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Article

Molecular Variation and Phylogeny within Fusarium avenaceum and Related Species

by
Tapani Yli-Mattila
1,*,
Asmaa Abbas
1,
Olga Gavrilova
2 and
Tatiana Gagkaeva
2
1
Laboratory of Molecular Plant Biology, Department of Life Technologies, University of Turku, 20014 Turku, Finland
2
Laboratory of Mycology and Phytopathology, All-Russian Institute of Plant Protection (VIZR), 196608 St. Petersburg, Russia
*
Author to whom correspondence should be addressed.
Diversity 2022, 14(7), 574; https://doi.org/10.3390/d14070574
Submission received: 12 May 2022 / Revised: 12 July 2022 / Accepted: 14 July 2022 / Published: 18 July 2022
(This article belongs to the Special Issue Diversity of Microbial Eukaryotes)
Browse Figures
Review Reports Versions Notes

Abstract

:
Many recent articles feature research on the Fusarium tricinctum species complex (FTSC), and their authors present different ideas on how the isolates of this species complex can be identified at the species level. In previous studies, our aim was to investigate the phylogeny of FTSC strains, which researchers have morphologically identified as Fusarium avenaceum, Fusarium arthrosporioides, and Fusarium anguioides. In the current study, our phylogenetic maximum parsimony and likelihood analyses of the DNA sequences of the translation elongation factor 1-alpha (TEF1) and combined sequences of TEF1 and beta-tubulin (TUB2) supported the existence of at least four main groups among these strains. Main Group I mainly contains F. avenaceum strains, while Main Group II contains two subgroups, one of which primarily includes F. arthrosporioides strains, and the other mainly includes European F. anguioides strains. Main Group III contains strains from different plants that originated from Asia, including two F. anguioides strains. F. avenaceum strains, which are mostly isolated from different trees, form Main Group IV. A fifth group (Main Group V) was only supported by TEF1 sequences. The main groups previously found by us based on TUB2 sequences could be connected to the new species of the FTSC, which were identified based on TEF1 sequences. In addition, we found strains that significantly differ from Main Groups I-V, and we grouped some of them as single, intermediate, or sister groups. All of the main groups of the present work, and some single and intermediate strains, may represent different species of the FTSC, while the two subgroups of Main Group II constitute intraspecific variation. Regardless of whether they belonged to the main groups, all the analysed strains were able to form different enniatins and 2-amino-14,16-dimethyloctadecan-3-ol, but did not produce beauvericin.

