Seogchan Kang’s research while affiliated with Pennsylvania State University and other places

Mass extinction has often paved the way for rapid evolutionary radiation, resulting in the emergence of diverse taxa within specific lineages. The emergence and diversification of carnivorous nematode-trapping fungi (NTF) in Ascomycota have been linked to the Permian-Triassic (PT) extinction, but the processes underlying NTF radiation remain unclear. We conducted phylogenomic analyses using 23 genomes that represent three NTF lineages, each employing distinct nematode traps—mechanical traps (Drechslerella spp.), three-dimensional (3D) adhesive traps (Arthrobotrys spp.), and two-dimensional (2D) adhesive traps (Dactylellina spp.), and the genome of one non-NTF species as the outgroup. These analyses revealed multiple mechanisms that likely contributed to the tempo of the NTF evolution and rapid radiation. The species tree of NTFs based on 2,944 single-copy orthologous genes suggested that Drechslerella emerged earlier than Arthrobotrys and Dactylellina. Extensive genome-wide phylogenetic discordance was observed, mainly due to incomplete lineage sorting (ILS) between lineages. Two modes of non-vertical evolution (introgression and horizontal gene transfer) also contributed to phylogenetic discordance. The ILS genes that are associated with hyphal growth and trap morphogenesis (e.g., those associated with the cell membrane system and polarized cell division) exhibited signs of positive selection. IMPORTANCE By conducting a comprehensive phylogenomic analysis of 23 genomes across three NTF lineages, the research reveals how diverse evolutionary mechanisms, including ILS and non-vertical evolution (introgression and horizontal gene transfer), contribute to the swift diversification of NTFs. These findings highlight the complex evolutionary dynamics that drive the rapid radiation of NTFs, providing valuable insights into the processes underlying their diversity and adaptation.

Diverse volatile organic compounds (VOCs) perform functions crucial for plant growth and health. However, studies on the nature and mechanisms of action of bioactive VOCs, except those mediating plant-insect interactions, lag considerably behind those on waterborne compounds. We built the Plant-Associated VOC Database (PVD) to facilitate research on VOCs released by plants and plant-associated microbes. This platform presents the physicochemical characteristics, biosynthetic pathways, and known or hypothesized functions of VOCs. We present the design, utility, and planned expansion of PVD. [Formula: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license .

Background Soybean cyst nematodes (SCN) as animal parasites of plants are not usually interested in killing the host but are rather focused on completing their life cycle to increase population, resulting in substantial yield losses. Remarkably, some agricultural soils after long-term crop monoculture show a significant decline in SCN densities and suppress disease in a sustainable and viable manner. However, relatively little is known about the microbes and mechanisms operating against SCN in such disease-suppressive soils. Results Greenhouse experiments showed that suppressive soils (S) collected from two provinces of China and transplantation soils (CS, created by mixing 10% S with 90% conducive soils) suppressed SCN. However, SCN suppressiveness was partially lost or completely abolished when S soils were treated with heat (80 °C) and formalin. Bacterial community analysis revealed that the specific suppression in S and CS was mainly associated with the bacterial phylum Bacteroidetes, specifically due to the enrichment of Chitinophaga spp. and Dyadobacter sp., in the cysts. SCN cysts colonized by Chitinophaga spp. showed dramatically reduced egg hatching, with unrecognizable internal body organization of juveniles inside the eggshell due to chitinase activity. Whereas, Dyadobacter sp. cells attached to the surface coat of J2s increased soybean resistance against SCN by triggering the expression of defence-associated genes. The disease-suppressive potential of these bacteria was validated by inoculating them into conducive soil. The Dyadobacter strain alone or in combination with Chitinophaga strains significantly decreased egg densities after one growing cycle of soybeans. In contrast, Chitinophaga strains alone required more than one growing cycle to significantly reduce SCN egg hatching and population density. Conclusion This study revealed how soybean monoculture for decades induced microbiota homeostasis, leading to the formation of SCN-suppressive soil. The high relative abundance of antagonistic bacteria in the cyst suppressed the SCN population both directly and indirectly. Because uncontrolled proliferation will likely lead to quick demise due to host population collapse, obligate parasites like SCN may have evolved to modulate virulence/proliferation to balance these conflicting needs. BVs6NXuQzznnTv7j41Q5n6Video Abstract

