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Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, P.O. Box 85167, NL-3508 AD Utrecht, The Netherlands
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The phylogenetic relationships of 17 selected Septoria spp. (eight with a known Mycosphaerella teleomorph), Phloeospora ulmi (teleomorph M. ulmi) and 18 additional taxa (10 with a Mycosphaerella teleomorph) were inferred from ITS and D2-LSU nrDNA sequences. In total, 10 anamorph genera associated with Mycosphaerella were represented. Intraspecific variation in ITS was limited in Septoria, with the exception of three strains that all were identified as S. rubi but originated from different Rubus spp. and probably belong to different species of Septoria. The results of D2 region sequencing confirmed Mycosphaerella sense lato (including Davidiella and Eruptio) as monophyletic. The cereal pathogen Septoria tritici, which is closely related to S. passerinii as found in ITS analysis, clusters with Ramularia spp. in the D2 analyses, distant from the other Septoria spp. The pathogens S. apiicola, S. linicola and S. populicola cluster in a major clade containing Phl. ulmi, and other Septoria spp. and Cercospora spp. Short branch lengths in this clade suggest a very recent evolution. Septoria castaneicola and S. pyricola also might represent relatively distant lineages. Both analyses of the regions indicated that Septoria is not monophyletic within Mycosphaerella and that conidiomatal structure (acervulus, pycnidium) has little value for predicting phylogenetic relatedness. As a consequence, the separation between the acervular Phloeospora and pycnidial Septoria is untenable. The loss of the teleomorph most likely has occurred several times in the evolutionary history of Mycosphaerella.
Key words: Cercospora, Didymella, morphology, Mycosphaerella, Phloeospora, Ramularia, Stagonospora
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Muthumary 1999). To date, more than 2000 names have been described in Septoria and, although groups that are associated with certain hosts families or geographical regions recently have been revised ( Jørstad 1965, 1967, Constantinescu 1984, Sutton and Pascoe 1987, 1989, Farr 1991, 1992, McPartland 1995, Wu et al 1996, Shin 1999), most taxa never have been re-examined since their introduction. In the late 19th and early 20th centuries numerous Septoria collections on previously unrecorded host plants were described as new species.
Septoria currently is characterized by pycnidial conidiomata, holoblastic, hyaline, smooth-walled conidiogenous cells with sympodial and/or percurrent proliferation, and filiform, hyaline, smooth-walled multiseptate conidia (Sutton 1980, Constantinescu 1984, Farr 1992). However, it also includes taxa with apparently nonproliferating, phialidic conidiogenous cells (sensu Sutton 1980), e.g., S. tritici, and species that vary in their conidiomatal structure from acervuloid to pycnidial. Due to the limited number of useful morphological characters and the paucity of physiological and other data in vitro, the taxonomy of the Septoria-like species still remains confusing and largely dependant on the host. As pointed out by Verkley and Priest (2002), Septoria-like anamorphs of Mycosphaerella are not always easy to distinguish morphologically from certain coelomycetous anamorphs of the Pleosporales (viz. Stagonospora anamorphs of Leptosphaeria and Phaeosphaeria).
Knowledge of the phylogenetic relationships among Septoria is still fragmentary. The sexual state of the type species is unknown, and only a relatively small number of other species have been linked unequivocally to teleomorphs, all of which now are classified in Mycosphaerella Johanson (Dothideales). Mycosphaerella is a species-rich ascomycete genus that has been associated with 27 anamorph genera, mostly hyphomycetous (von Arx 1983, Sutton and Hennebert 1994), 23 of which were accepted by Crous et al (2000). Recent molecular studies have shown that Mycosphaerella is monophyletic (Stewart et al 1999, Crous et al 2000, 2001b, Goodwin et al 2001), and that the taxa with anamorphs in Cladosporium s. str. that are associated with Mycosphaerella-like teleomorphs, such as M. tassiana (De Not.) Johanson, form a sister group of the Mycosphaerella clade (Braun et al 2003). In a study focussing primarily on cercosporoid anamorphs of Mycosphaerella, Crous et al (2001b) concluded that morphological characters such as conidiomatal structure (conidiophores solitary, fasciculate to synnematous, sporodochia, pycnidia, or acervuli) and conidial shape, size and septation are uninformative phylogenetically and are not useful for generic separation of Mycosphaerella anamorphs. In studies of other genera of ascomycetes, anamorphs similarly have been found to vary in conidiomatal structure from acervular through pycnidial to complex eustromatic (Samuels and Seifert 1987, Verkley 1999). In the foliicolous Septoria-like fungi, this raises the question whether Septoria with pycnidial conidiomata can be meaningfully distinguished from Phloeospora Wallr. (type species Phl. ulmi, teleomorph Mycosphaerella ulmi) with acervular conidiomata. Based on similarities of conidiomatal development, von Arx (1983) and Braun (1995) adopted a wider concept of Septoria that included Phloeospora. Another question is whether Septoria forms a monophyletic group within Mycosphaerella.