1. Introduction

The morphological and molecular descriptions of fungi that are closely related to Fusarium avenaceum (Fr.) Sacc. have been controversial, and researchers have presented different ideas on how to identify the isolates of this species group at the species level [1,2,3,4,5,6,7,8,9,10,11]. At present, we include F. avenaceum isolates, F. arthrosporioides and F. anguioides isolates, and the different morphologically intermediate isolates of the F. avenaceum species complex in the large Fusarium tricinctum species complex (FTSC) [9], which, according to Laraba et al. [11], consists of 36 phylogenetically different species, phylospecies FTSC 1–36, based on multilocus sequence analyses. The morphologically described species (morphospecies) F. avenaceum, F. arthrosporioides Sherb., and F. anguioides Sherb. are highly similar, do not have distinct phenotypic boundaries, and typically produce macroconidia, with five septa and little variation in size [12].
In the classical taxonomy, F. avenaceum and F. arthrosporioides belong to the section Roseum, but F. anguioides is a member of the section Arthrosporiella, based on the morphological features, such as the ability of the latter to form chlamydospore-like cells and blastic or phialidic conidiogenous cells, rarely with two conidiogenous loci [12]. The authors of the other manuals for Fusarium species identification do not even mention Fusarium anguioides [13,14].
In many cases, the identification of the isolates of these three species based only on morphology leads to species identities that differ from identities determined by DNA-sequence-based methods and mycotoxicological analyses [5,10,15,16,17,18]. Fusarium avenaceum is one of the Fusarium species that are most frequently isolated from plants cultivated in diverse geographic and climatic regions [19,20,21,22,23,24,25]. Fusarium anguioides and F. arthrosporioides occur frequently on different plant species, including cereals and dicotyledons. Both species are closely related to F. avenaceum and are often identified as F. avenaceum based on morphology [5,16,26]. In an analysis of the pathogenicity, the F. avenaceum and F. arthrosporioides strains were more aggressive than the F. anguioides strains in that they caused a greater reduction in the lengths and larger necroses in winter wheat seedlings [5]. All three species produce mycotoxins, such as moniliformin and enniatins (ENNs), particularly in cereals [10,11,18,23,27,28,29,30,31]. Furthermore, the presence of the enniatin synthase gene in multiple strains is consistent with ENN production [30,31,32]. There is a correlation between F. avenaceum DNA and the moniliformin and enniatin levels in cereal grains [17]. Enniatins also influence the virulence in potato tubers [33].
In Finland, Norway, and northwestern Russia, F. avenaceum is one of the most common Fusarium species in small-grain cereals [19,23,26,28,34,35]. A recent study on the occurrence of Fusarium species and mycotoxins in small-grain cereals grown in the Urals and western Siberia revealed that the proportions of F. avenaceum and F. anguioides among all morphologically identified Fusarium species reached 20% and 13%, respectively. However, the levels of moniliformin in the grain were only positively correlated with F. avenaceum infection in the grain [25]. Nelson et al. [36] neotypified F. anguioides using strains of the F. concolor species complex from China, which are more distantly related to F. avenaceum than to the F. anguioides strains that Nirenberg identified (e.g., strain BBA 69055 = CBS 173.12) [3,4,15,37]. According to Nelson et al. [36], BBA 69055 is not any more morphologically identifiable as F. anguioides, and, according to Jacobs-Venter et al. [3], the isolate CBS 173.12 belongs to F. avenaceum. According to Crous et al. [38], the strain BPI 72044 was designated as a neotype of F. anguioides, and it was erroneously stated that no material was available for epi- and lectotypification [36]. However, Sherbakoff provided an illustration with the original protologue of F. anguioides and deposited cultures of this species in the Cornell University Plant Pathology Herbarium as sample CUP-007479 [39].
According to phylogenetic analyses based on the DNA sequences of the beta-tubulin (TUB2) and transcription elongation factor 1-alpha (TEF1) genes, as well as the ribosomal intergenic spacer (IGS) region, F. avenaceum, F. arthrosporioides, and F. anguioides isolates form a clade that is closely related to F. tricinctum (Corda) Sacc. [5,10,11,15,16,31,40]. In these molecular analyses, isolates that had previously been identified by morphology were resolved as separate groups based on variations in the DNA sequences. Yli-Mattila et al. [5] named the four main groups based on TUB2 sequences and inter-simple sequence repeat (ISSR) fingerprints: Main Group I primarily contains morphologically F. avenaceum strains; Main Group II mostly contains morphologically F. arthrosporioides strains; Main Group III mostly contains morphologically F. anguioides strains that originated from Europe; Main Group IV includes strains that originated from Asia, one of which was identified as F. anguioides based on morphology.
In the present work, we aimed to investigate the diversity of the TEF1 sequences and mycotoxins of geographically and morphologically different strains of F. avenaceum and related species to ascertain whether any of the four main groups based on TUB2 sequences and ISSR fingerprints are supported by TEF1 sequences [4,5,32,40]. We also investigated how the main groups based on TUB2 sequences, as well as the TEF1 haplotypes defined by Kulik et al. [32] and the TEF1 sequences published by Stakheev et al. [40], correspond to the resolutions in the FTSC of O’Donnell et al. [4] and Laraba et al. [11]. We first compared the TEF1 sequences of the four main groups of F. avenaceum isolates [5] to the sequences in GenBank, and subsequently to the various groups of F. avenaceum isolates used in the different studies [4,11,24,32,40]. Finally, we analysed combined TUB2 and TEF1 sequences to confirm the results.

2. Materials and Methods

The list of the studied isolates and their abbreviations can be found in Table 1. Morphological analyses were performed macroscopically and microscopically [12,36,39]. DNA was extracted using the CTAB method, according to the common protocol [41] or by using a GenElute™ Plant 241 Genomic DNA Kit (Sigma-Aldrich, St. Louis, MO, USA), as described by Yli-Mattila et al. [42]. A fragment of TEF1 was amplified and sequenced from both ends using the oligonucleotide primers EF1 and EF2, as described by O’Donnell et al. [43]. Five DNA sequences were submitted to GenBank, with the accession numbers OK564509, OK564510, OK564511, OK564512, and OK564513. The TEF1 sequences were aligned using MUSCLE [44]. The maximum-parsimony (MP) and maximum-likelihood (ML) consensus trees were constructed using Mega 11 [45], in which clade support was assessed by 500 ML bootstrap pseudoreplicates of the data.
The sequence data for all the TUB2 and several TEF1 sequences were downloaded from GenBank, and we also referred to those reported in previous studies [4,11,16,32,40,46]. One can find all of the sequences in GenBank based on the strain names specified in Table 1. The accession numbers of the sequences used in Figure 1, Figure 2, Figure 3, Figure 4 and Figure 5 and Supplementary Figures S1–S5 can be found in Supplementary Table S1.
The mycotoxin production on cracked corn kernels in eight strains that were included in the phylogenetic analyses of the present work was evaluated, as previously described by [11]. In addition, mycotoxins were analysed in the strains MFG 151200, MFG 103100, MFG 108904, MFG 112804, MFG 48314, BBA 69055 [5], BBA 64134, BBA 64215, BBA 70561, BBA 67800 [16], the NRRL 13826 strain in F. avenaceum, the MFG 58549 strain in F. reticulatum Mont., the MFG 60500 strain in F. graminum Corda, and the strains MFG 42305, MFG 58674, and MFG 60360 in F. acuminatum (Table 2). After 15 days, cultures were extracted with 50 mL acetonitrile/water (86:14 v/v) by shaking at 30 rpm for 2 h. High-performance liquid chromatography–mass spectrometry (HPLC–MS) analyses of the extracts were performed using a Dionex Ultimate U3000 liquid chromatography system connected to a Q Exactive mass spectrometer (Thermo Fisher Scientific). The detection and quantification of the metabolites were based on comparisons of the retention times, masses, and mass spectra to purified standards, with a detection level of 1 ng toxin/μL.