Chemical pesticides help reduce crop loss during production and storage. However, the carbon footprints and ecological costs associated with this strategy are unsustainable. Here, we used three in vitro models to characterize how different Trichoderma species interact with two aflatoxin producers, Aspergillus flavus and Aspergillus parasiticus, to help develop a climate-resilient biological control strategy against aflatoxigenic Aspergillus species. The growth rate of Trichoderma species is a critical factor in suppressing aflatoxigenic strains via physical interactions. The dual plate assay suggests that Trichoderma mainly suppresses A. flavus via antibiosis, whereas the suppression of A. parasiticus occurs through mycoparasitism. Volatile organic compounds (VOCs) produced by Trichoderma inhibited the growth of A. parasiticus (34.6 ± 3.3%) and A. flavus (20.9 ± 1.6%). The VOCs released by T. asperellum BTU and T. harzianum OSK-34 were most effective in suppressing A. flavus growth. Metabolites secreted by T. asperellum OSK-38, T. asperellum BTU, T. virens OSK-13, and T. virens OSK-36 reduced the growth of both aflatoxigenic species. Overall, T. asperellum BTU was the most effective at suppressing the growth and aflatoxin B1 production of both species across all models. This work will guide efforts to screen for effective biological control agents to mitigate aflatoxin accumulation.

Nematode-trapping fungi (NTF), most of which belong to a monophyletic lineage in Ascomycota, cannibalize nematodes and other microscopic animals, raising questions regarding the types and mechanisms of genomic changes that enabled carnivorism and adaptation to the carbon-rich and nitrogen-poor environment created by the Permian-Triassic extinction event. Here, we conducted comparative genomic analyses of 21 NTF and 21 non-NTF to address these questions. Carnivorism-associated changes include expanded genes for nematode capture, infection, and consumption (e.g., adhesive proteins, CAP superfamily, eukaryotic aspartyl proteases, and serine-type peptidases). Although the link between secondary metabolite (SM) production and carnivorism remains unclear, we found that the numbers of SM gene clusters among NTF are significantly lower than those among non-NTF. Significantly expanded cellulose degradation gene families (GH5, GH7, AA9, and CBM1) and contracted genes for carbon-nitrogen hydrolases (enzymes that degrade organic nitrogen to ammonia) are likely associated with adaptation to the carbon-rich and nitrogen-poor environment. Through horizontal gene transfer events from bacteria, NTF acquired the Mur gene cluster (participating in synthesizing peptidoglycan of the bacterial cell wall) and Hyl (a virulence factor in animals). Disruption of MurE reduced NTF's ability to attract nematodes, supporting its role in carnivorism. This study provides new insights into how NTF evolved and diversified after the Permian-Triassic mass extinction event.

Mass extinction has often paved the way for rapid evolutionary radiation, resulting in the emergence of diverse taxa within specific lineages. While the emergence and diversification of carnivorous nematode-trapping fungi (NTF) in Ascomycota has been linked to the Permian-Triassic (PT) extinction, the processes underlying NTF radiation remain unclear. Here, we conducted phylogenomic analyses using 23 genomes spanning three NTF lineages, each employing distinct nematode traps - mechanical traps (Drechslerella spp.), three-dimensional (3-D) adhesive traps (Arthrobotrys spp.), and two-dimensional (2-D) adhesive traps (Dactylellina spp.), and one non-NTF species as the outgroup. This analysis revealed how diverse mechanisms contributed to the tempo of NTF evolution and rapid radiation. The genome-scale species tree of NTFs suggested that Drechslerella emerged earlier than Arthrobotrys and Dactylellina. Extensive genome-wide phylogenetic discordance was observed, mainly due to incomplete lineage sorting (ILS) between lineages (~81.3%). Modes of non-vertical evolution (i.e., introgression and horizontal gene transfer) also contributed to phylogenetic discordance. The ILS genes that are associated with hyphal growth and trap morphogenesis (e.g., those associated with the cell membrane system and cellular polarity division) exhibited signs of positive selection.

