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2 Life cycle of Rhodosporidium toruloides (Sporidiobolales). A. A transversely septate basidium arises from a teliospore and gives rise to spores. B. The spores bud and persist as yeasts. C. Yeast cells of the proper mating types fuse via a thin hyphal connection
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More than 8 % of all described Fungi belong to subphylum Pucciniomycotina, the basal lineage of Basidiomycota. Pucciniomycotina is well supported as monophyletic, as are eight of its nine classes, the exception being Agaricostilbomycetes. All members of the subphylum thus far studied have simple septal pores lacking dolipore swellings or septal por...
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... Cystobasidiomycetes species have diverse ecological roles, including in their roles as parasites, saprobes, and inhabitants of the phylloplane [53]. We isolated one unknown Cystobasidiomycetes species from two different lichen thalli (Candelaria concolor and one unidentified lichen species). ...
Lichens are symbiotic partnerships between a filamentous fungus and a photosymbiotic “alga”. Studies show that lichens harbor endothallic fungi, but that some taxa have been difficult to isolate from the main filamentous thallus-forming fungus and other faster growing lichenicolous/endothallic fungi. Therefore, we aimed to develop and evaluate liquid yeast-enrichment strategies to (1) isolate lichen-associated yeasts in pure culture, and (2) determine the taxonomic placement and breadth of the diversity of culturable yeasts. Eighty-two lichen samples were collected and washed with distilled water, and healthy thalli were ground up and added to seven different yeast-enrichment broths. Yeast colonies were isolated in pure culture and identified using molecular techniques. Initial isolates were identified using BLASTn analysis, and a taxonomic refinement was completed using PhyML analysis. In total, 215 isolates were obtained. The most prevalently isolated ascomycetous yeasts were within the Dothideomycetes (Aureobasidium, Plowrightia, and Dothiora), while the most frequently isolated basidiomycetous yeasts belonged to the genera Curvibasidium, Sporobolomyces, and Tremella. The generic placements could not be determined for 17 isolates, and in total 25 novel species were recovered. The results of this research indicate that (1) lichen-associated yeasts are diverse, (2) employing liquid enrichment strategies is effective for isolating many of these, and (3) lichen thalli represent a valuable untapped reservoir of diverse and novel yeast species.
... The global production of cereals is severely affected by rust diseases caused by a specialized group of fungi from the Pucciniales order 6 . This diverse and widely distributed group of plant pathogens with more than 7800 species may attack the most frequently sown cereals in the world including oat 7 . Stem rust caused by Puccinia graminis Pers. ...
A reliable qPCR experiment requires the selection of reference genes with a stable level of expression in a given experimental system. This study attempts to determine the reference genes (RGs) for the A. sativa–P. graminis experimental setup. We evaluated nine candidate reference genes in A. sativa (oat line Pg4 and the cultivar Kasztan) during compatible and incompatible interactions with different pathotypes of Puccinia graminis f. sp. avenae in six time points post-inoculation. The identification of genes with high expression stability was performed by four algorithms (geNorm, NormFinder, BestKeeper and ΔCt method). We found that the most appropriate combination of RGs for RT-qPCR data normalization were HNR (heterogeneous nuclear ribonucleoprotein 27C) + EF1A (elongation factor 1-alpha) + EIF4A (eukaryotic initiation factor 4A-3). The worst candidates for normalization in this dataset were CYP (cyclophilin) and TUA (alpha tubulin). Identified reference genes are suitable candidates for the standardization of gene expression studies in the A. sativa–P. graminis interaction system and potentially other related pathogens. To date, this is the first report of RGs selection in this pathosystem.
... This tendency is also observed in the entire subphylum Pucciniomycotina, to which Pucciniales belong, and in the subphylum Ustilaginomycotina, which exhibits at the contrary compact genomes with a reduced number of genes Kamper et al. 2006;Ullmann et al. 2022). Such a global reduction observed in Pucciniales and in some Basidiomycota subphyla likely reflects a specialization in their trophic modes, e.g., towards biotrophy, or adaptation to specific ecological niches (Aime et al. 2014;Spatafora et al. 2017). This transportome reduction in rust fungi is mostly due to contractions of transporter families falling in the class 2 (electrochemical potential-driven transporters) and class 4 (translocators), which altogether accounts for 45% of all rust transporters. ...