3. Results

3.1. Molecular Characterisation of Strains

According to the TEF1 sequences of 570 nucleotides, the strains can be divided into four main groups, which are supported by bootstrap values of >90% in the MP tree (Figure 1) and >83% in the ML tree (Supplementary Figure S1). Main Group I was represented by the F. avenaceum strains av48 and a2, the F. arthrosporioides strains ar57, ar7, and ar5, and the F. anguioides strain an41, which all originated from Europe [5], as well as the isolates MRC 1413 of unknown origin, F066 from Canada [48], CML 3538 from Brazil, and MRC 2195 from South Africa. Main Group II was represented by the F. arthrosporioides strain ar1 and the F. avenaceum strain NRRL 54939 from Finland [48], the NRRL 25128 strain from Poland, the F. anguioides strains an37 and an45 from the European part of Russia, and strain F093 from Canada [48]. Two subgroups within Main Group II were supported by bootstrap values of 75% and 61% in the MP and ML trees, respectively. The strains FRC R-09495 (USA) and CML 3545 (Brazil) were in an intermediate group that was between Main Groups I and II in the phylogenetic tree (Figure 1, Supplementary Figure S1).
The third main group included the F. anguioides strain an47, as well as other Asian strains, including MRC 2532 (FTSC 11), SICAUCC 18, and JRBK-5, the strain FRC R-9369 from Canada, and the strain CML 3541 from Brazil. BBA 69055 was separated from the other strains of Main Group III. The fourth main group was represented by strain a49 from Finland, strain 10992 from New Zealand, strain E19/2-4 from Slovenia, and strain NRRL 52726 (FTSC5) from Turkey. Most of the strains from Main Group IV were isolated from trees. The Fusarium arthrosporioides strain ar2 from Finland, the F. avenaceum strain a4 from Austria, and the F. avenaceum strain a5 from Germany were separated from all the other F. avenaceum strains, as well as from the F. tricinctum, F. acuminatum (Ellis and Everh), and F. torulosum (Berk. and M.A. Curtis) Nirenberg strains (Figure 1, Supplementary Figure S1).
When we compared the TEF1 sequences presented in Figure 1 to the 515 bp long sequences published by Kulik et al. [32], five main groups were supported by bootstrap values of >89% in the MP tree (Figure 2) and >82% in the ML tree (Supplementary Figure S2). Several strains of Main Groups I and II (strain CBS 15967, and six other European strains) belonged to the same TEF1 haplotype (Figure 2). Main Group II, including the strains that Kulik et al. analysed [32], belonged to the subgroup that the strain ar1 created.
The strain CBS 409.86 from the United States was in the intermediate group with the strain FRC R-9495. Strain DDPP 04401, which represents a European haplotype [32], and strains 379 and DDPP 09a1 from Europe, were also between Main Groups I and II in the ML tree (Supplementary Figure S2), while, in the MP tree, DDPP09a1 was in Main Group II (Figure 2). We found a new main group (Main Group V) of 14 strains of 2 TEF1 haplotypes [32] represented by strains 05-003, 376, and IBT 40026, which is related to Main Groups III and IV of the F. avenaceum species complex, based on the MP consensus tree. Strains ar2 and a4 formed their own main group in the parsimonious consensus tree, and they, together with strain a5, were again separated from all the other F. avenaceum strains (Figure 2, Supplementary Figure S2).
When we compared the TEF1 sequences used for the construction of Figure 1 to the 525 bp long TEF1 sequences of the strains published by Stakheev et al. [40], which represent the five main clusters of the phosphate permease gene (PHO) phylogenetic tree, four main groups were supported by bootstrap values of >72% in the MP tree (Figure 3) and >65% in the ML tree (Supplementary Figure S3). We found more strains related to the European F. anguioides strains of Main Groups I and II among the strains collected in Russia. Three of these strains (an42, MFG 74005, and MFG 111502) were morphologically identified as F. anguioides. The American strain F093 was again in the same subgroup with an37, an45, and MFG 74005, but MFG 111502 was closer to another subgroup of Main Group II. Strain K-2308 was in Main Group I, while strain F-2307 was between Main Groups I and II. Strain MFG 80310 from Russia and strain FRC R-09495 from the United States belonged to the intermediate group between Main Groups I and II. Strains a5, an42, a4, ar2, and MFG 80212 from the Russian Far East were located between Main Groups I and IV and the F. tricinctum strain BBA 64485. No strains of Main Groups III, IV, and V were found among the strains, which had been previously analysed by Stakheev et al. [40].
In the fourth comparison, in which we compared the TEF1 sequences of Figure 1 to the TEF1 sequences of Laraba et al. [11], five main groups were supported by bootstrap values higher than 86% in the MP tree (Figure 4) and 83% in the ML tree (Supplementary Figure S4). The isolates NRRL 53589 and NRRL 53729 had identical TEF1 sequences to the isolate IBT 40026 (Figure 2), while strain FRC R-6739 (FTSC 22) was in the same group as the isolate BBA 63201. We found a new subgroup formed by three strains in the intermediate group. BBA 69055 was separated from the other strains of Main Group III, and, according to the information from [11], it belongs to FTSC 27.
Finally, we added 443-nucleotide-long TUB2 sequences [5] to the TEF1 sequences. In the combined TEF1–TUB2 consensus tree of the selected strains, Main Groups I, II, III, and IV were supported by bootstrap values of >80% in the MP tree (Figure 5) and >81% in the ML tree (Supplementary Figure S5). Strains ar5 and a2 formed a subgroup in Main Group I. The American strain FRC R-9495 was again between Main Groups I and II, and strain BBA 69055 separated from Main Group III, while strain ar2 was in the same clade with strain a5, which was supported by bootstrap values of >90% in the MP and ML trees. The shorter TUB2 sequence of strain 10992 from New Zealand (accession number JX398943) is identical to that of strain a49 of Main Group IV, and it differs from the TUB2 sequences of all the other strains of the present work.

