Spike culture derived wheat (Triticum aestivum L.) variants exhibit improved resistance to multiple chemotypes of Fusarium graminearum
Autoři:
Chen Huang aff001; Manu P. Gangola aff001; Seedhabadee Ganeshan aff001; Pierre Hucl aff002; H. Randy Kutcher aff002; Ravindra N. Chibbar aff001
Působiště autorů:
Department of Plant Sciences, College of Agriculture and Bioresources, Campus Drive, University of Saskatchewan, Saskatoon, Saskatchewan, Canada
aff001; Crop Development Centre, College of Agriculture and Bioresources, Campus Drive, University of Saskatchewan, Saskatoon, Saskatchewan, Canada
aff002
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0226695
Souhrn
Fusarium head blight (FHB) in wheat (Triticum aestivum L.), predominantly caused by Fusarium graminearum, has been categorized into three chemotypes depending on the major mycotoxin produced. The three mycotoxins, namely, 3-acetyldeoxynivalenol (3-ADON), 15-acetyldeoxynivalenol (15-ADON) and nivalenol (NIV) also determine their aggressiveness and response to fungicides. Furthermore, prevalence of these chemotypes changes over time and dynamic changes in chemotypes population in the field have been observed. The objective of this study was to identify spike culture derived variants (SCDV) exhibiting resistance to multiple chemotypes of F. graminearum. First, the optimal volume of inoculum for point inoculation of the spikelets was determined using the susceptible AC Nanda wheat genotype. Fifteen μL of 105 macroconidia/mL was deemed optimal based on FHB disease severity assessment with four chemotypes. Following optimal inoculum volume determination, five chemotypes (Carman-NIV, Carman-705-2-3-ADON, M9-07-1-3-ADON, M1-07-2-15-ADON and China-Fg809-15-ADON) were used to point inoculate AC Nanda spikelets to confirm the mycotoxin produced and FHB severity during infection. Upon confirmation of the mycotoxins produced by the chemotypes, 55 SCDV were utilized to evaluate FHB severity and mycotoxin concentrations. Of the 55 SCDV, five (213.4, 244.1, 245.6, 250.2 and 252.3) resistant lines were identified with resistance to multiple chemotypes and are currently being utilized in a breeding program to develop wheat varieties with improved FHB resistance.
Klíčová slova:
Wheat – Fungal genetics – Population genetics – Fusarium – Canada – Cereal crops – Common wheat – Fusarium graminearum
Zdroje
1. Goswami RS, Kistler HC. Heading for disaster: Fusarium graminearum on cereal crops. Molecular Plant Pathology. 2004;5(6):515–25. doi: 10.1111/j.1364-3703.2004.00252.x 20565626
2. Malihipour A, Gilbert J, Piercey-Normore M, Cloutier S. Molecular Phylogenetic Analysis, Trichothecene Chemotype Patterns, and Variation in Aggressiveness of Fusarium Isolates Causing Head Blight in Wheat. Plant Disease. 2012;96(7):1016–25. doi: 10.1094/PDIS-10-11-0866-RE 30727210.
3. Rossi V, Ravanetti A, Pattori E, Giosuè S. Influence of temperature and humidity on the infection of wheat spikes by some fungi causing Fusarium head blight. Journal of Plant Pathology. 2001;83.
4. Xu X-M, Monger W, Ritieni A, Nicholson P. Effect of temperature and duration of wetness during initial infection periods on disease development, fungal biomass and mycotoxin concentrations on wheat inoculated with single, or combinations of, Fusarium species. Plant Pathology. 2007;56(6):943–56. doi: 10.1111/j.1365-3059.2007.01650.x
5. Chetouhi C, Bonhomme L, Lecomte P, Cambon F, Merlino M, Biron DG, Langin T. A proteomics survey on wheat susceptibility to Fusarium head blight during grain development. Eur J Plant Pathol. 2015;141(2):407–18. Epub 2015/02/11. doi: 10.1007/s10658-014-0552-0 25663750; PubMed Central PMCID: PMC4318354.
