolates from the eastern states while there was significant variation to a 1:1 mating type composition with isolates from WA. A chemotype-specific PCR assay indicated that all Fp isolates from eastern states and WA segregated for the 3-ADON trichothecene chemotype. Genetic diversity assessed using 21 cleaved amplified polymorphic sequence markers revealed a high level of genotypic variation within and between Fp populations from eastern Australian states and WA. Analysis of molecular variance (AMOVA) showed significant difference between populations from eastern states and WA. The genetic diversity measured by Shannon index ranged from 0.95 to 2.30 with the lowest and highest values detected in Hart and Rowena populations, respectively in the eastern states. Index of association analysis showed no significant linkage of markers among isolates within 60% of the populations, suggesting that sexual reproduction may be occurring in the pathogen from those locations. These results improve understanding of Fp population dynamics across Australia and highlight the importance of monitoring for shifts in the population which could have implications for disease management.

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References

  • Abramson, D., Clear, R., & Smith, D. (1993). Trichothecene production by Fusarium spp. isolated from Manitoba grain. Canadian Journal of Plant Pathology, 15(3), 147–152.

    CAS  Google Scholar 

  • Akinsanmi, O., Mitter, V., Simpfendorfer, S., Backhouse, D., & Chakraborty, S. (2004). Identity and pathogenicity of Fusarium spp. isolated from wheat fields in Queensland and northern New South Wales. Crop & Pasture Science, 55(1), 97–107.

    Google Scholar 

  • Akinsanmi, O., Backhouse, D., Simpfendorfer, S., & Chakraborty, S. (2006). Genetic diversity of Australian Fusarium graminearum and F. pseudograminearum. Plant Pathology, 55(4), 494–504.

    CAS  Google Scholar 

  • Alahmad, S., Simpfendorfer, S., Bentley, A., & Hickey, L. (2018). Crown rot of wheat in Australia: Fusarium pseudograminearum taxonomy, population biology and disease management. Australasian Plant Pathology, 47(3), 285–299.

    Google Scholar 

  • Aoki, T., & O’Donnell, K. (1999). Morphological characterization of Gibberella coronicola sp. nov., obtained through mating experiments of Fusarium pseudograminearum. Mycoscience, 40(6), 443–453.

    Google Scholar 

  • Bentley, A. R., Burgess, L. W., & Summerell, B. A. (2005). Genetic diversity in field populations of Fusarium pseudograminearum. In Proceedings of the 15th biennial Australasian Plant Pathology Society, (pp. P.382).

  • Bentley, A. R., Leslie, J. F., Liew, E. C., Burgess, L. W., & Summerell, B. A. (2008a). Genetic structure of Fusarium pseudograminearum populations from the Australian grain belt. Phytopathology, 98(2), 250–255.

    PubMed  Google Scholar 

  • Bentley, A. R., Summerell, B. A., & Burgess, L. W. (2008b). Sexual compatibility in Fusarium pseudograminearum (Gibberella coronicola). Mycological Research, 112(9), 1101–1106.

    PubMed  Google Scholar 

  • Bockus, W. W., Appel, J. A., Bowden, R. L., Fritz, A. K., Gill, B. S., Martin, T. J., Sears, R. G., Seifers, D. L., Brown-Guedira, G. L., & Eversmeyer, M. G. (2001). Success stories: breeding for wheat disease resistance in Kansas. Plant Disease, 85(5), 453–461.

    PubMed  Google Scholar 

  • Burgess, L. (2001). Crown rot of wheat. In ‘Fusarium: Paul E. Nelson memorial symposium’.(Eds BA Summerell, JF Leslie, D Backhouse, WL Bryden, LW Burgess) pp. 271–294. APS Press: St Paul, MN.

  • Chakraborty, S., Liu, C. J., Mitter, V., Scott, J. B., Akinsanmi, O. A., Ali, S., Dill-Macky, R., Nicol, J., Backhouse, D., & Simpfendorfer, S. (2006). Pathogen population structure and epidemiology are keys to wheat crown rot and Fusarium head blight management. Australasian Plant Pathology, 35(6), 643–655. https://doi.org/10.1071/AP06068.

    Article  Google Scholar 

  • Core Team, R. (2017). R: a language and environment for statistical computing. Vienna: R foundation for statistical computing.