The aim of the present study is to investigate the phylogenetic relationships of Septoria species and other anamorphic genera linked to Mycosphaerella. The D2 region of the 28S ribosomal RNA gene is relatively conserved and informative at the generic level and above. The ITS region was chosen to assess the phylogenetic relationships of a large set of taxa within the main Mycosphaerella clade, using Cladosporium as outgroup. In total we selected 17 taxa with Septoria anamorphs, eight of which have known Mycosphaerella teleomorphs. Other Mycosphaerella species and anamorph taxa were added, so that in total 10 anamorphic genera that have been associated with Mycosphaerella were included. To further investigate the value of the conidiomatal structure, we also included a strain of Phl. ulmi.
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MATERIAL AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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. Most are preserved in the CBS culture collection under the teleomorph name. Names of confirmed alternate states also are listed in TABLE I. Morphology in vitro was studied as described by Verkley (1998b).
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Sequence analysis. –
For ITS sequence analysis a part of the ribosomal RNA gene cluster was amplified by PCR using primer pairs V9D (de Hoog and Gerrits van den Ende 1998) and LS266 (Masclaux et al 1995), or V9G (de Hoog and Gerrits van den Ende 1998) and LR5 (Vilgalys and Hester 1990). PCR was performed in 50 µL reaction volumes and each reaction contained 10–100 ng of genomic DNA, 25 pM of each primer, 40 µM dNTP, 1.0 unit Supertaq DNA polymerase and 5 µL 10x PCR buffer (SphaeroQ, Leiden, The Netherlands). The amplification was performed in a thermocycler (Applied Biosystems Foster City, California), with this program: 1 min 95 C, 30x (1 min 95 C, 1 min 55 C, 2 min 72 C) followed by a final extension of 5 min at 72 C. PCR product was cleaned with GFx columns (Amersham Pharmacia 27-9602-01) and analyzed on a 2% agarose gel to estimate the concentration. The PCR product was sequenced using internal primers ITS5 and ITS4 or ITS1 and ITS4 (White et al 1990). Sequencing was performed with the BigDye terminator chemistry (Part number 403049, Applied Biosystems) following the manufacturer’s instructions. The sequencing products were cleaned with G50 Superfine Sephadex colums (Amerham Pharmacia 17-0041-01) and separated and analyzed on an automated sequencer (ABI Prism 3700 DNA Analyzer; Applied Biosystems). Forward and reversed sequences were matched using SeqMan from the Lasergene package (DNAstar Inc., Madison, Wisconsin). For D2 sequence analyses the MicroSeq; TM D2 LSU rDNA Fungal Sequencing Kit (Applied Biosystems) was used according to manufacturer’s instructions.