3.2. Mycotoxin Production of Strains

Different enniatins (ENNs) were produced in most of the isolates on cracked corn substrate, except in F. anguioides (BBA 63598), F. arthrosporioides (BBA 64215), and F. graminum (BBA 65242). The highest ENN levels were produced by the F. anguioides strain BBA 69055 from Main Group III (or FTSC 27) and by three F. acuminatum strains. The same three F. acuminatum strains were the only strains in which we detected ENN A. We only detected beauvericin in one F. avenaceum strain from the United States, which was not a part of the phylogenetic investigation. We found AOD levels >100 ng/mL in the F. anguioides strain MFG 58314 and the F. reticulatum strain MFG 58549.

4. Discussion

Researchers have repeatedly demonstrated the high genetic variability of the strains within the Fusarium tricinctum species complex, and they have attempted to classify individual species by highlighting main groups [5,32] or phylospecies [10,11]. However, until now, we have not had clear definitions or Latin binomial names for many species. In a recent study by Cowger et al. [8], more than 20% of the analysed strains closely related to F. avenaceum were represented by unnamed species. Moreover, in Mexico, researchers have found many unnamed strains related to F. avenaceum [48], which form four distinct evolutionary lineages, which may represent species-level diversity (FTSC species 26, 29, 31, and 32) [11]. In our work, 26% of the analysed strains significantly differed from the five named main groups (I–V), and we grouped them as single, intermediate, or sister groups (Unknown Groups I–IV).
The main groups in the clades that we obtained in the phylogenetic study by using TEF1 sequences were very similar to those obtained earlier by using TUB2 sequences [5]. Only the strains BBA 69055 and an42 were moved to another group based on the TEF1 sequences, and Main Groups II and III of the TUB2 phylogenetic trees were subgroups in Main Group II of the present work. The phylogenetic tree that we obtained using TEF1 sequences was in accordance with the phylogenetic tree of the combined TEF1 and TUB2 sequences. Based on the results of the present work, three F. avenaceum strains, for which the whole genomes were sequenced [49], belong to Main Groups I and II.
Kulik et al. [32] also found five main groups based on their TEF1 sequences. Their Main Groups I, IV, and V correspond to Main Groups I, II, and V in the present work. The phylogenetic tree of Stakheev et al. [40], based on TEF1 sequences, also supports Main Groups I and II, while the phylogenetic trees constructed by Kulik et al. [35] and Laraba et al. [11], based on TEF1 sequences, support Main Group V, which contains morphologically F. avenaceum strains like Main Group I.
However, Main Groups I and II could not be clearly found in the phylogenetic trees when other DNA sequences were combined with TEF1 sequences without TUB2 sequences [11]. Laraba et al. [11] had only one strain (NRRL 54939) of Main Group II, which was included in the FTSC 4 clade, with strains from Main Group I and the intermediate group in the TEF1 tree. However, when we added more strains of Main Group II to their phylogenetic TEF1 tree, Main Groups I and II were well-supported.
Main Groups I and II of the present work are well-supported in the phylogenetic trees based on the combined TEF1 and TUB2 sequences, as well as in those based only on TEF1 sequences. Thus, it may be necessary to divide FTSC4 into two species. In addition, the intermediate group between Main Groups I and II, based on the TEF1 sequences of the present work and those of Kulik et al. [32] and Laraba et al. [11], is well-supported. In our previous work, based on only TUB2 sequences, we could separate the two subgroups of Main Group II of the present work into two main groups [5]. Based on the results of the present work, the subgroup of Main Group II that mainly contains European F. anguioides strains is close to the other subgroup of Main Group II that mainly contains F. arthrosporioides strains. Thus, we can use morphological identification to indicate to which main group the isolates belong, but we cannot possibly identify the isolates of the F. avenaceum species complex by only using morphological characteristics.
According to the results of the TUB2 analysis, the F. anguioides strain BBA 69055 from Japan belongs to the group that is mostly formed by F. anguioides strains from Europe [5], while, according to the results of the TEF1 and combined TUB2–TEF1 analyses of the present work, the strain is close to, or belongs to, Main Group III of the FTSC strains from Asia, which is similar to the new Fusarium sp. nov.-9 (FTSC 11), for which O’Donnell et al. [4] presented only one strain: MRC 2532. According to Laraba et al. [11], BBA 69055 belongs to FTSC 27, which is a sister group of FTSC 11. Main Group III also includes another F. anguioides strain, an47, from the Russian Far East. Moreira et al. [24] found more strains that have TEF1 sequences that are similar to BBA 69055 and MRC 2532 from Brazil, and they identified their strains as FTSC 11. We suggest that it might be better to classify Main Group III (including FTSC 11 and its sister group, FTSC 27) as F. anguioides, rather than as the isolates neotypified by Nelson et al. [36], and a comparison of the isolates from Asia and Europe that we analysed in the present work to the original F. anguioides CUP-007479 sample of Sherbakoff [39] by using morphological, biochemical, and molecular characteristics would be informative.
