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New Perspectives on Entomopathogenic and Nematode-Trapping Fungi

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A special issue of Journal of Fungi (ISSN 2309-608X). This special issue belongs to the section "Fungi in Agriculture and Biotechnology".

Deadline for manuscript submissions: closed (30 June 2023) | Viewed by 19879

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Prof. Dr. Jinkui Yang

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State Key Laboratory for Conservation and Utilization of Bio-Resources, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan University, Kunming 650091, China
Interests: nematophagous fungi; fungal genetics; fungus–nematode interaction; signal transduction; fungal morphogenesis; fungal pathogenicity and development
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Prof. Dr. Xuemei Niu

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State Key Laboratory for Conservation and Utilization of Bio-Resources, Key Laboratory for Microbial Resources of the Ministry of Education, School of Life Sciences, Yunnan University, Kunming 650091, China
Interests: fungal metabolism; nematode-trapping fungi; fungus–host interaction
Special Issues, Collections and Topics in MDPI journals

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Dear Colleagues,

A large number of filamentous fungi are of agricultural importance, including the causal agents and biological control agents of arthropod and nematode pests. In recent decades, scientists have been interested in developing environmentally friendly biological control agents to control the population of crop pests. Entomopathogenic and nematode-trapping fungi play important roles in the natural control of host populations and have been widely applied for biological control of pest insects and nematodes. With the development of sequencing technology, multi-omics, including genomic, proteomic, transcriptomic, and metabolomic analyses, has been widely used to elucidate the molecular mechanisms that underlie fungus–host interactions to develop new programs and strategies for combating arthropod and nematode pests.

This Special Issue of the Journal of Fungi welcomes all kind of reviews, perspectives, and research articles on the topic of “New Perspectives on Entomopathogenic and Nematode-Trapping Fungi” to expand our understanding of fungus–host interactions.

Prof. Dr. Jinkui Yang
Prof. Dr. Xuemei Niu
Guest Editors

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Keywords

entomopathogenic fungi
nematode-trapping fungi
fungus–host interaction
fungal pathogenicity
fungal metabolism
biological control

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Published Papers (10 papers)

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Research

15 pages, 6340 KiB

Open AccessArticle

by Jin-Li Ding, Kang Wei, Ming-Guang Feng and Sheng-Hua Ying

J. Fungi 2023, 9(5), 543; https://doi.org/10.3390/jof9050543 - 6 May 2023

Cited by 2 | Viewed by 1531

Abstract

Autophagy is a conserved mechanism for the turnover of intracellular components. Among the ‘core’ autophagy-related genes (ATGs), the cysteine protease Atg4 plays an important role in the activation of Atg8 by exposing the glycine residue at its extreme carboxyl terminus. In the insect fungal pathogen Beauveria bassiana, a yeast ortholog of Atg4 was identified and functionally analyzed. Ablation of the BbATG4 gene blocks the autophagic process during fungal growth under aerial and submerged conditions. Gene loss did not affect fungal radial growth on various nutrients, but ΔBbatg4 exhibited an impaired ability to accumulate biomass. The mutant displayed increased sensitivity to stress caused by menadione and hydrogen peroxide. ΔBbatg4 generated abnormal conidiophores with reduced production of conidia. Additionally, fungal dimorphism was significantly attenuated in gene disruption mutants. Disruption of BbATG4 resulted in significantly weakened virulence in topical and intrahemocoel injection assays. Our study indicates that BbAtg4 contributes to the lifecycle of B. bassiana via its autophagic roles. Full article

(This article belongs to the Special Issue New Perspectives on Entomopathogenic and Nematode-Trapping Fungi)

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14 pages, 4370 KiB

Open AccessArticle

AoMae1 Regulates Hyphal Fusion, Lipid Droplet Accumulation, Conidiation, and Trap Formation in Arthrobotrys oligospora

by Yankun Liu, Meichen Zhu, Wenjie Wang, Xuemei Li, Na Bai, Meihua Xie and Jinkui Yang

