Abstract
The crop pathogen Fusarium graminearum often colonizes non-cultivated grasses, but the phenotypic variation found in isolates recovered from these hosts has not been thoroughly investigated or compared to that observed in isolates collected from crop hosts. Fusarium graminearum growth, perithecia formation, and virulence on crops (maize seedlings, wheat seedlings, wheat spikes) were measured in laboratory and greenhouse experiments using isolates (n = 24) recovered from three non-cultivated grasses (Bromus inermis, Dactylis glomerata, and Phalaris arundinacea) and winter wheat (Triticum aestivum) found at a single research farm in northeastern New York. While individual isolates varied significantly for all phenotypes measured, grass and wheat derived isolates displayed a comparable range of phenotypic values. Trichothecene genotypes were determined from the TRI12 and TRI1 loci, and mycotoxin production was quantified in mature wheat spikes. Trichothecene genotype and phenotype were largely concordant and were not related to isolate source. These findings support consideration of non-cultivated hosts as sources of diverse pathogen inoculum that may cause crop disease.
Data availability
Nucleotide sequences generated in this study are deposited with NCBI GenBank and individual accession numbers are listed within this text. All other data and material will be made available upon request to the corresponding author.
References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. J Roy Stat Soc Ser B (Methodol) 57:289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
Ellis ML, Broders KD, Paul PA, Dorrance AE (2011) Infection of soybean seed by Fusarium graminearum and effect of seed treatments on disease under controlled conditions. Plant Dis 95:401–407
Fox J, Weisberg S (2019) An {R} Companion to applied regression, 3rd edn. Sage, Thousand Oaks
Fuentes RG, Mickelson HR, Busch RH, Dill-Macky R, Evans CK, Thompson WG et al (2005) Resource allocation and cultivar stability in breeding for Fusarium head blight resistance in spring wheat. Crop Sci 45:1965–1972
Fulcher MR, Winans JB, Quan M, Oladipo ED, Bergstrom GC (2019) Population genetics of Fusarium graminearum at the interface of wheat and wild grass communities in New York. Phytopathology 109:2124–2131
Fulcher MR, Winans JB, Quan M, Bergstrom GC (2020) The incidence of Fusarium graminearum in wild grasses is associated with rainfall and cumulative host density in New York. Plant Dis (in press). https://doi.org/10.1094/PDIS-02-20-0286-RE
Geiser DM, del Mar Jiménez-Gasco M, Kang S, Makalowska I, Veeraraghavan N, Ward TJ et al (2004)FUSARIUM-ID v. 1.0: a DNA sequence database for identifying Fusarium. Eur J Plant Pathol 110:473–479
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363
Hsu JC (1996) Multiple comparisons: theory and methods. Chapman & Hall/CRC, Boca Raton
Ilić J, Ćosić J, Jurković D, Vrandečić K (2012) Pathogenicity of Fusarium spp. isolated from weeds and plant debris in eastern Croatia to wheat and maize. Poljoprivreda 18:7–11
Inch S, Gilbert J (2003) The incidence of Fusarium species recovered from inflorescences of wild grasses in southern Manitoba. Can J Plant Path 25:379–383
Kelly AC, Ward TJ (2018) Population genomics of Fusarium graminearum reveals signatures of divergent evolution within a major cereal pathogen. PLoS One 13:e0194616
Kosmidis I (2020) brglm2: Bias Reduction in Generalized Linear Models. R package version 0.6.2. https://CRAN.R-project.org/package=brglm2
Kuhnem PR, Spolti P, Del Ponte EM, Cummings JA, Bergstrom GC (2015) Trichothecene genotype composition of Fusarium graminearum not differentiated among isolates from maize stubble, maize ears, wheat spikes, and the atmosphere in New York. Phytopathology 105:695–699
Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280
Lenth R (2019) emmeans: Estimated marginal means, aka least-squares means. R package version 1.4.1. https://CRAN.R-project.org/package=emmeans
Leslie JF, Summerell BA (2006) The Fusarium Laboratory Manual. Blackwell Publishing, Hoboken
Liang JM, Xayamongkhon H, Broz K, Dong Y, Mccormick SP, Abramova S et al (2014) Temporal dynamics and population genetic structure of Fusarium graminearum in the upper Midwestern United States. Fungal Genet Biol 73:83–92
Liu YY, Sun HY, Li W, Xia YL, Deng YY et al (2017) Fitness of three chemotypes of Fusarium graminearum species complex in major winter wheat-producing areas of China. PLoS One 12:e0174040. https://doi.org/10.1371/journal.pone.0174040
Lofgren LA, LeBlanc NR, Certano AK, Nachtigall J, LaBine KM, Riddle J et al (2017)Fusarium graminearum: pathogen or endophyte of North American grasses? New Phytol 217:1203–1212
Lofgren L, Riddle J, Dong Y, Kuhnem PR, Cummings JA, Del Ponte EM et al (2018) A high proportion of NX-2 genotype strains are found among Fusarium graminearum isolates from northeastern New York State. Eur J Plant Pathol 150:791–796
