Phylogenetic diversity of Fusarium incarnatum-equiseti species complex isolated from Spanish wheat

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1 Antonie van Leeuwenhoek (204) 06: DOI 0.007/s x ORIGINAL PAPER Phylogenetic diversity of Fusarium incarnatum-equiseti species complex isolated from Spanish wheat G. Castellá F. J. Cabañes Received: 2 February 204 / Accepted: 20 May 204 / Published online: 3 June 204 Ó Springer International Publishing Switzerland 204 Abstract Wheat is the most important cereal grown in the European Union and is its fifth largest wheat producer. There is little information about Fusarium species associated with wheat in. Phylogenetic diversity of 5 strains belonging to Fusarium incarnatum-equiseti species complex (FI- ESC) isolated from Spanish wheat was investigated using partial sequences of the translation elongation factor gene (EF-a). Maximum-parsimony and Bayesian analysis of aligned DNA sequences resolved 8 haplotypes and 7 phylogenetic species. Strains morphologically identified as F. equiseti belonged to two different phylogenetic species, FIESC-5 and FIESC- 4. Some correlation between phylogenetic species and geographical region was found. The present results highlight the potential contribution of FIESC to the mycotoxin contamination of Spanish wheat. G. Castellá F. J. Cabañes Veterinary Mycology Group, Department of Animal Health and Anatomy, Universitat Autònoma de Barcelona, Bellaterra, Barcelona, G. Castellá (&) Grup de Micologia Veterinària. Departament de Sanitat i d Anatomia Animals, Facultat de Veterinària, Universitat Autònoma de Barcelona, E-0893 Bellaterra, Barcelona, Gemma.Castella@uab.cat Keywords Fusarium Wheat Elongation factor-a F. equiseti F. semitectum F. incarnatum Introduction Fusarium species have a worldwide distribution in cereal fields. The superficial contamination and infection of Fusarium in cereals are of great concern as plant pathogens and mycotoxin producers. The most important cereal grown in the European Union is wheat, followed by maize and barley. In, wheat production ranks second in the total production as a cereal crop, being the fifth wheat producer of the European Union (Eurostat 202). There is a lot of information about mycotoxigenic Fusarium species associated with wheat in North and Central Europe (Xu et al. 2005; Oerke et al. 200; Yli-Mattila 200), while information from South Europe is scarce (Logrieco et al. 2003; Mateo et al. 2004; Jurado et al. 2006). It has been reported that the species predominantly found associated with head blight of wheat in were Fusarium equiseti, F. graminearum, F. culmorum, F. sambucinum, F. avenaceum, F. udum and F. proliferatum. But there is no information about Fusarium infestation of wheat without visible symptoms of Fusarium disease in. Symptomless wheat can be infested with different Fusarium species and it s important to evaluate their role in mycotoxin contamination and the impact of climate change in their distribution and relative importance. The most 23

2 30 Antonie van Leeuwenhoek (204) 06: likely climate change impact would be shifts in the geographical distribution of host pathogens (Coakley et al. 999). Recent studies in Northern Europe showed that the predicted changes in climate towards 2050 are expected to slightly change Fusarium species composition (Parikka et al. 202). The identification of Fusarium species traditionally relies on morphological and physiological characters. However, these are limited in their ability to describe species boundaries. This is especially evident among very closely related Fusarium species, such as members of Fusarium incarnatum-equiseti species complex (FIESC), due to the high level of cryptic speciation and extreme morphological homoplasy. A series of molecular phylogenetic studies has led to the important conceptual advance that morphological