J. Fungi 2023, 9(4), 496; https://doi.org/10.3390/jof9040496 - 21 Apr 2023

Cited by 4 | Viewed by 1827

Abstract

Malate dehydrogenase (MDH) is a key enzyme in the tricarboxylic acid (TCA) cycle and is essential for energy balance, growth, and tolerance to cold and salt stresses in plants. However, the role of MDH in filamentous fungi is still largely unknown. In this study, we characterized an ortholog of MDH (AoMae1) in a representative nematode-trapping (NT) fungus Arthrobotrys oligospora via gene disruption, phenotypic analysis, and nontargeted metabolomics. We found that the loss of Aomae1 led to a weakening of MDH activity and ATP content, a remarkable decrease in conidia yield, and a considerable increase in the number of traps and mycelial loops. In addition, the absence of Aomae1 also caused an obvious reduction in the number of septa and nuclei. In particular, AoMae1 regulates hyphal fusion under low nutrient conditions but not in nutrient-rich conditions, and the volumes and sizes of the lipid droplets dynamically changed during trap formation and nematode predation. AoMae1 is also involved in the regulation of secondary metabolites such as arthrobotrisins. These results suggest that Aomae1 has an important role in hyphal fusion, sporulation, energy production, trap formation, and pathogenicity in A. oligospora. Our results enhance the understanding of the crucial role that enzymes involved in the TCA cycle play in the growth, development, and pathogenicity of NT fungi. Full article

(This article belongs to the Special Issue New Perspectives on Entomopathogenic and Nematode-Trapping Fungi)

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14 pages, 17874 KiB

Open AccessArticle

Arthrobotrys blastospora sp. nov. (Orbiliomycetes): A Living Fossil Displaying Morphological Traits of Mesozoic Carnivorous Fungi

by Fa Zhang, Saranyaphat Boonmee, Yao-Quan Yang, Fa-Ping Zhou, Wen Xiao and Xiao-Yan Yang

J. Fungi 2023, 9(4), 451; https://doi.org/10.3390/jof9040451 - 6 Apr 2023

Cited by 4 | Viewed by 2379

Abstract

The evolution of carnivorous fungi in deep time is still poorly understood as their fossil record is scarce. The approximately 100-million-year-old Cretaceous Palaeoanellus dimorphus is the earliest fossil of carnivorous fungi ever discovered. However, its accuracy and ancestral position has been widely questioned because no similar species have been found in modern ecosystems. During a survey of carnivorous fungi in Yunnan, China, two fungal isolates strongly morphologically resembling P. dimorphus were discovered and identified as a new species of Arthrobotrys (Orbiliaceae, Orbiliomycetes), a modern genus of carnivorous fungi. Phylogenetically, Arthrobotrys blastospora sp. nov. forms a sister lineage to A. oligospora. A. blastospora catches nematodes with adhesive networks and produces yeast-like blastospores. This character combination is absent in all other previously known modern carnivorous fungi but is strikingly similar to the Cretaceous P. dimorphus. In this paper, we describe A. blastospora in detail and discuss its relationship to P. dimorphus. Full article

(This article belongs to the Special Issue New Perspectives on Entomopathogenic and Nematode-Trapping Fungi)

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13 pages, 2990 KiB

Open AccessArticle

The Growth and Conidiation of Purpureocillium lavendulum Are Co-Regulated by Nitrogen Sources and Histone H3K14 Acetylation

by Ping Tang, Jing-Jing Han, Chen-Chen Zhang, Ping-Ping Tang, Feng-Na Qi, Ke-Qin Zhang and Lian-Ming Liang

J. Fungi 2023, 9(3), 325; https://doi.org/10.3390/jof9030325 - 6 Mar 2023

Cited by 2 | Viewed by 1867

Abstract

Plant-parasitic nematodes cause severe economic losses to agriculture. As important biocontrol agents, nematophagous fungi evolved the ability to obtain nitrogen sources from nematodes. However, the impact of nitrogen sources on the growth and development of these fungi is largely unknown. In this study, we aimed to better understand how nitrogen sources could influence vegetative growth and conidiation through epigenetic regulation in the nematophagous fungus, Purpureocillium lavendulum. Through nutrition screening, we found a phenomenon of the fungus, limited colony extension with a large amount of conidia production when cultured on PDA media, can be altered by adding ammonia nitrate. Characterized by site-directed mutagenesis, the histone H3K14 acetylation was found to be involved in the alternation. Furthermore, the acetyltransferase PlGCN5 was responsible for H3K14 acetylation. Knockout of Plgcn5 severely diminished conidiation in P. lavendulum. Chip-seq showed that H3K14ac distributed in conidiation regulating genes, and genes in the MAPK pathway which may be the downstream targets in the regulation. These findings suggest that histone modification and nitrogen sources coordinated lifestyle regulation in P. lavendulum, providing new insight into the mechanism of growth regulation by nutritional signals for the carnivorous fungus. Full article

