Distinction of Fusarium temperatum and F. subglutinans in the F. fujikuroi species complex

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Fusarium strains isolated from the different plant hosts and formerly identified as Fusarium subglutinans s. l. according to morphological characteristics were analyzed in detail. Based on phylogenetic analysis of three loci (TEF, tub, and RPB2) two strains isolated from stem of wheat and root of rape were re-identified as F. temperatum. This is first report of rape and wheat as a novel plant host for F. temperatum that mainly associated with maize. This is also the first detection of F. temperatum in Russia. Other strains turned out to be F. subglutinans s.str. The examination of morphological characters has not revealed remarkable variation between the species: the features of F. temperatum and F. subglutinans are sufficiently similar to exclude confidence in identification based on visual assessment. Two F. temperatum strains possess alternate MAT idiomorphs, whereas the both F. subglutinans strains contain only MAT-1 idiomorph. Fertile crossings were observed between two F. temperatum strains in the laboratory conditions. Both F. temperatum strains produced beauvericin in high amounts of 1665 and 6106 μg kg-1 in contrast to F. subglutinans strains. Additionally, one F. temperatum strain produced 3407 μg kg-1 moniliformin. No one from the analyzed strains produced the fumonisins. The differentiation of the F. temperatum and F. subglutinans species is possible only with the involvement of molecular genetics and chemotaxonomic methods.

