Physiological, genetic and transcriptional characterization of Fusarium graminearum isolates

Abstract

Fusarium graminearum is the primary cause of Fusarium head blight (FHB) epidemics world-wide. The characterization of F. graminearum isolates via physiological, genetic, and transcriptional analysis was aimed in the study. A total of 31 isolates and a reference strain were grown on potato dextrose agar (PDA) for 7 days. According to measurements on the 4th and 7th day of cultivation, their minimum and maximum mean linear growth rates (LGRs) were calculated as 9.62±0.44 to 13.32±0.69 mm/day, respectively. Isolates were grouped as x<10 mm/day and 10

Keywords

• Fusarium Graminearum
• Linear Growth Rate
• Gene Expression
• PCR-ITS-RFLP
• qRT-PCR

References

1. [1] Parry DW, Jenkinson P, McLeod L. Fusarium ear blight (scab) in small grain cereals—a review. Plant Pathol 1995;44:207238. [CrossRef]
2. [2] Goswami RS, Kistler HC. Heading for disaster: Fusarium graminearum on cereal crops. Mol Plant Pathol 2004; 5:515525. [CrossRef]
3. [3] Bai G, Shaner G. Management and resistance in wheat and barley to Fusarium head blight. Annu Rev Phytopathol 2004;42:135161. [CrossRef]
4. [4] Gutleb AC, Morrison E, Murk AJ. Cytotoxicity assays for mycotoxins produced by Fusarium strains: a review. Environ Toxicol Pharmacol 2002;11:309320. [CrossRef]
5. [5] Desjardins AE, Proctor RH. Molecular biology of Fusarium mycotoxins. Int J Food Microbiol 2007;119:4750. [CrossRef]
6. [6] Shin S, Son JH, Park JC, Kim KH, Yoon YM, Cheong YK, et al. Comparative pathogenicity of Fusarium graminearum isolates from wheat kernels in Korea. Plant Pathol J 2018;34:347. [CrossRef]
7. [7] McMullen M, Jones R, Gallenberg D. Scab of wheat and barley: a re-emerging disease of devastating impact. Plant Dis 1997;81:13401348. [CrossRef]
8. [8] Harris LJ, Desjardins AE, Plattner RD, Nicholson P, Butler G, Young JC, et al. Possible role of trichothecene mycotoxins in virulence of Fusarium graminearum on maize. Plant Dis 1999;83:954960. [CrossRef]

