Dataset Information

Transcription Factors in Fungi: TFome Dynamics, Three Major Families, and Dual-Specificity TFs.

ABSTRACT: Transcription factors (TFs) are essential regulators of gene expression in a cell; the entire repertoire of TFs (TFome) of a species reflects its regulatory potential and the evolutionary history of the regulatory mechanisms. In this work, I give an overview of fungal TFs, analyze TFome dynamics, and discuss TF families and types of particular interest. Whole-genome annotation of TFs in more than 200 fungal species revealed ~80 families of TFs that are typically found in fungi. Almost half of the considered genomes belonged to basidiomycetes and zygomycetes, which have been underrepresented in earlier annotations due to dearth of sequenced genomes. The TFomes were analyzed in terms of expansion strategies genome- and lineage-wise. Generally, TFomes are known to correlate with genome size; but what happens to particular families when a TFome is expanding? By dissecting TFomes into single families and estimating the impact of each of them, I show that in fungi the TFome increment is largely limited to three families (C6 Zn clusters, C2H2-like Zn fingers, and homeodomain-like). To see whether this is a fungal peculiarity or a ubiquitous eukaryotic feature, I also analyzed metazoan TFomes, where I observed a similar trend (limited number of TFome-shaping families) but also some important differences connected mostly with the increased complexity in animals. The expansion strategies of TF families are lineage-specific; I demonstrate how the patterns of the TF families' distributions, designated as "TF signatures," can be used as a taxonomic feature, e.g., for allocation of uncertain phyla. In addition, both fungal and metazoan genomes contain an intriguing type of TFs. While usually TFs have a single DNA-binding domain, these TFs possess two (or more) different DNA-binding specificities. I demonstrate that dual-specific TFs comprising various combinations of all major TF families are a typical feature of fungal and animal genomes and have an interesting evolutionary history involving gene duplications and domain losses.

SUBMITTER: Shelest E

PROVIDER: S-EPMC5415576 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Publications

Transcription Factors in Fungi: TFome Dynamics, Three Major Families, and Dual-Specificity TFs.

Shelest Ekaterina E

Frontiers in genetics 20170504

Transcription factors (TFs) are essential regulators of gene expression in a cell; the entire repertoire of TFs (TFome) of a species reflects its regulatory potential and the evolutionary history of the regulatory mechanisms. In this work, I give an overview of fungal TFs, analyze TFome dynamics, and discuss TF families and types of particular interest. Whole-genome annotation of TFs in more than 200 fungal species revealed ~80 families of TFs that are typically found in fungi. Almost half of th ...[more]

PMID: 28523015

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Project description:Historical mass extinction events had major impacts on biodiversity patterns. The most recent and intensively studied event is the Cretaceous - Paleogene (K-Pg) boundary (ca. 66 million years ago [MYA]). However, the factors that may have impacted diversification dynamics vary across lineages. We investigated the macroevolutionary dynamics with a specific focus on the impact of major historical events such as the K-Pg mass extinction event on two major subclasses - Lecanoromycetidae and Ostropomycetidae - of lichen-forming fungi and tested whether variation in the rate of diversification can be associated with the evolution of a specific trait state - macrolichen. Our results reveal accelerated diversification events in three families of morphologically complex lichen-forming fungi - Cladoniaceae, Parmeliaceae, and Peltigeraceae - which are from the subclass Lecanoromycetidae and mostly composed of macrolichens, those that form three dimensional structures. Our RTT plot result for the subclass Lecanoromycetidae also reveals accelerated diversification. Changes in diversification rates occurred around the transition between Mesozoic and Cenozoic eras and was likely related to the K-Pg mass extinction event. The phylogenetic positions for rate increases estimated based on marginal shift probability are, however, scattered from 100 to 40 MYA preventing us from making explicit inference. Although we reveal that the phenotypic state of macrolichens is associated with a higher diversification rate than microlichens, we also show that the evolution of macrolichens predated the K-Pg event. Furthermore, the association between macrolichens and increased diversification is not universal and can be explained, in part, by phylogenetic relatedness. By investigating the macroevolutionary dynamics of lichen-forming fungi our study provides a new empirical system suitable to test the effect of major historical event on shaping biodiversity patterns and to investigate why changes in biodiversity patterns are not in concordance across clades. Our results imply that multiple historical events during the transition from Mesozoic to Cenozoic eras, including the K-Pg mass extinction event, impacted the evolutionary dynamics in lichen-forming fungi. However, future studies focusing on individual lichen-forming fungal families are required to ascertain whether diversification rates are associated with growth form and certain geological events.

Project description:BackgroundTetraspanins are small membrane proteins that belong to a superfamily encompassing 33 members in human and mouse. These proteins act as organizers of membrane-signalling complexes. So far only two tetraspanin families have been identified in fungi. These are Pls1, which is required for pathogenicity of the plant pathogenic ascomycetes, Magnaporthe grisea, Botrytis cinerea and Colletotrichum lindemuthianum, and Tsp2, whose function is unknown. In this report, we describe a third family of tetraspanins (Tsp3) and a new family of tetraspanin-like proteins (Tpl1) in fungi. We also describe expression of some of these genes in M. grisea and a basidiomycete, Laccaria bicolor, and also their functional analysis in M. grisea.ResultsThe exhaustive search for tetraspanins in fungal genomes reveals that higher fungi (basidiomycetes and ascomycetes) contain three families of tetraspanins (Pls1, Tsp2 and Tsp3) with different distribution amongst phyla. Pls1 is found in ascomycetes and basidiomycetes, whereas Tsp2 is restricted to basidiomycetes and Tsp3 to ascomycetes. A unique copy of each of PLS1 and TSP3 was found in ascomycetes in contrast to TSP2, which has several paralogs in the basidiomycetes, Coprinus cinereus and Laccaria bicolor. A tetraspanin-like family (Tpl1) was also identified in ascomycetes. Transcriptional analyses in various tissues of L. bicolor and M. grisea showed that PLS1 and TSP2 are expressed in all tissues in L. bicolor and that TSP3 and TPL1 are overexpressed in the sexual fruiting bodies (perithecia) and mycelia of M. grisea, suggesting that these genes are not pseudogenes. Phenotypic analysis of gene replacementmutants Deltatsp3 and Deltatpl1 of M. grisea revealed a reduction of the pathogenicity only on rice, in contrast to Deltapls1 mutants, which are completely non-pathogenic on barley and rice.ConclusionA new tetraspanin family (Tsp3) and a tetraspanin-like protein family (Tpl1) have been identified in fungi. Functional analysis by gene replacement showed that these proteins, as well as Pls1, are involved in the infection process of the plant pathogenic fungus M. grisea. The next challenge will be to decipher the role(s) of tetraspanins in a range of symbiotic, saprophytic and human pathogenic fungi.

Dataset Information

Transcription Factors in Fungi: TFome Dynamics, Three Major Families, and Dual-Specificity TFs.

Publications

Transcription Factors in Fungi: TFome Dynamics, Three Major Families, and Dual-Specificity TFs.

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