A novel Asian clade within the Fusarium graminearum species complex includes a newly discovered cereal head blight pathogen from the Russian Far East

Abstract

We investigated Fusarium graminearum complex (Fg complex) species diversity and toxin potential in European and Asian regions of the Russian Federation and adjoining regions northwest to Finland and south near Harbin, Heilongjiang Province, China, to expand our knowledge of the host range and geographic distribution of these economically devastating cereal head blight pathogens. Results of a recently described multilocus genotyping (MLGT) assay revealed that F. graminearum was the sole Fg complex pathogen in northern Europe and the predominant one in Asia (90.5%). Even though isolates of F. graminearum were segregating for 3-acetyldeoxynivalenol (3ADON) and 15-acetyldeoxynivalenol (15ADON) chemotype in nearly equal frequencies in the regions sampled on both continents, significant differences in the geographic distribution of isolates producing these acetyl ester derivatives of deoxynivalenol (DON) were observed in Europe. While 93.5% of the isolates in southern Russia (n = 43 of 46) possessed the 15ADON chemotype, isolates of F. graminearum recovered in Finland and northwestern Russia (n = 40) were exclusively 3ADON producers. Based on results of the MLGT assay, species identity of 10 genetically novel Fg complex isolates from the Russian Far East was investigated further via molecular phylogenetic analyses of multilocus DNA sequence data. Results of these analyses resolved these isolates as a phylogenetically distinct, reciprocally monophyletic sister lineage of F. asiaticum, which together with F. vorosii form a newly discovered Asian clade within the Fg complex. Because this novel lineage fulfills the highly conservative criterion of genealogical exclusivity under phylogenetic species recognition it is formally described herein as F. ussurianum. In addition to morphologically characterizing isolates of F. ussurianum, experiments were conducted to assess pathogenicity to wheat and trichothecene toxin potential in planta.

Genetic and phenotypic diversity within the Fusarium graminearum species complex in Norway

“…The present work is the first study of FGSC species diversity in Norway. All FGSC isolates collected from Norwegian cereals were identified as F. graminearum, which is consistent with previous evidence that F. graminearum is the dominant species within this species complex in Europe (Laday et al 2004;O'Donnell et al 2004;Toth et al 2005;Yli-Mattila et al 2009;Talas et al 2011;Boutigny et al 2014). F. graminearum is also dominant in the United States and Canada (Starkey et al 2007;Gale et al 2007;Ward et al 2008;Schmale et al 2011), and is found on all continents with the exception of Antarctica (O'Donnell et al 2004;Aoki et al 2012;Backhouse 2014).…”

“…The isolates of Finnish and Russian origin were sent to us from Tapani Yli-Matila, University of Turku, Finland. Details about the Finish, Russian and German isolates were previously published (Carter et al 2002;Yli-Mattila et al 2009). More details regarding the isolate collections are presented in Table 1.…”

“…All 126 of the FGSC isolates were analysed using a multilocus genotyping assay (MLGT) for identification of species and trichothecene genotype as described by Ward et al (2008) with additional species probes described by O'Donnell et al (2008), Sarver et al (2011), andYli-Mattila et al (2009). DNA extraction was performed as described by Umpiérrez-Failache et al 2013. In vitro production of trichothecenes was analysed for three 3-ADON and three 15-ADON genotypes using liquid chromatography coupled to a linear ion trap mass spectrometer.…”

“…In addition, chemotype differences have been maintained by selection and may have important consequences for pathogen fitness in different environments (Ward et al 2002). In Europe, 15-ADON is observed in South and Central European countries (Boutigny et al 2014;Jennings et al 2004;Talas et al 2011;Toth et al 2005), whereas in northwestern parts of Europe, 3-ADON has dominated (Fredlund et al 2013;Langseth et al 1999;Nielsen et al 2012;Yli-Mattila et al 2009). …”

“…Sixteen phylogenetically distinct species have been identified within the FGSC (O'Donnell et al 2000;O'Donnell et al 2008;O'Donnell et al 2004;Starkey et al 2007;YliMattila et al 2009;Sarver et al 2011). F. graminearum has a cosmopolitan distribution (O'Donnell et al 2000;Backhouse 2014) and is the dominant member of the FGSC in Europe (Laday et al 2004;O'Donnell et al 2004;Toth et al 2005;Yli-Mattila et al 2009). In fact, F. graminearum has been the only representative of the FGSC reported from Europe with the exception of a small number of F. boothii and F. vorosii isolates from Hungary (Toth et al 2005;Starkey et al 2007), a similarly small numbers of F. cortaderiae and F. boothii × F. graminearum hybrids from France (Boutigny et al 2014), and two F. cortaderiae isolates from Italy (Somma et al 2014).…”