9. [9] Yazar S, Omurtag GZ. Fumonisins, trichothecenes and zearalenone in cereals. Int J Mol Sci 2008;9:20622090. [CrossRef]
10. [10] Mielniczuk E, Skwaryło-Bednarz B. Fusarium head blight, mycotoxins and strategies for their reduction. Agronomy 2020;10:509. [CrossRef]
11. [11] Kremery V, Jesenka Z, Spanik S, Gyarfas J, Nogova Botek R, et al. Fungemia due to Fusarium species in cancer patients. J Hosp Infect 1997;36:223228. [CrossRef]
12. [12] Mansoory D, Roozbahany NA, Mazinany H, Samimagam A. Chronic Fusarium infection in an adult patient with undiagnosed chronic granulomatous disease. Clin Infect Dis 2003;37:e107e108. [CrossRef]
13. [13] Nucci M, Elias A. "Fusarium infections in immunocompromised patients. CMR 2007;695704. [CrossRef]
14. [14] Muhammed M, Anagnostou T, Desalermos A, Kourkoumpetis TK, Carneiro HA, Glavis-Bloom J, et al. Fusarium infection: report of 26 cases and review of 97 cases from the literature. Medicine (Baltimore) 2013;92:305–316. [CrossRef]
15. [15] 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 Genet Biol 2008;45:473484. [CrossRef]
16. [16] Yli-Mattila T, Gagkaeva T. Molecular chemotyping of Fusarium graminearum, F. culmorum, and F. cerealis isolates from Finland and Russia. Berlin, Heidelberg, Springer; 2010. [CrossRef]
17. [17] Chilaka CA, De Boevre M, Atanda OO, De Saeger S. The status of Fusarium mycotoxins in sub-Saharan Africa: A review of emerging trends and post-harvest mitigation strategies towards food control. Toxins 2017;9:19. [CrossRef]
18. [18] O'Donnell K. Molecular phylogeny of the Nectria haematococca-Fusarium solani species complex. Mycologia 2000;92:919938. [CrossRef]
19. [19] Pasquali M, Beyer M, Logrieco A, Audenaert K, Balmas V, Basler R, et al. European database of Fusarium graminearum and F. culmorum trichothecene genotypes. Front Microbiol 2016;7:406. [CrossRef]
20. [20] Leslie JF, Summerell BA. The Fusarium Laboratory Manual. Ames, Iowa, Blackwell Professional; 2006.
21. [21] Puhalla JE. Classification of strains of Fusarium oxysporum on the basis of vegetative compatibility. Can J Bot 1985;63:179183. [CrossRef]
22. [22] Crous PW, Hawksworth DL, Wingfield MJ. Identifying and naming plant-pathogenic fungi: past, present, and future. Annu Rev Phytopathol 2015;53:247267. [CrossRef]
23. [23] Arif M, Zaidi NW, Haq QMR, Singh YP, Taj G, Kar CS, et al. Morphological and comparative genomic analyses of pathogenic and non-pathogenic Fusarium solani isolated from Dalbergia sissoo. Mol Biol Rep 2015;42:1107-1122. [CrossRef]
24. [24] Datta J, Lal N. Application of molecular markers for genetic discrimination of Fusarium wilt pathogen races affecting chickpea and pigeonpea in major regions of India. Cell Mol Biol 2012;58:5565.
25. [25] Nilsson RH, Ryberg M, Abarenkov K, Sjökvist E, Kristiansson E. The ITS region as a target for characterization of fungal communities using emerging sequencing technologies. FEMS Microbiol Lett 2009;296:97101. [CrossRef]
26. [26] Yahr R, Schoch CL, Dentinger BT. Scaling up discovery of hidden diversity in fungi: impacts of barcoding approaches. Philos Trans R Soc Lond B Biol Sci B 2016;371:20150336. [CrossRef]
27. [27] Rahman HU, Yue X, Ren X, Zhang W, Zhang Q, Li P. Multiplex PCR assay to detect Aspergillus, Penicillium and Fusarium species simultaneously. Food Addit Contam: Part A 2020;37;19391950.
28. [28] White TJ, Bruns TD, Lee SB, Taylor JW. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. New York, Academic Press; 1990. [CrossRef]
29. [29] Chehri, K, Salleh B, Yli-Mattila T, Reddy KRN, Abbasi S. Molecular characterization of pathogenic Fusarium species in cucurbit plants from Kermanshah province, Iran. Saudi J Biol Sci 2011;18:341351. [CrossRef]
30. [30] Kachuei R, Yadegari MH, Safaie N, Ghiasian A, Noorbakhsh F, Piranfar V, Rezaie S. PCR-RFLP patterns for the differentiation of the Fusarium species in virtue of ITS rDNA. Curr Med Mycol 2015;1:411. [CrossRef]
31. [31] Hou Z, Xue C, Peng Y, Katan T, Kistler HC, Xu JR. A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. MPMI 2002;15:11191127. [CrossRef]
32. [32] Irzykowska L, Bocianowski J, Baturo-Cieśniewska A. Association of mating-type with mycelium growth rate and genetic variability of Fusarium culmorum. Open Life Sci 2013;8:701711. [CrossRef]
33. [33] Jiang J, Liu X, Yin Y, Ma Z. Involvement of a velvet protein FgVeA in the regulation of asexual development, lipid and secondary metabolisms and virulence in Fusarium graminearum. PloS One 2011;6:e28291. [CrossRef]