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T. Gagkaeva

All-Russian Institute of Plant Protection

编辑信件的主要联系方式.
Email: t.gagkaeva@mail.ru
俄罗斯联邦, St. Petersburg

O. Gavrilova

All-Russian Institute of Plant Protection

Email: olgavrilova1@yandex.ru
俄罗斯联邦, St. Petersburg

A. Orina

All-Russian Institute of Plant Protection

Email: orina-alex@yandex.ru
俄罗斯联邦, St. Petersburg

参考

  1. Al-Hatmi A., Sandoval-Denis M., Nabet C. et al. Fusarium volatile, a new potential pathogen from a human respiratory sample. Fungal Syst. Evol. 2019. V. 4. P. 171–181. https://doi.org/10.3114/fuse.2019.04.09
  2. Bömke C., Tudzynski B. Diversity, regulation, and evolution of the gibberellin biosynthetic pathway in fungi compared to plants and bacteria. Phytochemistry. 2009. V. 70. P. 1876–1893. https://doi.org/10.1016/j.phytochem.2009.05.020
  3. Boutigny A.L., Scauflaire J., Ballois N. et al. Fusarium temperatum isolated from maize in France. Eur. J. Plant Pathol. 2017. V. 148. P. 997–1001. https://doi.org/10.1007/s10658–016–1137-x
  4. Brankovics B., van Dam P., Rep M. et al. Mitochondrial genomes reveal recombination in the presumed asexual Fusarium oxysporum species complex. BMC Genomics. 2017. V. 18. P. 735. https://doi.org/10.1186/s12864–017–4116–5
  5. Britz H., Steenkamp E.T., Coutinho T.A. et al. Two new species of Fusarium section Liseola associated with mango malformation. Mycologia. 2002. V. 94. P. 722–730. https://doi.org/10.2307/3761722
  6. Campos-Macías P., Arenas-Guzmán R., Hernández-Hernández F. Fusarium subglutinans: A new eumycetoma agent. Med. Mycol. Case. 2013. V. 2. P. 128–131. https://doi.org/10.1016/j.mmcr.2013.06.004
  7. Cosic J., Jurkovic D., Vrandecic K. et al. Pathogenicity of Fusarium species to wheat and barley ears. Cereal Res. Commun. 2007. V. 35. P. 529–532. https://doi.org/10.1556/crc.35.2007.2.91
  8. Costa M.M., Melo M.P., Carmo F.S. et al. Fusarium species from tropical grasses in Brazil and description of two new taxa. Mycol. Progress. 2021. V. 20. P. 61–72. https://doi.org/10.1007/s11557–020–01658–5
  9. Crous P.W., Lombard L., Sandoval-Denis M. et al. Fusarium: more than a node or a foot-shaped basal cell. Stud. Mycol. 2021. V. 98. P. e100116. https://doi.org/10.1016/j.simyco.2021.100116
  10. Czembor E., Stępień Ł., Waśkiewicz A. Effect of environmental factors on Fusarium species and associated mycotoxins in maize grain grown in Poland. PLOS One. 2015. V. 10. P. e0133644. https://doi.org/10.1371/journal.pone.0133644
  11. Demirözer O. Target-oriented dissemination of the entomopathogenic fungus Fusarium subglutinans 12A by the Western Flower Thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Phytoparasitica. 2019. V. 47. P. 393–403. https://doi.org/10.1007/s12600–019–00728-z
  12. Dewing C., Van der Nest M.A., Santana Q.C. et al. Characterization of host-specific genes from pine- and grass-associated species of the Fusarium fujikuroi species complex. Pathogens. 2022. V. 11. P. 858. https://doi.org/10.3390/pathogens11080858
  13. Fallahi M., Saremi H., Javan-Nikkhah M. et al. Isolation, molecular identification and mycotoxin profile of Fusarium species isolated from maize kernels in Iran. Toxins. 2019. V. 11. P. 297. https://doi.org/10.3390/toxins11050297
  14. Fumero M.V., Reynoso M.M., Chulze S. Fusarium temperatum and Fusarium subglutinans isolated from maize in Argentina. Int. J. Food Microbiol. 2015. V. 199. P. 86–92. https://doi.org/10.1016/j.ijfoodmicro.2015.01.011
  15. Fumero M.V., Villani A., Susca A. et al. Fumonisin and beauvericin chemotypes and genotypes of the sister species Fusarium subglutinans and Fusarium temperatum. Appl. Environ. Microbiol. 2020. V. 86. P. e00133–20. https://doi.org/10.1128/AEM.00133–20
  16. Geiser D.M., Ivey M.L., Hakiza G. et al. Gibberella xylarioides (anamorph: Fusarium xylarioides), a causative agent of coffee wilt disease in Africa, is a previously unrecognized member of the G. fujikuroi species complex. Mycologia. 2005. V. 97. P. 191–201. https://doi.org/10.3852/mycologia.97.1.191
  17. Glenn A.E., Richardson E.A., Bacon C.W. Genetic and morphological characterization of a Fusarium verticillioides conidiation mutant. Mycologia. 2004. V. 96. P. 968–980. https://doi.org/10.2307/3762081
  18. Jewell L.E., Hsiang T. Multigene differences between Microdochium nivale and Microdochium majus. Botany. 2013. V. 91. P. 99–106. https://doi.org/10.1139/cjb-2012–0178
  19. Kumar S., Stecher G., Li M. et al. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molec. Biol. Evol. 2018. V. 35. P. 1547–1549. https://doi.org/10.1093/molbev/msy096
  20. Lanza F.E., Mayfield D.A., Munkvold G.P. First report of Fusarium temperatum causing maize seedling blight and seed rot in North America. Plant Disease. 2016. V. 100. P. 1019. https://doi.org/10.1094/PDIS-11-15-1301-PDN