Nutrients acquisition by rust fungi during their biotrophic growth has been assigned to a few transporters expressed in haustorial infection structures. We performed a comparative genomic analysis of all transporter genes (hereafter termed transportome) classified according to the Transporter Classification Database (TCDB) focusing specifically on rust fungi (order Pucciniales) versus other species in the Dikarya. We also surveyed expression of transporter genes in the poplar rust fungus for which transcriptomics data are available across the whole life cycle. Despite a significant increase in gene number, rust fungi presented a reduced transportome compared to a vast majority of fungi in the Dikarya. However, a few transporter families in the subclass Porters showed significant expansions. Noteworthy, three metal transport-related families involved in the import, export and sequestration of metals were expanded in Pucciniales and expressed at various stages of the rust life cycle suggesting a tight regulation of metal homeostasis. The most remarkable gene expansion in the Pucciniales was observed for the oligopeptide transporter (OPT) family with 25 genes in average compared to seven to 14 genes in the other surveyed taxonomical ranks. A phylogenetic analysis showed several specific expansion events at the root of the order Pucciniales with subsequent expansions in rust taxonomical families. The OPT genes showed dynamic expression patterns along the rust life cycle and more particularly during infection of the poplar host tree, suggesting a possible specialization for the acquisition of nitrogen and sulfur through the transport of oligopeptides from the host during biotrophic growth.
... Obligate parasitic plant fungi are a large group among which rust and powdery mildew are the two largest groups. Rust fungi represent one of the most important fungal orders, consisting of more than 8,000 known species (Aime et al., 2014;Lorrain et al., 2019). These fascinating parasites attack a wide range of plants and cause severe damage . ...
Biotrophic plant pathogenic fungi are widely distributed and are among the most damaging pathogenic organisms of agriculturally important crops responsible for significant losses in quality and yield. However, the pathogenesis of obligate parasitic pathogenic microorganisms is still under investigation because they cannot reproduce and complete their life cycle on an artificial medium. The successful lifestyle of biotrophic fungal pathogens depends on their ability to secrete effector proteins to manipulate or evade plant defense response. By integrating genomics, transcriptomics, and effectoromics, insights into how the adaptation of biotrophic plant fungal pathogens adapt to their host populations can be gained. Efficient tools to decipher the precise molecular mechanisms of rust-plant interactions, and standardized routines in genomics and functional pipelines have been established and will pave the way for comparative studies. Deciphering fungal pathogenesis not only allows us to better understand how fungal pathogens infect host plants but also provides valuable information for plant diseases control, including new strategies to prevent, delay, or inhibit fungal development. Our review provides a comprehensive overview of the efforts that have been made to decipher the effector proteins of biotrophic fungal pathogens and demonstrates how rapidly research in the field of obligate biotrophy has progressed.
... Crop diseases caused by rust fungi, which are broadly distributed and varied with more than 7800 species worldwide, are responsible for major economic loss and environmental harm [3,17]. The main impacts on wheat production arise from attack by three types of rust, i.e., leaf (or brown) rust caused by Puccinia recondita Rob. ...
Rusts are a group of major diseases that have an adverse effect on crop production. Those targeting wheat are found in three principal forms: leaf, stripe, and stem rust. Leaf rust causes foliar disease in wheat; in Egypt, this causes a significant annual yield loss. The deployment of resistant genotypes has proved to be a relatively economical and environmentally sustainable method of controlling the disease. Gene pyramiding can be performed using traditional breeding techniques. Additionally, pathotypes can be introduced to examine specific leaf rust genes, or the breeder may conduct more complex breeding methods. Indirect selection via DNA markers linked to resistance genes may facilitate the transfer of targeted genes, either individually or in combination, even in a disease-free environment. The use of selective crosses to counter virulent races of leaf, stripe, and stem rust has resulted in the transfer of several resistance genes into new wheat germplasm from cultivated or wild species. Quantitative trait locus (QTL) technology has been adopted in a wide variety of novel approaches and is becoming increasingly recognized in wheat breeding. Moreover, several researchers have reported the transference of leaf and stripe rust resistance genes into susceptible wheat cultivars.