6. Del Ponte EM, Fernandes JMC, Bergstrom GC. Influence of Growth Stage on Fusarium Head Blight and Deoxynivalenol Production in Wheat. Journal of Phytopathology. 2007;155(10):577–81. doi: 10.1111/j.1439-0434.2007.01281.x
7. Moretti A, Panzarini G, Somma S, Campagna C, Stefano R, Logrieco A, Solfrizzo M. Systemic Growth of F. graminearum in Wheat Plants and Related Accumulation of Deoxynivalenol. Toxins. 2014;6:1308–24. doi: 10.3390/toxins6041308 24727554
8. Salgado JD, Madden LV, Paul PA. Quantifying the effects of fusarium head blight on grain yield and test weight in soft red winter wheat. Phytopathology. 2015;105(3):295–306. Epub 2014/10/16. doi: 10.1094/PHYTO-08-14-0215-R 25317842.
9. Gunupuru LR, Perochon A, Doohan FM. Deoxynivalenol resistance as a component of FHB resistance. Tropical Plant Pathology. 2017;42(3):175–83. doi: 10.1007/s40858-017-0147-3
10. Shah L, Ali A, Yahya M, Zhu Y, Wang S, Si H, Rahman H, Ma C. Integrated control of fusarium head blight and deoxynivalenol mycotoxin in wheat. Plant Pathology. 2018;67(3):532–48. doi: 10.1111/ppa.12785
11. Beres BL, Brûlé-Babel AL, Ye Z, Graf RJ, Turkington TK, Harding MW, Kutcher HR, Hooker DC. Exploring Genotype × Environment × Management synergies to manage fusarium head blight in wheat. Canadian Journal of Plant Pathology. 2018;40(2):179–88. doi: 10.1080/07060661.2018.1445661
12. Yoshizawa T. Thirty-five Years of Research on Deoxynivalenol, a Trichothecene Mycotoxin: with Special Reference to Its Discovery and Co-occurrence with Nivalenol in Japan. Food Safety. 2013;1(1):2013002–. doi: 10.14252/foodsafetyfscj.2013002
13. Liang J, Lofgren L, Ma Z, Ward TJ, Kistler HC. Population Subdivision of Fusarium graminearum from Barley and Wheat in the Upper Midwestern United States at the Turn of the Century. Phytopathology. 2015;105(11):1466–74. Epub 2015/06/25. doi: 10.1094/PHYTO-01-15-0021-R 26107972
14. Crippin T, Renaud JB, Sumarah MW, Miller JD. Comparing genotype and chemotype of Fusarium graminearum from cereals in Ontario, Canada. PLOS ONE. 2019;14(5):e0216735. doi: 10.1371/journal.pone.0216735 31071188
15. Kelly AC, Clear RM, O’Donnell K, McCormick S, Turkington TK, Tekauz A, Gilbert J, Kistler HC, Busman M, Ward TJ. Diversity of Fusarium head blight populations and trichothecene toxin types reveals regional differences in pathogen composition and temporal dynamics. Fungal Genetics and Biology. 2015;82:22–31. doi: 10.1016/j.fgb.2015.05.016 26127017
16. Varga E, Wiesenberger G, Hametner C, Ward TJ, Dong Y, Schofbeck D, McCormick S, Broz K, Stuckler R, Schuhmacher R, Krska R, Kistler HC, Berthiller F, Adam G. New tricks of an old enemy: isolates of Fusarium graminearum produce a type A trichothecene mycotoxin. Environmental Microbiology. 2015;17(8):2588–600. Epub 2014/11/19. doi: 10.1111/1462-2920.12718 25403493; PubMed Central PMCID: PMC4950012.
17. Li X, Michlmayr H, Schweiger W, Malachova A, Shin S, Huang Y, Dong Y, Wiesenberger G, McCormick S, Lemmens M, Fruhmann P, Hametner C, Berthiller F, Adam G, Muehlbauer GJ. A barley UDP-glucosyltransferase inactivates nivalenol and provides Fusarium Head Blight resistance in transgenic wheat. Journal of Experimental Botany. 2017;68(9):2187–97. Epub 2017/04/14. doi: 10.1093/jxb/erx109 28407119; PubMed Central PMCID: PMC5447872.
