Host-Pathogen Interactions: Insects vs Fungi

A special issue of Journal of Fungi (ISSN 2309-608X).

Deadline for manuscript submissions: closed (31 August 2020) | Viewed by 45972

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Guest Editor
Head of Laboratory of Biological Plant Protection and Biotechnology, Novosibirsk State Agrarian University, Dobrolubova Str. 160, 630039 Novosibirsk, Russia
Interests: insect immunity; entomopathogenic fungi; detoxification and antioxidant systems; fungal virulence factors; coevolution of host–parasite systems; microevolution of insect defense reactions; melanization; redox balance
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Dear Colleagues,

Although many insects successfully live in dangerous environments exposed to diverse communities of microbes, they are often exploited and killed by specialist pathogens. In the process of co-evolution of insects and entomopathogenic microorganisms, they develop various adaptive systems that determine the sustainable existence of dynamic host–parasite interactions at both the organismic and population levels. The host defences are designed to exclude the pathogen or mitigate the damage inflicted, while the pathogen counters with immune evasion and utilization of host resources. Entomopathogenic fungi neutralize their immediate surroundings on the insect integument and benefit from the physiochemical properties of the cuticle and its compounds that exclude competing microbes. They interplay host defence with factors which regulate adhesion to the cuticle, cuticle degradation, and stress management. Aspects concerning insects’ immune, detoxification, and antioxidant systems which work synergistically to combat infections and mitigate stress are also of interest. Some proteins demonstrate multifunctional properties, participating in metabolism, homeostasis, and pathogen recognition. This volume will also include studies of host–pathogen interactions with informative approaches (RNAseq, proteomics, RNAi, etc.) that provide valuable insights into the dynamics of the highly aggressive co-evolutionary arms race between entomopathogenic fungi and their arthropod hosts.

Dr. Ivan M. Dubovskiy
Guest Editor

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Keywords

  • entomopathogenic fungi
  • fungus–cuticle dynamics
  • Metarhizium
  • innate immunity
  • fungal virulence
  • pest management

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Published Papers (12 papers)

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Editorial

Jump to: Research, Review

2 pages, 188 KiB  
Editorial
Host–Pathogen Interactions: Insects vs. Fungi
by Ivan M. Dubovskiy
J. Fungi 2021, 7(3), 162; https://doi.org/10.3390/jof7030162 - 24 Feb 2021
Cited by 2 | Viewed by 2043
Abstract
Although many insects successfully live in dangerous environments exposed to diverse communities of microbes, they are often exploited and killed by specialist pathogens [...] Full article
(This article belongs to the Special Issue Host-Pathogen Interactions: Insects vs Fungi)