... Traditional multilocus studies have generally found weak support for various groupings of these clades (Swann and Taylor 1993;Berres et al. 1995;Aime et al. 2006;James et al. 2006;Hibbett et al. 2007;Matheny et al. 2007), whereas genome-scale studies have provided often strongly supported but conflicting relationships. In most previous studies, smuts and mushroom-forming fungi grouped together to the exclusion of rusts (referred to as R(S,M) topology hereafter) (Padamsee et al. 2012;Ebersberger et al. 2012;Zajc et al. 2013;Toome et al. 2014;Kohler et al. 2015;Sharma et al. 2015, Zhao et al. 2017, although rusts as the sister group of smuts (hereafter: M(R,S) topology) (Kohler et al. 2015) and rusts as the sister group of mushroom-forming fungi (hereafter: S(R,M) topology) (Medina et al. 2011;Nagy et al. 2014;Riley et al. 2014) have also been reported. Furthermore, analyses of the same data sets under different models or methods have yielded contradicting results (Kohler et al. 2015), suggestive of evolutionary processes not captured by the models or methods used. ...
... Biased taxon sampling can compromise phylogenomic inference (Dunn et al. 2008;Philippe et al. 2011;Simon et al. 2012;Pisani et al. 2015) and has been suggested as a potential factor underlying the difficulty of resolving basal Basidiomycota relationships (Nagy et al. 2016). Notably, members of both the rust and smut lineages have experienced massive gene losses compared to mushroom-forming fungi and Ascomycota Toome et al. 2014;Kijpornyongpan et al. 2018), which may impact the number of genes available for phylogenetic inference and thus the reconstructed relationships. It has also been suggested that basal relationships of the Basidiomycota might have been shaped by fast successive diversification events and thus be better described as a hard polytomy (Kohler et al. 2015). ...
... We used complete genome sequences of 67 species, representing the three subphyla of Basidiomycota plus 10 representatives of the Ascomycota and three representatives of Mucoromycota as outgroups (see Supplementary Table S1 available on Dryad at doi:10.5061/dryad.g0db883). The Basidiomycota included 54 species: 32 mushroom-forming fungi (Agaricomycotina, including representatives of the earliest-diverging lineage, Wallemiomycetes, fide Padamsee et al. 2012 andDentinger et al. 2016), 12 species from 9 orders from across the rust lineage (Pucciniomycotina, selected fide Aime et al. 2014) and 10 species from 6 orders across the smut lineage (Ustilaginomycotina, selected fide Kijpornyongpan et al. 2018). We performed all-versus-all BLAST on nonredundant predicted protein sequences in the 67 input genomes using mpiblast 1.6.0 ...
Resolving deep divergences in the tree of life is challenging even for analyses of genome-scale phylogenetic data sets. Relationships between Basidiomycota subphyla, the rusts and allies (Pucciniomycotina), smuts and allies (Ustilaginomycotina), and mushroom-forming fungi and allies (Agaricomycotina) were found particularly recalcitrant both to traditional multigene and genome-scale phylogenetics. Here, we address basal Basidiomycota relationships using concatenated and gene tree-based analyses of various phylogenomic data sets to examine the contribution of several potential sources of bias. We evaluate the contribution of biological causes (hard polytomy, incomplete lineage sorting) versus unmodeled evolutionary processes and factors that exacerbate their effects (e.g., fast-evolving sites and long-branch taxa) to inferences of basal Basidiomycota relationships. Bayesian Markov Chain Monte Carlo and likelihood mapping analyses reject the hard polytomy with confidence. In concatenated analyses, fast-evolving sites and oversimplified models of amino acid substitution favored the grouping of smuts with mushroom-forming fungi, often leading to maximal bootstrap support in both concatenation and coalescent analyses. On the contrary, the most conserved data subsets grouped rusts and allies with mushroom-forming fungi, although this relationship proved labile, sensitive to model choice, to different data subsets and to missing data. Excluding putative long-branch taxa, genes with high proportions of missing data and/or with strong signal failed to reveal a consistent trend toward one or the other topology, suggesting that additional sources of conflict are at play. While concatenated analyses yielded strong but conflicting support, individual gene trees mostly provided poor support for any resolution of rusts, smuts, and mushroom-forming fungi, suggesting that the true Basidiomycota tree might be in a part of tree space that is difficult to access using both concatenation and gene tree-based approaches. Inference-based assessments of absolute model fit strongly reject best-fit models for the vast majority of genes, indicating a poor fit of even the most commonly used models. While this is consistent with previous assessments of site-homogenous models of amino acid evolution, this does not appear to be the sole source of confounding signal. Our analyses suggest that topologies uniting smuts with mushroom-forming fungi can arise as a result of inappropriate modeling of amino acid sites that might be prone to systematic bias. We speculate that improved models of sequence evolution could shed more light on basal splits in the Basidiomycota, which, for now, remain unresolved despite the use of whole genome data.
