Highlights of the Didymellaceae - Studies in Mycology
Highlights of the Didymellaceae - Studies in Mycology
Highlights of the Didymellaceae - Studies in Mycology
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AveSkAMp et al.<br />
<strong>in</strong> morphology (Wollenweber & Hochapfel 1937, Brewer & Boerema<br />
1965, Boerema & Bollen 1975, Boerema 1997), physiology<br />
(Noordeloos et al. 1993, Faris-Mokaiesh et al. 1995), pathogenicity<br />
(Mendes-Perreira et al. 1999, Davidson et al. 2009) and nucleotide<br />
sequences (Faris-Mokaiesh et al. 1995, Fatehi et al. 2003, Schoch<br />
et al. 2006, Peever et al. 2007, Chilvers et al. 2009, De Gruyter<br />
et al. 2009). In <strong>the</strong> Saccardoan system, both genera were only<br />
dist<strong>in</strong>guished by <strong>the</strong> presence or absence <strong>of</strong> conidial septa, and<br />
by <strong>the</strong> type <strong>of</strong> substrate: Ascochyta species were considered to<br />
be specific leaf-pathogens, whereas Phoma was solely associated<br />
with stem lesions (Boerema & Bollen 1975).<br />
Brewer & Boerema (1965) contrasted <strong>the</strong> septation process<br />
<strong>of</strong> <strong>the</strong> conidia <strong>in</strong> Ascochyta pisi to this process <strong>in</strong> Phoma exigua.<br />
These authors suggested that <strong>in</strong> Phoma species euseptation occurs<br />
only after secession, whereas <strong>in</strong> Ascochyta <strong>the</strong> septation <strong>of</strong> <strong>the</strong><br />
spores was considered to be an elemental part <strong>of</strong> conidiogenesis.<br />
Later, this was determ<strong>in</strong>ed to be a genus-specific character<br />
(Boerema 1970). Additionally, Boerema and Bollen (1975) stated<br />
that both genera are dist<strong>in</strong>ct <strong>in</strong> conidiogenesis. Accord<strong>in</strong>g to <strong>the</strong>se<br />
authors, <strong>the</strong> Ascochyta species produce conidia from ei<strong>the</strong>r an<br />
accumulation <strong>of</strong> annelations, which give <strong>the</strong> conidigenous cell<br />
an annelidic appearance, or from a gradually thicken<strong>in</strong>g collar <strong>of</strong><br />
pericl<strong>in</strong>al annelations. In contrast, Phoma species produce true<br />
phialides with a collarette. This micromorphological difference <strong>of</strong> <strong>the</strong><br />
conidiogenesis can only be observed us<strong>in</strong>g electron microscopy,<br />
as <strong>the</strong> appearance <strong>of</strong> a Phoma collarette is highly similar to <strong>the</strong><br />
pericl<strong>in</strong>al thicken<strong>in</strong>g <strong>of</strong> Ascochyta species. This observation is<br />
however not consistent with <strong>the</strong> conidial ontogeny <strong>of</strong> Ph. fumosa,<br />
which was observed to be annellidic by Sutton & Sandhu (1969).<br />
The application <strong>of</strong> <strong>the</strong>se characters for <strong>the</strong> purpose <strong>of</strong> generic<br />
delimitation was heavily questioned (Punithal<strong>in</strong>gam 1979a), and<br />
nowadays <strong>the</strong>se characters are hardly applied <strong>in</strong> <strong>the</strong> taxonomy<br />
<strong>of</strong> both genera, simply because <strong>the</strong> use <strong>of</strong> electron microscopy<br />
is expensive and section<strong>in</strong>g <strong>of</strong> pycnidia is too time consum<strong>in</strong>g.<br />
Due to this unclear classification system, and to <strong>the</strong> fact that<br />
not all species produce exclusively septate or aseptate conidia,<br />
species had synonyms <strong>in</strong> both genera (Boerema 1972, Boerema<br />
& Dorenbosch 1973, Van der Aa et al. 2000, Mel’nik 2000). Even<br />