34. [34] Pasquali M, Spanu F, Scherm B, Balmas V, Hoffmann L, Hammond-Kosack KE, et al. FcStuA from Fusarium culmorum controls wheat foot and root rot in a toxin dispensable manner. PLoS One 2013;8:e57429. [CrossRef]
35. [35] Yörük E, Sefer Ö. FcMgv1, FcStuA and FcVeA based genetic characterization in fusarium culmorum (WG Smith). Trak Univ J Nat Sci 2018;19:6369. [CrossRef]
36. [36] Haratian M, Sharifnabi B, Alizadeh A, Safaie N. PCR analysis of the Tri13 gene to determine the genetic potential of Fusarium graminearum isolates from Iran to produce nivalenol and deoxynivalenol. Mycopathologia 2008;166:109116. [CrossRef]
37. [37] Popiel D, Kwasna A, Chelkowski J, Stepien L, Laskowska M. Impact of selected antagonistic fungi on Fusarium species-toxigenic cereal pathogens. Acta Mycol 2008;43:2940. [CrossRef]
38. [38] O'Donnell K. Fusarium and its near relatives. The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. Wallingford, UK, CAB International; 1993.
39. [39] Miedaner T, Cumagun CJR, Chakraborty S. Population genetics of three important head blight pathogens Fusarium graminearum, F. pseudograminearum and F. culmorum. J Phytopathol 2008;156:129139. [CrossRef]
40. [40] Albayrak G, Yörük E, Gazdağli A, Sharifnabi B. Genetic diversity among Fusarium graminearum and F. culmorum isolates based on ISSR markers. Arch Biol Sci 2016;68:333343. [CrossRef]
41. [41] Konstantinova P, Yli-Mattila T. IGS–RFLP analysis and development of molecular markers for identification of Fusarium poae, Fusarium langsethiae, Fusarium sporotrichioides and Fusarium kyushuense. Int J Food Microbiol 2004;95: 321331. [CrossRef]
42. [42] Llorens A, Hinojo MJ, Mateo R, Gonzalez-Jaen MT, Valle-Algarra FM, Logrieco A, Jiménez M. Characterization of Fusarium spp. isolates by PCR-RFLP analysis of the intergenic spacer region of the rRNA gene (rDNA). Int J Food Microbiol 2006;106:297306. [CrossRef]
43. [43] O'Donnell K. Ribosomal DNA internal transcribed spacers are highly divergent in the phytopathogenic ascomycete Fusarium sambucinum (Gibberella pulicaris). Curr Genet 1992;22:213220. [CrossRef]
44. [44] Duggal A, Dumas MT, Jeng RS, Hubbes M. Ribosomal variation in six species of shape Fusarium. Mycopathologia 1997;140:3549. [CrossRef]
45. [45] O'Donnell K, Cigelnik E. Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylogenet Evol 1997;7:103116. [CrossRef]
46. [46] Okeke CN, Kappe R, Zakikhani S, Nolte O, Sonntag HG. Ribosomal genes of Histoplasma capsulatum var. duboisii and var. farciminosum. Mycoses 1998;41:355362. [CrossRef]
47. [47] Iwen PC, Hinrichs SH, Rupp ME. Utilization of the internal transcribed spacer regions as molecular targets to detect and identify human fungal pathogens. Med Mycol 2002;40:87109. [CrossRef]
48. [48] Diguță CF, Proca IG, Jurcoane Ș, Matei F. Molecular characterization by PCR-RFLP of indigenous fungal isolates from hypersaline stream water in România. Folia Microbiol 2019;64:407414. [CrossRef]
49. [49] Yun Y, Liu Z, Zhang J, Shim WB, Chen Y, Ma Z. The MAPKK FgMkk1 of Fusarium graminearum regulates vegetative differentiation, multiple stress response, and virulence via the cell wall integrity and high‐osmolarity glycerol signaling pathways. Environ Microbiol 2014;16:20232037. [CrossRef]
50. [50] Kimura M, Tokai T, Takahashi-Ando N, Ohsato S, Fujimura M. Molecular and genetic studies of Fusarium trichothecene biosynthesis: pathways, genes, and evolution. Biosci Biotechnol Biochem 2007;71:2105-2123. [CrossRef]
51. [51] Yörük E, Albayrak G. Tri4 and tri5 gene expression analysis in Fusarium graminearum and F. culmorum isolates by qPCR. Plant Pathol J 2014;13:133. [CrossRef]
52. [52] Yörük E, Albayrak G. siRNA quelling of tri4 and tri5 genes related to deoxynivalenol synthesis in Fusarium graminearum and Fusarium culmorum. J Environ Biol 2019;40:370376. [CrossRef]
53. [53] Kim HK, Jo SM, Kim GY, Kim DW, Kim YK, Yun SH. A large-scale functional analysis of putative target genes of mating-type loci provides insight into the regulation of sexual development of the cereal pathogen Fusarium graminearum. PLOS Genet 2015;11:e1005486. [CrossRef]
54. [54] Wilson AM, Wilken PM, van der Nest MA, Wingfield MJ, Wingfiel BD. It’s all in the genes: the regulatory pathways of sexual reproduction in filamentous ascomycetes. Genes 2019;10:330. [CrossRef]