  21. Leslie J.F., Summerell B.A. The Fusarium laboratory manual. Blackwell Professional, Ames, 2006.
  22. Levic J., Munaut F., Scauflaire J. et al. Polyphasic approach used for distinguishing Fusarium temperatum from Fusarium subglutinans. J. Agric. Sci. Technol. 2019. V. 21. P. 221–232. http://r.istocar.bg.ac.rs/handle/123456789/614
  23. Lima C.S., Pfenning L.H., Costa S.S. et al. Fusarium tupiense sp. nov., a member of the Gibberella fujikuroi complex that causes mango malformation in Brazil. Mycologia. 2012. V. 104. P. 1408–1419. https://doi.org/10.3852/12-052
  24. Liu Y.J., Wehlen S., Hall B.D. Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Molec. Biol. Evol. 1999. V. 16. P. 1799–1808. https://doi.org/10.1093/oxfordjournals.molbev.a026092
  25. Lord E., Leclercq M., Boc A. et al. Armadillo 1.1: An original workflow platform for designing and conducting phylogenetic analysis and simulations. PLOS One. 2012. V. 7. P. e29903. https://doi.org/10.1371/journal.pone.002990
  26. Malachová A., Sulyok M., Beltrán E. et al. Optimization and validation of a quantitative liquid chromatography-tandem mass spectrometric method covering 295 bacterial and fungal metabolites including all regulated mycotoxins in four model food matrices. J. Chromatogr. A. 2014. V. 1362. P. 145–156. https://doi.org/10.1016/j.chroma.2014.08.037
  27. Moretti A., Mulé G., Ritieni A. et al. Cryptic subspecies and beauvericin production by Fusarium subglutinans from Europe. Int. J. Food Microbiol. 2008. V. 127. P. 312–315. https://doi.org/10.1016/j.ijfoodmicro.2008.08.003
  28. Nelson P.E., Toussoun T.A., Marasas W.F.O. Fusarium species: an illustrated manual for identification. The Pennsylvania State University Press. 1983.
  29. Niehaus E.-M., Münsterkötter M., Proctor R.H. et al. Comparative “omics” of the Fusarium fujikuroi species complex highlights differences in genetic potential and metabolite synthesis. Genome Biol. Evol. 2016. V. 8. P. 3574–3599. https://doi.org/10.1093/gbe/evw259
  30. Nirenberg H.I., O’Donnell K. New Fusarium species and combinations within the Gibberella fujikuroi species complex. Mycologia. 1998. V. 90. P. 434–458. https://doi.org/10.2307/3761403.
  31. 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. P. 103–116. https://doi.org/10.1006/mpev.1996.0376
  32. O’Donnell K., Cigelnik E., Nirenberg H.I. Molecular systematics and phylogeography of the Gibberella fujikuroi species complex. Mycologia. 1998. V. 90. P. 465–493. https://doi.org/10.1080/00275514.1998.12026933
  33. O’Donnell K., Nirenberg H.I., Aoki T. et al. A multigene phylogeny of the Gibberella fujikuroi species complex: detection of additionally phylogenetically distinct species. Mycoscience. 2000. V. 41. P. 61–78. https://doi.org/10.1007/BF02464387
  34. O‘Donnell K., Sarver B.A., Brandt M. et al. Phylogenetic diversity and microsphere array-based genotyping of human pathogenic Fusaria, including isolates from the multistate contact lens-associated U.S. keratitis outbreaks of 2005 and 2006. J. Clin. Microbiol. 2007. V. 45. P. 2235–2248. https://doi.org/10.1128/JCM.00533–07
  35. O’Donnell K., Rooney A.P., Proctor R.H. et al. Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria. Fungal Gen. Biol. 2013. V. 52. P. 20–31. https://doi.org/10.1016/j.fgb.2012.12.004
  36. Okello P.N., Mathew F.M. Cross pathogenicity studies show South Dakota isolates of Fusarium acuminatum, F. equiseti, F. graminearum, F. oxysporum, F. proliferatum, F. solani, and F. subglutinans from either soybean or corn are pathogenic to both crops. Plant Health Prog. 2019. V. 20. P. 44–49. https://doi.org/10.1094/PHP-10–18–0056-RS
  37. Pérez-Vázquez M.A.K., Morales-Mora L.A., Romero-Arenas O. et al. First report of Fusarium temperatum causing fruit blotch of Capsicum pubescens in Puebla, México. Plant Dis. 2022. V. 106. 1758. https://doi.org/10.1094/PDIS-09–21–1941-PDN
  38. Pfordt A., Schiwek S., Rathgeb A. et al. Occurrence, pathogenicity, and mycotoxin production of Fusarium temperatum in relation to other Fusarium species on maize in Germany. Pathogens. 2020. V. 9. P. 864. https://doi.org/10.3390/pathogens9110864
  39. Proctor R.H., Van Hove F., Susca A. et al. Birth, death and horizontal transfer of the fumonisin biosynthetic gene cluster during the evolutionary diversification of Fusarium. Mol. Microbiol. 2013. V. 90. P. 290–306. https://doi.org/10.1111/mmi.12362.
  40. Qiu J., Lu Y., He D. et al. Fusarium fujikuroi species complex associated with rice, maize, and soybean from Jiangsu Province, China: phylogenetic, pathogenic, and toxigenic analysis. Plant Dis. 2020. V. 104. P. 2193–2201. https://doi.org/10.1094/PDIS-09-19-1909-RE
