Genomics and Evolution of Macrofungi

A special issue of Journal of Fungi (ISSN 2309-608X). This special issue belongs to the section "Fungal Genomics, Genetics and Molecular Biology".

Deadline for manuscript submissions: closed (31 July 2022) | Viewed by 20039

Special Issue Editors


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Guest Editor
Institute of Applied Mycology, Huazhong Agricultural University, Wuhan 430070, China
Interests: population genomics; adaptive evolution

E-Mail Website
Guest Editor
Fungal Genomics and Evolution Lab, Synthetic and Systems Biology Unit, Institute of Biochemistry, Biological Research Centre, 6726 Szeged, Hungary
Interests: evolutionary genomics; evo-devo; wood decay; fruiting body development

Special Issue Information

Dear Colleagues,

Over the past two decades, fungal genomics has experienced unprecedented advances, since the expansion of the genome sequence databases has been generated in an increasing number of fungal taxa. Fungi are ideal organisms for illuminating the evolutionary mechanisms in eukaryotes because of their contrasting ecological niches, short generation times, generally compact genomes, and simple morphologies, approaches in fungal genomics supported by robust bioinformatics serving as important tools in the study of the biology and evolution of fungi. Hitherto, the evolutionary processes of diverse fungi have been extensively studied based on genomics methods, but such advances are achieved less often in fruiting body-forming fungi in the Asco- and Basidiomycota kingdoms. To provide a platform for collecting recent significant advances in the genomics and evolution of macrofungi, we have organized this Special Issue, aiming to assemble a diverse array of papers focusing on the genomics and evolution of fruiting body-forming Asco- and Basidiomycota fungi, including, but not limited to, population genomics, comparative genomics, transcriptomics, epigenomics, and their applications in the evolution of macrofungi, as well as bioinformatics approaches associated with the study of genome evolution, and excluding papers merely describing genome assemblies and annotation, which do not fall within the scope of this Special Issue.

Dr. Yang Xiao
Dr. László Nagy
Guest Editors

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Keywords

  • population genomics
  • comparative genomics
  • evolutionary genomics
  • transcriptomics
  • epigenomics
  • bioinformatics for genome and evolution
  • pangenomics
  • biodegradation
  • fruiting body development
  • environmental adaptation

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Published Papers (7 papers)