    Google Scholar 

  • De Boevre, M., Di Mavungu, J. D., Landschoot, S., Audenaert, K., Eeckhout, M., Maene, P., et al. (2012). Natural occurrence of mycotoxins and their masked forms in food and feed products. World Mycotoxin Journal, 5(3), 207–219.

    Google Scholar 

  • Excoffier, L., & Lischer, H. E. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and windows. Molecular Ecology Resources, 10(3), 564–567.

    PubMed  Google Scholar 

  • Forknall, C. R., Simpfendorfer, S., & Kelly, A. M. (2019). Using yield response curves to measure variation in the tolerance and resistance of wheat cultivars to Fusarium crown rot. Phytopathology, 109(6), 932–941.

    PubMed  Google Scholar 

  • Francis, R. G., & Burgess, L. (1977). Characteristics of two populations of Fusarium roseum ‘Graminearum’ in eastern Australia. Transactions of the British Mycological Society, 68(3), 421–427.

    Google Scholar 

  • Gardiner, D. M., McDonald, M. C., Covarelli, L., Solomon, P. S., Rusu, A. G., Marshall, M., Kazan, K., Chakraborty, S., McDonald, B. A., & Manners, J. M. (2012). Comparative pathogenomics reveals horizontally acquired novel virulence genes in fungi infecting cereal hosts. PLoS Pathogens, 8(9), e1002952.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gardiner, D. M., Benfield, A. H., Stiller, J., Stephen, S., Aitken, K., Liu, C., & Kazan, K. (2018). A high-resolution genetic map of the cereal crown rot pathogen Fusarium pseudograminearum provides a near-complete genome assembly. Molecular Plant Pathology, 19(1), 217–226.

    CAS  PubMed  Google Scholar 

  • Gargouri, S., Mtat, I., Kammoun, L. G., Zid, M., & Hajlaoui, M. R. (2011). Molecular genetic diversity in populations of Fusarium pseudograminearum from Tunisia. Journal of Phytopathology, 159(4), 306–313.

    Google Scholar 

  • Geiser, D. M., del Mar Jiménez-Gasco, M., Kang, S., Makalowska, I., Veeraraghavan, N., Ward, T. J., Zhang, N., Kuldau, G. A., & O'donnell, K. (2004). FUSARIUM-ID v. 1.0: A DNA sequence database for identifying Fusarium. European Journal of Plant Pathology, 110(5–6), 473–479.

    CAS  Google Scholar 

  • Jurgenson, J., Bowden, R., Zeller, K., Leslie, J., Alexander, N., & Plattner, R. (2002). A genetic map of Gibberella zeae (Fusarium graminearum). Genetics, 160(4), 1451–1460.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kazan, K., & Gardiner, D. M. (2018). Fusarium crown rot caused by Fusarium pseudograminearum in cereal crops: recent progress and future prospects. Molecular Plant Pathology, 19(7), 1547–1562.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kerényi, Z., Moretti, A., Waalwijk, C., Oláh, B., & Hornok, L. (2004). Mating type sequences in asexually reproducing Fusarium species. Applied and Environmental Microbiology, 70(8), 4419–4423.

    PubMed  PubMed Central  Google Scholar 

  • Khudhair, M., Thatcher, L., Gardiner, D., Kazan, K., Roper, M., Aitken, E., et al. (2019). Comparative analysis of genetic structures and aggressiveness of Fusarium pseudograminearum populations from two surveys undertaken in 2008 and 2015 at two sites in the wheat belt of Western Australia. Plant Pathology, 68(7), 1337–1349.

    Google Scholar 

  • Kirkegaard, J., Simpfendorfer, S., Holland, J., Bambach, R., Moore, K., & Rebetzke, G. (2004). Effect of previous crops on crown rot and yield of durum and bread wheat in northern NSW. Crop & Pasture Science, 55(3), 321–334.

    Google Scholar 

  • McDonald, B. A., & Linde, C. (2002). The population genetics of plant pathogens and breeding strategies for durable resistance. Euphytica, 124(2), 163–180.

    CAS  Google Scholar 

  • Miedaner, T., Schilling, A. G., & Geiger, H. H. (2001). Molecular genetic diversity and variation for aggressiveness in populations of Fusarium graminearum and Fusarium culmorum sampled from wheat fields in different countries. Journal of Phytopathology, 149, 641–648.