O’Donnell K, Kistler HC, Cigelnik E, Ploetz RC (1998) Multiple evolutionary origins of the fungus causing Panama disease of banana: Concordant evidence from nuclear and mitochondrial gene genealogies. Proc Natl Acad Sci 95:2044–2049
O’Donnell K, Sutton DA, Rinaldi MG, Sarver BAJ, Balajee SA et al (2010)Internet-accessible DNA sequence database for identifying fusaria from human and animal infections. J Clin Microbiol 48:3708–3718
O’Donnell K, Ward TJ, Robert VARG, Crous PW, Geiser DM, Kang S (2015) DNA sequence-based identification of Fusarium: Current status and future directions. Phytoparasitica 43:583–595
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2019) vegan: community ecology package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan
Postic J, Cosic J, Vrandecic K, Jurkovic D, Saleh AA, Leslie JF (2012) Diversity of Fusarium species isolated from weeds and plant debris in Croatia. J Phytopathol 160:76–81
Puri KD, Zhong S (2010) The 3ADON population of Fusarium graminearum found in North Dakota is more aggressive and produces a higher level of DON than the prevalent 15ADON population in spring wheat. Phytopathology 100:1007–1014. https://doi.org/10.1094/PHYTO-12-09-0332
R Core Team (2019) R: A language and environment for statistical computing. Version 3.6.0. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
Ramdass AC, Villafana RT, Rampersad SN (2020) TRI Genotyping and chemotyping: A balance of power. Toxins 12:64. https://doi.org/10.3390/toxins12020064
Sneideris D, Ivanauskas A, Prakas P, Butkauskas D, Treikale O, Kadziene G, Rasiukeviciute N, Kelpsiene J, Suproniene S (2020) Population structure of Fusarium graminearum isolated from different sources in one area over the course of three years. Phytopathology (in press). https://doi.org/10.1094/PHYTO-08-19-0298-R
Spolti P, Del Ponte EM, Cummings JA, Dong Y, Bergstrom GC (2014) Fitness attributes of Fusarium graminearum isolates from wheat in New York possessing a 3-ADON or 15-ADON trichothecene genotype. Phytopathology 104:513–519
Starkey DE, Ward TJ, Aoki T, Gale LR, Kistler HC, Geiser DM et al (2007) Global molecular surveillance reveals novel Fusarium head blight species and trichothecene toxin diversity. Fungal Genet Biol 44:1191–1204
Suproniene S, Kadziene G, Irzykowski W, Sneideris D, Ivanauskas A, Sakalauskas S et al (2019) Weed species within cereal crop rotations can serve as alternative hosts for Fusarium graminearum causing Fusarium head blight of wheat. Fungal Ecology 37:30–37
Tschanz AT, Horst RK, Nelson PE (1976) The effect of environment on sexual reproduction of Gibberella zeae. Mycologia 68:327–340. https://doi.org/10.1080/00275514.1976.12019914
Turkington TK, Clear RM, Demeke T, Lange R, Xi K, Kumar K (2011) Isolation of Fusarium graminearum from cereal, grass and corn residues from Alberta, 2001–2003. Can J Plant Path 33:179–186
USDA National Agricultural Statistics Service (2019) Cropland data layer. https://nassgeodata.gmu.edu/CropScape/. Accessed 8 Apr 2019
Venables WN, Ripley BD (2002) Modern Applied Statistics with S. Fourth Edition. Springer, New York
Ward TJ, Clear RM, Rooney AP, O’Donnell K, Gaba D, Patrick S, Starkey DE, Gilbert J, Geiser DM, Nowicki TW (2008) An adaptive evolutionary shift in Fusarium head blight pathogen populations is driving the rapid spread of more toxigenic Fusarium graminearum in North America. Fungal Genet Biol 45:473–484. https://doi.org/10.1016/j.fgb.2007.10.003
Acknowledgements
The authors thank Mike Davis, Manager of the Willsboro Research Farm for assistance with sample collection. Funding: Atkinson Center for a Sustainable Future, Sustainable Biodiversity Fund, National Institute of Food and Agriculture Hatch Project NYC153437. This material is also based, in part, upon work supported by the U.S. Department of Agriculture, under Agreement No. 59-0206-4-006. This is a cooperative project with the U.S. Wheat & Barley Scab Initiative. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the view of the U.S. Department of Agriculture.
Funding
This work was funded by Atkinson Center for a Sustainable Future, Sustainable Biodiversity Fund; U.S. Department of Agriculture, National Institute of Food and Agriculture, Cornell University Hatch Project NYC153437; and U.S. Department of Agriculture, Agricultural Research Service, under Agreement No. 59-0206-4-006. The latter is a cooperative project with the U.S. Wheat & Barley Scab Initiative. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the view of the U.S. Department of Agriculture.
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Fulcher, M.R., Winans, J.B. & Bergstrom, G.C. Fusarium graminearum isolates obtained from wheat and wild grasses in northeastern New York display comparable range of phenotypes, including virulence on crop hosts. J Plant Pathol 103, 71–77 (2021). https://doi.org/10.1007/s42161-020-00717-w
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DOI: https://doi.org/10.1007/s42161-020-00717-w