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The fungal class Sordariomycetes includes numerous important plant and animal pathogens. It also provides model systems for studying fungal fruiting body development, as its members develop fruiting bodies with a few well-characterized tissue types on common growth media and have rich genomic resources that enable comparative and functional analyses. Gene expression divergence through evolutionary processes is thought to be important for achieving programmed development in multicellular organisms. To test this premise in filamentous fungi, we investigated transcriptional profiles of 3,942 single-copy orthologous genes (SCOGs) in five related sordariomycete species that have morphologically diverged in the formation of their flask-shaped perithecia. We compared expression of the SCOGs to inferred gene expression levels of the most recent common ancestor of the five species, ranking genes from their largest increases to smallest increases in expression during perithecial development in each of the five species. We found that a large proportion of the genes that exhibited evolved increases in gene expression were important for normal perithecial development in Fusarium graminearum . Many of these genes were previously uncharacterized, encoding hypothetical proteins without any known functional protein domains. Interestingly, the developmental stages during which aberrant knockout phenotypes appeared largely coincided with the elevated expression of the deleted genes. In addition, we identified novel genes that affected normal perithecial development in Magnaporthe oryzae and Neurospora crassa , which were functionally and transcriptionally diverged from the orthologous counterparts in F. graminearum . Furthermore, comparative analysis of developmental transcriptomes and phylostratigraphic analysis suggested that genes encoding hypothetical proteins are generally young and transcriptionally divergent between related species. This study provides tangible evidence of shifts in gene expression that led to acquisition of novel function of orthologous genes in each lineage and demonstrates that several genes with hypothetical function are crucial for shaping multicellular fruiting bodies. IMPORTANCE The fungal class Sordariomycetes includes numerous important plant and animal pathogens. It also provides model systems for studying fungal fruiting body development, as its members develop fruiting bodies with a few well-characterized tissue types on common growth media and have rich genomic resources that enable comparative and functional analyses. To understand transcriptional divergence of key developmental genes between five related sordariomycete fungi, we performed targeted knockouts of genes inferred to have evolved significant upward shifts in expression. We found that many previously uncharacterized genes play indispensable roles at different stages of fruiting body development, which have undergone transcriptional activation in specific lineages. These novel genes are predicted to be phylogenetically young and tend to be involved in lineage- or species-specific function. Transcriptional activation of genes with unknown function seems to be more frequent than ever thought, which may be crucial for rapid adaption to changing environments for successful sexual reproduction.

Based on morphological and molecular phylogenetic markers and the fertility of sexual crosses, two novel species of Fusarium associated with Dactylopius opuntiae (Hemiptera: Dactylopiidae) and Aleurocanthus woglumi (Hemiptera: Aleyrodidae) from northeastern Brazil are described as Fusarium caatingaense and F. pernambucanum. Partial sequences of five loci were generated for 29 entomopathogenic Fusarium isolates. Multilocus phylogenetic analyses demonstrated that F. caatingaense and F. pernambucanum belong to the Incarnatum clade of the Fusarium incarnatum-equiseti species complex (FIESC). These species displayed common morphological characters such as the production of various types of aerial conidia formed on monophialides and polyphialides and differ from each other mainly in the dimensions and morphology of their sporodochial conidia. Mating type polymerase chain reaction (PCR) revealed 17 MAT1-1 isolates and 12 MAT1-2 isolates, all of them heterothallic. Fertile perithecia were produced in 4.2% of infraspecific crosses of F. caatingaense and in 13.3% of infraspecific crosses of F. pernambucanum after 2-3 wk. Crosses between F. caatingaense and F. pernambucanum did not result in fertile perithecia. We demonstrate the existence of a sexual stage in species of the Incarnatum clade and describe the morphological characters of these sexual morphs for the first time. These results suggest that previously unknown sexual cycles contribute to the high genetic diversity within FIESC.

Plant-pathogenic fungi form intimate interactions with their associated bacterial microbiota during their entire life cycle. However, little is known about the structure, functions and interaction mechanisms of bacterial communities associated with fungal fruiting bodies (perithecia). Here we examined the bacterial microbiome of perithecia formed by Fusarium graminearum , the major pathogenic fungus causing Fusarium head blight in cereals. A total of 111 shared bacterial taxa were identified in the microbiome of 65 perithecium samples collected from 13 geographic locations. Within a representative culture collection, 113 isolates exhibited antagonistic activity against F. graminearum , with Pantoea agglomerans ZJU23 being the most efficient in reducing fungal growth and infectivity. Herbicolin A was identified as the key antifungal compound secreted by ZJU23. Genetic and chemical approaches led to the discovery of its biosynthetic gene cluster. Herbicolin A showed potent in vitro and in planta efficacy towards various fungal pathogens and fungicide-resistant isolates, and exerted a fungus-specific mode of action by directly binding and disrupting ergosterol-containing lipid rafts. Furthermore, herbicolin A exhibited substantially higher activity (between 5- and 141-fold higher) against the human opportunistic fungal pathogens Aspergillus fumigatus and Candida albicans in comparison with the clinically used fungicides amphotericin B and fluconazole. Its mode of action, which is distinct from that of other antifungal drugs, and its efficacy make herbicolin A a promising antifungal drug to combat devastating fungal pathogens, both in agricultural and clinical settings. Antifungal produced by Fusarium perithecium bacterium Pantoea agglomerans is a promising drug lead.