Phylogenetic analyses. –
Pairwise and global alignment of consensus sequences were performed in Bionumerics 2.5 (Applied Maths, Kortrijk, Belgium). Manual adjustments were made in the global alignment where necessary. Maximum-parsimony and neighbor-joining distance methods were used to infer phylogenetic hypotheses. Parsimony analyses were done using PAUP version 4.0b10 (Swofford 2002). The heuristic searches were performed with these parameters: characters were unordered with equal weight, and random taxon addition. The tree bisection-reconnection (TBR) algorithm was used in branch swapping, with branches collapsing if the maximum branch length was zero. The maximum number of trees was set at 10 000. Alignment gaps were treated as fifth base in the D2 analyses, where they were confined to highly conserved regions. In the ITS analyses, gaps were treated as missing data because they also had to be introduced in less conserved regions. Parsimony bootstrap analyses were performed using the full heuristic search option, random stepwise addition and 1000 replicates, with maxtrees set at 100. Forty-six strains were included in the analysis of D2, with two species of the order Helotiales, (viz. Lachnellula willkommii [CBS 170.35] and L. occidentalis [CBS160.35]) as multitaxon outgroup. Several pleosporalean taxa were included in the selection for this region but not for the more variable ITS region, because the sequences could not be unambiguously aligned. Seventy-three strains were included in the analysis of ITS, with three strains of Cladosporium herbarum as multitaxon out-group. Neighbor-joining analyses were performed in Bionumerics and PAUP, in both cases without pairwise corrections. Stability of clades was tested using 1000 neighbor-joining bootstrap replications.
The following additional sequences were retrieved from GenBank (teleomorph names in TABLE I
or here in brackets): Septoria tritici, AF181692, AF181693; Cercospora apii, CA1; C. beticola, CB4; C. kikuchii, CK35, CK39; Paracercospora fijiensis var. fijiensis (Morelet) Deighton [M. fijiensis Meredith & Lawrence], PF7; Pa. fijiensis var. difformis ( J. L. Mulder & R. H. Stover) Deighton [M. fijiensis var. difformis J. L. Mulder & R. H. Stover], PFD9; Pseudocercospora musae (Zimm.) Deighton [M. musicola J. L. Mulder], PM10, PM11; Ps. cruenta (Sacc.) Deighton [M. cruenta Latham], PCR18; Mycosphaerella latebrosa, AF362051 (CBS 183.97), AF362067 (CBS 652.85); Septoria passerini, AF181697, AF181699; Dothidea sambuci Pers. : Fr., AF382387; and Pleospora herbarum, AF382386.
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RESULTS |
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. Maximum bootstrap support (100%) was found for the major Mycosphaerella clade and its direct sister, a strain of Cladosporium herbarum. Within Mycosphaerella, the two species of Ramularia clustered with two strains of S. tritici (M. graminicola) (95%). These clusters showed 100% internal homology in D2 sequences: (i) Septoria glycines and S. calendulae; (ii) S. gerberae and S. aciculosa, and the two strains of S. linicola; and (iii) Cercospora apii, C. kikuchii, C. nicotianae and C. beticola. Cercospora zonata and C. carotae had divergent D2 sequences. Dothidea sambuci and Sydowia polyspora, the only other Dothideales represented in this selection, clustered in a well-supported sister group (96%) of Mycosphaerella, but for all represented Dothideales there was less support (72%). Additional well-supported clusters were the Didymella spp., the two formae speciales of Phaeosphaeria avenaria, and two strains representing Pleospora herbarum and Pl. papaveracea. CBS 191.86 is most likely misidentified as Pl. herbarum. These results agree with those of the neighbor-joining analyses (FIG. 2). Again, in neighbor joining there was high support for the Ramularia spp. and M. graminicola, which clustered with M. laricina (anamorph Pseudocercospora sp.). Within Mycosphaerella, a large cluster with 93% bootstrap support comprised Phl. ulmi, M. harthensis, M. brassisicola, all Cercospora and Septoria spp. except S. tritici and S. pyricola. In parsimony analysis the support for this cluster was 84%.