species recognition within Fusarium greatly underestimates its species diversity (O Donnell et al. 2000, 2004, 2008). Recently, a multilocus sequence typing scheme analysis has been applied to members of FIESC and revealed that it comprises 30 phylogenetically distinct species (O Donnell et al. 2009, 202), evenly divided among two clades designated Incarnatum and Equiseti. The multilocus species nomenclature identified each phylogenetic species by an Arabic number and the different haplotypes by lowercase Roman letters. The result is that Latin binomials can be applied with confidence to only 3 of the 30 species within the FIESC, all of them in the Equiseti clade: namely, F. lacertatum (FIESC 4), F. scirpi (FIESC 9) and F. equiseti (FIESC 4) and none of the species within the Incarnatum clade. F. equiseti is a cosmopolitan soil inhabitant fungus that has been isolated from roots and plant tissues from many parts of the world (Leslie and Summerell 2006). The current description of F. equiseti includes at least two varieties, with different morphological types (Samson et al. 2004). F. incarnatum is extremely widespread and common in the tropics and subtropics but also found in Mediterranean and occasionally in temperate regions (Leslie and Summerell 2006). F. incarnatum has a history of taxonomic and nomenclatural disagreements because of morphological variability among isolates (Nirenberg 990). The aims of the present study were to determine the phylogenetic relationships among the different species of F. incarnatum-equiseti species complex commonly occurring in Spanish wheat, as well to reveal underlying patterns such as geographic distribution and its implication in mycotoxin contamination of wheat. Materials and methods Fusarium strains A total of 5 strains were isolated from healthy wheat grains cultivated in three different regions of : Aragón (3 strains), Castilla-La (8 strains) and Catalonia (30 strains). Morphological identification of Fusarium isolates was done on SNA and PDA media according to the taxonomy of Nelson et al. (983) and Leslie and Summerell (2006). All strains were freeze dried in skim milk and stored in our culture collection at the Universitat Autònoma de Barcelona. DNA extraction and molecular species identification Genomic DNA was extracted and purified from cultures in PDA according to the FastDNA Spin kit protocol with the FastPrep FP-24 instrument (MP Biomedicals, Biolink, Barcelona, ). The DNA was kept at -20 C until used as template for PCR amplification. Following the DNA extraction, the elongation factor -alpha region was amplified by PCR with the primer pair EF and EF2 (O Donnell et al. 2008). PCR products were purified with Multi- Screen filter plates (Millipore, Barcelona, ) following the manufacturer s protocol. The purified product was used as a template for sequencing. Sequencing of both DNA strands was performed with the Big-Dye Terminator v3. Cycle Sequencing kit (Applied Biosystems) and primers EF3 and F22T (O Donnell et al. 2008) as specified by the manufacturer. An Applied Biosystems 3730 sequencer was employed to obtain the DNA sequences. Sequences were compared to sequences in GenBank and the Fusarium ID-database ( Geiser et al. 2004) for identification. Phylogenetic analysis Sequence alignments were performed using the software program Clustal X v2.0.2 (Larkin et al. 2007). 23