(This article belongs to the Special Issue New Perspectives on Entomopathogenic and Nematode-Trapping Fungi)

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14 pages, 5300 KiB

Open AccessArticle

Co-Regulatory Roles of WC1 and WC2 in Asexual Development and Photoreactivation of Beauveria bassiana

by Si-Yuan Xu, Lei Yu, Xin-Cheng Luo, Sheng-Hua Ying and Ming-Guang Feng

J. Fungi 2023, 9(3), 290; https://doi.org/10.3390/jof9030290 - 23 Feb 2023

Cited by 8 | Viewed by 1846

Abstract

The white collar proteins WC1 and WC2 interact with each other to form a white collar complex acting as a well-known transcription regulator required for the operation of the circadian clock in Neurospora, but their roles in insect-pathogenic fungal lifecycles remain poorly understood. Here, we report that WC1 and WC2 orthologs co-regulate the conidiation capacity and conidial resistance to solar ultraviolet-B (UVB) irradiation in Beauveria bassiana, after their high activities in the photorepair of UVB-induced DNA damages were elucidated previously in the insect mycopathogen, which features non-rhythmic conidiation and high conidiation capacity. The conidial yield, UVB resistance, and photoreactivation rate of UVB-impaired conidia were greatly reduced in the null mutants of wc1 and wc2 compared to their control strains. However, many other lifecycle-related phenotypes, except the antioxidant response, were rarely affected in the two mutants. Transcriptomic analysis revealed largely overlapping roles for WC1 and WC2 in regulating the fungal gene networks. Most of the differentially expressed genes identified from the null mutants of wc1 (1380) and wc2 (1001) were co-downregulated (536) or co-upregulated (256) at similar levels, including several co-downregulated genes required for aerial conidiation and DNA photorepair. These findings expand a molecular basis underlying the fungal adaptation to solar UV irradiation and offer a novel insight into the genome-wide co-regulatory roles of WC1 and WC2 in B. bassiana’s asexual development and in vivo photoreactivation against solar UV damage. Full article

(This article belongs to the Special Issue New Perspectives on Entomopathogenic and Nematode-Trapping Fungi)

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14 pages, 5467 KiB

Open AccessArticle

Divergent Physiological Functions of Four Atg22-like Proteins in Conidial Germination, Development, and Virulence of the Entomopathogenic Fungus Beauveria bassiana

by Jin-Li Ding, Hao Zhang, Ming-Guang Feng and Sheng-Hua Ying

J. Fungi 2023, 9(2), 262; https://doi.org/10.3390/jof9020262 - 15 Feb 2023

Cited by 4 | Viewed by 1762

Abstract

In yeast, Atg22 functions as a vacuolar efflux transporter to release the nutrients from the vacuole to the cytosol after the degradation of autophagic bodies. There are more than one Atg22 domain-containing proteins in filamentous fungi, but their physiological roles are largely unknown. In this study, four Atg22-like proteins (BbAtg22A through D) were functionally characterized in the filamentous entomopathogenic fungus Beauveria bassiana. These Atg22-like proteins exhibit different sub-cellular distributions. BbAtg22A localizes in lipid droplets. BbAtg22B and BbAtg22C are completely distributed in the vacuole, and BbAtg22D has an additional association with the cytomembrane. The ablation of Atg22-like proteins did not block autophagy. Four Atg22-like proteins systematically contribute to the fungal response to starvation and virulence in B. bassiana. With the exception of ∆Bbatg22C, the other three proteins contribute to dimorphic transmission. Additionally, BbAtg22A and BbAtg22D are required for cytomembrane integrity. Meanwhile, four Atg22-like proteins contribute to conidiation. Therefore, Atg22-like proteins link distinct sub-cellular structures for the development and virulence in B. bassiana. Our findings provide a novel insight into the non-autophagic roles of autophagy-related genes in filamentous fungi. Full article