... Septal pores are simple, without dolipores. The cell wall contains mannose, but lacks xylose (Aime, Toome, & McLaughlin, 2014). Pucciniomycotina is generally considered the earliest-splitting lineage within the Basidiomycota, and consistent with this view they share some characteristics in their cell division and spindle-pole-body formation with the Ascomycota. ...
The fungal kingdom comprises a hyperdiverse clade of heterotrophic eukaryotes characterized by the presence of a chitinous cell wall, the loss of phagotrophic capabilities and cell organizations that range from completely unicellular monopolar organisms to highly complex syncitial filaments that may form macroscopic structures. Fungi emerged as a ‘Third Kingdom’, embracing organisms that were outside the classical dichotomy of animals versus vegetals. The taxonomy of this group has a turbulent history that is only now starting to be settled with the advent of genomics and phylogenomics. We here review the current status of the phylogeny and taxonomy of fungi, providing an overview of the main defined groups. Based on current knowledge, nine phylum‐level clades can be defined: Opisthosporidia, Chytridiomycota, Neocallimastigomycota, Blastocladiomycota, Zoopagomycota, Mucoromycota, Glomeromycota, Basidiomycota and Ascomycota. For each group, we discuss their main traits and their diversity, focusing on the evolutionary relationships among the main fungal clades. We also explore the diversity and phylogeny of several groups of uncertain affinities and the main phylogenetic and taxonomical controversies and hypotheses in the field.
... Parasitic Agaricomycetes usually infect the fruiting bodies of other fungi, although species infecting hyphae or conidia are also known (Tzean & Estey, 1978;Jeffries, 1995). Mycoparasitism is widespread within Pucciniomycotina, where it seems to be an ancestral lifestyle (Aime, Toome & McLaughlin, 2014;Wang et al., 2015b;Oberwinkler, 2017) (Fig. 3). Finally, the best-studied groups of mycoparasites lie within the Pezizomycotina, with representatives within the Sordariomycetes (Goh & Vujanovic, 2010;Vujanovic & Kim, 2017) and particularly in the Hypocreales (Inglis & Kawchuk, 2002;Atanasova et al., 2013;Quandt, Bushley & Spatafora, 2015), Dothideomycetes, Eurotiomycetes and Orbiliomycetes (Tzean & Estey, 1976;Jeffries, 1995), as well as in the genera Pyxidiophora (Laboulbeniomycetes) (Blackwell, 1994;Kirschner, 2003;Goldmann & Weir, 2018) and Teratosperma (Pezizomycotina incertae sedis) (Parfitt, Coley-Smith & Jeves, 1983) (Fig. 3). ...
... Basidiomycetous yeasts can be found within the Pucciniomycotina and the Ustilaginomycotina. Pucciniomycotina forms the most diverse of these yeast lineages, with the yeast lifestyle evolving independently in at least four lineages (Microbotryomycetes, Spiculogloeomycetes, Agaricostylbomycetes and Cystobasidiomycetes) (Aime, Toome & McLaughlin, 2014;Wang et al., 2015b ;Oberwinkler, 2017). Many of these lineages include dimorphic fungi that can be cultured as unicellular fungi, a trait that appears additionally in the Mixiomycetes and the Cryptomycocolacomycetes, considered as yeasts by some authors. ...
... Red yeasts are in need of taxonomic revision, with some important genera (e.g. Rhodotorula) being clearly paraphyletic (Aime, Toome & McLaughlin, 2014;Oberwinkler, 2017). The genomes of several red yeasts are available. ...
Fungi are a highly diverse group of heterotrophic eukaryotes characterized by the absence of phagotrophy and the presence of a chitinous cell wall. While unicellular fungi are far from rare, part of the evolutionary success of the group resides in their ability to grow indefinitely as a cylindrical multinucleated cell (hypha). Armed with these morphological traits and with an extremely high metabolical diversity, fungi have conquered numerous ecological niches and have shaped a whole world of interactions with other living organisms. Herein we survey the main evolutionary and ecological processes that have guided fungal diversity. We will first review the ecology and evolution of the zoosporic lineages and the process of terrestrialization, as one of the major evolutionary transitions in this kingdom. Several plausible scenarios have been proposed for fungal terrestralization and we here propose a new scenario, which considers icy environments as a transitory niche between water and emerged land. We then focus on exploring the main ecological relationships of Fungi with other organisms (other fungi, protozoans, animals and plants), as well as the origin of adaptations to certain specialized ecological niches within the group (lichens, black fungi and yeasts). Throughout this review we use an evolutionary and comparative‐genomics perspective to understand fungal ecological diversity. Finally, we highlight the importance of genome‐enabled inferences to envision plausible narratives and scenarios for important transitions.
