Although Glomerella glycines, Colletotrichum magnum and C. orchidearum are known as causal agents of anthracnose of soybean, Cucurbitaceae and Orchidaceae, respectively, their taxonomy remains unresolved. In preliminary analyses based on ITS, strains of these species appear basal in Colletotrichum phylogenies, clustering close to C. cliviae, C. brevisporum and other recently described species from tropical or subtropical regions. Phylogenetic analyses (ITS, GAPDH, CHS-1, HIS3, ACT, TUB2) of 102 strains previously identified as Ga. glycines, C. magnum and C. orchidearum as well as other related strains from different culture collections and studies placed these taxa in three species complexes, and distinguished at least 24 species, including 11 new species. In this study, C. magnum, C. orchidearum and C. piperis were epitypified and their taxonomy resolved, while C. cliviicola was proposed as a new name for C. cliviae. Furthermore, a sexual morph was observed for C. yunnanense, while C. brevisporum, C. cliviicola and C. tropicicola were reported from new hosts or countries. Regarding their conidial morphology, species in the C. dracaenophilum, C. magnum and C. orchidearum species complexes are reminiscent of C. gloeosporioides or C. boninense s. lat., and were likely to be confused with them in the past.
Novel species of fungi described in this study include those from various countries as follows: Australia, Austroboletus asper on soil, Cylindromonium alloxyli on leaves of Alloxylon pinnatum, Davidhawksworthia quintiniae on leaves of Quintinia sieberi, Exophiala prostantherae on leaves of Prostanthera sp., Lactifluus lactiglaucus on soil, Linteromyces quintiniae (incl. Linteromyces gen. nov.) on leaves of Quintinia sieberi, Lophotrichus medusoides from stem tissue of Citrus garrawayi, Mycena pulchra on soil, Neocalonectria tristaniopsidis (incl. Neocalonectria gen. nov.)and Xyladictyochaeta tristaniopsidis on leaves of Tristaniopsis collina, Parasarocladium tasmanniae on leaves of Tasmannia insipida, Phytophthora aquae-cooljarloo from pond water, Serendipita whamiae as endophyte from roots of Eriochilus cucullatus, Veloboletus limbatus (incl. Veloboletus gen. nov.)onsoil. Austria, Cortinarius glaucoelotus onsoil. Bulgaria, Suhomyces rilaensis from the gut of Bolitophagus interruptus found on a Polyporus sp. Canada, Cantharellus betularum among leaf litter of Betula, Penicillium saanichii from house dust. Chile, Circinella lampensis on soil, Exophiala embothrii from rhizosphere of Embothrium coccineum. China, Colletotrichum cycadis on leaves of Cycas revoluta. Croatia, Phialocephala melitaea on fallen branch of Pinus halepensis. Czech Republic, Geoglossum jirinae on soil, Pyrenochaetopsis rajhradensis from dead wood of Buxus sempervirens. Dominican Republic, Amanita domingensis on litter of deciduous wood, Melanoleuca dominicana on forest litter. France, Crinipellis nigrolamellata (Martinique) on leaves of Pisonia fragrans, Talaromyces pulveris from bore dust of Xestobium rufovillosum infesting floorboards. French Guiana, Hypoxylon hepaticolor on dead corticated branch. Great Britain, Inocybe ionolepis on soil. India, Cortinarius indopurpurascens among leaf litter of Quercus leucotrichophora. Iran, Pseudopyricularia javanii on infected leaves of Cyperus sp., Xenomonodictys iranica (incl. Xenomonodictys gen. nov.) on wood of Fagus orientalis. Italy, Penicillium vallebormidaense from compost. Namibia, Alternaria mirabibensis on plant litter, Curvularia moringae and Moringomyces phantasmae (incl. Moringomyces gen. nov.) on leaves and flowers of Moringa ovalifolia, Gobabebomyces vachelliae (incl. Gobabebomyces gen. nov.) on leaves of Vachellia erioloba, Preussia procaviae on dung of Procavia capensis. Pakistan, Russula shawarensis from soil on forest floor. Russia, Cyberlindnera dauci from Daucus carota. South Africa, Acremonium behniae on leaves of Behnia reticulata, Dothiora aloidendri and Hantamomyces aloidendri (incl. Hantamomyces gen. nov.) on leaves of Aloidendron dichotomum, Endoconidioma euphorbiae on leaves of Euphorbia mauritanica , Eucasphaeria proteae on leaves of Protea neriifolia , Exophiala mali from inner fruit tissue of Malus sp., Graminopassalora geissorhizae on leaves of Geissorhiza splendidissima, Neocamarosporium leipoldtiae on leaves of Leipoldtia schultzii, Neocladosporium osteospermi on leaf spots of Osteospermum moniliferum, Neometulocladosporiella seifertii on leaves of Combretum caffrum, Paramyrothecium pituitipietianum on stems of Grielum humifusum, Phytopythium paucipapillatum from roots of Vitis sp., Stemphylium carpobroti and Verrucocladosporium carpobroti on leaves of Carpobrotus quadrifolius, Suttonomyces cephalophylli on leaves of Cephalophyllum pilansii. Sweden, Coprinopsis rubra on cow dung, Elaphomyces nemoreus fromdeciduouswoodlands. Spain, Polyscytalum pini-canariensis on needles of Pinus canariensis, Pseudosubramaniomyces septatus from stream sediment, Tuber lusitanicum on soil under Quercus suber. Thailand, Tolypocladium flavonigrum on Elaphomyces sp. USA, Chaetothyrina spondiadis on fruits of Spondias mombin, Gymnascella minnisii from bat guano, Juncomyces patwiniorum on culms of Juncus effusus, Moelleriella puertoricoensis on scale insect, Neodothiora populina (incl. Neodothiora gen. nov.) on stem cankers of Populus tremuloides, Pseudogymnoascus palmeri fromcavesediment. Vietnam, Cyphellophora vietnamensis on leaf litter, Tylopilus subotsuensis on soil in montane evergreen broadleaf forest. Morphological and culture characteristics are supported by DNA barcodes.