A new genus and eight new species, all with isaria-like phialides, are described in Cordycipitaceae from Thailand. The new genus, Samsoniella, is segregated from Akanthomyces based on morphological and molecular evidence. Samsoniella differs from Akanthomyces in producing orange cylindrical to clavate stromata with superficial perithecia and orange conidiophores with isaria-like phialides and white to cream conidia. A new combination for CBS 240.32, originally identified as Paecilomyces farinosus (Isaria farinosa), and CBS 262.58, originally identified as Penicillium alboaurantium, respectively, is made in Samsoniella. Two new species, Samsoniella aurantia and S. inthanonensis, are described from lepidopteran larvae. Two new species of Cordyceps, C. blackwelliae and C. lepidopterorum, were also found on coleopteran and lepidopteran larvae. Both produce isaria-like morphs with globose phialides and attenuated long necks and white mycelium in culture. The authors established a sexual-asexual link for Cordyceps javanica (= Isaria javanica) on lepidopteran larvae. Four new species, Akanthomyces kanyawimiae, A. sulphureus, A. thailandicus, and A. waltergamsii, were pathogenic on spiders, with some strains of A. kanyawimiae also found on unidentified insect larvae. These four species of Akanthomyces occur on the underside of leaves and produce white to cream white powdery conidia, whereas S. aurantia and S. inthanonensis were found in leaf litter and produce bright orange stromata and synnemata with white conidia. Another new combination, Akanthomyces ryukyuensis, is proposed. Phylogenetic analyses based on a combined data set comprising the nuc rDNA region encompassing the internal transcribed spacers 1 and 2 along with the 5.8S rDNA (ITS), nuc 28S rDNA (28S), partial sequences of translation elongation factor 1-α gene (TEF1), and the genes for RNA polymerase II largest (RPB1) and second-largest (RPB2) subunits strongly support the delimitation of these new species of Cordyceps, Akanthomyces, and in a new genus Samsoniella in Cordycipitaceae.

Twenty-five fructicolous and seminicolous species of Xylaria are classified into three groups by stromatal morphology: (i) the X. ianthinovelutina group; (ii) the X. carpophila group; and (iii) the X. heloidea group. Xylaria reevesiae, X. rossmanae, and X. vivantii are described as new species. Xylaria reevesiae belongs to the X. carpophila group, resembling X. euphorbiicola but differing from it mainly by having conspicuous perithecial mounds and growing on fallen fruits of a different host plant. Xylaria rossmanae and X. vivantii belong to the X. ianthinovelutina group. Xylaria rossmanae differs from the species of the group mainly by larger, paler, fusoid-inequilateral ascospores, and X. vivantii differs by larger ascospores with a slightly oblique germ slit. A dichotomous key is provided for identifying the 25 species. Doubtful names are also listed and annotated.

Although fungi lack adenosine deaminase acting on RNA (ADAR) enzymes, adenosine to inosine (A-to-I) RNA editing was reported recently in Fusarium graminearum during sexual reproduction. In this study, we profiled the A-to-I editing landscape and characterized its functional and adaptive properties in the model filamentous fungus Neurospora crassa. A total of 40,677 A-to-I editing sites were identified, and approximately half of them displayed stage-specific editing or editing levels at different sexual stages. RNA-sequencing analysis with the Δstc-1 and Δsad-1 mutants confirmed A-to-I editing occurred before ascus development but became more prevalent during ascosporogenesis. Besides fungal-specific sequence and secondary structure preference, 63.5% of A-to-I editing sites were in the coding regions and 81.3% of them resulted in nonsynonymous recoding, resulting in a significant increase in the proteome complexity. Many genes involved in RNA silencing, DNA methylation, and histone modifications had extensive recoding, including sad-1, sms-3, qde-1, and dim-2. Fifty pseudogenes harbor premature stop codons that require A-to-I editing to encode full-length proteins. Unlike in humans, nonsynonymous editing events in N. crassa are generally beneficial and favored by positive selection. Almost half of the nonsynonymous editing sites in N. crassa are conserved and edited in Neurospora tetrasperma. Furthermore, hundreds of them are conserved in F. graminearum and had higher editing levels. Two unknown genes with editing sites conserved between Neurospora and Fusarium were experimentally shown to be important for ascosporogenesis. This study comprehensively analyzed A-to-I editing in N. crassa and showed that RNA editing is stage-specific and generally adaptive, and may be functionally related to repeat induced point mutation and meiotic silencing by unpaired DNA.