In the current study, we could finally discover more strains (Main Group IV), isolated from trees (pine, fir, and acer) of different geographic origins and related to strain a49 (= NRRL 26893), isolated from apple from Finland, which is very different from other isolates based on the isozyme, the RAPD-PCR results, and the IGS and TUB2 sequences [16,17,47]. These isolates of Main Group IV include strain 10992 from New Zealand, strain E19/2-4 from Slovenia, and strain NRRL 52726 from Turkey [4,37]. According to Laraba et al. [11], strain NRRL 52726 and strain NRRL 26893 belong to FTSC5.
Main Group V is supported based on the TEF1 sequences obtained in the investigations in [11,32], but it is not supported by the other sequences used by Laraba et al. [11]. This is why Main Group V was included in the FTSC 4 species, although, in the TEF 1 tree, it is closer to other FTSC species. Thus, the isolates of Main Group V should be further investigated. Based on the TEF1 and TUB2 sequences, it seems that Main Groups I–IV of the present work may represent different phylogenetic species of the FTSC, while the two subgroups of Main Group II are more representative of intraspecific variation.
A few isolates could not be grouped with any known isolates, while strain BBA 63201 (= a4) could be grouped with strain FRC R-6739 of FTSC 22 [11]. We found more isolates between the main groups among the isolates based on the TEF1 sequences that have been analysed in different studies [11,32,40]. The phylogenetic trees based on TEF1 and TUB2 sequences support the group of intermediate isolates, which contains two subgroups. Thus, the intermediate group of isolates may also represent a phylogenetic species, as well as other isolates, such as a4, ar2, and a5, and MFG 80212. According to Laraba et al. [11], ar2 is the only strain that represents FTSC 30, and a5 is the only strain that represents FTSC 34, while, according to our results, a4 belongs to FTSC 22. We can use the nucleotides, which are different between the main groups, as markers for identifying isolates.
We found strains producing different ENNs in all the main groups and species that we investigated. This result is in line with the published information on the high amounts of ENNs and the absence of any detected BEA amounts produced by F. avenaceum and FTSC strains of different origins [10,21,29,30,31]. These strains produced different types of ENNs in vitro on rice, but all of them were nonproducers of BEA. BEA production is very rare in FTSC isolates, and researchers have detected it in only two studies [50,51]. Thus, the only strain producing a small amount of BEA in the present work should be further investigated. Our results also correspond to previous studies in which, within a group of ENNs, researchers detected ENN B at the highest level, followed by ENN B1, ENN A1, and ENN A [29,30,31]. ENN A was specific to the F. acuminatum strains. Only two strains, BBA 63598 (isolated from pea in 1928) and the unknown BBA 64215, which belong to Main Groups I and II, respectively, were not able to produce ENNs. More recently, researchers showed that most of the strains of F. avenaceum and closely related species produced AOD in amounts of 5.9–2139.3 ng/mL, which indicates the broadly distributed and variable ability to produce this secondary metabolite across the FTSC [10]. Among the strains that we analysed in our study, the maximum amount of AOD was 125.8 ng/mL, and we detected it in the MFG 58314 strain from Main Group III, which was isolated from rudbeckia from the Far East. We found no clear differentiation in the mycotoxin production between the FTSC strains from the different main groups.
We confirmed a significant intraspecific structure of F. avenaceum and related species, as well as the complexity of splitting them into phylogenetic species with the assignment of binominal names that reflect their properties; the FTSC4 of Laraba et al. [11] could be divided into three main groups and one intermediate group. In the future, whole-genome sequencing should be used to confirm the results of the present work, which deals with F. avenaceum and related species.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d14070574/s1, Table S1: Accession numbers of Fusarium strains used in the present study. Figure S1: Maximum-likelihood consensus tree of TEF1 sequences. Bootstrap values are indicated above nodes based on 500 pseudoreplicates of the data. Only branches present in more than 50% of the trees are shown. F. tricinctum and F. acuminatum strains are outgroups. Figure S2: Maximum likelihood consensus tree of TEF1 sequences, including strains from the work of Kulik et al. (2011). Bootstrap values are indicated above nodes based on 500 pseudoreplicates of the data. Only branches present in more than 50% of the trees are shown. Fusarium tricinctum and F. acuminatum strains are outgroups. Figure S3: Maximum-likelihood consensus tree of TEF1 sequences, including strains from the work of Stakheev et al. (2016). Bootstrap values are indicated above nodes based on 500 pseudoreplicates of the data. Only branches present in more than 50% of the trees are shown. Fusarium tricinctum and F. acuminatum strains are outgroups. Figure S4: Maximum-likelihood consensus tree of TEF1 sequences, including strains from the work of Laraba et al. (2022). Bootstrap values are indicated above nodes based on 500 pseudoreplicates of the data. Only branches present in more than 50% of the trees are shown. F. tricinctum and F. acuminatum strains are outgroups. Figure S5: Maximum-likelihood consensus tree for combined TEF1 and TUB2 sequences. Bootstrap values are indicated above nodes based on 500 pseudoreplicates of the data. Only branches present in more than 50% of the trees are shown. F. tricinctum and F. acuminatum strains are outgroups.