DNA methylation is found throughout all domains of life, yet the extent and function of DNA methylation differ between eukaryotes. Many strains of the plant pathogenic fungus Zymoseptoria tritici appeared to lack cytosine DNA methylation (5mC) because gene amplification followed by Repeat-Induced Point mutation (RIP) resulted in the inactivation of the Ztdim2 DNA methyltransferase gene. 5mC is, however, present in closely related sister species. We demonstrate that inactivation of Ztdim2 occurred recently as some Z. tritici isolates carry a functional Ztdim2 gene. Moreover, we show that Ztdim2 inactivation occurred by a different path than previously hypothesized. We mapped the genome-wide distribution of 5mC in strains with and without functional Ztdim2. Presence of functional Ztdim2 correlated with high levels of 5mC in transposable elements (TEs), suggesting a role in genome defense.We identified low levels of 5mC in strains carrying inactive Ztdim2 alleles, suggesting that 5mC is maintained over time, presumably by an active Ztdnmt5 gene. Integration of a functional Ztdim2 allele in strains with mutated Ztdim2 restored normal 5mC levels, demonstrating de novo cytosine methylation activity of Ztdim2. To assess the importance of 5mC for genome evolution, we performed an evolution experiment, comparing genomes of strains with high levels of 5mC to genomes of strains lacking Ztdim2. We found that the presence of Ztdim2 alters nucleotide composition by promoting C to T transitions (C→T) specifically at CpA (CA) sites during mitosis, likely contributing to TE inactivation. Our results show that dense 5mC at TEs is a polymorphic trait in Z. tritici populations that can impact genome evolution. SignificanceCytosine DNA methylation (5mC) is known to silence transposable elements in fungi and thereby appears to contribute to genome stability. The genomes of plant pathogenic fungi are highly diverse, differing substantially in transposon content and distribution. Here, we show extensive differences of 5mC levels within a single species of an important wheat pathogen that were caused by inactivation of the DNA methyltransferase ZtDim2 in the majority of studied isolates. Presence of widespread 5mC increased point mutation rates in regions with active or mutated transposable elements during mitosis. The mutation pattern is dependent on the presence of ZtDim2 and resembles a mitotic version of Repeat-Induced Point mutation (RIP). Thus, loss of 5mC may represent an evolutionary trade-off offering adaptive potential at the cost of transposon control. occurred recently as two closely related sister species of Z. tritici, Zymoseptoria ardabiliae and Zymoseptoria pseudotritici were shown to carry a single intact dim2 gene and have 5mC (25).By genome analyses of multiple Z. tritici isolates from the center of origin of the pathogen, the Middle East, we discovered several Z. tritici isolates with an intact Ztdim2 gene. This finding suggests that the loss of 5mC not only occurred very recently but is a polymorphic trait in Z.triti...
DNA methylation is found throughout all domains of life, yet the extent and function of DNA methylation differ among eukaryotes. Strains of the plant pathogenic fungus Zymoseptoria tritici appeared to lack cytosine DNA methylation (5mC) because gene amplification followed by Repeat-Induced Point mutation (RIP) resulted in the inactivation of the dim2 DNA methyltransferase gene. 5mC is, however, present in closely related sister species. We demonstrate that inactivation of dim2 occurred recently as some Z. tritici isolates carry a functional dim2 gene. Moreover, we show that dim2 inactivation occurred by a different path than previously hypothesized. We mapped the genome-wide distribution of 5mC in strains with or without functional dim2 alleles. Presence of functional dim2 correlates with high levels of 5mC in transposable elements (TEs), suggesting a role in genome defense. We identified low levels of 5mC in strains carrying non-functional dim2 alleles, suggesting that 5mC is maintained over time, presumably by an active Dnmt5 DNA methyltransferase. Integration of a functional dim2 allele in strains with mutated dim2 restored normal 5mC levels, demonstrating de novo cytosine methylation activity of Dim2. To assess the importance of 5mC for genome evolution, we performed an evolution experiment, comparing genomes of strains with high levels of 5mC to genomes of strains lacking functional dim2. We found that presence of a functional dim2 allele alters nucleotide composition by promoting C to T transitions (C→T) specifically at CpA (CA) sites during mitosis, likely contributing to TE inactivation. Our results show that 5mC density at TEs is a polymorphic trait in Z. tritici populations that can impact genome evolution.
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