3 Antonie van Leeuwenhoek (204) 06: Regions of ambiguous alignment were removed with Gblocks (Castresana 2000). Parsimony analyses were conducted using PAUP * version 4.0b0 software (Swofford 2002). One hundred heuristic searches were conducted with random sequence addition and tree bisection reconnection branch-swapping algorithms, collapsing zero-length branches and saving all minimal-length trees (MulTrees) on different data sets. Gaps were treated as missing data and support of internal branches was assessed using heuristic parsimony search of,000 bootstrapped data sets. Tree length, consistency index (CI), retention index (RI) and the rescaled consistency index (RC) values were also calculated. Bayesian inference was conducted using MrBayes v (Ronquist and Huelsenbeck 2003). Bayesian analyses were run for,000,000 generations in two independent analyses with a sample frequency of in,000. To obtain the consensus tree and Bayesian inference posterior probabilities, 0 % of the generations were removed to discard trees sampled before likelihood values had reached a plateau. We used the most complex model of evolution available for nucleotides (GTR? Gamma distribution? Invariant positions). Results All the strains were morphologically identified as members of FIESC. Sixteen strains were identified as F. equiseti, and the remaining strains showed compatible morphological characters with FIESC. Amplification of EF-a of the 5 isolates produced a fragment ranging from 677 to 685 bp. Comparison of the EF-a sequences with the Fusarium-ID database showed that the 5 strains generated 8 haplotypes and were assigned to 7 different phylogenetic species: FIESC- (3 strains, 2 haplotypes), FIESC-5 (26 strains, 5 haplotypes), FIESC-0 ( strain), FIESC- 4 (F. equiseti, 3 strains, haplotype), FIESC-24 (2 strains, 2 haplotypes), FIESC-25 (7 strains, 3 haplotypes), and FIESC-28 (9 strains, 4 haplotypes). Strains assigned to FIESC- (F-66, F-745, and F-07) and FIESC-0 (F-05) showed a low percentage of identity (94 %) in Fusarium-ID database. In a Gen- Bank search, strains from FIESC- showed % sequence similarity to strain NRRL identified as belonging to FIESC-29 (O Donnell et al. 202), and strain F-05 from FIESC-0 showed 94 % sequence Table Strains DNA typed in this study. The same accession number was given to identical EF-a sequences Designation Location FRIUM-ID EFa blast (%) GenBank acc. no. F-647 Catalonia FIESC-28a (00) F-969 F-66 Catalonia FIESC-a (94.4) F-07 F-662 Catalonia FIESC-5c (99.7) KF F-669 a Catalonia FIESC-5c (00) F-97 F-670 Catalonia FIESC-24a (00) KF96295 F-672 Catalonia FIESC-25b (98.3) F-758 F-685 Catalonia FIESC-25b (00) KF F-689 Catalonia FIESC-5f (99.9) Identical to F-94 F-69 Catalonia FIESC-5c (00) F-97 F-7 a Catalonia FIESC-28a (99.9) KF F-74 Catalonia FIESC-24b (99.) KF F-735 Catalonia FIESC-5c (99.7) F-662 F-739 Catalonia FIESC-5c (00) F-97 F-743 Catalonia FIESC-28a (99.7) KF F-745 a Catalonia FIESC-a (94.6) KF F-758 a Catalonia FIESC-25b (98.3) KF F-760 a Catalonia FIESC-5c (00) F-97 F-766 Catalonia FIESC-28a (99.7) F-743 F-767 a Catalonia FIESC-25b (99.7) KF F-770 Catalonia FIESC-25b (99.7) F-767 F-774 Catalonia FIESC-5c (00) F-97 F-776 Catalonia FIESC-5c (00) F-97 F-795 a Catalonia FIESC-5c (00) F-97 F-802 a Catalonia FIESC-5c (00) F-97 F-88 Catalonia FIESC-28a (00) F-969 F-827 Catalonia FIESC-5c (00) F-97 F-830 a Catalonia FIESC-25b (98.3) F-758 F-888 Aragón FIESC-28a (99.7) F

4 32 Antonie van Leeuwenhoek (204) 06: Table continued Designation Location FRIUM-ID EFa blast (%) GenBank acc. no. F-907 Aragón FIESC-28a (99.7) F-743 F-94 Castilla-La FIESC-28a (99.6) KF F-97 Castilla-La FIESC-5c (00) KF F-938 Castilla-La F-940 Castilla-La F-94 Castilla-La F-943 Castilla-La F-945 a Castilla-La F-968 a Castilla-La F-969 Castilla-La F-978 Castilla-La F-980 Castilla-La F-983 a Castilla-La F-990 Castilla-La F-992 a Castilla-La F-002 Castilla-La F-008 a Castilla-La FIESC-5c (99.7) FIESC-5c (00) FIESC-5f (99.9) FIESC-5c (00) FIESC-4c (99.6) FIESC-5f (99.9) FIESC-28a (00) FIESC-5c (00) FIESC-5b (00) FIESC-4c (99.6) FIESC-5f (99.6) FIESC-5c (00) FIESC-4c (99.6) FIESC-5f (99.6) F-662 F-97 KF F-97 F-002 F-008 KF F-97 KF F-002 F-008 F-97 KF KF96294 F-03 a Catalonia FIESC-25b (99.7) F-767 F-05 Aragón FIESC-0a (94.4) KF F-06 Catalonia FIESC-5c (00) F-97 F-07 Catalonia FIESC-a (94.4) KF F-09 Castilla-La