  41. Robles-Barrios F., Ramírez-Granillo A., Medina-Canales M.G. et al. Fusarium temperatum shows a hemibiotrophic infection process and differential pathogenicity over different maize breeds from Mexico. J. Phytopathol. 2022. V. 170. P. 21–33. https://doi.org/10.1111/jph.13052
  42. Scauflaire J., Gourgue M., Callebaut A. et al. Fusarium temperatum, a mycotoxin-producing pathogen of maize. Eur. J. Plant Pathol. 2012. V. 133. P. 911–922. https://doi.org/10.1007/s10658-012-9958-8
  43. Scauflaire J., Gourgue M., Munaut F. Fusarium temperatum sp. nov. from maize, an emergent species closely related to Fusarium subglutinans. Mycologia. 2011. V. 103. P. 586–597. https://doi.org/10.3852/10–135
  44. Shin J.H., Han J.H., Lee J.K. et al. Characterization of the maize stalk rot pathogens Fusarium subglutinans and F. temperatum and the effect of fungicides on their mycelial growth and colony formation. Plant Pathol. J. 2014. V. 30. P. 397–406. https://doi.org/10.5423/PPJ.OA.08.2014.0078
  45. Steenkamp E.T., Wingfield B.D., Coutinho T.A. et al. PCR-based identification of MAT-1 and MAT-2 in the Gibberella fujikuroi species complex. Appl. Environ. Microbiol. 2000. V. 66. P. 4378–4382. https://doi.org/10.1128/AEM.66.10.4378–4382.2000
  46. Steenkamp E.T., Wingfield B.D., Desjardins A.E. et al. Cryptic speciation in Fusarium subglutinans. Mycologia. 2002. V. 94. P. 1032–1035. https://doi.org/10.2307/3761868
  47. Stępień Ł., Gromadzka K., Chełkowski J. et al. Diversity and mycotoxin production by Fusarium temperatum and Fusarium subglutinans as causal agents of pre-harvest Fusarium maize ear rot in Poland. J. Appl. Genet. 2019. V. 60. P. 113–121. https://doi.org/10.1007/s13353-018-0478-x
  48. Tsavkelova E., Oeser B., Oren-Young L. et al. Identification and functional characterization of indole-3-acetamide-mediated IAA biosynthesis in plant-associated Fusarium species. Fungal Genet. Biol. 2012. V. 49. P. 48–57. https://doi.org/10.1016/j.fgb.2011.10.005
  49. Tudzynski B., Hölter K. Gibberellin biosynthetic pathway in Gibberella fujikuroi: evidence for a gene cluster. Fungal Genet. Biol. 1998. V. 25. P. 157–170. https://doi.org/10.1006/fgbi.1998.1095
  50. Van Hove F., Waalwijk C., Logrieco A. et al. Gibberella musae (Fusarium musae) sp. nov., a recently discovered species from banana is sister to F. verticillioides. Mycologia. 2011. V. 103. P. 570–585. https://doi.org/10.3852/10–038
  51. Vermeulen M., Rothmann L.A., Swart W.J. et al. Fusarium casha sp. nov. and F. curculicola sp. nov. in the Fusarium fujikuroi species complex isolated from Amaranthus cruentus and threeweevil species in South Africa. Diversity. 2021. V. 13. 472. https://doi.org/10.3390/d13100472
  52. Vrabka J., Niehaus E.-M., Münsterkötter M. et al. Production and role of hormones during interaction of Fusarium species with maize (Zea mays L.) seedlings. Front. Plant Sci. 2019. V. 9. 1936. https://doi.org/10.3389/fpls.2018.01936.
  53. Wang J.-H., Zhang J.-B., Li H.-P. et al. Molecular identification, mycotoxin production and comparative pathogenicity of Fusarium temperatum isolated from maize in China. J. Phytopathol. 2014. V. 162. P. 147–157. https://doi.org/10.1111/jph.12164
  54. Wang M.M., Crous P.W., Sandoval-Denis M. et al. Fusarium and allied genera from China: species diversity and distribution. Persoonia. 2022. V. 48. P. 1–53. https://doi.org/10.3767/persoonia.2022.48.01
  55. Wit M., Ochodzki P., Warzecha R. et al. Influence of endosperm starch composition on maize response to Fusarium temperatum Scaufl. et Munaut. Toxins. 2022. V. 14. P. 200. https://doi.org/10.3390/toxins14030200
  56. Xi K., Shan L., Yang Y. et al. Species diversity and chemotypes of Fusarium species associated with maize stalk rot in Yunnan province of Southwest China. Front. Microbiol. 2021. V. 12. P. 652062. https://doi.org/10.3389/fmicb.2021.652062
  57. Yang X., Xu X., Wang S. et al. Identification, pathogenicity, and genetic diversity of Fusarium spp. associated with maize sheath rot in Heilongjiang Province, China. Int. J. Mol. Sci. 2022. V. 23. 10821. https:// doi.org/10.3390/ijms231810821
  58. Yilmaz N., Sandoval-Denis M., Lombard L. et al. Redefining species limits in the Fusarium fujikuroi species complex. Persoonia. 2021. V. 46. P. 129–162. https://doi.org/10.3767/persoonia.2021.46.05
  59. Zhang H., Brankovics B., Luo W. et al. Crops are a main driver for species diversity and the toxigenic potential of Fusarium isolates in maize ears in China. World Mycotoxin J. 2016. V. 9. P. 701–715 https://doi.org/10.3920/WMJ2015.2004
  60. Zheng W., Zhao X., Xie Q. et al. A conserved homeobox transcription factor Htf1 is required for phialide development and conidiogenesis in Fusarium species. PLOS One. 2012. V. 7. P. e45432. https://doi.org/10.1371/journal.pone.0045432