Details

Primary Language

English

Subjects

Structural Biology

Journal Section

Research Article

Authors

Tuğba Teker
Türkiye

Syeda Anum Khalid This is me
0000-0002-6705-4228
Türkiye

Emre Yörük
Türkiye

Gülruh Albayrak ^*
Türkiye

Publication Date

April 30, 2024

Submission Date

April 1, 2022

Acceptance Date

May 28, 2022

Published in Issue

Year 2024 Volume: 42 Number: 2

IZ

https://izlik.org/JA34XL68EX

Cite

RIS / Bibtex

APA

Teker, T., Khalid, S. A., Yörük, E., & Albayrak, G. (2024). Physiological, genetic and transcriptional characterization of Fusarium graminearum isolates. Sigma Journal of Engineering and Natural Sciences, 42(2), 450-458. https://izlik.org/JA34XL68EX

AMA

1.Teker T, Khalid SA, Yörük E, Albayrak G. Physiological, genetic and transcriptional characterization of Fusarium graminearum isolates. SIGMA. 2024;42(2):450-458. https://izlik.org/JA34XL68EX

Chicago

Teker, Tuğba, Syeda Anum Khalid, Emre Yörük, and Gülruh Albayrak. 2024. “Physiological, Genetic and Transcriptional Characterization of Fusarium Graminearum Isolates”. Sigma Journal of Engineering and Natural Sciences 42 (2): 450-58. https://izlik.org/JA34XL68EX.

EndNote

Teker T, Khalid SA, Yörük E, Albayrak G (April 1, 2024) Physiological, genetic and transcriptional characterization of Fusarium graminearum isolates. Sigma Journal of Engineering and Natural Sciences 42 2 450–458.

IEEE

[1]T. Teker, S. A. Khalid, E. Yörük, and G. Albayrak, “Physiological, genetic and transcriptional characterization of Fusarium graminearum isolates”, SIGMA, vol. 42, no. 2, pp. 450–458, Apr. 2024, [Online]. Available: https://izlik.org/JA34XL68EX

ISNAD

Teker, Tuğba - Khalid, Syeda Anum - Yörük, Emre - Albayrak, Gülruh. “Physiological, Genetic and Transcriptional Characterization of Fusarium Graminearum Isolates”. Sigma Journal of Engineering and Natural Sciences 42/2 (April 1, 2024): 450-458. https://izlik.org/JA34XL68EX.

JAMA

1.Teker T, Khalid SA, Yörük E, Albayrak G. Physiological, genetic and transcriptional characterization of Fusarium graminearum isolates. SIGMA. 2024;42:450–458.

MLA

Teker, Tuğba, et al. “Physiological, Genetic and Transcriptional Characterization of Fusarium Graminearum Isolates”. Sigma Journal of Engineering and Natural Sciences, vol. 42, no. 2, Apr. 2024, pp. 450-8, https://izlik.org/JA34XL68EX.