Fusarium graminearum is an important plant pathogen that causes head blight of major cereal crops. The fungus produces mycotoxins that are harmful to animal and human. In this study, a systematic analysis of 17 phenotypes of the mutants in 657 Fusarium graminearum genes encoding putative transcription factors (TFs) resulted in a database of over 11,000 phenotypes (phenome). This database provides comprehensive insights into how this cereal pathogen of global significance regulates traits important for growth, development, stress response, pathogenesis, and toxin production and how transcriptional regulations of these traits are interconnected. In-depth analysis of TFs involved in sexual development revealed that mutations causing defects in perithecia development frequently affect multiple other phenotypes, and the TFs associated with sexual development tend to be highly conserved in the fungal kingdom. Besides providing many new insights into understanding the function of F. graminearum TFs, this mutant library and phenome will be a valuable resource for characterizing the gene expression network in this fungus and serve as a reference for studying how different fungi have evolved to control various cellular processes at the transcriptional level.

Calmodulin (CaM) is a primary Ca 2+ sensor that binds and activates numerous target proteins and regulates several cellular processes in eukaryotes. CaM is essential in Neurospora crassa ; therefore, we generated a CaM mutant using repeat-induced point (RIP) mutation and investigated the cmd RIP mutant phenotypes. We also studied knockout mutants of four Ca 2+ /CaM kinases ( camk-1 , 2 , 3 , and 4 ) for their role during stress conditions and sexual development. The cmd RIP , ∆ camk-1 , and ∆ camk-2 mutants showed reduced survival and growth rates under heat stress, oxidative stress, pH, and ER stress conditions. In addition, under the heat stress conditions, expression of the heat shock protein genes hsp70 and hsp80 was reduced in the cmd RIP , ∆ camk-1 , and ∆ camk-2 mutants. The cmd RIP mutant was also defective in cell fusion, its vegetative hyphae could not support the fertilized wild type perithecia graft, and female sterile. Furthermore, the expression of pheromone signaling genes pre-1 , pre-2 , ccg-4 , mfa-1 , and fmf-1 was reduced in the cmd RIP , ∆ camk-1 , and ∆ camk-2 mutants. Therefore, CaM, Ca 2+ /CaMK-1 and 2 are involved in the tolerance to heat stress conditions and sexual development by regulating the heat shock and pheromone response pathways, respectively, in N. crassa.

The increasing use of plastics in human activities has resulted in an enormous amount of residues which became a matter of great environmental concern. Scientific studies on the microbial degradation of natural and synthetic molecules show the potential of fungal application on cleaning technologies. The biodegradation of PCL (polycaprolactone) and PVC (polyvinyl chloride) films by Aspergillus brasiliensis (ATCC 9642), Penicillium funiculosum (ATCC 11797), Chaetomium globosum (ATCC 16021), Trichoderma virens (ATCC 9645), and Paecilomyces variotii (ATCC 16023) was studied. According to ISO 846-1978—“Testing of Plastics - Influence of fungi and bacteria”, samples of the studied polymers were inoculated with a mix suspension of 106 fungal inoculum and maintained in moisture glass chambers in a bacteriological incubator at 28 °C for 28 days. The samples were analyzed by means of morphological and color changes, mass loss, optical microscopy (OM), and scanning electron microscopy (SEM) after 28 days of culturing. After the incubation period, visual observations of the PCL films showed many micropores and cracks, pigmentation, surface erosion and hyphal adhesion on the sample surfaces, and a mass loss of up to 75%. On the contrary, there was no evidence of PVC biodegradation, such as changes in color and significant mass loss. Chaetomium globosum ATCC 16021 was a pioneer in the colonization and attack of PCL, resulting in significant mass losses. Although PVC was less attacked by the ascomycete, the polymer supported the adhesion and growth of its fertile structures (perithecia), suggesting the fungal potential to degrade both plastics.

Abstract Rice blast fungus (Pyricularia oryzae) is a heterothallic ascomycete that causes the most destructive disease in cultivated rice worldwide. This fungus reproduces sexually and asexually, and its mating type is determined by the MAT1 locus, MAT1-1 or MAT1-2. Interestingly, most rice-infecting field isolates show a loss of female fertility, but the MAT1 locus is highly conserved in female-sterile isolates. In this study, we performed a functional analysis of MAT1 using the CRISPR/Cas9 system in female- and male-fertile isolates and female-sterile (male-fertile) isolates. Consistent with a previous report, MAT1 was essential for sexual reproduction but not for asexual reproduction. Meanwhile, deletion mutants of MAT1-1-1, MAT1-1-2, and MAT1-1-3 exhibited phenotypes different from those of other previously described isolates, suggesting that the function of MAT1-1 genes and/or their target genes in sexual reproduction differs among strains or isolates. The MAT1 genes, excluding MAT1-2-6, retained their functions even in female-sterile isolates, and deletion mutants lead to loss or reduction of male fertility. Although MAT1 deletion did not affect microconidia (spermatia) production, microconidia derived from the mutants could not induce perithecia formation. These results indicated that MAT1 is required for microconidia-mediated male fertility in addition to female fertility in P. oryzae . MAT1 is required for microconidia-mediated male fertility in addition to female fertility in the rice blast fungus Pyricularia oryzae.