A higher-rank classification for rust fungi, with notes on genera.

The rust fungi (Pucciniales) with 7000+ species comprise one of the largest orders of Fungi, and one for which taxonomy at all ranks remains problematic. Here we provide a taxonomic framework, based on 16 years of sampling that includes ca. 80 % of accepted genera including type species wherever possible, and three DNA loci used to resolve the deeper nodes of the rust fungus tree of life. Pucciniales are comprised of seven suborders - Araucariomycetineae subord. nov., Melampsorineae, Mikronegeriineae, Raveneliineae subord. nov., Rogerpetersoniineae subord. nov., Skierkineae subord. nov., and Uredinineae - and 18 families - Araucariomycetaceae fam. nov., Coleosporiaceae, Crossopsoraceae fam. nov., Gymnosporangiaceae, Melampsoraceae, Milesinaceae fam. nov., Ochropsoraceae fam. & stat. nov., Phakopsoraceae, Phragmidiaceae, Pileolariaceae, Pucciniaceae, Pucciniastraceae, Raveneliaceae, Rogerpetersoniaceae fam. nov., Skierkaceae fam. & stat. nov., Sphaerophragmiaceae, Tranzscheliaceae fam. & stat. nov., and Zaghouaniaceae. The new genera Araucariomyces (for Aecidium fragiforme and Ae. balansae), Neoolivea (for Olivea tectonae), Rogerpetersonia (for Caeoma torreyae), and Rossmanomyces (for Chrysomyxa monesis, Ch. pryrolae, and Ch. ramischiae) are proposed. Twenty-one new combinations and one new name are introduced for: Angiopsora apoda, Angiopsora chusqueae, Angiopsora paspalicola, Araucariomyces balansae, Araucariomyces fragiformis, Cephalotelium evansii, Cephalotelium neocaledoniense, Cephalotelium xanthophloeae, Ceropsora weirii, Gymnotelium speciosum, Lipocystis acaciae-pennatulae, Neoolivea tectonae, Neophysopella kraunhiae, Phakopsora pipturi, Rogerpetersonia torreyae, Rossmanomyces monesis, Rossmanomyces pryrolae, Rossmanomyces ramischiae, Thekopsora americana, Thekopsora potentillae, Thekopsora pseudoagrimoniae, and Zaghouania notelaeae. Higher ranks are newly defined with consideration of morphology, host range and life cycle. Finally, we discuss the evolutionary and diversification trends within Pucciniales. Citation: Aime MC, McTaggart AR (2020). A higher-rank classification for rust fungi, with notes on genera. Fungal Systematics and Evolution 7: 21-47. doi: 10.3114/fuse.2021.07.02.

Population genomics reveals historical and ongoing recombination in the Fusarium oxysporum species complex.

The Fusarium oxysporum species complex (FOSC) is a group of closely related plant pathogens long-considered strictly clonal, as sexual stages have never been recorded. Several studies have questioned whether recombination occurs in FOSC, and if it occurs its nature and frequency are unknown. We analysed 410 assembled genomes to answer whether FOSC diversified by occasional sexual reproduction interspersed with numerous cycles of asexual reproduction akin to a model of predominant clonal evolution (PCE). We tested the hypothesis that sexual reproduction occurred in the evolutionary history of FOSC by examining the distribution of idiomorphs at the mating locus, phylogenetic conflict and independent measures of recombination from genome-wide SNPs and genes. A phylogenomic dataset of 40 single copy orthologs was used to define structure a priori within FOSC based on genealogical concordance. Recombination within FOSC was tested using the pairwise homoplasy index and divergence ages were estimated by molecular dating. We called SNPs from assembled genomes using a k-mer approach and tested for significant linkage disequilibrium as an indication of PCE. We clone-corrected and tested whether SNPs were randomly associated as an indication of recombination. Our analyses provide evidence for sexual or parasexual reproduction within, but not between, clades of FOSC that diversified from a most recent common ancestor about 500 000 years ago. There was no evidence of substructure based on geography or host that might indicate how clades diversified. Competing evolutionary hypotheses for FOSC are discussed in the context of our results.

The PhyloCode applied to Cintractiellales, a new order of smut fungi with unresolved phylogenetic relationships in the Ustilaginomycotina.