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. Bootstrap supports of more than 50% are indicated. The results of the neighbor-joining analysis obtained with Bionumerics and PAUP were the same (FIG. 4) and largely agreed with those of the parsimony analysis in PAUP (FIG. 3). As expected, most strains of the same species clustered in highly supported clades in the bootstrap analysis and showed 100% homology or differed by a single position. A difference on 2–4 positions was observed within the strain pairs of Pseudocercospora musae, M. punctiformis, S. castaneicola and outgroup strains of Cladosporium herbarum. The three strains of S. rubi showed a higher diversity, with CBS 109017 (isolated from Rubus idaeus, Austria) differing from CBS 238.37 (from R. strigosus, Illinois) by 5 base positions in ITS 1, 2 positions in the 5.8 S gene, and 6 in ITS 2. It differed from CBS 102327 (from R. fruticosus s.l., Netherlands) by 11 positions in ITS 1, also 2 positions in the 5.8S gene and 5 in ITS 2. CBS 238.37 differed from 102327 by 10 positions in ITS 1 and 3 in ITS 2 (5.8 S gene identical).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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No more than four Septoria species previously have been included in molecular phylogenetic studies. Goodwin and Zismann (2001) sequenced the 5.8 S ribosomal RNA gene and flanking internal-transcribed spacers (ITS 1 and ITS 2) for a dozen strains of S. tritici and S. passerini. These authors demonstrated that S. passerini (teleomorph unknown) belongs in Mycosphaerella and is closely related to S. tritici (teleomorph M. graminicola). Based on ITS sequence analysis, Crous et al (2001b) found that two strains of S. aceris (teleomorph M. latebrosa) clustered with Cercospora spp., distant from a third strain, which belonged to S. tritici. They suspected that several possible lineages within Mycosphaerella were associated with Septoria anamorphs.
All Septoria species clustered within Mycosphaerella. Septoria has been regarded a heterogeneous assemblage due to the considerable variation in its conidial morphology, conidiogenesis and conidiomatal structures (Sutton 1980, Constantinescu 1984, Sutton and Hennebert 1994, Verkley 1998a, b, Muthumary 1999). We were unable to obtain material of S. cytisi, the type species of Septoria. This species has been studied extensively in planta, and several new varieties have been described recently (Farr 1992, Muthumary 1999). Morphologically this species certainly can be regarded as a typical Septoria, with well-developed pycnidia, sympodial as well as percurrent conidiogenous cell proliferation and relatively long, pluriseptate conidia. Transmission electron microscopy (TEM) of S. chrysanthemella Sacc., S. quercicola Sacc. and S. aceris has shown that these species also exhibit percurrent and sympodial proliferation, even in a single conidiogenous cell (Verkley 1998a, b). According to Sutton (1980), S. tritici and S. apiicola have phialidic conidiogenous cells. We observed percurrent and sympodial proliferation in all sporulating Septoria cultures used in the present study, including those of S. apiicola and also S. passerini, which is closely related to S. tritici (Goodwin and Zismann 2001). Our cultures of S. tritici seemed to confirm that the species is phialidic, but the conidiogenous cells are small and should be studied by TEM. Sutton’s observations on conidiogenesis in S. apiicola probably are based on cryptically proliferating cells, which under the light microscope easily can be mistaken for phialides, as reported for S. chrysanthemella (Verkley 1998a).
Representatives of the order Pleosporales were included in this study to detect possible affinities with Septoria species, but none were found. Leptosphaeria Ces. & De Not. and Phaeosphaeria I. Miyake species have anamorphs in Stagonospora (Sacc.) Sacc., that sometimes have been placed in Septoria. For example, Stagonospora nodorum (Berk.) Castell. & Germano, the anamorph of the cosmopolitan wheat pathogen Phaeosphaeria nodorum (E. Müll.) Hedjar. (syn. Leptosphaeria nodorum E. Müll.), still often is referred to as Septoria nodorum (Berk.) Berk. Verkley and Priest (2000) pointed out that it may be impossible to delimit Septoria from Stagonospora by strict morphological criteria alone.
Our results support the conclusions of Crous et al (2001b), that conidiomatal structure has little value for predicting phylogenetic relatedness among taxa in Mycosphaerella. Phloeospora ulmi, the type species of the anamorph genus Phloeospora, is characterized by acervuli on the host. It clustered in our phylogenetic analyses with Cercospora spp. forming caespituli and most Septoria spp. forming pycnidia. Septoria aceris, which also clusters among these fungi, often forms conidiomata that are similar to the acervuli of Phl. ulmi, for which it has been treated under Phloeospora by Jørstad (1965). Phloeospora ulmi and S. aceris also agree in conidiogenesis. It seems unlikely that a separation between Phloeospora and Septoria is tenable.