(This article belongs to the Special Issue New Perspectives on Entomopathogenic and Nematode-Trapping Fungi)

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14 pages, 4259 KiB

Open AccessArticle

Comparative Roles of Rad4A and Rad4B in Photoprotection of Beauveria bassiana from Solar Ultraviolet Damage

by Lei Yu, Si-Yuan Xu, Xin-Cheng Luo, Sheng-Hua Ying and Ming-Guang Feng

J. Fungi 2023, 9(2), 154; https://doi.org/10.3390/jof9020154 - 23 Jan 2023

Cited by 9 | Viewed by 1690

Abstract

The Rad4-Rad23-Rad33 complex plays an essential anti-ultraviolet (UV) role depending on nucleotide excision repair (NER) in budding yeast but has been rarely studied in filamentous fungi, which possess two Rad4 paralogs (Rad4A/B) and orthologous Rad23 and rely on the photorepair of UV-induced DNA lesions, a distinct mechanism behind the photoreactivation of UV-impaired cells. Previously, nucleocytoplasmic shuttling Rad23 proved to be highly efficient in the photoreactivation of conidia inactivated by UVB, a major component of solar UV, due to its interaction with Phr2 in Beauveria bassiana, a wide-spectrum insect mycopathogen lacking Rad33. Here, either Rad4A or Rad4B was proven to localize exclusively in the nucleus and interact with Rad23, which was previously shown to interact with the white collar protein WC2 as a regulator of two photorepair-required photolyases (Phr1 and Phr2) in B. bassiana. The Δrad4A mutant lost ~80% of conidial UVB resistance and ~50% of activity in the photoreactivation of UVB-inactivated conidia by 5 h light exposure. Intriguingly, the reactivation rates of UVB-impaired conidia were observable only in the presence of rad4A after dark incubation exceeding 24 h, implicating extant, but infeasible, NER activity for Rad4A in the field where night (dark) time is too short. Aside from its strong anti-UVB role, Rad4A played no other role in B. bassiana’s lifecycle while Rad4B proved to be functionally redundant. Our findings uncover that the anti-UVB role of Rad4A depends on the photoreactivation activity ascribed to its interaction with Rad23 linked to WC2 and Phr2 and expands a molecular basis underlying filamentous fungal adaptation to solar UV irradiation on the Earth’s surface. Full article

(This article belongs to the Special Issue New Perspectives on Entomopathogenic and Nematode-Trapping Fungi)

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16 pages, 8457 KiB

Open AccessArticle

SNARE Protein AoSec22 Orchestrates Mycelial Growth, Vacuole Assembly, Trap Formation, Stress Response, and Secondary Metabolism in Arthrobotrys oligospora

by Yingmei Zhu, Duanxu Zhou, Na Bai, Qianqian Liu, Na Zhao and Jinkui Yang

J. Fungi 2023, 9(1), 75; https://doi.org/10.3390/jof9010075 - 4 Jan 2023

Cited by 11 | Viewed by 2098

Abstract

Soluble N-ethylmaleimide-sensitive factor attachment protein receptors (SNAREs) facilitate intracellular vesicle trafficking and membrane fusion in eukaryotes and play a vital role in fungal growth, development, and pathogenicity. However, the functions of SNAREs are still largely unknown in nematode-trapping fungi. Arthrobotrys oligospora is a representative species of nematode-trapping fungi that can produce adhesive networks (traps) for nematode predation. In this study, we characterized AoSec22 in A. oligospora, a homolog of the yeast SNARE protein Sec22. Deletion of Aosec22 resulted in remarkable reductions in mycelial growth, the number of nuclei, conidia yield, and trap formation, especially for traps that failed to develop mature three-dimensional networks. Further, absence of Aosec22 impaired fatty acid utilization, autophagy, and stress tolerance; in addition, the vacuoles became small and fragmented in the hyphal cells of the ∆Aosec22 mutant, and large vacuoles failed to form. The reduced sporulation capacity correlated with the transcriptional repression of several sporulation-related genes, and the impaired accumulation of lipid droplets is in line with the transcriptional repression of several genes involved in fatty acid oxidation. Moreover, absence of Aosec22 remarkably impaired secondary metabolism, resulting in 4717 and 1230 compounds upregulated and downregulated in the ∆Aosec22 mutant, respectively. Collectively, our data highlighted that the SNARE protein AoSec22 plays a pleiotropic role in mycelial growth and development, vacuole assembly, lipid metabolism, stress response, and secondary metabolism; in particular, it is required for the proper development of traps in A. oligospora. Full article