    CAS  Google Scholar 

  • Mishra, P. K., Fox, R. T. V., & Culham, A. (2003). Inter-simple sequence repeat and aggressiveness analyses revealed high genetic diversity, recombination and long-range dispersal in Fusarium culmorum. Annals of Applied Biology, 143, 291–301.

    CAS  Google Scholar 

  • Mishra, P. K., Tewari, J. P., Clear, R. M., & Turkington, T. K. (2006). Genetic diversity and recombination within populations of Fusarium pseudograminearum from western Canada. International Microbiology, 9(1), 65–68.

    CAS  PubMed  Google Scholar 

  • Monds, R. D., Cromey, M. G., Lauren, D. R., di Menna, M., & Marshall, J. (2005). Fusarium graminearum, F. cortaderiae and F. pseudograminearum in New Zealand: molecular phylogenetic analysis, mycotoxin chemotypes and co-existence of species. Mycological Research, 109(4), 410–420. https://doi.org/10.1017/S0953756204002217.

    Article  CAS  PubMed  Google Scholar 

  • Moolhuijzen, P. M., Manners, J. M., Wilcox, S. A., Bellgard, M. I., & Gardiner, D. M. (2013). Genome sequences of six wheat-infecting Fusarium species isolates. Genome Announcements, 1(5), e00670–e00613.

    PubMed  PubMed Central  Google Scholar 

  • Murray, G. M., & Brennan, J. P. (2009). Estimating disease losses to the Australian wheat industry. Australasian Plant Pathology, 38(6), 558–570. https://doi.org/10.1071/AP09053.

    Article  Google Scholar 

  • Nicol, J., Bagci, A., Hekimhan, H., Bolat, N., Braun, H., & Trethowan, R. (2004). Strategy for the identification and breeding of resistance to dryland root rot complex for international spring and winter wheat breeding programs. In Proceedings of the 4th International Crop Science Congress, 26th Sep–1st Oct.

  • Ophel-Keller, K., McKay, A., Hartley, D., & Curran, J. (2008). Development of a routine DNA-based testing service for soilborne diseases in Australia. Australasian Plant Pathology, 37(3), 243–253.

    CAS  Google Scholar 

  • Paulitz, T. C. (2006). Low input no-till cereal production in the Pacific northwest of the US: the challenges of root diseases. European Journal of Plant Pathology, 115(3), 271–281.

    Google Scholar 

  • Paulitz, T. C., Smiley, R. W., & Cook, R. J. (2002). Insights into the prevalence and management of soilborne cereal pathogens under direct seeding in the Pacific northwest, USA. Canadian Journal of Plant Pathology, 24(4), 416–428.

    Google Scholar 

  • Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reynolds, J., Weir, B. S., & Cockerham, C. C. (1983). Estimation of the co-ancestry coefficient: Basis for a short-term genetic distance. Genetics, 105, 767–777.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Scott, J. B., & Chakraborty, S. (2006). Multilocus sequence analysis of Fusarium pseudograminearum reveals a single phylogenetic species. Mycological Research, 110(12), 1413–1425. https://doi.org/10.1016/j.mycres.2006.09.008.

    Article  CAS  PubMed  Google Scholar 

  • Scott, J. B., & Chakraborty, S. (2010). Genotypic diversity in Fusarium pseudograminearum populations in Australian wheat fields. Plant Pathology, 59(2), 338–347. https://doi.org/10.1111/j.1365-3059.2009.02219.x.

    Article  CAS  Google Scholar 

  • Slatkin, M. (1995). A measure of population subdivision based on microsatellite allele frequencies. Genetics, 139, 457–462.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Smiley, R. W., Gourlie, J. A., Easley, S. A., Patterson, L.-M., & Whittaker, R. G. (2005). Crop damage estimates for crown rot of wheat and barley in the Pacific northwest. Plant Disease, 89(6), 595–604. https://doi.org/10.1094/PD-89-0595.

    Article  PubMed  Google Scholar 

  • Summerell, B., & Burgess, L. (1988). Stubble management practices and the survival of Fusarium graminearum group 1 in wheat stubble residues. Australasian Plant Pathology, 17(4), 88–93.

    Google Scholar 

  • Summerell, B., Burgess, L., & Klein, T. (1989). The impact of stubble management on the incidence of crown rot of wheat. Animal Production Science, 29(1), 91–98.

