Trichothecenes B and ergosterol content evaluation in mature grains of durum wheat genotypes contaminated by Fusarium culmorum
DOI:
https://doi.org/10.6092/issn.2531-7342/14712Keywords:
Durum wheat, fusarium head blight, Algeria, Trichotecenes B, ergosterolAbstract
The interest of this present work is to compare two selected durum wheat lines (G1 and G4) with their sensitive parents to fusarium head blight by determining the mycotoxin and ergosterol content in their mature grains. These lines are homozygous, fixed, obtained by the classical genealogical selection, and composed of seeds from diallel crosses between 4 parental varieties Saadi, Simeto, Ardente, and Waha. For this purpose, the grains of the studied genotypes (lines and parental varieties) were tested in the laboratory for their content of Trichothecenes B mycotoxins (TCTB) and ergosterol at full grain maturity using high-performance liquid chromatographic – diode array detection (HPLC-DAD). Fungal biomass was estimated by the content of ergosterol. However, the level of toxins was assessed by the levels of TCTB produced by the different studied isolates. The results obtained showed that the lines derived from crosses and, especially the G1 line, accumulated levels of TCTB and ergosterol significantly lower than their parents. Our findings open up a new avenue of investigation into fusarium head blight in Algeria, including the search for mycotoxins as potential causes of poorly understood human diseases and the factors that contribute to their accumulation in grains.
References
Abdallah-Nekache N, Laraba I, Ducos C, Barreau C, Bouznad Z, Boureghda H (2019) Occurrence of fusarium head blight and fusarium crown rot in Algerian wheat: identification of associated species and assessment of aggressiveness. European Journal of Plant Pathology 154(3):499–512. https://doi.org/10.1007/s10658-019-01673-7
Abedi-Tizaki M, Sabbagh SK (2012) Morphological and molecular identification of fusarium head blight isolates from wheat in North of Iran. Australian Journal of Crop Science 6(9):1356–1361. https://search.informit.org/doi/abs/10.3316/informit.732638038640515
Abramson D, Gan Z, Clear RM, Gilbert J, Marquardt RR (1998) Relationships among deoxynivalenol, ergosterol and Fusarium exoantigens in Canadian hard and soft wheat. International Journal of Food Microbiology 45(3):217–224. https://doi.org/10.1016/S0168-1605(98)00164-0
Adami Ghamsari F, Tajabadi Ebrahimi M, Bagheri Varzaneh M, Iranbakhsh A, Akhavan Sepahi A (2021) In vitro reduction of mycotoxin deoxynivalenol by organic adsorbent. Journal of Food Processing and Preservation 45(3):1–8. https://doi.org/10.1111/jfpp.15212
Alassane-Kpembi I, Puel O, Oswald IP (2015) Toxicological interactions between the mycotoxins deoxynivalenol, nivalenol and their acetylated derivatives in intestinal epithelial cells. Archives of Toxicology 89(8):1337–1346. https://doi.org/10.1007/s00204-014-1309-4
Alkadri D, Nipoti P, Döll K, Karlovsky P, Prodi A, Pisi A (2013) Study of fungal colonization of wheat kernels in Syria with a focus on Fusarium species. International Journal of Molecular Sciences 14(3):5938–5951. https://doi.org/10.3390/ijms14035938
Álvarez M, Rodríguez A, Bermúdez E, Roncero E, Andrade MJ (2021) Development of a methodology for estimating the ergosterol in meat product-borne toxigenic moulds to evaluate antifungal agents. Foods 10(2):1–14. https://doi.org/10.3390/foods10020438