The results also indicate that Septoria is not monophyletic within Mycosphaerella and that the development of pycnidial forms with multiseptate hyaline conidia might have occurred more than once. Three lineages roughly are indicated here (viz. a major clade of Septoria spp. closely related to Cercospora spp., including several notorious pathogens such as S. apiicola, S. linicola and S. populicola, a second lineage containing the cereal pathogens Septoria tritici and S. passerini and possibly separate from these two lineages, one represented by S. castaneicola, and another by S. pyricola). A clade including S. tritici and species with Ramularia anamorphs was supported by high bootstrap values in the D2 analyses only. The ITS analyses of Crous et al (2001b) and Goodwin et al (2001) also suggest a close relationship of S. tritici and S. passerinii with Ramularia, one which contrasts with many morphological differences distinguishing Ramularia and Septoria anamorphs. The addition of S. pyricola, S. castaneicola and M. laricina to our ITS dataset may explain why this relationship is not confirmed in the analyses of that region. Ramularia spp. clustered in a single group within Mycosphaerella in earlier studies (Crous et al 2001b, Goodwin et al 2001), although the numbers of included strains were small.
Crous et al (2001b) already reported the clustering of Cercospora species with two strains of S. aceris (M. latebrosa), as well as M. brassicicola. Three out of four Cercospora spp. with identical D2 sequences (C. apii, C. kikuchii, C. beticola) also clustered in the analyses of ITS with high bootstrap support (parsimony 96%, neighbor joining 98%). Cercospora zonata and C. carotae, which were included here only in the analysis of the D2 region, did not cluster with these species. Stewart et al (1999) analyzed ITS and partial LSU rDNA sequences of selected cercosporoid anamorphs and identified a robust Cercospora cluster including C. apii, C. beticola, C. kikuchii, C. nicotianae and C. hayi Calp. Goodwin et al (2001) found some divergence within C. kikuchii. We included the ex-type strain of C. kikuchii (CBS 128.27), and it clustered with another isolate of that species, CK 39, which fell within Cercospora sensu Stewart et al (1999). The short branch lengths among the species of Cercospora suggest a relatively recent development from a shared common ancestor (Goodwin et al 2001).
The variation seen in the D2 region was lower than in the ITS region. The D2 sequences of S. aciculosa, S. gerberae and S. linicola were identical, indicating that this region is too conserved for species recognition, and the ITS sequences of these species also were similar. For example, S. gerberae CBS 410.61, isolated from Gerbera in Italy, differed from S. linicola CBS 316.37, from Linum in Argentina by only a single base position in ITS 2 (A-T). The isolates of Septoria scabiosicola originating from Knautia and Succissa (Dipsacaceae) differed from the two strains of S. lamiicola from Lamium album (Lamiaceae) by one position in ITS 1 and one in ITS 2. These species are also similar in their morphology in planta and in vitro and most likely are related closely although they occur on plants of different families.
S. rubi strains were isolated from three different Rubus species and most likely represent three distinct species. CBS 238.37, isolated from R. strigosus from Illinois and preserved in CBS culture collection as M. rubi, unfortunately is now degenerated and sterile. However, we were able to compare the morphology of the two European isolates in culture. On oatmeal agar (OA), CBS 102327 (R. fruticosus, Netherlands) formed 1–5-septate conidia 30–80 x 1.2–2.0 µm, similar to those seen in planta. According to Jørstad (1965), the conidia of S. rubi measure 24–64 x 1.5–2 µm on R. idaeus, while Teterevnikova-Babayan (1987) gives 20–90 x 1.5–2 µm as conidial measurements for this species. CBS 109017 (R. idaeus, Austria) produced 3–8-septate conidia 58–108 x 2.8–3.2 µm on OA, slightly longer than those formed in planta. These conidia clearly are wider than those of S. rubi and agree more with those of S. rosae Desm. (40–72 x 2.5–3.5 µm cf. Jørstad 1965; 48–95 x 2.5–4.5 µm, cf. Teterevnikova-Babayan 1987). That species, however, is only known from Rosa. A dozen Septoria names have been described from the host genus Rubus. As noted by Jørstad (1965), the taxonomy and host specificity of Septoria spp. and possibly related Mycosphaerella spp. described on Rubus and other Rosaceae still are unclear.