    Google Scholar 

  • Summerell, B., Burgess, L., Klein, T., & Pattison, A. (1990). Stubble management and the site of penetration of wheat by Fusarium graminearum group 1. Phytopathology, 80(9), 877–879.

    Google Scholar 

  • Summerell, B., Burgess, L., Backhouse, D., Bullock, S., & Swan, L. (2001). Natural occurrence of perithecia of Gibberella coronicola on wheat plants with crown rot in Australia. Australasian Plant Pathology, 30(4), 353–356.

    Google Scholar 

  • Talas, F., Kalih, R., & Miedaner, T. (2012). Within-field variation of Fusarium graminearum isolates for aggressiveness and deoxynivalenol production in wheat head blight. Phytopathology, 102, 128–134.

    CAS  PubMed  Google Scholar 

  • Tunali, B., Obanor, F., Erginbaş, G., Westecott, R. A., Nicol, J., & Chakraborty, S. (2012). Fitness of three Fusarium pathogens of wheat. FEMS Microbiology Ecology, 81(3), 596–609.

    CAS  PubMed  Google Scholar 

  • Verrell, A. G., Simpfendorfer, S., & Moore, K. J. (2017). Effect of row placement, stubble management and ground engaging tool on crown rot and grain yield in a no-till continuous wheat sequence. Soil and Tillage Research, 165, 16–22.

    Google Scholar 

  • Ward, T. J., Bielawski, J. P., Kistler, H. C., Sullivan, E., & O'Donnell, K. (2002). Ancestral polymorphism and adaptive evolution in the trichothecene mycotoxin gene cluster of phytopathogenic Fusarium. Proceedings of the National Academy of Sciences, 99(14), 9278–9283.

    CAS  Google Scholar 

  • Wright, S. (1949). The genetical structure of populations. Annals of Human Genetics, 15(1), 323–354.

    Google Scholar 

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Acknowledgements

Stubble samples from which we collected Fp isolates for this study were kindly supplied by Dr. Daniel Hüberli (Department of Primary Industries and Regional Development) for WA, Dr. Margaret Evans (SARDI) for SA, Dr. Andrew Milgate (NSW DPI) for Cowra and Wagga Wagga, Dr. Grant Hollaway for Horsham and Simon Craig (Birchip Cropping Group) for Birchip. The resulting collection, isolation and DNA extraction of samples from the 98 isolates from the SARDI population was funded by the Grains Research and Development Corporation projects DAN00175 and DAS00137. M. Khudhair was supported by a PhD fellowship from the Iraqi Ministry of Science and Technology.

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Authors and Affiliations

  1. CSIRO Agriculture and Food, 306 Carmody Road, St Lucia, Qld, 4067, Australia

    Mohammed Khudhair, K. Kazan & D. M. Gardiner

  2. School of Agriculture and Food Science, The University of Queensland, St Lucia, Qld, 4072, Australia

    Mohammed Khudhair & E. Aitken

  3. Grains Research and Development Corporation, 4 National Circuit, Barton, ACT, 2600, Australia

    F. Obanor

  4. Primary Industries and Regions South Australia, South Australian Research and Development Institute, Hartley Grove, Urrbrae, South Australia, 5064, Australia

    A. McKay & D. Giblot-Ducray

  5. New South Wales Department of Primary Industries, Tamworth Agricultural Institute, 4 Marsden Park Road, Calala, NSW, 2340, Australia

    S. Simpfendorfer

  6. CSIRO Agriculture and Food, 147 Underwood Avenue, Floreat, WA, 6014, Australia

    L. F. Thatcher

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  1. Mohammed Khudhair
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Correspondence to Mohammed Khudhair.

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Supplementary Information

Supplementary figure 1

Structure analysis using 2.3.4. software grouped the Fusarium pseudograminearum populations from Western Australia (WA) and eastern Australian states of New South Wales (NSW), Victoria (Vic) and South Australia (SA) into four putative groups. (PDF 119 kb)

Supplemental Table 1

The 21 polymorphic cleaved amplified polymorphic sequence (CAPS) primers used to study the genotypic diversity of Fusarium pseudograminearum from Western Australia and Eastren Australian states wheat fields. (DOCX 16.5 kb)

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Khudhair, M., Obanor, F., Kazan, K. et al. Genetic diversity of Australian Fusarium pseudograminearum populations causing crown rot in wheat. Eur J Plant Pathol 159, 741–753 (2021). https://doi.org/10.1007/s10658-020-02198-0

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