The PhyloCode is used to classify taxa based on their relation to a most recent common ancestor as recovered from a phylogenetic analysis. We examined the first specimen of Cintractiella (Ustilaginomycotina) collected from Australia and determined its systematic relationship to other Fungi. Three ribosomal DNA loci were analysed both with and without constraint to a phylogenomic hypothesis of the Ustilaginomycotina. Cintractiella did not share a most recent common ancestor with other orders of smut fungi. We used the PhyloCode to define the Cintractiellales, a monogeneric order with four species of Cintractiella, including C. scirpodendri sp. nov. on Scirpodendron ghaeri. The Cintractiellales may have shared a most recent common ancestor with the Malasseziomycetes, but are otherwise unresolved at the rank of class.

Diversity of gall-forming rusts (Uromycladium, Pucciniales) on Acacia in Australia.

Uromycladium tepperianum has been reported on over 100 species of Acacia, as well as on the closely related plant genera, Falcataria, Racosperma and Paraserianthes. Previous studies have indicated that U. tepperianum may represent a complex of host-specific, cryptic species. The phylogenetic relationships between 79 specimens of Uromycladium were determined based on a concatenated dataset of the Small Subunit, the Internal Transcribed Spacer and the Large Subunit regions of nuclear ribosomal DNA, and the mitochondrial cytochrome c oxidase subunit 3. This study showed that the host range of U. tepperianum s.str. was restricted to species of Acacia in the 'A. bivenosa group' sensu Chapman & Maslin (1992). An epitype of U. tepperianum on A. ligulata is designated to create a stable taxonomy for the application of this name. Sixteen novel species of Uromycladium are described, based on host preference, morphology and a phylogenetic species concept.

Genera of phytopathogenic fungi: GOPHY 1.

Genera of Phytopathogenic Fungi (GOPHY) is introduced as a new series of publications in order to provide a stable platform for the taxonomy of phytopathogenic fungi. This first paper focuses on 21 genera of phytopathogenic fungi: Bipolaris, Boeremia, Calonectria, Ceratocystis, Cladosporium, Colletotrichum, Coniella, Curvularia, Monilinia, Neofabraea, Neofusicoccum, Pilidium, Pleiochaeta, Plenodomus, Protostegia, Pseudopyricularia, Puccinia, Saccharata, Thyrostroma, Venturia and Wilsonomyces. For each genus, a morphological description and information about its pathology, distribution, hosts and disease symptoms are provided. In addition, this information is linked to primary and secondary DNA barcodes of the presently accepted species, and relevant literature. Moreover, several novelties are introduced, i.e. new genera, species and combinations, and neo-, lecto- and epitypes designated to provide a stable taxonomy. This first paper includes one new genus, 26 new species, ten new combinations, and four typifications of older names.

Saprophytic and pathogenic fungi in the Ceratocystidaceae differ in their ability to metabolize plant-derived sucrose.

BACKGROUND: Proteins in the Glycoside Hydrolase family 32 (GH32) are carbohydrate-active enzymes known as invertases that hydrolyse the glycosidic bonds of complex saccharides. Fungi rely on these enzymes to gain access to and utilize plant-derived sucrose. In fungi, GH32 invertase genes are found in higher copy numbers in the genomes of pathogens when compared to closely related saprophytes, suggesting an association between invertases and ecological strategy. The aim of this study was to investigate the distribution and evolution of GH32 invertases in the Ceratocystidaceae using a comparative genomics approach. This fungal family provides an interesting model to study the evolution of these genes, because it includes economically important pathogenic species such as Ceratocystis fimbriata, C. manginecans and C. albifundus, as well as saprophytic species such as Huntiella moniliformis, H. omanensis and H. savannae. RESULTS: The publicly available Ceratocystidaceae genome sequences, as well as the H. savannae genome sequenced here, allowed for the identification of novel GH32-like sequences. The de novo assembly of the H. savannae draft genome consisted of 28.54 megabases that coded for 7 687 putative genes of which one represented a GH32 family member. The number of GH32 gene family members appeared to be related to the ecological adaptations of these fungi. The pathogenic Ceratocystis species all contained two GH32 family genes (a putative cell wall and a putative vacuolar invertase), while the saprophytic Huntiella species had only one of these genes (a putative cell wall invertase). Further analysis showed that the evolution of the GH32 gene family in the Ceratocystidaceae involved transposable element-based retro-transposition and translocation. As an example, the activity of a Fot5-like element likely facilitated the assembly of the genomic regions harbouring the GH32 family genes in Ceratocystis. CONCLUSIONS: This study provides insight into the evolutionary history of the GH32 gene family in Ceratocystidaceae. Our findings suggest that transposable elements shaped the evolution of the GH32 gene family, which in turn determines the sucrolytic activities and related ecological strategies of the Ceratocystidaceae species that harbour them. The study also provides insights into the role of carbohydrate-active enzymes in plant-fungal interactions and adds to our understanding of the evolution of these enzymes and their role in the life style of these fungi.

