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Abstract The phenotype of an organism is shaped by gene expression within developing tissues. This shaping relates the evolution of gene expression to phenotypic evolution, through divergence in gene expression and consequent phenotype. Rates of phenotypic evolution receive extensive attention. However, the degree to which divergence in the phenotype of gene expression is subject to heterogeneous rates of evolution across developmental stages has not previously been assessed. Here, we analyzed the evolution of the expression of single-copy orthologs within 9 species of Sordariomycetes Fungi, across 9 developmental stages within asexual spore germination and sexual reproduction. Rates of gene expression evolution exhibited high variation both within and among developmental stages. Furthermore, rates of gene expression evolution were correlated with nonsynonymous to synonymous substitution rates (dN/dS), suggesting that gene sequence evolution and expression evolution are indirectly or directly driven by common evolutionary forces. Functional pathway analyses demonstrate that rates of gene expression evolution are higher in labile pathways such as carbon metabolism, and lower in conserved pathways such as those involved in cell cycle and molecular signaling. Lastly, the expression of genes in the meiosis pathway evolved at a slower rate only across the stages where meiosis took place, suggesting that stage-specific low rates of expression evolution implicate high relevance of the genes to developmental operations occurring between those stages. 

Abstract The origin of new genes has long been a central interest of evolutionary biologists. However, their novelty means that they evade reconstruction by the classical tools of evolutionary modelling. This evasion of deep ancestral investigation necessitates intensive study of model species within well‐sampled, recently diversified, clades. One such clade is the model genusNeurospora, members of which lack recent gene duplications. SeveralNeurosporaspecies are comprehensively characterized organisms apt for studying the evolution of lineage‐specific genes (LSGs). Using gene synteny, we documented that 78% ofNeurosporaLSG clusters are located adjacent to the telomeres featuring extensive tracts of non‐coding DNA and duplicated genes. Here, we report several instances of LSGs that are likely from regional rearrangements and potentially from gene rebirth. To broadly investigate the functions of LSGs, we assembled transcriptomics data from 68 experimental data points and identified co‐regulatory modules using Weighted Gene Correlation Network Analysis, revealing that LSGs are widely but peripherally involved in known regulatory machinery for diverse functions. The ancestral status of the LSGmas‐1, a gene with roles in cell‐wall integrity and cellular sensitivity to antifungal toxins, was investigated in detail alongside its genomic neighbours, indicating that it arose from an ancient lysophospholipase precursor that is ubiquitous in lineages of the Sordariomycetes. Our discoveries illuminate a “rummage region” in theN. crassagenome that enables the formation of new genes and functions to arise via gene duplication and relocation, followed by fast mutation and recombination facilitated by sequence repeats and unconstrained non‐coding sequences. 

In opportunistic human pathogenic fungi, changes in gene expression play a crucial role in the progression of growth stages from early spore germination through host infection. Comparative transcriptomics between diverse fungal pathogens and non-pathogens provided insights into regulatory mechanisms behind the initiation of infectious processes. We examined the gene expression patterns of 3,845 single-copy orthologous genes (SCOGs) across five phylogenetically distinct species, including the opportunistic human pathogens Fusarium oxysporum, Aspergillus fumigatus, and A. nidulans, and nonpathogenic species Neurospora crassa and Trichoderma asperelloides, at four sequential stages of spore germination. Ancestral status of gene expression was inferred for nodes along the phylogeny. By comparing expression patterns of the SCOGs with their most recent common ancestor (MRCA), we identified genes that exhibit divergent levels of expression during spore germination when comparing fungal pathogens to non-pathogens. We focused on genes related to the MAPK pathway, nitrogen metabolism, asexual development, G-protein signaling, and conidial-wall integrity. Notably, orthologs of the transcription activator abaA, a known central regulator of conidiation, exhibited significant divergence in gene expression in F. oxysporum. This dramatic expression change in abaA was accompanied by structural modifications of phialides in F. oxysporum, and revealed how these changes impact development of offspring, formation of aerial hyphae, spore production, and pathogenicity. Our research provides insights into ecological adaptations observed during the divergence of these species, specifically highlighting how divergence in gene expression during spore germination contributes to their ability to thrive in distinct environments. 

Fusarium head blight (FHB) is one of the most devastating diseases of cereal crops, causing severe reduction in yield and quality of grain worldwide. In the United States, the major causal agent of FHB is the mycotoxigenic fungus, Fusarium graminearum. The contamination of grain with mycotoxins, including deoxynivalenol and zearalenone, is a particularly serious concern due to its impact on the health of humans and livestock. For the past few decades, multidisciplinary studies have been conducted on management strategies designed to reduce the losses caused by FHB. However, effective management is still challenging due to the emergence of fungicidetolerant strains of F. graminearum and the lack of highly resistant wheat and barley cultivars. This review presents multidisciplinary approaches that incorporate advances in genomics, genetic-engineering, new fungicide chemistries, applied biocontrol, and consideration of the disease cycle for management of FHB. 

Lineage-specific genes (LSGs) have long been postulated to play roles in the establishment of genetic barriers to intercrossing and speciation. In the genome ofNeurospora crassa, most of the 670NeurosporaLSGs that are aggregated adjacent to the telomeres are clustered with 61% of the HET-domain genes, some of which regulate self-recognition and define vegetative incompatibility groups. In contrast, the LSG-encoding proteins possess few to no domains that would help to identify potential functional roles. Possible functional roles of LSGs were further assessed by performing transcriptomic profiling in genetic mutants and in response to environmental alterations, as well as examining gene knockouts for phenotypes. Among the 342 LSGs that are dynamically expressed during both asexual and sexual phases, 64% were detectable on unusual carbon sources such as furfural, a wildfire-produced chemical that is a strong inducer of sexual development, and the structurally-related furan 5-hydroxymethyl furfural (HMF). Expression of a significant portion of the LSGs was sensitive to light and temperature, factors that also regulate the switch from asexual to sexual reproduction. Furthermore, expression of the LSGs was significantly affected in the knockouts ofadv-1andpp-1that regulate hyphal communication, and expression of more than one quarter of the LSGs was affected by perturbation of the mating locus. These observations encouraged further investigation of the roles of clustered lineage-specific and HET-domain genes in ecology and reproduction regulation inNeurospora, especially the regulation of the switch from the asexual growth to sexual reproduction, in response to dramatic environmental conditions changes. 

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. 

Fusarium graminearumandMagnaporthe oryzaeare two of the most important pathogens of cereal grains worldwide. Despite years of research, strong host resistance has not been identified forF. graminearum, so other methods of control are essential.