Vancouver

1.Tuğba Teker, Syeda Anum Khalid, Emre Yörük, Gülruh Albayrak. Physiological, genetic and transcriptional characterization of Fusarium graminearum isolates. SIGMA [Internet]. 2024 Apr. 1;42(2):450-8. Available from: https://izlik.org/JA34XL68EX

References

1. [1] Parry DW, Jenkinson P, McLeod L. Fusarium ear blight (scab) in small grain cereals—a review. Plant Pathol 1995;44:207238. [CrossRef]
2. [2] Goswami RS, Kistler HC. Heading for disaster: Fusarium graminearum on cereal crops. Mol Plant Pathol 2004; 5:515525. [CrossRef]
3. [3] Bai G, Shaner G. Management and resistance in wheat and barley to Fusarium head blight. Annu Rev Phytopathol 2004;42:135161. [CrossRef]
4. [4] Gutleb AC, Morrison E, Murk AJ. Cytotoxicity assays for mycotoxins produced by Fusarium strains: a review. Environ Toxicol Pharmacol 2002;11:309320. [CrossRef]
5. [5] Desjardins AE, Proctor RH. Molecular biology of Fusarium mycotoxins. Int J Food Microbiol 2007;119:4750. [CrossRef]
6. [6] Shin S, Son JH, Park JC, Kim KH, Yoon YM, Cheong YK, et al. Comparative pathogenicity of Fusarium graminearum isolates from wheat kernels in Korea. Plant Pathol J 2018;34:347. [CrossRef]
7. [7] McMullen M, Jones R, Gallenberg D. Scab of wheat and barley: a re-emerging disease of devastating impact. Plant Dis 1997;81:13401348. [CrossRef]
8. [8] Harris LJ, Desjardins AE, Plattner RD, Nicholson P, Butler G, Young JC, et al. Possible role of trichothecene mycotoxins in virulence of Fusarium graminearum on maize. Plant Dis 1999;83:954960. [CrossRef]