Atanassov Z, Nakamura C, Yoshizawa T, Kato H, Murai K, Kaneda C (1993) Effect of Fusarium mycotoxins on wheat response to fusarium head blight. Wheat information service 76:50–52
Atlin GN, Enerson PM, McGirr LG, Hunter RB (1983) Gibberella ear rot development and zearalenone and vomitoxin production as affected by maize genotype and Gibberella zeae strain. Canadian Journal of Plant Science 63(4):847–853. https://doi.org/10.4141/cjps83-107
Aupanun S, Poapolathep S, Phuektes P, Giorgi M, Zhang Z, Oswald IP, Poapolathep A (2019) Individual and combined mycotoxins deoxynivalenol, nivalenol, and fusarenon-X induced apoptosis in lymphoid tissues of mice after oral exposure. Toxicon 165:83–94. https://doi.org/10.1016/j.toxicon.2019.04.017
Bouanaka H, Bellil I, Harrat W, Boussaha S, Benbelkacem A, Khelifi D (2021) On the biocontrol by Trichoderma afroharzianum against Fusarium culmorum responsible of fusarium head blight and crown rot of wheat in Algeria. Egyptian Journal of Biological Pest Control 31(1). https://doi.org/10.1186/s41938-021-00416-3
Cuperlovic-Culf M, Loewen M, Rajagopalan N, Surendra A (2017) Perspectives on the specific targeting of Fusarium graminearum for the development of alternative head blight treatment approaches. Plant Pathology 66(9):1391–1403. https://doi.org/10.1111/ppa.12726
Dohnal V, Jezkova A, Pavlikova L, Musilek K, Jun D, Kuca K (2010) Fluctuation in the ergosterol and deoxynivalenol content in barley and malt during malting process. Analytical and Bioanalytical Chemistry 397(1):109–114. https://doi.org/10.1007/s00216-010-3585-z
Góral T, Wiśniewska H, Ochodzki P, Twardawska A, Walentyn-Góral D(2021) Resistance to fusarium head blight, kernel damage, and concentrations of Fusarium mycotoxins in the grain of winter wheat lines. Agronomy 11(9). https://doi.org/10.3390/agronomy11010016
Hadjout S, Chéreau S, Atanasova-Pénichon V, Marchegay G, Mekliche L, Boureghda H, Barreau C, Touati-Hattab S, Bouznad Z, Richard-Forget F (2017) Phenotypic and biochemical characterization of new advanced durum wheat breeding lines from Algeria that show resistance to fusarium head blight and to mycotoxin accumulation. Journal of Plant Pathology 99(3):671–680. http://dx.doi.org/10.4454/jpp.v99i3.3954
Hadjout S, Chéreau S, Mekliche L, Marchegay G, Ducos C, Boureghda H, Zouidi M, Barreau C, Bouznad Z, Richard-Forget F (2022a) Molecular identification of some Fusarium isolates and their chemotypes involved in fusarium head blight on durum wheat in Algeria. Archives of Phytopathology and Plant Protection 55(4):499–513. https://doi.org/10.1080/03235408.2022.2034363
Hadjout S, Bouznad Z, Mekliche L, Zouidi M (2022b) Field resistance phenotyping of durum wheat to fusarium head blight in Algeria. Acta Agriculturae Slovenica118(3):1–9. http://dx.doi.org/10.14720/aas.2022.118.3.2279
Hofstad AN, Nussbaumer T, Akhunov E, Shin S, Kugler KG, Kistler HC, Mayer KFX, Muehlbauer GJ (2016) Examining the transcriptional response in wheat Fhb1 near‐isogenic lines to Fusarium graminearum infection and deoxynivalenol treatment. The Plant Genome 9(1):1–15. https://doi.org/10.3835/plantgenome2015.05.0032
Huang C, Gangola MP, Chibbar RN (2020) Utilization of wheat spike culture to assess fusarium head blight disease progression and mycotoxin accumulation. Canadian Journal of Plant Pathology 42(1):62–71. https://doi.org/10.1080/07060661.2019.1621935