A co-evolutionary relationship exists between Endoraecium (Pucciniales) and its Acacia hosts in Australia.

Endoraecium is a genus of rust fungi that infects several species of Acacia in Australia, South-East Asia and Hawaii. This study investigated the systematics of Endoraecium from 55 specimens in Australia based on a combined morphological and molecular approach. Phylogenetic analyses were conducted on partitioned datasets of loci from ribosomal and mitochondrial DNA. The recovered molecular phylogeny supported a recently published taxonomy based on morphology and host range that divided Endoraecium digitatum into five species. Spore morphology is synapomorphic and there is evidence Endoraecium co-evolved with its Acacia hosts. The broad host ranges of E. digitatum, E. parvum, E. phyllodiorum and E. violae-faustiae are revised in light of this study, and nine new species of Endoraecium are described from Australia based on host taxonomy, morphology and phylogenetic concordance.

Fungal Planet description sheets: 107-127.

Novel species of microfungi described in the present study include the following from Australia: Phytophthora amnicola from still water, Gnomoniopsis smithogilvyi from Castanea sp., Pseudoplagiostoma corymbiae from Corymbia sp., Diaporthe eucalyptorum from Eucalyptus sp., Sporisorium andrewmitchellii from Enneapogon aff. lindleyanus, Myrmecridium banksiae from Banksia, and Pilidiella wangiensis from Eucalyptus sp. Several species are also described from South Africa, namely: Gondwanamyces wingfieldii from Protea caffra, Montagnula aloes from Aloe sp., Diaporthe canthii from Canthium inerne, Phyllosticta ericarum from Erica gracilis, Coleophoma proteae from Protea caffra, Toxicocladosporium strelitziae from Strelitzia reginae, and Devriesia agapanthi from Agapanthus africanus. Other species include Phytophthora asparagi from Asparagus officinalis (USA), and Diaporthe passiflorae from Passiflora edulis (South America). Furthermore, novel genera of coelomycetes include Chrysocrypta corymbiae from Corymbia sp. (Australia), Trinosporium guianense, isolated as a contaminant (French Guiana), and Xenosonderhenia syzygii, from Syzygium cordatum (South Africa). Pseudopenidiella piceae from Picea abies (Czech Republic), and Phaeocercospora colophospermi from Colophospermum mopane (South Africa) represent novel genera of hyphomycetes. Morphological and culture characteristics along with ITS DNA barcodes are provided for all taxa.

A review of the Ustilago-Sporisorium-Macalpinomyces complex.

The fungal genera Ustilago, Sporisorium and Macalpinomyces represent an unresolved complex. Taxa within the complex often possess characters that occur in more than one genus, creating uncertainty for species placement. Previous studies have indicated that the genera cannot be separated based on morphology alone. Here we chronologically review the history of the Ustilago-Sporisorium-Macalpinomyces complex, argue for its resolution and suggest methods to accomplish a stable taxonomy. A combined molecular and morphological approach is required to identify synapomorphic characters that underpin a new classification. Ustilago, Sporisorium and Macalpinomyces require explicit re-description and new genera, based on monophyletic groups, are needed to accommodate taxa that no longer fit the emended descriptions. A resolved classification will end the taxonomic confusion that surrounds generic placement of these smut fungi.

Soral synapomorphies are significant for the systematics of the Ustilago-Sporisorium-Macalpinomyces complex (Ustilaginaceae).