Trichoderma spp. are widely used to enhance crop growth and suppress diverse diseases. However, inconsistent field efficacy remains a major barrier to their use as a reliable alternative to synthetic pesticides. Various strategies have been investigated to enhance the robustness of their application. Here, we evaluated how T. virens application methods (pre-, at-, and post-transplant) affect the growth of two tomato varieties and their rhizosphere fungal and bacterial communities. Although the greatest rhizosphere abundance of T. virens was observed in the post-transplant application, the at-transplant application promoted tomato growth the most, indicating that greater rhizosphere abundance does not necessarily result in better tomato growth. None of the application methods significantly altered the global rhizosphere fungal and bacterial communities of the tested varieties. Changes in specific microbial genera and guilds may underpin the enhanced tomato growth. We also investigated whether the resulting microbiome changes affect the mycelial growth and conidial germination of Fusarium oxysporum f. sp. lycopersici and F. oxysporum f. sp. radicis-lycopersici , soilborne fungal pathogens of tomato, upon exposure to volatile compounds emitted by culturable rhizosphere microbes and metabolites extracted from the rhizosphere soils after Trichoderma treatments. Volatile compounds produced by cultured rhizosphere microbes after the at-transplant application suppressed the mycelial growth of both pathogens better than those after the other treatments. Similarly, water-soluble metabolites extracted from the rhizosphere soil samples after the at-transplant application most effectively suppressed the germination rate of F. oxysporum spores. Overall, our results suggest that the at-transplant application is most advantageous for promoting the growth of the tested tomato varieties and building soil suppressiveness against the tested fusaria. However, further studies are needed before applying this method to support tomato production. We discuss critical future questions.

Verticillium dahliae is a xylem‐invading fungal pathogen that causes vascular wilt in a wide range of angiosperms. The pathogen uses a variety of virulence factors to invade and colonize its hosts. Here, we report that VdNEP, an NLP (Necrosis and ethylene inducing peptide 1‐Like Protein), functions as one such factor in multiple hosts. Eggplant leaves treated with VdNEP developed necrotic symptoms. Overexpression of VdNEP by incorporating extra copies of the VdNEP gene increased virulence to cotton, eggplant and tomato plants, suggesting its role as a virulence factor in diverse plants. Increased expression of VdNEP among the transformants did not correlate with the number of VdNEP inserts, suggesting that its expression was affected by the genomic context of the insertion sites. Interestingly, a transformant derived from a defoliating strain with high VdNEP transcript levels caused disease symptoms in tomato plants, whereas the corresponding wild‐type strain did not cause visible symptoms. The amount of V . dahliae DNA in plants infected with this VdNEP ‐overexpressing transformant was 22 times higher than that in plants infected with the wild‐type isolate, further supporting the critical role of VdNEP in infection. A VdNEP‐EGFP fusion was constructed to follow its localization in fungal cells and during infection.

Fusion of individual vesicles carrying membrane-building materials with the plasma membrane (PM) enables gradual cell expansion and shape change. Constricting ring (CR) cells of carnivorous fungi triple in size within 0.1-1 s to capture passing nematodes. Here, we investigated how a carnivorous fungus, Drechslerella dactyloides, executes rapid and irreversible PM expansion during CR inflation. During CR maturation, vesicles carrying membrane-building materials accumulate and fuse, forming a structure named the Palisade-shaped Membrane-building Structure (PMS) around the rumen side of ring cells. After CR inflation, the PMS disappears, with partially inflated cells displaying wavy PM and fully inflated cells exhibiting smooth PM, suggesting that the PMS serves as the reservoir for membrane-building materials to enable rapid and extensive PM expansion. The DdSnc1, a v-SNARE protein, accumulates at the inner side of ring cells and is necessary for PMS formation and CR inflation. This study elucidates the unique cellular mechanisms underpinning rapid CR inflation.