18. Mandala G, Tundo S, Francesconi S, Gevi F, Zolla L, Ceoloni C, D'Ovidio R. Deoxynivalenol Detoxification in Transgenic Wheat Confers Resistance to Fusarium Head Blight and Crown Rot Diseases. Molecular plant-microbe interactions: MPMI. 2019;32(5):583–92. Epub 2018/11/14. doi: 10.1094/MPMI-06-18-0155-R 30422742.
19. Puri KD, Zhong S. 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. 2010;100(10):1007–14. Epub 2010/09/16. doi: 10.1094/PHYTO-12-09-0332 20839936.
20. Ward TJ, Clear RM, Rooney AP, O’Donnell K, Gaba D, Patrick S, Starkey DE, Gilbert J, Geiser DM, Nowicki TW. An adaptive evolutionary shift in Fusarium head blight pathogen populations is driving the rapid spread of more toxigenic Fusarium graminearum in North America. Fungal Genetics and Biology. 2008;45(4):473–84. doi: 10.1016/j.fgb.2007.10.003 18035565
21. Chakraborty S, Newton AC. Climate change, plant diseases and food security: an overview. Plant Pathology. 2011;60(1):2–14. doi: 10.1111/j.1365-3059.2010.02411.x
22. Simsek S, Burgess K, Whitney KL, Gu Y, Qian SY. Analysis of Deoxynivalenol and Deoxynivalenol-3-glucoside in wheat. Food Control. 2012;26(2):287–92. https://doi.org/10.1016/j.foodcont.2012.01.056.
23. Pierron A, Mimoun S, Murate LS, Loiseau N, Lippi Y, Bracarense AP, Liaubet L, Schatzmayr G, Berthiller F, Moll WD, Oswald IP. Intestinal toxicity of the masked mycotoxin deoxynivalenol-3-beta-D-glucoside. Arch Toxicol. 2016;90(8):2037–46. Epub 2015/09/26. doi: 10.1007/s00204-015-1592-8 26404761.
24. Nakagawa H, He X, Matsuo Y, Singh PK, Kushiro M. Analysis of the Masked Metabolite of Deoxynivalenol and Fusarium Resistance in CIMMYT Wheat Germplasm. Toxins (Basel). 2017;9(8). Epub 2017/08/02. doi: 10.3390/toxins9080238 28758925; PubMed Central PMCID: PMC5577572.
25. Anukul N, Vangnai K, Mahakarnchanakul W. Significance of regulation limits in mycotoxin contamination in Asia and risk management programs at the national level. Journal of Food and Drug Analysis. 2013;21(3):227–41. https://doi.org/10.1016/j.jfda.2013.07.009.
26. Siegel D, Babuscio T. Mycotoxin management in the European cereal trading sector. Food Control. 2011;22(8):1145–53. https://doi.org/10.1016/j.foodcont.2011.02.022.
27. Yuan J, Sun C, Guo X, Yang T, Wang H, Fu S, Li C, Yang H. A rapid Raman detection of deoxynivalenol in agricultural products. Food Chemistry. 2017;221:797–802. doi: 10.1016/j.foodchem.2016.11.101 27979275
28. Ryu JC, Ohtsubo K, Izumiyama N, Nakamura K, Tanaka T, Yamamura H, Ueno Y. The acute and chronic toxicities of nivalenol in mice. Fundamental and applied toxicology: official journal of the Society of Toxicology. 1988;11(1):38–47. Epub 1988/07/01. doi: 10.1016/0272-0590(88)90268-0 3209016.
29. Takahashi M, Shibutani M, Sugita-Konishi Y, Aihara M, Inoue K, Woo GH, Fujimoto H, Hirose M. A 90-day subchronic toxicity study of nivalenol, a trichothecene mycotoxin, in F344 rats. Food and chemical toxicology: an international journal published for the British Industrial Biological Research Association. 2008;46(1):125–35. Epub 2007/09/04. doi: 10.1016/j.fct.2007.07.005 17765382.