The genera Ustilago, Sporisorium and Macalpinomyces are a polyphyletic complex of plant pathogenic fungi. The four main morphological characters used to define these genera have been considered homoplasious and not useful for resolving the complex. This study re-evaluates character homology and discusses the use of these characters for defining monophyletic groups recovered from a reconstructed phylogeny using four nuclear loci. Generic delimitation of smut fungi based on their hosts is also discussed as a means for identifying genera within this group. Morphological characters and host specificity can be used to circumscribe genera within the Ustilago-Sporisorium-Macalpinomyces complex.

Taxonomic revision of Ustilago, Sporisorium and Macalpinomyces.

Morphological characters within the Ustilago-Sporisorium-Macalpinomyces complex are defined explicitly. The genera Sporisorium and Anthracocystis are emended to reflect morphological synapomorphies. Three new genera, Langdonia, Stollia and Triodiomyces are described based on soral synapomorphies and host classification. The new classification of the Ustilago-Sporisorium-Macalpinomyces complex incorporates 142 new taxonomic combinations.

A Systematic Study Reveals that Xylella fastidiosa Strains from Pecan Are Part of X. fastidiosa subsp. multiplex.

Xylella fastidiosa causes disease in a number of economically important crops, ornamental plants, and shade trees, including grapevine, citrus, oleander, and sycamore. In pecan, X. fastidiosa causes pecan bacterial leaf scorch (PBLS), which leads to defoliation and reduces nut yield. No economically effective treatments are available for PBLS. In order to improve PBLS management practices, it is necessary to determine the subspecies of X. fastidiosa strains that infect pecan so that potential sources of inoculum may be identified. Multiprimer polymerase chain reaction (PCR) and phylogenetic analyses using nucleotide sequence data from the 16S-23S rRNA intergenic transcribed spacer (ITS) region and pglA consistently identified strains of X. fastidiosa isolated from pecan as X. fastidiosa subsp. multiplex. Enterobacterial repetitive intergenic consensus PCR and repetitive extragenic palindromic (REP)-PCR analyses were congruent with phylogenetic analyses. REP-PCR analyses indicated genetic variation within strains of X. fastidiosa from pecan. From these same analyses, X. fastidiosa strains from sycamore, grapevine, and oleander from Louisiana were identified as subsp. multiplex, subsp. fastidiosa, and subsp. sandyi, respectively. This study provides additional information about the host ranges of X. fastidiosa subspecies.

First Report of Uromyces plumbarius, Rust of Gaura, in Louisiana and a new host, Guara lindheimeri.

Gaura lindheimeri Engelm. & A. Gray (Onagraceae) is an ornamental shrub that is native to southern Louisiana and Texas. Its texture and form make it a popular perennial border plant. In April 2010 and 2011, three collections of Guara leaf samples with signs and symptoms of a rust disease were made from a home garden in Baton Rouge, LA. Infected leaves showed chlorotic lesions on the adaxial surface and were associated with scattered, hypophyllous uredinia. Urediniospores were globose to obovoid, echinulate, had two equatorial germ pores, and measured 16 to 21 × 18 to 25 µm with a wall 2 µm thick. Telia and teliospores were not observed on any of the collected samples. The pathogen was identified as Uromyces plumbarius Peck on the basis of the uredinial characters compared with four U.S. National Fungus (BPI 1103868, 0013551, 0013554, and 0013557) collections of U. plumbarius. The three collections from Louisiana have been deposited in the Bernard Lowy Mycological Herbarium. DNA was extracted from all three specimens and the nuclear ribosomal large subunit (28S) was amplified according to the protocol outlined by Aime (1). The three Louisiana collections had identical large subunit sequences (GenBank Accession Nos. JQ312670, JQ312671, and JQ312672). No sequences of U. plumbarius were available for comparison in GenBank; a BLAST search was 99% similar over 100% query coverage to Puccinia dioicae Magnus (Accession No. GU058019) and P. silvatica J. Schröt. (Accession No. AY222048). The uredinial/telial hosts of P. dioicae and P. silvatica are in the Cyperaceae, whereas U. plumbarius is an autoecious rust on Onagraceae. It is interesting to note that the aecial stage of P. dioicae occurs on Onagraceae and that it has a high sequence identity to U. plumbarius, supporting the hypothesis that these are correlated species (2). U. plumbarius has been recorded on several species of Gaura within the United States. To our knowledge, this is the first record of U. plumbarius in Louisiana and the first report of U. plumbarius on G. lindheimeri. References: (1) M. C. Aime. Mycoscience 47:112, 2006. (2) C. R. Orton. Mycologia 4:194, 1912.