nowadays <strong>the</strong> status <strong>of</strong> many species is unclear as Phoma and<br />
Ascochyta synonyms are <strong>of</strong>ten used simultaneously. Examples are<br />
Ph. rabiei and its synonym A. rabiei (S<strong>in</strong>gh & Reddy 1993, S<strong>in</strong>gh<br />
et al. 1997, Barve et al. 2003, Chongo et al. 2004, Pande et al.<br />
2005, Hernandez-Bello et al. 2006, Peever et al. 2007), and Ph.<br />
gossypiicola and its synonym, A. gossypii (e.g. Shen et al. 2005).<br />
The concept <strong>of</strong> Ph. clematid<strong>in</strong>a has appeared to comprise several<br />
taxa belong<strong>in</strong>g <strong>in</strong> multiple genera, amongst which a Didymella with<br />
an unnamed Ascochyta anamorph (Woudenberg et al. 2009).<br />
The results presented <strong>in</strong> this study fur<strong>the</strong>r suggest a close<br />
relation between Microsphaeropsis and Phoma. Morphological<br />
studies <strong>of</strong> members <strong>of</strong> both genera (Jones 1976) reveal that<br />
conidiogenesis is similar, although <strong>the</strong> conidia <strong>of</strong> Microsphaeropsis<br />
differ from those <strong>of</strong> Phoma by <strong>the</strong> dark pigmentation and <strong>the</strong><br />
presence <strong>of</strong> a double-layered cell wall. The pigmentation occurs<br />
only after conidial secession. Therefore, young pycnidia with<br />
colourless pycnidia may be easily confused with a Phoma species<br />
(Boerema et al. 2004).<br />
In general, it can be concluded that Phoma should only<br />
be regarded as a general concept, as members shar<strong>in</strong>g this<br />
morphology are found throughout <strong>the</strong> Pleosporales, although most<br />
members are found <strong>in</strong> <strong>the</strong> <strong>Didymellaceae</strong>. The type species <strong>of</strong><br />
Phoma is only distantly related to <strong>the</strong> o<strong>the</strong>r members <strong>of</strong> this genus,<br />
but relatively close to Ascochyta pisi, <strong>the</strong> type species <strong>of</strong> <strong>the</strong> older<br />
52<br />
name Ascochyta. However, based on <strong>the</strong> results observed <strong>in</strong> <strong>the</strong><br />
present study, this genus is poorly elucidated. Therefore, we opt<br />
to reta<strong>in</strong> <strong>the</strong> taxonomy <strong>of</strong> Phoma as is, with <strong>the</strong> exception <strong>of</strong> <strong>the</strong><br />
groups that can be resolved fur<strong>the</strong>r, such as Boeremia, Epicoccum,<br />
Peyronellaea and Stagonosporopsis.<br />
Taxonomic revisions<br />
The observations presented <strong>in</strong> <strong>the</strong> present paper suggest that<br />
LSU and SSU data, which conta<strong>in</strong> approximately 270 <strong>in</strong>formative<br />
sites <strong>in</strong> <strong>the</strong> alignment, are sufficient to dist<strong>in</strong>guish various major<br />
groups <strong>in</strong> <strong>the</strong> Pleosporales. However, o<strong>the</strong>r, more variable loci<br />
should also be analysed to determ<strong>in</strong>e <strong>the</strong> phylogenetical basis for<br />
<strong>the</strong> species that are congeneric with <strong>the</strong> ex-type stra<strong>in</strong> <strong>of</strong> Phoma.<br />
These species were found throughout <strong>the</strong> pleosporalean phylogeny<br />
that was reconstructed <strong>in</strong> <strong>the</strong> present paper. Molecular studies<br />
on <strong>the</strong> species that are currently accommodated <strong>in</strong> <strong>the</strong> section<br />
Plenodomus and Pilosa are <strong>in</strong> progress (De Gruyter et al. <strong>in</strong> prep.).<br />
The type species <strong>of</strong> <strong>the</strong> genus Phoma, Ph. herbarum, resides<br />