30. Kongkapan J, Polapothep A, Owen H, Giorgi M. A brief overview of our current understanding of nivalenol: A growing potential danger yet to be fully investigated. Israel Journal of Veterinary Medicine. 2016;71(1):3–9.
31. Guo XW, Fernando WGD, Seow-Brock HY. Population Structure, Chemotype Diversity, and Potential Chemotype Shifting of Fusarium graminearum in Wheat Fields of Manitoba. Plant Disease. 2008;92(5):756–62. Epub 2008/05/01. doi: 10.1094/PDIS-92-5-0756 30769598.
32. Kelly AC, Ward TJ. Population genomics of Fusarium graminearum reveals signatures of divergent evolution within a major cereal pathogen. PLOS ONE. 2018;13(3):e0194616. doi: 10.1371/journal.pone.0194616 29584736
33. van der Lee T, Zhang H, van Diepeningen A, Waalwijk C. Biogeography of Fusarium graminearum species complex and chemotypes: a review. Food additives & contaminants Part A, Chemistry, analysis, control, exposure & risk assessment. 2015;32(4):453–60. Epub 2014/12/23. doi: 10.1080/19440049.2014.984244 25530109; PubMed Central PMCID: PMC4376211.
34. Ganeshan S, Chibbar RN. A simple novel expedited spike culture-derived variation creation strategy in wheat. Cereal Research Communications. 2017;45(4):539–48. doi: 10.1556/0806.45.2017.047
35. Sharma P, Gangola MP, Huang C, Kutcher HR, Ganeshan S, Chibbar RN. Single Nucleotide Polymorphisms in B-Genome Specific UDP-Glucosyl Transferases Associated with Fusarium Head Blight Resistance and Reduced Deoxynivalenol Accumulation in Wheat Grain. Phytopathology. 2018;108(1):124–32. doi: 10.1094/PHYTO-04-17-0159-R 29063821
36. Sadasivaiah RS, Perkovic SM, Pearson DC, Postman B. Registration of ‘AC Nanda’ Wheat. Crop Science. 2000;40(2):579–80. doi: 10.2135/cropsci2000.0029rcv
37. Ganeshan S, Drinkwater JM, Repellin A, Chibbar RN. Selected Carbohydrate Metabolism Genes Show Coincident Expression Peaks in Grains of In Vitro-Cultured Immature Spikes of Wheat (Triticum aestivum L.). Journal of Agricultural and Food Chemistry. 2010;58(7):4193–201. doi: 10.1021/jf903861q 20235533
38. Ganeshan S, Leis M, Drinkwater JM, Madsen LT, Jain JC, Chibbar RN. In vitro-cultured wheat spikes provide a simplified alternative for studies of cadmium uptake in developing grains. Journal of the Science of Food and Agriculture. 2012;92(8):1740–7. doi: 10.1002/jsfa.5540 22173723
39. Huang C, Gangola MP, Chibbar RN. Utilization of wheat spike culture to assess Fusarium head blight disease progression and mycotoxin accumulation. Canadian Journal of Plant Pathology. 2019:null-null. doi: 10.1080/07060661.2019.1621935
40. Gilbert J, Brûlé-Babel A, Guerrieri AT, Clear RM, Patrick S, Slusarenko K, Wolfe C. Ratio of 3-ADON and 15-ADON isolates of Fusarium graminearum recovered from wheat kernels in Manitoba from 2008 to 2012. Canadian Journal of Plant Pathology. 2014;36(1):54–63. doi: 10.1080/07060661.2014.887033
41. Goswami RS, Kistler HC. Pathogenicity and In Planta Mycotoxin Accumulation Among Members of the Fusarium graminearum Species Complex on Wheat and Rice. Phytopathology. 2005;95(12):1397–404. Epub 2008/10/24. doi: 10.1094/PHYTO-95-1397 18943550.
42. Ferrigo D, Raiola A, Causin R. Fusarium Toxins in Cereals: Occurrence, Legislation, Factors Promoting the Appearance and Their Management. Molecules. 2016;21(5). Epub 2016/05/18. doi: 10.3390/molecules21050627 27187340; PubMed Central PMCID: PMC6274039.