F-038 a Castilla-La FIESC-5c (00) FIESC-5b (00) a Strains identified morphologically as F. equiseti F-97 F-980 similarity to strain NRRL3020, identified as FIESC- 0a (O Donnell et al. 2009). Within the strains assigned to FIESC-25, strains F-672, F-758 and F-830 showed 98 % sequence similarity to FIESC- 25b, as in a GenBank search. Representative nucleotide sequences of the different haplotypes determined in this study have been deposited in the GenBank and their accession numbers are given in Table. The same accession number was given to identical EF-a sequences. In the phylogenetic analysis we included representative strains from all the haplotypes described since now in FIESC and also sequences of the two different morphological types described in F. equiseti. The EF- a data set included 433 characters excluding sites with gaps/missing data, with 30 conserved and 32 variable characters of which 90 are parsimony informative. Maximum parsimony and Bayesian analyses produced phylogenetic trees with the same topology. Strains clustered in two major phylogenetic groups: 8 strains were clustered in the Incarnatum clade (Fig. ) and 33 strains in the Equiseti clade (Fig. 2). Within the Incarnatum clade, our strains were grouped in 3 different phylogenetic species: FIESC-24 (78 % bootstrap), FIESC-25 (70 % bootstrap) and FIESC-28 (54 % bootstrap). Strains from FIESC-24 and FIESC- 25 were isolated only in Catalonia. Within the Equiseti clade, our strains were grouped in 4 different phylogenetic species: FIESC-5 (78 % bootstrap), FIESC-0 (86 % bootstrap), FIESC-4 (98 % bootstrap) and FIESC-29 (99 % bootstrap). Most of the strains (26/ 33) clustered with FIESC-5, and this clade also contains strains of F. equiseti type II, whereas F. equiseti type I clustered with strains belonging to FIESC-4. Only one strain grouped with FIESC-0 and 3 strains, all of them from Castilla-La, were grouped in FIESC-4. Three strains clustered with FIESC-29 and all of them were isolated from wheat samples from Catalonia. Discussion FIESC represents a complex of morphologically similar species (F. equiseti/f.semitectum/f.incarnatum) that comprises 30 phylogenetically distinct species (O Donnell et al. 2009, 202). In our study, we only recovered 7 phylogenetic species. This is a low genetic diversity when compared with the 20 phylogenetic species found in isolates from human and animal source (O Donnell et al. 2009) or the 5 phylogenetic species found in insects (O Donnell et al. 23

5 Antonie van Leeuwenhoek (204) 06: EF-α 433 characters Tree length= 234 CI= 0.72 RI= 0.9 RC= NRRL32868 FIESC 25-c F-685 NRRL22244 FIESC 25-a China NRRL32993 FIESC 25-b F-767 F-758 NRRL2647 FIESC 26-a NRRL2874 FIESC 26-b NRRL34005 FIESC 24-a Cuba Costa Rica F-670 F-74 NRRL43297 FIESC 24-b NRRL3379 FIESC 23-b NRRL32867 FIESC 23-a NRRL34002 FIESC 22-a NRRL3335 FIESC 2-a NRRL32865 FIESC 2-b 98 Origin India Australia Brazil Equiseti clade F-969 F-7 NRRL28577 FIESC 28-a Romania F-743 F-94 NRRL20722 FIESC 27-a Kenya NRRL34003 FIESC 20-a NRRL36575 FIESC 20-b NRRL43639 FIESC 9-a 99 NRRL36548 FIESC 7-b NRRL32864 FIESC 7-a NRRL34070 FIESC 7-c NRRL34056 FIESC 6-b NRRL43730 FIESC 6-c NRRL34004 FIESC 6-a NRRL367 FIESC 8-a NRRL32522 FIESC 8-b NRRL3400 FIESC 5-e NRRL34008 FIESC 5-d NRRL3282 FIESC 5-b NRRL4369 FIESC 5-a Congo NRRL3400 FIESC 5-c NRRL 3459 F. concolor Incarnatum clade 5 Fig. Molecular phylogenetic tree inferred by maximum parsimony and Bayesian inference analysis of partial EF-a sequences of the Fusarium incarnatum-equiseti species complex for selected strains in the Incarnatum clade. Maximum parsimony bootstrap values ([ 50 %) are indicated above internodes and Bayesian inference posterior probability ([0.95) is indicated below internodes. The tree is rooted on a sequence of Fusarium concolor NRRL3459. CI consistency index, RI retention index, RC rescaled consistency index 23