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Research

18 pages, 1685 KiB  
Article
Uniparental Inheritance and Recombination as Strategies to Avoid Competition and Combat Muller’s Ratchet among Mitochondria in Natural Populations of the Fungus Amanita phalloides
by Yen-Wen Wang, Holly Elmore and Anne Pringle
J. Fungi 2023, 9(4), 476; https://doi.org/10.3390/jof9040476 - 15 Apr 2023
Cited by 3 | Viewed by 2263
Abstract
Uniparental inheritance of mitochondria enables organisms to avoid the costs of intracellular competition among potentially selfish organelles. By preventing recombination, uniparental inheritance may also render a mitochondrial lineage effectively asexual and expose mitochondria to the deleterious effects of Muller’s ratchet. Even among animals [...] Read more.
Uniparental inheritance of mitochondria enables organisms to avoid the costs of intracellular competition among potentially selfish organelles. By preventing recombination, uniparental inheritance may also render a mitochondrial lineage effectively asexual and expose mitochondria to the deleterious effects of Muller’s ratchet. Even among animals and plants, the evolutionary dynamics of mitochondria remain obscure, and less is known about mitochondrial inheritance among fungi. To understand mitochondrial inheritance and test for mitochondrial recombination in one species of filamentous fungus, we took a population genomics approach. We assembled and analyzed 88 mitochondrial genomes from natural populations of the invasive death cap Amanita phalloides, sampling from both California (an invaded range) and Europe (its native range). The mitochondrial genomes clustered into two distinct groups made up of 57 and 31 mushrooms, but both mitochondrial types are geographically widespread. Multiple lines of evidence, including negative correlations between linkage disequilibrium and distances between sites and coalescent analysis, suggest low rates of recombination among the mitochondria (ρ = 3.54 × 10−4). Recombination requires genetically distinct mitochondria to inhabit a cell, and recombination among A. phalloides mitochondria provides evidence for heteroplasmy as a feature of the death cap life cycle. However, no mushroom houses more than one mitochondrial genome, suggesting that heteroplasmy is rare or transient. Uniparental inheritance emerges as the primary mode of mitochondrial inheritance, even as recombination appears as a strategy to alleviate Muller’s ratchet. Full article
(This article belongs to the Special Issue Genomics and Evolution of Macrofungi)
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15 pages, 5012 KiB  
Article
HOG1 Mitogen-Activated Protein Kinase Pathway–Related Autophagy Induced by H2O2 in Lentinula edodes Mycelia
by Dong Yan, Yangyang Fan, Shuang Song, Yuan Guo, Yu Liu, Xiaoling Xu, Fang Liu, Qi Gao and Shouxian Wang
J. Fungi 2023, 9(4), 413; https://doi.org/10.3390/jof9040413 - 28 Mar 2023
Cited by 1 | Viewed by 1813
Abstract
Mycelial ageing is associated with ROS and autophagy in Lentinula edodes. However, the underlying cellular and molecular mechanisms between ROS and autophagy remain obscure. This study induced autophagy in L. edodes mycelia through exogenous H2O2 treatment. Results showed that [...] Read more.
Mycelial ageing is associated with ROS and autophagy in Lentinula edodes. However, the underlying cellular and molecular mechanisms between ROS and autophagy remain obscure. This study induced autophagy in L. edodes mycelia through exogenous H2O2 treatment. Results showed that 100 μM H2O2 treatment for 24 h significantly inhibited mycelial growth. H2O2 caused the depolarisation of MMP and accumulation of TUNEL-positive nuclei, which was similar to the ageing phenotype of L. edodes mycelia. Transcriptome analysis showed that differentially expressed genes were enriched in the mitophagic, autophagic, and MAPK pathways. LeAtg8 and LeHog1 were selected as hub genes. RNA and protein levels of LeATG8 increased in the H2O2-treated mycelia. Using fluorescent labelling, we observed for the first time the classic ring structure of autophagosomes in a mushroom, while 3D imaging suggested that these autophagosomes surrounded the nuclei to degrade them at specific growth stages. Phospho-LeHOG1 protein can translocate from the cytoplasm to the nucleus to regulate mycelial cells, resisting ROS-induced oxidative stress. Furthermore, LeATG8 expression was suppressed when LeHOG1 phosphorylation was inhibited. These results suggest that the LeATG8-dependent autophagy in L. edodes mycelial is closely associated with the activity or even phosphorylation of LeHOG1. Full article
(This article belongs to the Special Issue Genomics and Evolution of Macrofungi)
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15 pages, 6084 KiB  
Article
Insights into the Global Transcriptome Response of Lentinula edodes Mycelia during Aging
by Qi Gao, Yangyang Fan, Sai Wei, Shuang Song, Yuan Guo, Shouxian Wang, Yu Liu and Dong Yan
J. Fungi 2023, 9(3), 379; https://doi.org/10.3390/jof9030379 - 20 Mar 2023
Cited by 3 | Viewed by 2079
Abstract
The spawn of Lentinula edodes and other basidiomycete fungi tend to age with long-term culture. This causes heavy yield losses if aging spawn is used for propagation. In this study, we cultivated dikaryotic L. edodes mycelia in plates for 60 days to produce [...] Read more.