Jia B, Yu S, Yu D, Liu N, Zhang S, Wu A (2021) Mycotoxin deoxynivalenol affects myoblast differentiation via downregulating cytoskeleton and ECM-integrin-FAK-RAC-PAK signaling pathway. Ecotoxicology and Environmental Safety 226:112850. https://doi.org/10.1016/j.ecoenv.2021.112850
Karlsson I, Persson P, Friberg H (2021) Fusarium head blight from a microbiome perspective. Frontiers in Microbiology 12:1–17. https://doi.org/10.3389/fmicb.2021.628373
Kikot GE, Moschini R, Consolo VF, Rojo R, Salerno G, Hours RA, Gasoni L, Arambarri AM, Alconada TM (2011) Occurrence of different species of Fusarium from wheat in relation to disease levels predicted by a weather-based model in Argentina Pampas region. Mycopathologia 171(2):139–149. https://doi.org/10.1007/s11046-010-9335-0
Laraba I, Boureghda H, Abdallah N, Bouaicha O, Obanor F, Moretti A, Geiser MD, Kim H, McCormick SP, Proctor RH, Kelly AC, Ward TJ, O'Donnell K (2017) Population genetic structure and mycotoxin potential of the wheat crown rot and head blight pathogen Fusarium culmorum in Algeria. Fungal Genetics and Biology 1(3):34–41. https://doi.org/10.1016/j.fgb.2017.04.001
Leslie JF, Summerell BA (2006) The Fusarium laboratory manual. Blackwell Publishers, Ames, Iowa, USA, pp 388.
Lori GA, Sisterna MN, Sarandón SJ, Rizzo I, Chidichimo H (2009) Fusarium head blight in wheat: impact of tillage and other agronomic practices under natural infection. Crop Protection 28(6):495–502. https://doi.org/10.1016/j.cropro.2009.01.012
Malbrán I, Mourelos CA, Pardi M, Oufensou S, Balmas V, Delogu G, Migheli Q, Lori GA, Juárez MP, Girotti JR (2020) Commercially available natural inhibitors of trichothecene production in Fusarium graminearum: A strategy to manage fusarium head blight of wheat. Crop Protection 138. https://doi.org/10.1016/j.cropro.2020.105313
Malihipour A, Gilbert J, Piercey-Normore M, Cloutier S (2012) Molecular phylogenetic analysis, trichothecene chemotype patterns, and variation in aggressiveness of fusarium isolates causing head blight in wheat. Plant Disease 96(7):1016–1025. https://doi.org/10.1094/PDIS-10-11-0866-RE
Marín S, Ramos AJ, Sanchis V (2005) Comparison of methods for the assessment of growth of food spoilage moulds in solid substrates. International Journal of Food Microbiology 99(3):329–341. https://doi.org/10.1016/j.ijfoodmicro.2004.10.035
Mayer E, Novak B, Springler A, Schwartz-Zimmermann HE, Nagl V, Reisinger N, Hessenberger S, Schatzmayr G (2017) Effects of deoxynivalenol (DON) and its microbial biotransformation product deepoxy-deoxynivalenol (DOM-1) on a trout, pig, mouse, and human cell line. Mycotoxin Research 33(4):297–308. https://doi.org/10.1007/s12550-017-0289-7
Mesterházy Á (2002) Role of deoxynivalenol in aggressiveness of Fusarium graminearum and F. culmorum and in resistance to fusarium head blight. European Journal of Plant Pathology 108(7):675–684. https://doi.org/10.1023/A:1020631114063
Miedaner T, Reinbrecht C, Schilling AG (2000) Association among aggressiveness, fungal colonization, and mycotoxin production of 26 isolates of Fusarium graminearum in winter rye head blight / Beziehung zwischen Aggressivität, Myzelwachstum und Mykotoxinproduktion von 26 Fusarium graminearum-Isolaten. Journal of Plant Diseases and Protection 107(2):124–134. http://www.jstor.org/stable/43226852