Author Contributions

Conceptualisation, T.Y.-M.; methodology, A.A. and T.Y.-M.; validation, A.A. and T.Y.-M.; formal analysis, T.Y.-M.; investigation, A.A., O.G. and T.Y.-M.; resources, T.Y.-M. and T.G.; data curation, T.Y.-M.; writing—original draft preparation, T.Y.-M.; writing—review and editing, O.G., T.G. and T.Y.-M.; visualisation, T.Y.-M.; supervision, T.Y.-M.; project administration, T.Y.-M.; funding acquisition, A.A. and T.Y.-M. All authors have read and agreed to the published version of the manuscript.

Funding

This work was funded by the Finnish Cultural Foundation (grants 00171173, 00182381, 00192433 and 00221140) to T.Y.-M., and by travelling grants 324397 and 324819 of the Academy of Finland to T.Y.-M., T.G., and O.G. The A.A. travel grant to Finland was from the Centre for International Mobility, Finland (CIMO).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The DNA sequences of the present work are available in GenBank.

Acknowledgments

The authors would like to thank Mark Busman (ARS-USDA, Peoria) for his help with the mycotoxin analyses, and Robert Proctor (ARS-USDA, Peoria) for his valuable comments on the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

References

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Diversity 14 00574 g001 550
Figure 1. Maximum-parsimony consensus tree of translation elongation factor 1-alpha (TEF1) sequences. Bootstrap values are indicated above nodes based on 500 pseudoreplicates of the data. Only branches present in more than 50% of the trees are shown. Fusarium tricinctum and F. acuminatum strains are outgroups.
Figure 1. Maximum-parsimony consensus tree of translation elongation factor 1-alpha (TEF1) sequences. Bootstrap values are indicated above nodes based on 500 pseudoreplicates of the data. Only branches present in more than 50% of the trees are shown. Fusarium tricinctum and F. acuminatum strains are outgroups.
Diversity 14 00574 g001
Diversity 14 00574 g002 550
Figure 2. Maximum-parsimony consensus tree of translation elongation factor 1-alpha (TEF1) sequences, including strains from the work of Kulik et al. [32] (2011). Bootstrap values are indicated above nodes based on 500 pseudoreplicates of the data. Only branches present in more than 50% of the trees are shown. Fusarium tricinctum and F. acuminatum strains are outgroups.
Figure 2. Maximum-parsimony consensus tree of translation elongation factor 1-alpha (TEF1) sequences, including strains from the work of Kulik et al. [32] (2011). Bootstrap values are indicated above nodes based on 500 pseudoreplicates of the data. Only branches present in more than 50% of the trees are shown. Fusarium tricinctum and F. acuminatum strains are outgroups.
Diversity 14 00574 g002
Diversity 14 00574 g003 550
Figure 3. Maximum-parsimony consensus tree of translation elongation factor 1-alpha (TEF1) sequences, including strains from the work of Stakheev et al. [40] (2016). Bootstrap values are indicated above nodes based on 500 pseudoreplicates of the data. Only branches present in more than 50% of the trees are shown. Fusarium tricinctum and F. acuminatum strains are outgroups.
Figure 3. Maximum-parsimony consensus tree of translation elongation factor 1-alpha (TEF1) sequences, including strains from the work of Stakheev et al. [40] (2016). Bootstrap values are indicated above nodes based on 500 pseudoreplicates of the data. Only branches present in more than 50% of the trees are shown. Fusarium tricinctum and F. acuminatum strains are outgroups.
Diversity 14 00574 g003
Diversity 14 00574 g004 550
Figure 4. Maximum-parsimony consensus tree of translation elongation factor 1-alpha (TEF1) sequences, including strains from the work of Laraba et al. [11] (2022). Bootstrap values are indicated above nodes based on 500 pseudoreplicates of the data. Only branches present in more than 50% of the trees are shown. F. tricinctum and F. acuminatum strains are outgroups.