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2. Fig. 1. A dendrogram of the phylogenetic similarity of species of the Fusarium fujikuroi complex, constructed on the basis of combined nucleotide sequences of TEF, tub, and RPB2 fragments of the genome by the maximum likelihood method. The nodes contain bootstrap support values (> 70%) for maximum likelihood and maximum economy analysis, as well as Bayesian a posteriori probability values (> 0.95). The F. oxysporum NRRL 22902 strain was used as an external group.

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3. Fig. 2. Morphology of cultures of Fusarium temperatum and F. subglutinans strains on the seventh day on Cz and KDA media at 25 ° C and different lighting modes. In each photo, there is a culture surface on the left, and a reverse on the right.

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4. Fig. 3. Micromorphology of Fusarium temperatum: A — false heads in the aerial mycelium above the sporodochium located on the surface of the agar; B –I — conidiophores, phialid and blastic conidiogenic cells; K — false head; L, M — microconidia on phialid holes on the surface of the hyphae; H, O — branched sporodochial conidiophores; P — mesoconidia; P — sickle-shaped macroconidia. The photos of I–M were taken using transparent adhesive tape (scotch). Scale: A — 200 microns; B–P — 20 microns.

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5. Fig. 4. Micromorphology of Fusarium subglutinans: A — sporodochium on the surface of the wheatgrass stem; B — sporodochia on the surface of SNA; C, G — aerial mycelium, conidiophores and false heads; D–K — conidiophores, phialid and blastic conidiogenic cells; L — aerial mycelium and conidiophores; M — mesoconidia; H — sickle-shaped macroconidia. The photos of the D–L were taken using transparent adhesive tape (scotch). Scale: A — 500 microns; B — 50 microns; C, D — 100 microns; D–H — 20 microns.

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6. Fig. 5. Teleomorph of Fusarium temperatum: A, B — formation of perithecia when crossing strains on KDA with fragments of wheatgrass; C, D — fertile perithecium; E, E — perithecium with altered color under the influence of 90% lactic acid; G — asci and ascospores released from perithecium; Z — ascospores. Scale: B — 1 mm; C–E — 100 microns; W, W — 20 microns.

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