In the ITS analyses, S. castaneicola is closer to M. laricina and species with Pseudocercospora anamorphs than are other Septoria spp. We were unable to obtain D2 sequences for these species. Compared to most Septoria spp., S. castaneicola has much darker colonies on OA and is slow growing. The conidia are relatively wide and clearly constricted at the septa, but those features also are observed in other taxa, e.g., Phl. ulmi. A Pseudocercospora/Paracercospora clade was identified by Stewart et al (1999), based on ITS and partial LSU sequence data, and was confirmed in later studies (Crous et al 2001b, Goodwin et al 2001). As a result, Paracercospora recently was placed in the synonymy of Pseudocercospora by Crous et al (2001b).
Septoria pyricola (teleomorph M. pyri) also seems distant from other Septoria species, and its conidia are aberrant because of their pale greenish pigmentation. The ITS and D2 analyses indicate a possible relationship to M. milleri, but the anamorph of that species, Cercosporidium magnoliae (Phaeoisariopsis magnoliae [Ell. & Harkn.] Jong & Morris), is vastly divergent from S. pyricola. It is cercosporoid, with synnema-like caespituli and sympodial conidiogenous cells producing hyaline to pale olivaceous, smooth to slightly verruculose, (1–)2(–3)-septate conidia. It would fit Passalora Fr. or Pseudocercospora in the sense of Crous et al (2001b). In this case, only the conidial pigmentation supports the molecular results, which is interesting in light of the suggestion of Crous et al (2001b) that the presence or absence of pigmentation in conidiophores and conidia is a character of value at generic level in anamorphs of Mycosphaerella.
Mycosphaerella marksii and Stenella parkii (teleomorph M. parkii) cluster in a clade that is well supported by ITS analyses. Crous et al (2000) found a clustering of two other strains representing these species, based on ITS sequence data. The anamorph of M. marksii is unknown, but Crous et al (2000) found verruculose hyphae in culture and suggested that the species might form an anamorph similar to Stenella Syd., which is characterized by pigmented verruculose superficial hyphae and mononematous scattered conidiophores. However, as shown by Goodwin et al (2001), some Mycosphaerella species with Stenella anamorphs may not be closely related (viz. St. citrigrisea [Fisher] Sivan. [teleomorph M. citri J. O. Whiteside] and also the type species of Stenella, St. araguata Syd). A strain of St. araguata (CBS 486.80) was sequenced by these authors and found to cluster with Uwebraunia juvenis Crous & M. J. Wingf. (teleomorph M. juvenis Crous & M. J. Wingf.).
In addition to Septoria, Mycosphaerella also produces two other pycnidial anamorphs, Phaeophleospora Rangel and Sonderhenia H. Swart & J. Walker. These genera differ considerably in morphology from Septoria. Phaeophleospora and Sonderhenia both have brown and percurrent conidiogenous cells, but in the former genus these cells are verruculose, while in the latter they are smooth-walled. Conidia are brown and smooth to verruculose in both genera, yet are distoseptate in Sonderhenia and euseptate in Phaeophleospora. In earlier ITS and LSU sequence studies, Sonderhenia was found to cluster with Pseudocercospora Speg. and Mycovellosiella Rangel (Crous et al 2001a). Phaeophleospora clustered in ITS studies with the acervular Colletogloeopsis Crous & M. J. Wingf. and the mononematous Scolecostigmina U. Braun, distant from the included Septoria spp. (Crous et al 2001b). Because of the affinities among taxa with pycnidial and nonpycnidial anamorphs, Crous et al (2001b) suggested that conidiomatal structure is less reliable as a phylogenetic marker in Mycosphaerella than are other characters such as conidiogenesis and conidial pigmentation (Crous et al 2001b). Our results confirm this, but they also suggest that conidiogenous cell proliferation may be poorly informative in these fungi.
Species with unknown teleomorph affinities group with pleomorphic species in well-supported clades (see TABLE I). Some taxa that have been extensively studied have likely lost the teleomorph, e.g., Septoria passerini and S. apiicola. In some species, there would seem to be a sound ecological reason for failure to produce a teleomorph. For example, Septoria lamiicola and S. scabiosicola are found only in summer on living leaves and these leaves are degraded in the fall before teleomorph development can occur. We conclude that the loss of the teleomorph most likely has occurred several times in the evolutionary history of Mycosphaerella and that it also involved taxa with Septoria anamorphs.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 Corresponding author. E-mail: verkley{at}cbs.knaw.nl
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LITERATURE CITED |
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