6 34 Antonie van Leeuwenhoek (204) 06: Fig. 2 Molecular phylogenetic tree inferred by maximum parsimony and Bayesian inference analysis of partial EF-a sequences of the Fusarium incarnatum-equiseti species complex for selected strains in the Equiseti clade. Maximum parsimony bootstrap values ([50 %) are indicated above internodes and Bayesian inference posterior probability ([0.95) is indicated below internodes. The tree is rooted on a sequence of Fusarium concolor NRRL3459. CI consistency index, RI retention index, RC rescaled consistency index. Trichothecene production reported by Marín et al. (202): T B, trichothecene type B production; T A?B, trichothecene type A and B production EF-α 433 characters Tree length= 234 CI= 0.72 RI= 0.9 RC= 0.66 NRRL43640 FIESC -a NRRL34039 FIESC -b 62 NRRL34034 FIESC -c NRRL3640 FIESC 2-a 0.96 NRRL36448 FIESC 2-b NRRL28029 FIESC 3-b NRRL3638 FIESC 3-a NRRL20423 FIESC 4-a NRRL3623 FIESC 4-b NRRL36269 FIESC 2-b NRRL36392 FIESC 2-c NRRL6548 FIESC 2-a NRRL5537 FIESC 8-a NRRL43498 FIESC 8-b NRRL32997 FIESC 7-a NRRL52758 FIESC 30-a NRRL43638 FIESC 6-a NRRL45998 FIESC 6-b 99 Origin Mozambique Sudan Unknown India Unknown Croatia Germany Germany Costa Rica F-07 F-745 NRRL25084 FIESC 29-a Austria NRRL52765 FIESC 29-b NRRL43635 FIESC 3-a Papua New Guinea NRRL3020 FIESC 0-a Unknown F-05 NRRL36372 FIESC -a Netherlands Antilles NRRL26922 FIESC 9-c NRRL3402 FIESC 9-b NRRL2934 FIESC 9-a NRRL2649 FIESC 4-a NRRL20697 FIESC 4-b AJ F. equiseti I NRRL43636 FIESC 4-c NRRL34035 FIESC 5-d France Australia Australia Germany Chile Denmark F-002 JF F. equiseti I T B Equiseti clade F-97 JF F. equiseti II T B JF F. equiseti II T A+B JF F. equiseti II T B NRRL25795 FIESC 5-c Germany F-662 F-980 NRRL45995 FIESC 5-b NRRL3287 FIESC 5-a JF F. equiseti II T B JF F. equiseti II T A+B 6 F-008 JF F. equiseti II NRRL45997 FIESC 5-f F-94 JF F. equiseti II T B JF F. equiseti II T B JF49657 F. equiseti II Incarnatum clade NRRL 3459 F. concolor 5 23

7 Antonie van Leeuwenhoek (204) 06: ). Geographical area and climate are the most important factors that influence in the occurrence and the pattern of infestation by various Fusarium species. Our results are in agreement with those obtained from a survey of endemic fusaria inhabiting Sardinian soils (Balmas et al. 200). In this survey, only 4 phylogenetic species were found, F. scripi (FIESC-9), F. equiseti (FIESC-4) and two putatively undescribed F. equiseti-like species (FIESC-5, and FIESC- 29) (Balmas et al. 200). The current description of F. equiseti includes at least two varieties, with different morphological types (Samson et al. 2004). Morphotype I produced short apical cells while morphotype II had long apical cells. This morphological variation corresponds to some extent to the variation of their chemical and also IGS sequence profiles. The available data suggests that type I predominates in Northern Europe while type II is predominant in Southern Europe (Kosiak et al. 2005; Jurado et al. 2006; Marín et al. 202). In our study, sequences of morphotype II strains clustered with FIESC-5, while sequences of morphotype I strains clustered with FIESC-4. Thus, our data indicates these two morphotypes are distinct phylogenetic species within the Equiseti clade. Most of our strains clustered with morphotype II, as has been described by other authors (Kosiak et al. 2005; Marín et al. 202). Both morphotypes have been reported as producers of a wide range of mycotoxins, including beauvericin, fusarochromanone, nivalenol, diacetoxyscirpenol, 5-monoacetoxy-scirpentriol, neosolaniol, and zearalenone (Kosiak et al. 2005; Leslie and Summerell 2006). Moreover, in a recent study more than 80 % of F. equiseti strains from were able to produce deoxynivalenol and 25 % produced nivalenol (Marín et al. 202). Within the Incarnatum clade, our strains grouped with