(This article belongs to the Special Issue New Perspectives on Entomopathogenic and Nematode-Trapping Fungi)

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11 pages, 1614 KiB

Open AccessArticle

Inhibition of Dopamine Activity and Response of Rhipicephalus microplus Challenged with Metarhizium anisopliae

by Victória Silvestre Bório, Thaís Almeida Corrêa, Jéssica Fiorotti, Emily Mesquita, Laura Nóbrega Meirelles, Mariana Guedes Camargo, Vânia Rita Elias Pinheiro Bittencourt and Patrícia Silva Golo

J. Fungi 2022, 8(12), 1312; https://doi.org/10.3390/jof8121312 - 17 Dec 2022

Viewed by 1713

Abstract

Dopamine modulates ticks and insect hemocytes and links these arthropods’ nervous and immune systems. For the first time, the present study analyzed the effect of a dopamine receptor antagonist on the survival, biological parameters, phagocytic index, and dopamine detection in the hemocytes of ticks challenged by Metarhizium anisopliae. The survival and egg production index of Rhipicephalus microplus were negatively impacted when ticks were inoculated with the antagonist and fungus. Five days after the treatment, the survival of ticks treated only with fungus was 2.2 times higher than ticks treated with the antagonist (highest concentration) and fungus. A reduction in the phagocytic index of hemocytes of 68.4% was observed in the group inoculated with the highest concentration of the antagonist and fungus compared to ticks treated only with fungus. No changes were detected in the R. microplus levels of intrahemocytic dopamine or hemocytic quantification. Our results support the hypothesis that dopamine is crucial for tick immune defense, changing the phagocytic capacity of hemocytes and the susceptibility of ticks to entomopathogenic fungi. Full article

(This article belongs to the Special Issue New Perspectives on Entomopathogenic and Nematode-Trapping Fungi)

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20 pages, 6216 KiB

Open AccessArticle

The Multifaceted Gene 275 Embedded in the PKS-PTS Gene Cluster Was Involved in the Regulation of Arthrobotrisin Biosynthesis, TCA Cycle, and Septa Formation in Nematode-Trapping Fungus Arthrobotrys oligospora

by Jiao Zhou, Qun-Fu Wu, Shu-Hong Li, Jun-Xian Yan, Li Wu, Qian-Yi Cheng, Zhi-Qiang He, Xu-Tong Yue, Ke-Qin Zhang, Long-Long Zhang and Xue-Mei Niu

J. Fungi 2022, 8(12), 1261; https://doi.org/10.3390/jof8121261 - 29 Nov 2022

Cited by 6 | Viewed by 2101

Abstract

The predominant nematode-trapping fungus Arthrobotrys oligospora harbors a unique polyketide synthase-prenyltransferase (PKS-PTS) gene cluster AOL_s00215g responsible for the biosynthesis of sesquiterpenyl epoxy-cyclohexenoids (SECs) that are involved in the regulation of fungal growth, adhesive trap formation, antibacterial activity, and soil colonization. However, the function of one rare gene (AOL_s00215g275 (275)) embedded in the cluster has remained cryptic. Here, we constructed two mutants with the disruption of 275 and the overexpression of 275, respectively, and compared their fungal growth, morphology, resistance to chemical stress, nematicidal activity, transcriptomic and metabolic profiles, and infrastructures, together with binding affinity analysis. Both mutants displayed distinct differences in their TCA cycles, SEC biosynthesis, and endocytosis, combined with abnormal mitochondria, vacuoles, septa formation, and decreased nematicidal activity. Our results suggest that gene 275 might function as a separator and as an integrated gene with multiple potential functions related to three distinct genes encoding the retinoic acid induced-1, cortactin, and vacuolar iron transporter 1 proteins in this nematode-trapping fungus. Our unexpected findings provide insight into the intriguing organization and functions of a rare non-biosynthetic gene in a biosynthetic gene cluster. Full article

(This article belongs to the Special Issue New Perspectives on Entomopathogenic and Nematode-Trapping Fungi)

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