Fungal Planet description sheets: 69-91.

Novel species of microfungi described in the present study include the following from Australia: Bagadiella victoriae and Bagadiella koalae on Eucalyptus spp., Catenulostroma eucalyptorum on Eucalyptus laevopinea, Cercospora eremochloae on Eremochloa bimaculata, Devriesia queenslandica on Scaevola taccada, Diaporthe musigena on Musa sp., Diaporthe acaciigena on Acacia retinodes, Leptoxyphium kurandae on Eucalyptus sp., Neofusicoccum grevilleae on Grevillea aurea, Phytophthora fluvialis from water in native bushland, Pseudocercospora cyathicola on Cyathea australis, and Teratosphaeria mareebensis on Eucalyptus sp. Other species include Passalora leptophlebiae on Eucalyptus leptophlebia (Brazil), Exophiala tremulae on Populus tremuloides and Dictyosporium stellatum from submerged wood (Canada), Mycosphaerella valgourgensis on Yucca sp. (France), Sclerostagonospora cycadis on Cycas revoluta (Japan), Rachicladosporium pini on Pinus monophylla (Netherlands), Mycosphaerella wachendorfiae on Wachendorfia thyrsifolia and Diaporthe rhusicola on Rhus pendulina (South Africa). Novel genera of hyphomycetes include Noosia banksiae on Banksia aemula (Australia), Utrechtiana cibiessia on Phragmites australis (Netherlands), and Funbolia dimorpha on blackened stem bark of an unidentified tree (USA). Morphological and culture characteristics along with ITS DNA barcodes are provided for all taxa.

Carbon isotopic fractionation associated with lipid biosynthesis by a cyanobacterium: relevance for interpretation of biomarker records.

For the cyanobacterium Synechocystis UTEX 2470, grown photoautotrophically to a logarithmic stage of growth, the total lipid extract is depleted in 13C by 4.8% relative to average biomass. Depletions observed for acetogenic (straight-chain) lipids range from 7.6 (hexadecanoic acid) to 9.9% (a C16 n-alkyl chain bound in a polar-lipid fraction), with a mass-weighted average of 9.1%. Polyisoprenoid lipids fall into two isotopic groups, with phytol, diplopterol, and diploptene depleted by 6.4-6.9% and bishomohopanol (produced from the extracts by the preparative degradation of bacteriohopanepolyol) depleted by 8.4%. Analysis of the pattern of depletions indicates that two carbon positions in each C5 biomonomer leading to polyisoprenoid products are probably depleted in 13C relative to average biomass. The depletion of bacteriohopanepolyol relative to other polyisoprenoids can be ascribed to changes that occur over the life of each cell: (1) the 13C content of carbon flowing to lipid biosynthesis decreases as the cell size increases and (2) a greater proportion of the bacteriohopanepolyol which, unlike other polyisoprenoids, is present mainly in the cytoplasm rather than in membranes and is synthesized when cells are larger. Chlorophyll a is depleted relative to average biomass by O.7%. Given the observed depletion of 13C in phytol, the heteroaromatic, chlorophyllide portion of chlorophyll must be enriched in 13C by 2.7%. This enrichment is large relative to that in chlorophyllides produced by eukaryotes and may be related to a parallel enrichment of 13C in cyanobacterial glutamic acid. As in many previous investigations of cyanobacterial lipids, long-chain n-alkanes (C22-C29) are found in the extracts. They are, however, enriched in 13C relative to biomass and have isotopic compositions suggesting that they are contaminants of petrochemical origin. Available results indicate that cyanobacterial lipids will be depleted relative to dissolved CO2 that has served as a carbon source by 22-30% and that a wider range of depletions will be characteristic of eukaryotic products. The absence of long-chain n-alkanes in cyanobacteria reduces the possibility that petroleum ever formed from pre-eukaryotic sedimentary debris.