Figure 4. Maximum-parsimony consensus tree of translation elongation factor 1-alpha (TEF1) sequences, including strains from the work of Laraba et al. [11] (2022). Bootstrap values are indicated above nodes based on 500 pseudoreplicates of the data. Only branches present in more than 50% of the trees are shown. F. tricinctum and F. acuminatum strains are outgroups.
Diversity 14 00574 g004
Diversity 14 00574 g005 550
Figure 5. Maximum-parsimony consensus tree for combined translation elongation factor 1-alpha (TEF1) and TUB2 sequences. Bootstrap values are indicated above nodes based on 500 pseudoreplicates of the data. Only branches present in more than 50% of the trees are shown. Fusarium tricinctum and F. acuminatum strains are outgroups.
Figure 5. Maximum-parsimony consensus tree for combined translation elongation factor 1-alpha (TEF1) and TUB2 sequences. Bootstrap values are indicated above nodes based on 500 pseudoreplicates of the data. Only branches present in more than 50% of the trees are shown. Fusarium tricinctum and F. acuminatum strains are outgroups.
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Table
Table 1. Fusarium strains used in the present study and identified based on morphological and molecular characteristics.
Table 1. Fusarium strains used in the present study and identified based on morphological and molecular characteristics.
GroupFTSC *Morphological SpeciesStrain No.Alternative Strain No. **OriginSubstrateYear
Main Group I4F. avenaceumMFG 118702av48 cRussia, Pskovbarley, grain2009
F. arthrosporioidesMFG 58655ar57 cRussia, Leningradoat, grain2013
F. avenaceumBBA 64151a2 bGermanySolanum1980
F. arthrosporioidesBBA 71186ar7 bGermanyBellis1999
F. anguioidesMFG 114605an41 cRussia, Kaliningradbarley, grain2008
F. anguioidesMFG 119913an42 cRussia, Kirovoat, grain2008
F. anguioidesMFG 108904an45 cRussia, Pskovbarley, grain2008
F. arthrosporioidesBBA 67701ar5 bFrancecereals1993
F. avenaceumDDPP 04401NA ***PolandwheatNA
F. avenaceumKK12NAHungarywheatNA
F. avenaceumF1NAHungarywheatNA
F. avenaceum18NAHungarywheatNA
F. avenaceumDDPP 042836NAPolandwheatNA
F. avenaceumDDPP 04032NAPolandwheatNA
F. avenaceumK-0238NARussiawheatNA
F. avenaceumFCR R6679NAAustraliasoilNA
F. avenaceumNRRL 26890NAFinlandwheatNA
F. avenaceumFRC R-671NAUSA, New YorkalfalfaNA
F. avenaceumFaLH27NA dCanadawinter wheat2001
Main Group II4F. anguioidesMFG 112804an37 cRussia, Novgorodbarley, grain2008
F. arthrosporioidesBBA 70576ar1 bFinlandbarley1986
F. avenaceumFaLH03NA dCanadaspring wheat2001
F. avenaceumNRRL 54939Fa05001 dFinlandbarley2005
F. avenaceumF093NACanadalupinNA
F. avenaceumNRRL 25128NAPolandIchneumonidaeNA
F. avenaceumCBS 15957NAItalyFagus sylvaticaNA
F. avenaceumDDPP 09a1NAPolandwheatNA
F. anguioidesMFG 74005NARussiawheatNA
F. avenaceumF-132NARussiawheatNA
F. anguioidesMFG 111502NARussiabarleyNA
Main Group V4F. avenaceumNRRL 36069CBS 101627UKcarnationNA
F. avenaceumNRRL 53589CBS 386.62Netherlandswinter wheatNA
F. avenaceumNRRL 53729CBS 121289Switzerlandwinter wheatNA
F. avenaceumCBS 409.86NAUSAbarleyNA
F. avenaceum05-003NASwitzerlandwheatNA
F. avenaceum376NASwitzerlandwheatNA
Intermediate4F. avenaceumIBT 40026NADenmarkwheatNA
Group F. avenaceumCBS 409.86NAUSAbarleyNA
Between Main Groups I and II F. avenaceumDDPP 04401NAPolandwheatNA
F. avenaceum379NASwitzerlandwheatNA
F. avenaceumCML 3545NABrazilwheatNA
F. avenaceumFCR R-9495NAUSA, CalifornialisianthusNA
F. avenaceumMFG 80310NARussiaoatNA
F. avenaceumF-2307NAGermanywheatNA
F. avenaceumNRRL 36374CBS 239.94NetherlandscarnationNA
Gibberella tricinctaNRRL 39591ICMP 5244New Zealandgarden peaNA
F. avenaceumNRRL 53733CBS 121294Switzerlandwinter wheatNA
Unknown Group I22F. avenaceumFRC R-6739NAGermanycodling mothNA
F. avenaceumBBA 63201a4 bAustriaUlmus scabra1974
