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  1. Abstract Convergent evolution is pervasive in nature, but it is poorly understood how various constraints and natural selection limit the diversity of evolvable phenotypes. Here, we analyze the transcriptome across fruiting body development to understand the independent evolution of complex multicellularity in the two largest clades of fungi—the Agarico- and Pezizomycotina. Despite >650 My of divergence between these clades, we find that very similar sets of genes have convergently been co-opted for complex multicellularity, followed by expansions of their gene families by duplications. Over 82% of shared multicellularity-related gene families were expanding in both clades, indicating a high prevalence of convergence also at the gene family level. This convergence is coupled with a rich inferred repertoire of multicellularity-related genes in the most recent common ancestor of the Agarico- and Pezizomycotina, consistent with the hypothesis that the coding capacity of ancestral fungal genomes might have promoted the repeated evolution of complex multicellularity. We interpret this repertoire as an indication of evolutionary predisposition of fungal ancestors for evolving complex multicellular fruiting bodies. Our work suggests that evolutionary convergence may happen not only when organisms are closely related or are under similar selection pressures, but also when ancestral genomic repertoires render certain evolutionary trajectories more likely than others, even across large phylogenetic distances. 
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  2. ABSTRACT The origins and maintenance of the rich fungal diversity have been longstanding issues in evolutionary biology. To investigate how differences in expression regulation contribute to divergences in development and ecology among closely related species, transcriptomes were compared between Chaetomium globosum , a homothallic pathogenic fungus thriving in highly humid ecologies, and Neurospora crassa , a heterothallic postfire saprotroph. Gene expression was quantified in perithecia at nine distinct morphological stages during nearly synchronous sexual development. Unlike N. crassa , expression of all mating loci in C. globosum was highly correlated. Key regulators of the initiation of sexual development in response to light stimuli—including orthologs of N. crassa sub-1 , sub-1 -dependent gene NCU00309, and asl-1 —showed regulatory dynamics matching between C. globosum and N. crassa . Among 24 secondary metabolism gene clusters in C. globosum , 11—including the cochliodones biosynthesis cluster—exhibited highly coordinated expression across perithecial development. C. globosum exhibited coordinately upregulated expression of histidine kinases in hyperosmotic response pathways—consistent with gene expression responses to high humidity we identified in fellow pathogen Fusarium graminearum . Bayesian networks indicated that gene interactions during sexual development have diverged in concert with the capacities both to reproduce asexually and to live a self-compatible versus self-incompatible life cycle, shifting the hierarchical roles of genes associated with conidiation and heterokaryon incompatibility in N. crassa and C. globosum . This divergence supports an evolutionary history of loss of conidiation due to unfavorable combinations of heterokaryon incompatibility in homothallic species. IMPORTANCE Fungal diversity has amazed evolutionary biologists for decades. One societally important aspect of this diversity manifests in traits that enable pathogenicity. The opportunistic pathogen Chaetomium globosum is well adapted to a high-humidity environment and produces numerous secondary metabolites that defend it from predation. Many of these chemicals can threaten human health. Understanding the phases of the C. globosum life cycle in which these products are made enables better control and even utilization of this fungus. Among its intriguing traits is that it both is self-fertile and lacks any means of propagule-based asexual reproduction. By profiling genome-wide gene expression across the process of sexual reproduction in C. globosum and comparing it to genome-wide gene expression in the model filamentous fungus N. crassa and other closely related fungi, we revealed associations among mating-type genes, sexual developmental genes, sexual incompatibility regulators, environmentally responsive genes, and secondary metabolic pathways. 
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  3. ABSTRACT Fungal spores germinate and undergo vegetative growth, leading to either asexual or sexual reproductive dispersal. Previous research has indicated that among developmental regulatory genes, expression is conserved across nutritional environments, whereas pathways for carbon and nitrogen metabolism appear highly responsive—perhaps to accommodate differential nutritive processing. To comprehensively investigate conidial germination and the adaptive life history decision-making underlying these two modes of reproduction, we profiled transcription of Neurospora crassa germinating on two media: synthetic Bird medium, designed to promote asexual reproduction; and a natural maple sap medium, on which both asexual reproduction and sexual reproduction manifest. A later start to germination but faster development was observed on synthetic medium. Metabolic genes exhibited altered expression in response to nutrients—at least 34% of the genes in the genome were significantly downregulated during the first two stages of conidial germination on synthetic medium. Knockouts of genes exhibiting differential expression across development altered germination and growth rates, as well as in one case causing abnormal germination. A consensus Bayesian network of these genes indicated especially tight integration of environmental sensing, asexual and sexual development, and nitrogen metabolism on a natural medium, suggesting that in natural environments, a more dynamic and tentative balance of asexual and sexual development may be typical of N. crassa colonies. IMPORTANCE One of the most remarkable successes of life is its ability to flourish in response to temporally and spatially varying environments. Fungi occupy diverse ecosystems, and their sensitivity to these environmental changes often drives major fungal life history decisions, including the major switch from vegetative growth to asexual or sexual reproduction. Spore germination comprises the first and simplest stage of vegetative growth. We examined the dependence of this early life history on the nutritional environment using genome-wide transcriptomics. We demonstrated that for developmental regulatory genes, expression was generally conserved across nutritional environments, whereas metabolic gene expression was highly labile. The level of activation of developmental genes did depend on current nutrient conditions, as did the modularity of metabolic and developmental response network interactions. This knowledge is critical to the development of future technologies that could manipulate fungal growth for medical, agricultural, or industrial purposes. 