The spawn of Lentinula edodes and other basidiomycete fungi tend to age with long-term culture. This causes heavy yield losses if aging spawn is used for propagation. In this study, we cultivated dikaryotic L. edodes mycelia in plates for 60 days to produce intrinsic aging phenotypes. We found that intracellular reactive oxygen species levels increased in contrast to mitochondrial depolarization and also observed greater DNA fragmentation with longer culture time. Transcriptome analysis of mycelia at different growth stages revealed pronounced expression differences between short- and long-term cultures. In particular, “phenylalanine, tyrosine, and tryptophan biosynthesis”, “mitophagy and autophagy”, “MAPK signaling pathway”, and “ABC transporter” were among the enriched terms in the mycelial aging process. Weighted correlation network analysis identified LeAtg8, LeHog1, LePbs2, and LemTOR as key genes during aging. Western blotting confirmed that LeATG8 and phosphorylated LeHOG1 protein levels were significantly upregulated in aging mycelia. Our combined analytical approach provides insights into the mechanisms that regulate mycelial aging, indicating that autophagy/mitophagy plays a major role in counteracting the effects of age on mycelial growth development. Full article
(This article belongs to the Special Issue Genomics and Evolution of Macrofungi)
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16 pages, 2007 KiB  
Article
Organization and Unconventional Integration of the Mating-Type Loci in Morchella Species
by Hongmei Chai, Ping Liu, Yuanhao Ma, Weimin Chen, Nan Tao and Yongchang Zhao
J. Fungi 2022, 8(7), 746; https://doi.org/10.3390/jof8070746 - 19 Jul 2022
Cited by 3 | Viewed by 2126
Abstract
True morels (Morchella spp.) are a group of delicious fungi in high demand worldwide, and some species of morels have been successfully cultivated in recent years. To better understand the sexual reproductive mechanisms of these fungi, we characterized the structure of the [...] Read more.
True morels (Morchella spp.) are a group of delicious fungi in high demand worldwide, and some species of morels have been successfully cultivated in recent years. To better understand the sexual reproductive mechanisms of these fungi, we characterized the structure of the mating-type loci from ten morel species, and seven of them were obtained using long-range PCR amplification. Among the studied species, eight were heterothallic, two were homothallic, and four types of composition were observed in the MAT loci. In three of the five black morel species, the MAT1-1-1, MAT1-1-10, and MAT1-1-11 genes were in the MAT1-1 idiomorph, and only the MAT1-2-1 gene was in the MAT1-2 idiomorph, while an integration event occurred in the other two species and resulted in the importation of the MAT1-1-11 gene into the MAT1-2 idiomorph and survival as a truncated fragment in the MAT1-1 idiomorph. However, the MAT1-1-11 gene was not available in the four yellow morels and one blushing morel species. M. rufobrunnea, a representative species of the earliest diverging branch of true morels, along with another yellow morel Mes-15, were confirmed to be homothallic, and the MAT1-1-1, MAT1-1-10, and MAT1-2-1 genes were arranged in a tandem array. Therefore, we hypothesized that homothallism should be the ancestral reproductive state in Morchella. RT-PCR analyses revealed that four mating genes could be constitutively expressed, while the MAT1-1-10 gene underwent alternative splicing to produce different splice variants. Full article
(This article belongs to the Special Issue Genomics and Evolution of Macrofungi)
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23 pages, 5441 KiB  
Article
Dynamic Genome-Wide Transcription Profiling and Direct Target Genes of CmWC-1 Reveal Hierarchical Light Signal Transduction in Cordyceps militaris
by Jiaojiao Zhang, Fen Wang, Mengqian Liu, Mingjia Fu and Caihong Dong
J. Fungi 2022, 8(6), 624; https://doi.org/10.3390/jof8060624 - 11 Jun 2022
Cited by 6 | Viewed by 2463
Abstract
Light is necessary for primordium differentiation and fruiting body development for most edible fungi; however, light perception and signal transduction have only been well studied in model fungi. In this study, a hierarchical network of transcriptional response to light in Cordyceps militaris, [...] Read more.
Light is necessary for primordium differentiation and fruiting body development for most edible fungi; however, light perception and signal transduction have only been well studied in model fungi. In this study, a hierarchical network of transcriptional response to light in Cordyceps militaris, one of the edible fungi, has been described on a genome-wide scale using dynamic transcriptome analysis. It was shown that light regulated the transcript of 1722 genes, making up 18% of the whole genome of C. militaris. Analysis of light-responsive genes in C. militaris identified 4 categories: immediate-early, early, late, and continuous light-responsive genes, and the gene number increased distinctly with prolonged light exposure. Light-responsive genes with distinct functional categories showed specific time-dependent regulation. The target genes of CmWC-1, the most important photoreceptor, were revealed by ChIP-seq. A total of 270 significant peaks corresponding to 427 genes were identified to be directly regulated by CmWC-1, among which 143 genes respond to light. Based on 270 ChIP-seq peaks, the binding site for CmWC-1 was identified as AAATCAGACCAC/GTGGTCTGATTT, differing from the binding site by the homolog in Neurospora crassa. Elucidating the mechanisms of light perception and signal transduction will be helpful for further research on the fruiting body development in edible fungi. Full article