Main Group III11F. anguioidesMFG 58314an47 cRussia, Vladivostokrudbeckia, leaves2010
Fusarium sp.CML 3541NABrazilwheatNA
F. avenaceumFRC-R9369NACanadalisianthusNA
F. avenaceumJRBK-5NAChina, HubeiwalnutNA
F. avenaceumSICAUCC 18NAChinaPolygonatum cyrtonemaNA
F. sp. nov-9MRC 2532NAJapansoybeanNA
F. avenaceumFv5-9NAChinaFragaria ananassaNA
27F. anguioidesBBA 69055an3 bJapanwheat, grain1994
Main Group IV5F. avenaceumBBA 70177a49 a, NRRL 26893FinlandappleNA
Fusarium sp.NRRL 52726NATurkeyNANA
Fusarium sp.KOD 810NAUSA, New HampshirefirNA
F. avenaceum10992NANew ZealandPinus radiataNA
F. avenaceumE19/2-4NASloveniaAcer pseudoplatanusNA
Unknown Group II30F. arthrosporioidesBBA 70561 b,ear2 bFinlandbarley1986
Unknown Group III?F. avenaceumMFG 80212NARussiaoatNA
Unknown Group IV34F. avenaceumBBA 70575 b,ea5 bGermanyCytisus1997
9F. torulosumNRRL 22747NAHungarybarleyNA
3F. tricinctumNRRL 25481NANANANA
F. tricinctumBBA 64485t6 bGermanywheat1986
2F. acuminatumNRRL 36147NANANANA
F. acuminatumNRRL 62622CS4907NANANA
* FTSC marked according to [11]; ** alternative names of strains are from [5,16,46,47,48], for a, b, c, d, and e, respectively; *** NA: not available.
Table
Table 2. Mycotoxins produced by strains of the Fusarium tricinctum species complex compared with F. graminum and F. reticulatum strains on cracked corn substrate.
Table 2. Mycotoxins produced by strains of the Fusarium tricinctum species complex compared with F. graminum and F. reticulatum strains on cracked corn substrate.
Main Group/FTSC *Morphological SpeciesStrain No. **Mycotoxin Amount (ng/mL)
BEA ***ENN BENN B1ENN AENN A1AOD
−/4F. avenaceumNRRL 138261.020.05.20LOQLOQ
I/4F. arthrosporioidesBBA 71186 a022.75.80LOQ41.5
I/4F. anguioidesBBA 63598 a00000LOQ
I/4F. avenaceumMFG 151200 b010.51.50LOQ20.1
II/4F. arthrosporioidesBBA 64134 a05.2LOQ0LOQ19.6
II/4F. arthrosporioidesBBA 64215 a00000LOQ
II/4F. anguioidesMFG 103100 b08.42.20LOQ31.5
II/4F. anguioidesMFG 108904 b0LOQLOQ0LOQ13.9
II/4F. anguioidesMFG 112804 b02.0LOQ0LOQ11.2
III/11F. anguioidesMFG 58314 b01.6LOQ00125.8
III/27F. anguioidesBBA 69055 a,b041.221.203.9LOQ
–/22F. avenaceumBBA 63201 a04.8LOQ0LOQLOQ
−/30F. arthrosporioidesBBA 70561 a0LOQLOQ01.71.5
−/3F. tricinctumBBA 64485 b0LOQLOQ0LOQ4.3
−/2F. acuminatumMFG 423050LOQLOQ001.2
−/2F. acuminatumBBA 67800 a036.038.5LOQ19.827.6
−/2F. acuminatumMFG 58674025.122.5LOQ10.321.8
−/2F. acuminatumMFG 60360022.120.4LOQ8.112.3
−/−F. graminumBBA 65242 a00000LOQ
−/−F. graminumMFG 605000LOQLOQ0LOQLOQ
−/−F. reticulatumMFG 58549042.801.1170.9
* FTSC marked according to [11]; ** strain numbers are from [16] and [5] for a and b, respectively. *** BEA: beauvericin; ENN: enniatin; AOD: 2-amino-14,16-dimethyloctadecan-3-ol. LOQ values are below the limit of mycotoxin quantitation (<1 ng/mL). “0” means that no toxin was detected.
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Yli-Mattila, T.; Abbas, A.; Gavrilova, O.; Gagkaeva, T. Molecular Variation and Phylogeny within Fusarium avenaceum and Related Species. Diversity 2022, 14, 574. https://doi.org/10.3390/d14070574

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Yli-Mattila T, Abbas A, Gavrilova O, Gagkaeva T. Molecular Variation and Phylogeny within Fusarium avenaceum and Related Species. Diversity. 2022; 14(7):574. https://doi.org/10.3390/d14070574

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Yli-Mattila, Tapani, Asmaa Abbas, Olga Gavrilova, and Tatiana Gagkaeva. 2022. "Molecular Variation and Phylogeny within Fusarium avenaceum and Related Species" Diversity 14, no. 7: 574. https://doi.org/10.3390/d14070574

APA Style

Yli-Mattila, T., Abbas, A., Gavrilova, O., & Gagkaeva, T. (2022). Molecular Variation and Phylogeny within Fusarium avenaceum and Related Species. Diversity, 14(7), 574. https://doi.org/10.3390/d14070574

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