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  4. ABSTRACT Long noncoding RNA (lncRNA) plays important roles in sexual development in eukaryotes. In filamentous fungi, however, little is known about the expression and roles of lncRNAs during fruiting body formation. By profiling developmental transcriptomes during the life cycle of the plant-pathogenic fungus Fusarium graminearum , we identified 547 lncRNAs whose expression was highly dynamic, with about 40% peaking at the meiotic stage. Many lncRNAs were found to be antisense to mRNAs, forming 300 sense-antisense pairs. Although small RNAs were produced from these overlapping loci, antisense lncRNAs appeared not to be involved in gene silencing pathways. Genome-wide analysis of small RNA clusters identified many silenced loci at the meiotic stage. However, we found transcriptionally active small RNA clusters, many of which were associated with lncRNAs. Also, we observed that many antisense lncRNAs and their respective sense transcripts were induced in parallel as the fruiting bodies matured. The nonsense-mediated decay (NMD) pathway is known to determine the fates of lncRNAs as well as mRNAs. Thus, we analyzed mutants defective in NMD and identified a subset of lncRNAs that were induced during sexual development but suppressed by NMD during vegetative growth. These results highlight the developmental stage-specific nature and functional potential of lncRNA expression in shaping the fungal fruiting bodies and provide fundamental resources for studying sexual stage-induced lncRNAs. IMPORTANCE Fusarium graminearum is the causal agent of the head blight on our major staple crops, wheat and corn. The fruiting body formation on the host plants is indispensable for the disease cycle and epidemics. Long noncoding RNA (lncRNA) molecules are emerging as key regulatory components for sexual development in animals and plants. To date, however, there is a paucity of information on the roles of lncRNAs in fungal fruiting body formation. Here we characterized hundreds of lncRNAs that exhibited developmental stage-specific expression patterns during fruiting body formation. Also, we discovered that many lncRNAs were induced in parallel with their overlapping transcripts on the opposite DNA strand during sexual development. Finally, we found a subset of lncRNAs that were regulated by an RNA surveillance system during vegetative growth. This research provides fundamental genomic resources that will spur further investigations on lncRNAs that may play important roles in shaping fungal fruiting bodies. 
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  5. ABSTRACT Rapid responses to changes in incident light are critical to the guidance of behavior and development in most species. Phytochrome light receptors in particular play key roles in bacterial physiology and plant development, but their functions and regulation are less well understood in fungi. Nevertheless, genome-wide expression measurements provide key information that can guide experiments that reveal how genes respond to environmental signals and clarify their role in development. We performed functional genomic and phenotypic analyses of the two phytochromes in Neurospora crassa , a fungal model adapted to a postfire environment that experiences dramatically variable light conditions. Expression of phy-1 and phy-2 was low in early sexual development and in the case of phy-2 increased in late sexual development. Under light stimulation, strains with the phytochromes deleted exhibited increased expression of sexual development-related genes. Moreover, under red light, the phy-2 knockout strain commenced sexual development early. In the evolution of phytochromes within ascomycetes, at least two duplications have occurred, and the faster-evolving phy-2 gene has frequently been lost. Additionally, the three key cysteine sites that are critical for bacterial and plant phytochrome function are not conserved within fungal phy-2 homologs. Through the action of phytochromes, transitions between asexual and sexual reproduction are modulated by light level and light quality, presumably as an adaptation for fast asexual growth and initiation of sexual reproduction of N. crassa in exposed postfire ecosystems. IMPORTANCE Environmental signals, including light, play critical roles in regulating fungal growth and pathogenicity, and balance of asexual and sexual reproduction is critical in fungal pathogens’ incidence, virulence, and distribution. Red light sensing by phytochromes is well known to play critical roles in bacterial physiology and plant development. Homologs of phytochromes were first discovered in the fungal model Neurospora crassa and then subsequently in diverse other fungi, including many plant pathogens. Our study investigated the evolution of red light sensors in ascomycetes and confirmed—using the model fungus Neurospora crassa —their roles in modulating the asexual-sexual reproduction balance in fungi. Our findings also provide a key insight into one of the most poorly understood aspects of fungal biology, suggesting that further study of the function of phytochromes in fungi is critical to reveal the genetic basis of the asexual-sexual switch responsible for fungal growth and distribution, including diverse and destructive plant pathogens. 
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