Research

Jump to: Editorial, Review

19 pages, 2069 KiB  
Article
Screening and Virulence of the Entomopathogenic Fungi Associated with Chilo suppressalis Walker
by Morteza Shahriari, Arash Zibaee, Seyyed Akbar Khodaparast and Mahmoud Fazeli-Dinan
J. Fungi 2021, 7(1), 34; https://doi.org/10.3390/jof7010034 - 7 Jan 2021
Cited by 22 | Viewed by 3529
Abstract
The current study aimed to explore the entomopathogenic fungi associated with the larvae of Chilo suppressalis Walker, a serious pest of rice, in northern Iran. The collected specimens were cultured and identified through morphological and molecular methods. The 38 specimens were identified by [...] Read more.
The current study aimed to explore the entomopathogenic fungi associated with the larvae of Chilo suppressalis Walker, a serious pest of rice, in northern Iran. The collected specimens were cultured and identified through morphological and molecular methods. The 38 specimens were identified by microscopic examination and genetic sequencing of the ITS region as follows: twenty-one isolates of Beauveria bassiana, five isolates of Akanthomyces lecanii, four isolates of Akanthomyces muscarious, three isolates of Metarhizium anisopliae, two isolates of Hirsutella subulata, two isolates of Trichoderma sp. and one isolate of Aspergillus sp. All the identified isolates were treated on the larvae through bioassay, evaluating the amount of hydrophobin and the activities of proteases, chitinases and lipase to find their virulence. Moreover, the percentage of thermotolerant and cold activity of the isolates were tested to determine their environmental persistence. The overall results revealed the isolates of B. bassiana, including BBRR1, BBAL1 and BBLN1 as the most virulent and environmental adaptive isolates among the fungi associated with C. suppressalis. Full article
(This article belongs to the Special Issue Host-Pathogen Interactions: Insects vs Fungi)
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8 pages, 264 KiB  
Article
Fungi Recorded on Folivorous Lepidoptera: High Diversity Despite Moderate Prevalence
by Robin Gielen, Hendrik Meister, Toomas Tammaru and Kadri Põldmaa
J. Fungi 2021, 7(1), 25; https://doi.org/10.3390/jof7010025 - 5 Jan 2021
Cited by 5 | Viewed by 2046
Abstract
The knowledge about the diversity and ecological role of entomopathogenic fungi is primarily based on agroecosystems whereas information derived from natural insect populations is much more limited. To contribute to filling this gap, we recorded the prevalence of fungal infections in laboratory rearing [...] Read more.
The knowledge about the diversity and ecological role of entomopathogenic fungi is primarily based on agroecosystems whereas information derived from natural insect populations is much more limited. To contribute to filling this gap, we recorded the prevalence of fungal infections in laboratory rearing experiments with five species of Lepidoptera, and in a field rearing experiment including one of these moths. The diversity of detected fungi was found to be high; we isolated 25 species of fungi from insects that had died in the course of these experiments. Six species belonged to the family Cordycipitaceae known to include unambiguous insect pathogens. The trophic niche of the representatives of other taxa is less clear and requires further studies. Regarding the most abundant species, Cordyceps farinosa, in which this question could be addressed, there was no indication of specialization on particular insect hosts, whereas several of the less common species may have been recorded from lepidopteran hosts for the first time. Across the subsets of the data, the prevalence of fungal infections generally remained below 5%. Our results are thus consistent with the idea that entomopathogenic fungi are always present in insect populations but rarely reach epizootic levels. The detected species richness shows that much is to be gained from mapping the diversity of fungal species associated with folivorous insects in natural populations. Full article
(This article belongs to the Special Issue Host-Pathogen Interactions: Insects vs Fungi)
10 pages, 2639 KiB  
Communication
Low Efficacy of Isaria fumosorosea against Box Tree Moth Cydalima perspectalis: Are Host Plant Phytochemicals Involved in Herbivore Defence against Fungal Pathogens?
by Rostislav Zemek, Jana Konopická and Zain Ul Abdin
J. Fungi 2020, 6(4), 342; https://doi.org/10.3390/jof6040342 - 6 Dec 2020
Cited by 14 | Viewed by 4462
Abstract
Buxus sp. is an important native and ornamental tree in Europe threatened by a serious invasive pest Cydalima perspectalis. The larvae of this moth are able to defoliate box trees and cause their death. The development of novel biopesticides targeting this pest [...] Read more.
Buxus sp. is an important native and ornamental tree in Europe threatened by a serious invasive pest Cydalima perspectalis. The larvae of this moth are able to defoliate box trees and cause their death. The development of novel biopesticides targeting this pest might help protect Buxus trees grown wildly or in city parks. Laboratory experiments were conducted to assess the efficacy of entomopathogenic fungus Isaria fumosorosea strain CCM 8367 against C. perspectalis. The last-instar larvae of the box tree moth were treated by the suspension of fungus conidia at concentrations ranging from 1 × 104 to 1 × 108 spores per 1 mL. Fungus infection was observed mostly in pupae, but the maximum mortality did not exceed 60%, indicating a very low susceptibility of C. perspectalis to I. fumosorosea. Furthermore, a number of ungerminated fungal conidia were found on larval cuticles using a low-temperature scanning electron microscopy. Our data also reveal that the hydroalcoholic extract from B. sempervirens leaves significantly inhibits both the germination of I. fumosorosea conidia and fungus growth. It can be speculated that the strain CCM 8367 of I. fumosorosea is not a potent biocontrol agent against C. perspectalis and low virulence of the fungus might be due to the accumulation of host plant phytochemicals having antimicrobial activity in larval cuticle of the pest. Full article
(This article belongs to the Special Issue Host-Pathogen Interactions: Insects vs Fungi)
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8 pages, 774 KiB  
Article
Effect of Juvenile Hormone on Resistance against Entomopathogenic Fungus Metarhizium robertsii Differs between Sexes
by Markus J. Rantala, Ivan M. Dubovskiy, Mari Pölkki, Tatjana Krama, Jorge Contreras-Garduño and Indrikis A. Krams
J. Fungi 2020, 6(4), 298; https://doi.org/10.3390/jof6040298 - 19 Nov 2020
Cited by 12 | Viewed by 2607
Abstract