9. [9] Yazar S, Omurtag GZ. Fumonisins, trichothecenes and zearalenone in cereals. Int J Mol Sci 2008;9:20622090. [CrossRef]
10. [10] Mielniczuk E, Skwaryło-Bednarz B. Fusarium head blight, mycotoxins and strategies for their reduction. Agronomy 2020;10:509. [CrossRef]
11. [11] Kremery V, Jesenka Z, Spanik S, Gyarfas J, Nogova Botek R, et al. Fungemia due to Fusarium species in cancer patients. J Hosp Infect 1997;36:223228. [CrossRef]
12. [12] Mansoory D, Roozbahany NA, Mazinany H, Samimagam A. Chronic Fusarium infection in an adult patient with undiagnosed chronic granulomatous disease. Clin Infect Dis 2003;37:e107e108. [CrossRef]
13. [13] Nucci M, Elias A. "Fusarium infections in immunocompromised patients. CMR 2007;695704. [CrossRef]
14. [14] Muhammed M, Anagnostou T, Desalermos A, Kourkoumpetis TK, Carneiro HA, Glavis-Bloom J, et al. Fusarium infection: report of 26 cases and review of 97 cases from the literature. Medicine (Baltimore) 2013;92:305–316. [CrossRef]
15. [15] 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 Genet Biol 2008;45:473484. [CrossRef]
16. [16] Yli-Mattila T, Gagkaeva T. Molecular chemotyping of Fusarium graminearum, F. culmorum, and F. cerealis isolates from Finland and Russia. Berlin, Heidelberg, Springer; 2010. [CrossRef]
17. [17] Chilaka CA, De Boevre M, Atanda OO, De Saeger S. The status of Fusarium mycotoxins in sub-Saharan Africa: A review of emerging trends and post-harvest mitigation strategies towards food control. Toxins 2017;9:19. [CrossRef]
18. [18] O'Donnell K. Molecular phylogeny of the Nectria haematococca-Fusarium solani species complex. Mycologia 2000;92:919938. [CrossRef]
19. [19] Pasquali M, Beyer M, Logrieco A, Audenaert K, Balmas V, Basler R, et al. European database of Fusarium graminearum and F. culmorum trichothecene genotypes. Front Microbiol 2016;7:406. [CrossRef]
20. [20] Leslie JF, Summerell BA. The Fusarium Laboratory Manual. Ames, Iowa, Blackwell Professional; 2006.
21. [21] Puhalla JE. Classification of strains of Fusarium oxysporum on the basis of vegetative compatibility. Can J Bot 1985;63:179183. [CrossRef]
22. [22] Crous PW, Hawksworth DL, Wingfield MJ. Identifying and naming plant-pathogenic fungi: past, present, and future. Annu Rev Phytopathol 2015;53:247267. [CrossRef]
23. [23] Arif M, Zaidi NW, Haq QMR, Singh YP, Taj G, Kar CS, et al. Morphological and comparative genomic analyses of pathogenic and non-pathogenic Fusarium solani isolated from Dalbergia sissoo. Mol Biol Rep 2015;42:1107-1122. [CrossRef]
24. [24] Datta J, Lal N. Application of molecular markers for genetic discrimination of Fusarium wilt pathogen races affecting chickpea and pigeonpea in major regions of India. Cell Mol Biol 2012;58:5565.
25. [25] Nilsson RH, Ryberg M, Abarenkov K, Sjökvist E, Kristiansson E. The ITS region as a target for characterization of fungal communities using emerging sequencing technologies. FEMS Microbiol Lett 2009;296:97101. [CrossRef]
26. [26] Yahr R, Schoch CL, Dentinger BT. Scaling up discovery of hidden diversity in fungi: impacts of barcoding approaches. Philos Trans R Soc Lond B Biol Sci B 2016;371:20150336. [CrossRef]
27. [27] Rahman HU, Yue X, Ren X, Zhang W, Zhang Q, Li P. Multiplex PCR assay to detect Aspergillus, Penicillium and Fusarium species simultaneously. Food Addit Contam: Part A 2020;37;19391950.
28. [28] White TJ, Bruns TD, Lee SB, Taylor JW. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. New York, Academic Press; 1990. [CrossRef]
29. [29] Chehri, K, Salleh B, Yli-Mattila T, Reddy KRN, Abbasi S. Molecular characterization of pathogenic Fusarium species in cucurbit plants from Kermanshah province, Iran. Saudi J Biol Sci 2011;18:341351. [CrossRef]
30. [30] Kachuei R, Yadegari MH, Safaie N, Ghiasian A, Noorbakhsh F, Piranfar V, Rezaie S. PCR-RFLP patterns for the differentiation of the Fusarium species in virtue of ITS rDNA. Curr Med Mycol 2015;1:411. [CrossRef]
31. [31] Hou Z, Xue C, Peng Y, Katan T, Kistler HC, Xu JR. A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. MPMI 2002;15:11191127. [CrossRef]
32. [32] Irzykowska L, Bocianowski J, Baturo-Cieśniewska A. Association of mating-type with mycelium growth rate and genetic variability of Fusarium culmorum. Open Life Sci 2013;8:701711. [CrossRef]
33. [33] Jiang J, Liu X, Yin Y, Ma Z. Involvement of a velvet protein FgVeA in the regulation of asexual development, lipid and secondary metabolisms and virulence in Fusarium graminearum. PloS One 2011;6:e28291. [CrossRef]