... The Pucciniales (rust fungi) represent one of the largest fungal orders, with > 8000 species already described (Aime et al., 2014). These intriguing parasites have the ability to infect a wide variety of host plants, from ferns to monocots and gymnosperms to angiosperms, which suggests an ancestral adaptation to the biotrophic lifestyle (Aime et al., 2014). ...
... The Pucciniales (rust fungi) represent one of the largest fungal orders, with > 8000 species already described (Aime et al., 2014). These intriguing parasites have the ability to infect a wide variety of host plants, from ferns to monocots and gymnosperms to angiosperms, which suggests an ancestral adaptation to the biotrophic lifestyle (Aime et al., 2014). Worldwide, rust fungi are considered among the most serious threats to both agricultural crops (e.g. ...
... Fig. 1). In early autumn, uredinia differentiate into telia, which go through an overwintering period during which karyogamy will occur, giving rise to diploid dormant teliospores (examples of typical heteroecious cycles can be found in Hacquard et al. (2011) and Aime et al. (2014)). ...
Rust fungi (Pucciniales) are the largest group of plant pathogens and represent one of the most devastating threats to agricultural crops worldwide. Despite the economic importance of these highly specialized pathogens, many aspects of their biology remain obscure, largely because rust fungi are obligate biotrophs. The rise of genomics and advances in high‐throughput sequencing technology have presented new options for identifying candidate effector genes involved in pathogenicity mechanisms of rust fungi. Transcriptome analysis and integrated bioinformatics tools have led to the identification of key genetic determinants of host susceptibility to infection by rusts. Thousands of genes encoding secreted proteins highly expressed during host infection have been reported for different rust species, which represents significant potential towards understanding rust effector function. Recent high‐throughput in planta expression screen approaches (effectoromics) have pushed the field ahead even further towards predicting high‐priority effectors and identifying avirulence genes. These new insights into rust effector biology promise to inform future research and spur the development of effective and sustainable strategies for managing rust diseases.
... Pathogenic members of these orders, in contrast to 40 the majority of smut fungi that infect herbaceous hosts, are specific to woody perennial plants (Begerow et al. 2014). Teliospores are also present in other fungal groups, such as in rust fungi (Pucciniomycetes, Pucciniomycotina), anther smut fungi and relatives (Microbotryomycetes,45 Pucciniomycotina) and root gall-forming fungi (Entorrhizomycetes, Entorrhizomycota) (Aime et al. 2014;Bauer et al. 2015)-some members of which can infect both woody and herbaceous plants. Teliospores in these non-Ustilaginomycotina fungi are functionally equivalent to 50 those produced in the smut fungi as they give rise to basidia, which subsequently undergo meiosis to produce haploid basidiospores. ...
Ustilaginomycotina is home to a broad array of fungi including important plant pathogens collectively called smut fungi. Smuts are biotrophs that produce characteristic perennating propagules called teliospores, one of which, Ustilago maydis, is a model genetic organism. Broad exploration of smut biology has been hampered by limited phylogenetic resolution of Ustilaginiomycotina as well as an overall lack of genomic data for members of this subphylum. In this study, we sequenced eight Ustilaginomycotina genomes from previously unrepresented lineages, deciphered ordinal-level phylogenetic relationships for the subphylum, and performed comparative analyses. Unlike other Basidiomycota subphyla, all sampled Ustilaginomycotina genomes are relatively small and compact. Ancestral state reconstruction analyses indicate that teliospore formation was present at the origin of the subphylum. Divergence time estimation dates the divergence of most extant smut fungi after that of grasses (Poaceae). However, we found limited conservation of well-characterized genes related to smut pathogenesis from U. maydis, indicating dissimilar pathogenic mechanisms exist across other smut lineages. The genomes of Malasseziomycetes are highly diverged from the other sampled Ustilaginomycotina, likely due to their unique history as mammal-associated lipophilic yeasts. Despite the extensive genomic data, the phylogenetic placement of this class remains ambiguous. Although the sampled Ustilaginomycotina members lack many core enzymes for plant cell wall decomposition and starch catabolism, we identified several novel carbohydrate active enzymes potentially related to pectin breakdown. Finally, about 50% of Ustilaginomycotina species-specific genes are present in previously undersampled and rare lineages, highlighting the importance of exploring fungal diversity as a resource for novel gene discovery.