Miller JD (1989) Effects of Fusarium graminearum metabolites on wheat cells.. In: Phytotoxins and Plant Pathogenesis (Graniti A, Durbin RD, BA, eds). NATO ASI Series (Series H: Cell Biology), Vol. 27. Springer, Berlin, Heidelberg, pp 449–452. https://doi.org/10.1007/978-3-642-73178-5_57
Miller JD, Arnison PG (1986) Degradation of deoxynivalenol by suspension cultures of the fusarium head blight resistant wheat cultivar frontana. Canadian Journal of Plant Pathology 8(2):147–150. https://doi.org/10.1080/07060668609501818
Miller JD, Young JC, Sampson DR (1985) Deoxynivalenol and fusarium head blight resistance in spring cereals. Journal of Phytopathology 113:359–367. https://doi.org/10.1111/j.1439-0434.1985.tb04837.x
Mirocha CJ, Xie W, Xu Y, Wilcoxson RD, Woodward RP, Etebarian RH, Behele G (1994) Production of trichothecene mycotoxins by Fusarium graminearum and Fusarium culmorum on barley and wheat. Mycopathologia 128:19–23. https://doi.org/10.1007/BF01104274
Montibus M, Ducos C, Bonnin-Verdal MN, Bormann J, Ponts N, Richard-Forget F, Barreau C (2013) The bZIP transcription factor Fgap1 mediates oxidative stress response and trichothecene biosynthesis but not virulence in Fusarium graminearum. PLoS ONE 8(12):e83377. https://doi.org/10.1371/journal.pone.0083377
Müller HM, Schwadorf K (1990) Ergosterol as a measure of fungal growth in feedstuffs. Archives of Animal Nutrition 40(4):385-395. https://doi.org/10.1080/17450399009430934
Nagashima H, Nakagawa H, Kushiro M, Iwashita K (2009) The in vitro approach to the cytotoxicity of a trichothecene mycotoxin nivalenol. Japan Agricultural Research Quarterly 43(1):7–11. https://doi.org/10.6090/jarq.43.7
Oufensou S, Dessì A, Dallocchio R, Balmas V, Azara E, Carta P, Migheli Q, Delogu G (2021) Molecular docking and comparative inhibitory efficacy of naturally occurring compounds on vegetative growth and deoxynivalenol biosynthesis in Fusarium culmorum. Toxins 13(11):1–23. https://doi.org/10.3390/toxins13110759
Palacios SA, Del Canto A, Erazo J, Torres AM (2021)Fusarium cerealis causing fusarium head blight of durum wheat and its associated mycotoxins. International Journal of Food Microbiology 346(July 2020):109161. https://doi.org/10.1016/j.ijfoodmicro.2021.109161
Pasquali M, Giraud F, Brochot C, Cocco E, Hoffmann L, Bohn T (2010) Genetic Fusarium chemotyping as a useful tool for predicting nivalenol contamination in winter wheat. International Journal of Food Microbiology 137(2–3):246–253. https://doi.org/10.1016/j.ijfoodmicro.2009.11.009
Perkowski J, Buśko M, Stuper K, Kostecki M, Matysiak A, Szwajkowska-Michałek L (2008) Concentration of ergosterol in small-grained naturally contaminated and inoculated cereals. Biologia 63(4):542–547. https://doi.org/10.2478/s11756-008-0083-2
Perkowski J, Kiecana I, Schumacher U, Müller HM, Chełkowski J, Goliński P (1996) Head blight and biosynthesis of Fusarium toxins in barley kernels field inoculated with Fusarium culmorum. European Journal of Plant Pathology 102:491–496. https://doi.org/10.1007/BF01877143
Pietsch C, Michel C, Kersten S, Valenta H, Dänicke S, Schulz C, Kloas W, Burkhardt-Holm P (2014) In vivo effects of deoxynivalenol (DON) on innate immune responses of carp (Cyprinus carpio L.). Food and Chemical Toxicology 68:44–52. https://doi.org/10.1016/j.fct.2014.03.012
Rocha O, Ansari K, Doohan FM (2005) Effects of trichothecene mycotoxins on eukaryotic cells: a review. Food Additives and Contaminants 22(4):369–378. https://doi.org/10.1080/02652030500058403