43. Wang J-H, Zhang J-B, Chen F, Li H, Ndoye M, Liao Y-C. A multiplex PCR assay for genetic chemotyping of toxigenic Fusarium graminearum and wheat grains for 3-acetyldeoxynivalenol, 15-acetyldeoxynivalenol and nivalenol mycotoxin. Journal of Food, Agriculture & Environment. 2012;10:505–11.
44. Ward TJ, Bielawski JP, Kistler HC, Sullivan E, O'Donnell K. Ancestral polymorphism and adaptive evolution in the trichothecene mycotoxin gene cluster of phytopathogenic Fusarium. Proceedings of the National Academy of Sciences of the United States of America. 2002;99(14):9278–83. Epub 06/21. doi: 10.1073/pnas.142307199 12080147.
45. Alexander NJ, McCormick SP, Waalwijk C, van der Lee T, Proctor RH. The genetic basis for 3-ADON and 15-ADON trichothecene chemotypes in Fusarium. Fungal genetics and biology: FG & B. 2011;48(5):485–95. Epub 2011/01/11. doi: 10.1016/j.fgb.2011.01.003 21216300.
46. Burlakoti RR, Ali S, Secor GA, Neate SM, McMullen MP, Adhikari TB. Comparative Mycotoxin Profiles of Gibberella zeae Populations from Barley, Wheat, Potatoes, and Sugar Beets. Applied and Environmental Microbiology. 2008;74(21):6513–20. doi: 10.1128/AEM.01580-08 18791024
47. Desjardins AE, Proctor RH, Bai G, McCormick SP, Shaner G, Buechley G, Hohn TM. Reduced virulence of trichothecene-nonproducing mutants of Gibberella zeae in wheat field tests. Molecular plant-microbe interactions. 1996;1996 v.9 no.9(no. 9):pp. 775–0. doi: 10.1094/mpmi-9-0775 PubMed PMID: 26933.
48. Bai G-H, Plattner R, Desjardins A, Kolb F, McIntosh RA. Resistance to Fusarium head blight and deoxynivalenol accumulation in wheat. Plant Breeding. 2001;120(1):1–6. doi: 10.1046/j.1439-0523.2001.00562.x
49. von der Ohe C, Gauthier V, Tamburic-Ilincic L, Brule-Babel A, Fernando WGD, Clear R, Ward TJ, Miedaner T. A comparison of aggressiveness and deoxynivalenol production between Canadian Fusarium graminearum isolates with 3-acetyl and 15-acetyldeoxynivalenol chemotypes in field-grown spring wheat. European Journal of Plant Pathology. 2010;127(3):407–17. doi: 10.1007/s10658-010-9607-z
50. Liu Y-Y, Sun H-Y, Li W, Xia Y-L, Deng Y-Y, Zhang A-X, Chen H-G. Fitness of three chemotypes of Fusarium graminearum species complex in major winter wheat-producing areas of China. PLOS ONE. 2017;12(3):e0174040. doi: 10.1371/journal.pone.0174040 28306726
51. Serajazari M, Hudson K, Kaviani M, Navabi A. Fusarium graminearum Chemotype-Spring Wheat Genotype Interaction Effects in Type I and II Resistance Response Assays. Phytopathology. 2019;109(4):643–9. Epub 2018/11/20. doi: 10.1094/PHYTO-10-18-0394-R 30451634.
52. Amarasinghe CC, Tittlemier SA, Fernando WGD. Nivalenol-producing Fusarium cerealis associated with fusarium head blight in winter wheat in Manitoba, Canada. Plant Pathology. 2015;64(4):988–95. doi: 10.1111/ppa.12329
53. Miedaner T, Reinbrecht C, Lauber U, Schollenberger M, Geiger HH. Effects of genotype and genotype—environment interaction on deoxynivalenol accumulation and resistance to Fusarium head blight in rye, triticale, and wheat. Plant Breeding. 2001;120(2):97–105. doi: 10.1046/j.1439-0523.2001.00580.x
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