(This article belongs to the Special Issue Genomics and Evolution of Macrofungi)
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14 pages, 1992 KiB  
Article
Pan-Genomes Provide Insights into the Genetic Basis of Auricularia heimuer Domestication
by Yuxiu Guo, Zhenhua Liu, Yongping Fu, Yu Li, Yueting Dai and Shijun Xiao
J. Fungi 2022, 8(6), 581; https://doi.org/10.3390/jof8060581 - 29 May 2022
Cited by 2 | Viewed by 2697
Abstract
In order to reveal the genetic variation signals of Auricularia heimuer that have occurred during their domestication and to find potential functional gene families, we constructed a monokaryotic pan-genome of A. heimuer representing four cultivated strains and four wild strains. The pan-genome contained [...] Read more.
In order to reveal the genetic variation signals of Auricularia heimuer that have occurred during their domestication and to find potential functional gene families, we constructed a monokaryotic pan-genome of A. heimuer representing four cultivated strains and four wild strains. The pan-genome contained 14,089 gene families, of which 67.56% were core gene families and 31.88% were dispensable gene families. We screened substrate utilization-related genes such as the chitinase gene ahchi1 of the glycoside hydrolase (GH) 18 family and a carbohydrate-binding module (CBM)-related gene from the dispensable families of cultivated populations. The genomic difference in the ahchi1 gene between the wild and cultivated genomes was caused by a 33 kb presence/absence variation (PAV). The detection rate of the ahchi1 gene was 93.75% in the cultivated population, significantly higher than that in the wild population (17.39%), indicating that it has been selected in cultivated strains. Principal component analysis (PCA) of the polymorphic markers in fragments near the ahchi1 gene was enriched in cultivated strains, and this was caused by multiple independent instances of artificial selection. We revealed for the first time the genetic basis of the ahchi1 gene in domestication, thereby providing a foundation for elucidating the potential function of the ahchi1 gene in the breeding of A. heimuer. Full article
(This article belongs to the Special Issue Genomics and Evolution of Macrofungi)
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23 pages, 5216 KiB  
Article
Phylogenomics and Comparative Genomics Highlight Specific Genetic Features in Ganoderma Species
by Yi-Fei Sun, Annie Lebreton, Jia-Hui Xing, Yu-Xuan Fang, Jing Si, Emmanuelle Morin, Shingo Miyauchi, Elodie Drula, Steven Ahrendt, Kelly Cobaugh, Anna Lipzen, Maxim Koriabine, Robert Riley, Annegret Kohler, Kerrie Barry, Bernard Henrissat, Igor V. Grigoriev, Francis M. Martin and Bao-Kai Cui
J. Fungi 2022, 8(3), 311; https://doi.org/10.3390/jof8030311 - 18 Mar 2022
Cited by 15 | Viewed by 5200
Abstract
The Ganoderma species in Polyporales are ecologically and economically relevant wood decayers used in traditional medicine, but their genomic traits are still poorly documented. In the present study, we carried out a phylogenomic and comparative genomic analyses to better understand the genetic blueprint [...] Read more.
The Ganoderma species in Polyporales are ecologically and economically relevant wood decayers used in traditional medicine, but their genomic traits are still poorly documented. In the present study, we carried out a phylogenomic and comparative genomic analyses to better understand the genetic blueprint of this fungal lineage. We investigated seven Ganoderma genomes, including three new genomes, G. australe, G. leucocontextum, and G. lingzhi. The size of the newly sequenced genomes ranged from 60.34 to 84.27 Mb and they encoded 15,007 to 20,460 genes. A total of 58 species, including 40 white-rot fungi, 11 brown-rot fungi, four ectomycorrhizal fungi, one endophyte fungus, and two pathogens in Basidiomycota, were used for phylogenomic analyses based on 143 single-copy genes. It confirmed that Ganoderma species belong to the core polyporoid clade. Comparing to the other selected species, the genomes of the Ganoderma species encoded a larger set of genes involved in terpene metabolism and coding for secreted proteins (CAZymes, lipases, proteases and SSPs). Of note, G. australe has the largest genome size with no obvious genome wide duplication, but showed transposable elements (TEs) expansion and the largest set of terpene gene clusters, suggesting a high ability to produce terpenoids for medicinal treatment. G. australe also encoded the largest set of proteins containing domains for cytochrome P450s, heterokaryon incompatibility and major facilitator families. Besides, the size of G. australe secretome is the largest, including CAZymes (AA9, GH18, A01A), proteases G01, and lipases GGGX, which may enhance the catabolism of cell wall carbohydrates, proteins, and fats during hosts colonization. The current genomic resource will be used to develop further biotechnology and medicinal applications, together with ecological studies of the Ganoderma species. Full article
(This article belongs to the Special Issue Genomics and Evolution of Macrofungi)
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