Transcriptional Divergence Underpinning Sexual Development in the Fungal Class Sordariomycetes

Kim

et al. 2023

Front. Fungal Biol.

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Advances in genomics and transcriptomics accompanying the rapid accumulation of omics data have provided new tools that have transformed and expanded the traditional concepts of model fungi. Evolutionary genomics and transcriptomics have flourished with the use of classical and newer fungal models that facilitate the study of diverse topics encompassing fungal biology and development. Technological advances have also created the opportunity to obtain and mine large datasets. One such continuously growing dataset is that of the Sordariomycetes, which exhibit a richness of species, ecological diversity, economic importance, and a profound research history on amenable models. Currently, 3,574 species of this class have been sequenced, comprising nearly one-third of the available ascomycete genomes. Among these genomes, multiple representatives of the model genera Fusarium, Neurospora, and Trichoderma are present. In this review, we examine recently published studies and data on the Sordariomycetes that have contributed novel insights to the field of fungal evolution via integrative analyses of the genetic, pathogenic, and other biological characteristics of the fungi. Some of these studies applied ancestral state analysis of gene expression among divergent lineages to infer regulatory network models, identify key genetic elements in fungal sexual development, and investigate the regulation of conidial germination and secondary metabolism. Such multispecies investigations address challenges in the study of fungal evolutionary genomics derived from studies that are often based on limited model genomes and that primarily focus on the aspects of biology driven by knowledge drawn from a few model species. Rapidly accumulating information and expanding capabilities for systems biological analysis of Big Data are setting the stage for the expansion of the concept of model systems from unitary taxonomic species/genera to inclusive clusters of well-studied models that can facilitate both the in-depth study of specific lineages and also investigation of trait diversity across lineages. The Sordariomycetes class, in particular, offers abundant omics data and a large and active global research community. As such, the Sordariomycetes can form a core omics clade, providing a blueprint for the expansion of our knowledge of evolution at the genomic scale in the exciting era of Big Data and artificial intelligence, and serving as a reference for the future analysis of different taxonomic levels within the fungal kingdom.

Section: The Need For the Evolutionary Integration Of Multiple Modelsmentioning

confidence: 99%

Section: New Details and New Omics Data On The Sordariomycetes Contin...mentioning

confidence: 99%

The Sordariomycetes: an expanding resource with Big Data for mining in evolutionary genomics and transcriptomics

Kim

et al. 2023

Front. Fungal Biol.

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“…Most importantly, F. graminearum does not form appressoria and utilizes distinct strategies to penetrate the epidermal cells of the host plants. Both F. graminearum and M. oryzae belong to the Sordariomycetes but fall into different orders, Hypocreales and Magnaporthales, respectively ( 64 ). RNA-seq analyses indicated significant divergence in gene expression including autophagy-related genes during conidial germination and infection processes between F. graminearum and M. oryzae ( 61 ).…”

Section: Discussionmentioning

confidence: 99%

Phylogenetic and functional analyses of N ⁶ -methyladenosine RNA methylation factors in the wheat scab fungus Fusarium graminearum