34. [34] Pasquali M, Spanu F, Scherm B, Balmas V, Hoffmann L, Hammond-Kosack KE, et al. FcStuA from Fusarium culmorum controls wheat foot and root rot in a toxin dispensable manner. PLoS One 2013;8:e57429. [CrossRef]
35. [35] Yörük E, Sefer Ö. FcMgv1, FcStuA and FcVeA based genetic characterization in fusarium culmorum (WG Smith). Trak Univ J Nat Sci 2018;19:6369. [CrossRef]
36. [36] Haratian M, Sharifnabi B, Alizadeh A, Safaie N. PCR analysis of the Tri13 gene to determine the genetic potential of Fusarium graminearum isolates from Iran to produce nivalenol and deoxynivalenol. Mycopathologia 2008;166:109116. [CrossRef]
37. [37] Popiel D, Kwasna A, Chelkowski J, Stepien L, Laskowska M. Impact of selected antagonistic fungi on Fusarium species-toxigenic cereal pathogens. Acta Mycol 2008;43:2940. [CrossRef]
38. [38] O'Donnell K. Fusarium and its near relatives. The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. Wallingford, UK, CAB International; 1993.
39. [39] Miedaner T, Cumagun CJR, Chakraborty S. Population genetics of three important head blight pathogens Fusarium graminearum, F. pseudograminearum and F. culmorum. J Phytopathol 2008;156:129139. [CrossRef]
40. [40] Albayrak G, Yörük E, Gazdağli A, Sharifnabi B. Genetic diversity among Fusarium graminearum and F. culmorum isolates based on ISSR markers. Arch Biol Sci 2016;68:333343. [CrossRef]
41. [41] Konstantinova P, Yli-Mattila T. IGS–RFLP analysis and development of molecular markers for identification of Fusarium poae, Fusarium langsethiae, Fusarium sporotrichioides and Fusarium kyushuense. Int J Food Microbiol 2004;95: 321331. [CrossRef]
42. [42] Llorens A, Hinojo MJ, Mateo R, Gonzalez-Jaen MT, Valle-Algarra FM, Logrieco A, Jiménez M. Characterization of Fusarium spp. isolates by PCR-RFLP analysis of the intergenic spacer region of the rRNA gene (rDNA). Int J Food Microbiol 2006;106:297306. [CrossRef]
43. [43] O'Donnell K. Ribosomal DNA internal transcribed spacers are highly divergent in the phytopathogenic ascomycete Fusarium sambucinum (Gibberella pulicaris). Curr Genet 1992;22:213220. [CrossRef]
44. [44] Duggal A, Dumas MT, Jeng RS, Hubbes M. Ribosomal variation in six species of shape Fusarium. Mycopathologia 1997;140:3549. [CrossRef]
45. [45] O'Donnell K, Cigelnik E. Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylogenet Evol 1997;7:103116. [CrossRef]
46. [46] Okeke CN, Kappe R, Zakikhani S, Nolte O, Sonntag HG. Ribosomal genes of Histoplasma capsulatum var. duboisii and var. farciminosum. Mycoses 1998;41:355362. [CrossRef]
47. [47] Iwen PC, Hinrichs SH, Rupp ME. Utilization of the internal transcribed spacer regions as molecular targets to detect and identify human fungal pathogens. Med Mycol 2002;40:87109. [CrossRef]
48. [48] Diguță CF, Proca IG, Jurcoane Ș, Matei F. Molecular characterization by PCR-RFLP of indigenous fungal isolates from hypersaline stream water in România. Folia Microbiol 2019;64:407414. [CrossRef]
49. [49] Yun Y, Liu Z, Zhang J, Shim WB, Chen Y, Ma Z. The MAPKK FgMkk1 of Fusarium graminearum regulates vegetative differentiation, multiple stress response, and virulence via the cell wall integrity and high‐osmolarity glycerol signaling pathways. Environ Microbiol 2014;16:20232037. [CrossRef]
50. [50] Kimura M, Tokai T, Takahashi-Ando N, Ohsato S, Fujimura M. Molecular and genetic studies of Fusarium trichothecene biosynthesis: pathways, genes, and evolution. Biosci Biotechnol Biochem 2007;71:2105-2123. [CrossRef]
51. [51] Yörük E, Albayrak G. Tri4 and tri5 gene expression analysis in Fusarium graminearum and F. culmorum isolates by qPCR. Plant Pathol J 2014;13:133. [CrossRef]
52. [52] Yörük E, Albayrak G. siRNA quelling of tri4 and tri5 genes related to deoxynivalenol synthesis in Fusarium graminearum and Fusarium culmorum. J Environ Biol 2019;40:370376. [CrossRef]
53. [53] Kim HK, Jo SM, Kim GY, Kim DW, Kim YK, Yun SH. A large-scale functional analysis of putative target genes of mating-type loci provides insight into the regulation of sexual development of the cereal pathogen Fusarium graminearum. PLOS Genet 2015;11:e1005486. [CrossRef]
54. [54] Wilson AM, Wilken PM, van der Nest MA, Wingfield MJ, Wingfiel BD. It’s all in the genes: the regulatory pathways of sexual reproduction in filamentous ascomycetes. Genes 2019;10:330. [CrossRef]