three different phylogenetic species, FIESC-24, FIESC-25 and FIESC-28. These groups had been also reported in insecticolous fusaria (O Donnell et al. 202). It s not possible to apply Latin binomial names in this clade because of unresolved taxonomic and nomenclatural problems associated with applying validly published names. Although the name F. semitectum has been used in the literature more than any other species within the Incarnatum clade, study of the type collection revealed that this binomial has been misapplied because it is a later synonym of Colletotrichum musae (O Donnell et al. 2009). Traditionally, F. semitectum has been considered to produce moniliformin, trichothecenes and zearalenone. In fact, members of F. incarnatum-equiseti species complex showed the same TRI and TRI0 genes as F. graminerarum and F. sporotrichioides but with a different arrangement (Proctor et al. 2009). In a recent study, FIESC is placed within the lineage of trichothecene-producing fusaria together with the F. sambucinum and F. chlamydosporum species complexes (O Donnell et al. 203). Some strains showed a low percentage of identity in Fusarium-ID database, but the correct identification was assessed by a combination of phylogenetic analysis and a GenBank search. Strains F- 66, F-745 and F-07 were finally identified as FIESC- 29, a species not updated in Fusarium-ID database. With 98 % sequence similarity strains F-672, F-758 and F-830 could represent a new allele of FIESC-25 and with 95 % sequence similarity strain F-05 could represent a new species phylogenetically related to FIESC-0. In both cases, data from additional loci would be necessary to confirm it. Some of the phylogenetic species were isolated from single geographical areas in the current study. For example, FIESC-4 has been isolated only in Castilla-La and FIESC-24, FIESC-25 and FIESC-29 only in Catalonia. Castilla-La has a continental climate characteristic of dry regions of, where winters are cold enough for snow and most rainfall occurs in late spring and summers are hot. On the contrary the climate of Catalonia is typically Mediterranean, where winters are generally mild and summers vary in intensity depending on the area but temperatures are moderate. Additional studies are needed to determine if this distribution is related to the different climate of these regions. To our knowledge, this is the first study of the F. incarnatum-equiseti species complex on Spanish wheat with no symptoms of Fusarium disease employing DNA sequence data. Their wide occurrence in wheat and the importance and variety of the mycotoxins produced by FIESC highlight the potential contribution to the mycotoxin contamination of Spanish wheat. Several studies had reported the presence of nivalenol, deoxynivalenol and zearalenone in wheat and wheat based food products in the Spanish market (Serrano et al. 202; Vidal et al. 203). Although no alarming values for these mycotoxins were reported in these studies, monitoring of the 23

8 36 Antonie van Leeuwenhoek (204) 06: Fusarium infestation in cereals is needed in order to determine its distribution and evolution with the new climate change scenarios. Acknowledgments We thank C. Gómez for her valuable technical assistance and J. Serra and G. Capellades from the Field Station IRTA-Mas Badia Foundation and other members of the GENVCE group for kindly providing us wheat grain samples from various areas of. This research was supported by the Ministerio de Ciencia e Innovación of the Spanish Government (AGL C04-02). Conflict of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. References Balmas V, Migheli Q, Schern B, Garau P, O Donnell K, Ceccherelli G, Kang S, Geiser D (200) Multilocus phylogenetics show high levels of endemic fusaria inhabiting Sardinian soils (Tyrrhenian Islands). 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