Kim,

Hu,

Kang

et al. 2024

mSphere

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In eukaryotes, N 6 -methyladenosine (m 6 A) RNA modification plays a crucial role in governing the fate of RNA molecules and has been linked to various developmental processes. However, the phyletic distribution and functions of genetic factors responsible for m 6 A modification remain largely unexplored in fungi. To get insights into the evolution of m 6 A machineries, we reconstructed global phylogenies of potential m 6 A writers, readers, and erasers in fungi. Substantial copy number variations were observed, ranging from up to five m 6 A writers in early-diverging fungi to a single copy in the subphylum Pezizomycotina, which primarily comprises filamentous fungi. To characterize m 6 A factors in a phytopathogenic fungus Fusarium graminearum , we generated knockout mutants lacking potential m 6 A factors including the sole m 6 A writer MTA1 . However, the resulting knockouts did not exhibit any noticeable phenotypic changes during vegetative and sexual growth stages. As obtaining a homozygous knockout lacking MTA1 was likely hindered by its essential role, we generated MTA1 -overexpressing strains ( MTA1 -OE). The MTA1 -OE5 strain showed delayed conidial germination and reduced hyphal branching, suggesting its involvement during vegetative growth. Consistent with these findings, the expression levels of MTA1 and a potential m 6 A reader YTH1 were dramatically induced in germinating conidia, followed by the expression of potential m 6 A erasers at later vegetative stages. Several genes including transcription factors, transporters, and various enzymes were found to be significantly upregulated and downregulated in the MTA1 -OE5 strain. Overall, our study highlights the functional importance of the m 6 A methylation during conidial germination in F. graminearum and provides a foundation for future investigations into m 6 A modification sites in filamentous fungi. IMPORTANCE N 6 -methyladenosine (m 6 A) RNA methylation is a reversible posttranscriptional modification that regulates RNA function and plays a crucial role in diverse developmental processes. This study addresses the knowledge gap regarding phyletic distribution and functions of m 6 A factors in fungi. The identification of copy number variations among fungal groups enriches our knowledge regarding the evolution of m 6 A machinery in fungi. Functional characterization of m 6 A factors in a phytopathogenic filamentous fungus Fusarium graminearum provides insights into the essential role of the m 6 A writer MTA1 in conidial germination and hyphal branching. The observed effects of overexpressing MTA1 on fungal growth and gene expression patterns of m 6 A factors throughout the life cycle of F. graminearum further underscore the importance of m 6 A modification in conidial germination. Overall, this study significantly advances our understanding of m 6 A modification in fungi, paving the way for future research into its roles in filamentous growth and potential applications in disease control.

“…and BcPKS13 (related to the PKS15 family), are developmentally-regulated and responsible for melanization of sclerotia and conidia, respectively [58]. Tissue-specific regulations of different pigment systems are also observed in perithecial wall pigments in Fusarium species [77,78]. The role of the PKS13 and PKS15 NR-PKS families in lichens are currently unknown, however it may have evolved to have tissue-specific roles during the life cycle of lichens.…”

Section: Discussionmentioning

confidence: 99%

Identification of a biosynthetic gene cluster for a red pigment cristazarin produced by a lichen-forming fungus Cladonia metacorallifera

et al. 2023

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Lichens are known to produce many novel bioactive metabolites. To date, approximately 1,000 secondary metabolites have been discovered, which are predominantly produced by the lichen mycobionts. However, despite the extensive studies on production of lichen secondary metabolites, little is known about the responsible biosynthetic gene clusters (BGCs). Here, we identified a putative BGC that is implicated in production of a red pigment, cristazarin (a naphthazarin derivative), in Cladonia metacorallifera. Previously, cristazarin was shown to be specifically induced in growth media containing fructose as a sole carbon source. Thus, we performed transcriptome analysis of C. metacorallifera growing on different carbon sources including fructose to identify the BGC for cristazarin. Among 39 polyketide synthase (PKS) genes found in the genome of C. metacorallifera, a non-reducing PKS (coined crz7) was highly expressed in growth media containing either fructose or glucose. The borders of a cristazarin gene cluster were delimited by co-expression patterns of neighboring genes of the crz7. BGCs highly conserved to the cristazarin BGC were also found in C. borealis and C. macilenta, indicating that these related species also have metabolic potentials to produce cristazarin. Phylogenetic analysis revealed that the Crz7 is sister to fungal PKSs that biosynthesize an acetylated tetrahydoxynaphthalene as a precursor of melanin pigment. Based on the phylogenetic placement of the Crz7 and putative functions of its neighboring genes, we proposed a plausible biosynthetic route for cristazarin. In this study, we identified a lichen-specific BGC that is likely involved in the biosynthesis of a naphthazarin derivative, cristazarin, and confirmed that transcriptome profiling under inducing and non-inducing conditions is an effective strategy for linking metabolites of interest to biosynthetic genes.