Ropelewska E (2018) Relationship of thermal properties and ergosterol content of barley grains. Journal of Cereal Science 79:328–334. https://doi.org/10.1016/j.jcs.2017.11.018
Saraf A, Larsson L, Burge H, Milton D (1997) Quantification of ergosterol and 3-hydroxy fatty acids in settled house dust by gas chromatography-mass spectrometry: comparison with fungal culture and determination of endotoxin by a Limulus amebocyte lysate assay. Applied and Environmental Microbiology 63(7):2554–2559. https://doi.org/10.1128/aem.63.7.2554-2559.1997
Savoie JM, Mata G, Atanasova Penichon V, Foulonge-Oriol M (2019) Using mushroom-forming fungi in preventing and reducing mycotoxins in cereal products. Scientia Fungorum 49:e1256. https://doi.org/10.33885/sf.2019.49.1256
Snijders CHA, Krechting CF (1992) Inhibition of deoxynivalenol translocation and fungal colonization in fusarium head blight resistant wheat. Canadian Journal of Botany 70(8):1570–1576. https://doi.org/10.1139/b92-198
Spanic V, Lemmens M, Drezner G (2010) Morphological and molecular identification of Fusarium species associated with head blight on wheat in East Croatia. European Journal of Plant Pathology 128(4):511–516. https://doi.org/10.1007/s10658-010-9682-1
Stȩpień Ł, Chełkowski J (2010) Fusarium head blight of wheat: pathogenic species and their mycotoxins. World Mycotoxin Journal 3(2):107–119. https://doi.org/10.3920/WMJ2009.1193
Touati-Hattab S, Barreau C, Verdal-Bonnin MN, Chereau S, Richard-Forget F, Hadjout S, Mekliche L, Bouznad Z (2016) Pathogenicity and trichothecenes production of Fusarium culmorum strains causing head blight on wheat and evaluation of resistance of the varieties cultivated in Algeria. European Journal of Plant Pathology 145(4):797–814. https://doi.org/10.1007/s10658-016-0869-y
Wagacha JM, Muthomi JW (2007) Fusarium culmorum: Infection process, mechanisms of mycotoxin production and their role in pathogenesis in wheat. Crop Protection 26(7):877–885. https://doi.org/10.1016/j.cropro.2006.09.003
Wang Y, Miller JD (1988) Effects of Fusarium graminearum metabolites on wheat tissue in relation to fusarium head blight resistance. Journal of Phytopathology 122:118–125. https://doi.org/10.1111/j.1439-0434.1988.tb00998.x
Wiwart M, Perkowski J, Budzyński W, Suchowilska E, Buśko M, Matysiak A (2011) Concentrations of ergosterol and trichothecenes in the grains of three triticum species. Czech Journal of Food Sciences 29(4):430–440. https://doi.org/10.17221/229/2010-CJFS
Yekkour A, Toumatia O, Meklat A, Verheecke C, Sabaou N, Zitouni A, Mathieu F (2015) Deoxynivalenol-producing ability of Fusarium culmorum strains and their impact on infecting barley in Algeria. World Journal of Microbiology and Biotechnology 31(6):875–881. https://doi.org/10.1007/s11274-015-1841-2
Zhao M, Wang G, Leng Y, Wanjugi H, Xi P, Grosz MD, Mergoum M, Zhong S (2018) Molecular mapping of fusarium head blight resistance in the spring wheat line ND2710. Phytopathology 108(8):972–979. https://doi.org/10.1094/PHYTO-12-17-0392-R
Zingales V, Fernández-Franzón M, Ruiz MJ (2021) Occurrence, mitigation and in vitro cytotoxicity of nivalenol, a type B trichothecene mycotoxin – Updates from the last decade (2010–2020). Food and Chemical Toxicology 152. https://doi.org/10.1016/j.fct.2021.112182
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