<strong>in</strong> <strong>the</strong> <strong>Didymellaceae</strong> clade, a result that is <strong>in</strong> congruence with <strong>the</strong><br />
observations <strong>of</strong> De Gruyter et al. (2009). However, based on <strong>the</strong> data<br />
generated <strong>in</strong> <strong>the</strong> present study, also <strong>the</strong> type species <strong>of</strong> Ascochyta<br />
(A. pisi), Chaetasbolisia (C. erysiphoides), and Microsphaeropis (M.<br />
olivaceae) are located <strong>in</strong> <strong>the</strong> same group (Fig. 2). Of those species,<br />
Phoma carries <strong>the</strong> oldest name, which was deposited by Fries <strong>in</strong><br />
1821, but as Phoma sensu Saccardo (1880) was conserved aga<strong>in</strong>st<br />
Phoma Fries (McNeill et al. 2006), <strong>the</strong> genus Ascochyta, which was<br />
erected <strong>in</strong> 1830, would be <strong>the</strong> preferred name for <strong>the</strong> species <strong>in</strong> this<br />
genus. Never<strong>the</strong>less, because <strong>of</strong> <strong>the</strong> impact that recomb<strong>in</strong>ation <strong>of</strong><br />
Phoma <strong>in</strong> Ascochyta would have <strong>in</strong> phytopathology, we suggest to<br />
keep both generic names <strong>in</strong> use for <strong>the</strong> unresolved species <strong>in</strong> <strong>the</strong><br />
<strong>Didymellaceae</strong>, disregard<strong>in</strong>g <strong>the</strong> fact that both names are polyphyletic.<br />
Both genera can be regarded as polyphyletic concepts, until a<br />
proper study <strong>of</strong> <strong>the</strong> teleomorph genera related to <strong>the</strong> <strong>Didymellaceae</strong><br />
has been conducted. Also <strong>the</strong> younger genera Chaetasbolisia<br />
and Microsphaeropsis should be reta<strong>in</strong>ed as separate taxonomic<br />
entities, until at least all taxa are restudied both morphologically and<br />
phylogenetically. However, <strong>the</strong> clades that are resolved, and that are<br />
characterised by shared morphological or physiological characters,<br />
or have a shared ecological role, are elevated to generic level here.<br />
Consequences <strong>of</strong> this approach are <strong>the</strong> re<strong>in</strong>statement <strong>of</strong> <strong>the</strong> genus<br />
Peyronellaea Goid., expansion <strong>of</strong> <strong>the</strong> formerly monotypic genus<br />
Epicoccum L<strong>in</strong>k, emendment <strong>of</strong> <strong>the</strong> concept <strong>of</strong> Stagonosporopsis<br />
Died. and <strong>the</strong> erection <strong>of</strong> <strong>the</strong> novel genus Boeremia.<br />
Teleomorph relations<br />
In Phoma several teleomorphs have been recognised, but for <strong>the</strong><br />
majority <strong>of</strong> Phoma species <strong>the</strong> sexual structures have yet to be<br />
discovered, as <strong>the</strong> <strong>in</strong>duction <strong>of</strong> <strong>the</strong>se structures requires special<br />
conditions; or simply because <strong>the</strong> species has lost its ability to<br />
propagate sexually. Boerema et al. (2004) only recognised ca. 40<br />
species that produce teleomorphs.<br />
The f<strong>in</strong>d<strong>in</strong>g <strong>of</strong> multiple teleomorphs with phenotypically<br />
<strong>in</strong>dist<strong>in</strong>guishable associated anamorphs is not uncommon <strong>in</strong><br />
mycology, yet unwanted, and should be resolved <strong>in</strong> due course as<br />
more data become available. For example, such a situation also<br />
applies to major genera such as Aspergillus (Pitt & Samson 2007),<br />
Botryosphaeria (Crous et al. 2006), Geotrichum (De Hoog & Smith<br />
2004), Mycosphaerella (Crous et al. 2009a, b) and Penicillium (Pitt<br />
1979).