Juvenile hormone has been suggested to be a potential mediator in the trade-off between mating and insects’ immunity. Studies on various insect taxons have found that juvenile hormone interferes with humoral and cellular immunity. Although this was shown experimentally, studies using highly virulent [...] Read more.
Juvenile hormone has been suggested to be a potential mediator in the trade-off between mating and insects’ immunity. Studies on various insect taxons have found that juvenile hormone interferes with humoral and cellular immunity. Although this was shown experimentally, studies using highly virulent parasites or pathogens are lacking so far. In this study, we tested if juvenile hormone administration affected resistance against entomopathogenic fungi, Metarhizium robertsii, in the mealworm beetle, Tenebrio molitor. In previous studies with T. molitor, juvenile hormone has been found to reduce a major humoral immune effector-system (phenoloxidase) in both sexes and decrease the encapsulation response in males. Here, we found that juvenile hormone administration prolonged survival time after infection with M. robertsii in males but reduced survival time in females. This study indicates that the effects of juvenile hormone on insect immunity might be more complicated than previously considered. We also suggest that there might be a trade-off between specific and non-specific immunity since, in males, juvenile hormone enhances specific immunity but corrupts non-specific immunity. Our study highlights the importance of using real parasites and pathogens in immuno-ecological studies. Full article
(This article belongs to the Special Issue Host-Pathogen Interactions: Insects vs Fungi)
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14 pages, 2364 KiB  
Article
Insights into the Gryllus bimaculatus Immune-Related Transcriptomic Profiling to Combat Naturally Invading Pathogens
by Abid Hussain, Muhammad Waqar Ali, Ahmed Mohammed AlJabr and Saad Naser AL-Kahtani
J. Fungi 2020, 6(4), 232; https://doi.org/10.3390/jof6040232 - 18 Oct 2020
Cited by 6 | Viewed by 2986
Abstract
Natural pathogen pressure is an important factor that shapes the host immune defense mechanism. The current study primarily aimed to explore the molecular basis of the natural immune defense mechanism of a sporadic pest, Gryllus bimaculatus, during swarming by constructing cDNA libraries [...] Read more.
Natural pathogen pressure is an important factor that shapes the host immune defense mechanism. The current study primarily aimed to explore the molecular basis of the natural immune defense mechanism of a sporadic pest, Gryllus bimaculatus, during swarming by constructing cDNA libraries of the female mid-gut, male mid-gut, testes, and ovaries. The Illumina HiSeq platform generated an average of 7.9 G, 11.77 G, 10.07 G, and 10.07 G bases of outputs from the male mid-gut, female mid-gut, testes, and ovaries and libraries, respectively. The transcriptome of two-spotted field crickets was assembled into 233,172 UniGenes, which yielded approximately 163.58 million reads. On the other hand, there were 43,055 genes in common that were shared among all the biological samples. Gene Ontology analysis successfully annotated 492 immune-related genes, which comprised mainly Pattern Recognition Receptors (62 genes), Signal modulators (57 genes), Signal transduction (214 genes), Effectors (36 genes), and another immune-related 123 genes. In summary, the identified wide range of immune-related genes from G. bimaculatus indicates the existence of a sophisticated and specialized broad spectrum immune mechanism against invading pathogens, which provides, for the first time, insights into the molecular mechanism of disease resistance among two-spotted field crickets. Full article
(This article belongs to the Special Issue Host-Pathogen Interactions: Insects vs Fungi)
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13 pages, 2005 KiB  
Article
Isolation of Beauveria bassiana from the Chagas Disease Vector Triatoma infestans in the Gran Chaco Region of Argentina: Assessment of Gene Expression during Host–Pathogen Interaction
by Linda Vanesa Baldiviezo, Nicolás Pedrini, Marianela Santana, María Constanza Mannino, Lucía Beatriz Nieva, Alberto Gentile and Rubén Marino Cardozo
J. Fungi 2020, 6(4), 219; https://doi.org/10.3390/jof6040219 - 12 Oct 2020
Cited by 12 | Viewed by 2990
Abstract
A native strain of the entomopathogenic fungus Beauveria bassiana (Bb-C001) was isolated from a naturally infected Triatoma infestans, Klug (Hemiptera: Reduviidae) adult cadaver in the Gran Chaco region, Salta province, Argentina. The isolate was both phenotypic and molecularly characterized in a context [...] Read more.
A native strain of the entomopathogenic fungus Beauveria bassiana (Bb-C001) was isolated from a naturally infected Triatoma infestans, Klug (Hemiptera: Reduviidae) adult cadaver in the Gran Chaco region, Salta province, Argentina. The isolate was both phenotypic and molecularly characterized in a context of fungus-insect interaction, by measuring the expression pattern of toxin genes during infection and immune response of T. infestans. The commercial strain GHA of B. bassiana, which was previously used in field interventions to control these vectors, was used as reference in this study. The phylogenetic trees based on both ribosomal internal transcribed spacer (ITS) and elongation factor 1-alpha (EF1-α) indicated that Bb-C001 fits into a B. bassiana cluster, and the sequence-characterized amplified regions (SCAR) showed that Bb-C001 is different from the GHA strain. There were no differences between both strains regarding viability, radial growth, and conidia production, either in the median survival time or insect mortality. However, Bb-C001 showed a higher expression than GHA of the bassianolide synthetase gene (BbbslS) during infection, and similar levels of the beauvericin synthetase gene (BbbeaS). Immune-related genes of T. infestans nymphs (limpet-2 and defensin-1, -2, and -6) were later expressed and thus insects failed to stop the infection process. These results showed that B. bassiana Bb-C001 is a promised fungal strain to be incorporated in the current biological control programs of T. infestans in Salta province, Argentina. Full article
(This article belongs to the Special Issue Host-Pathogen Interactions: Insects vs Fungi)
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14 pages, 9091 KiB  
Article
Target Activity of Isaria tenuipes (Hypocreales: Clavicipitaceae) Fungal Strains against Dengue Vector Aedes aegypti (Linn.) and Its Non-Target Activity Against Aquatic Predators
by Sengodan Karthi, Prabhakaran Vasantha-Srinivasan, Raja Ganesan, Venkatachalam Ramasamy, Sengottayan Senthil-Nathan, Hanem F. Khater, Narayanaswamy Radhakrishnan, Kesavan Amala, Tae-Jin Kim, Mohamed A. El-Sheikh and Patcharin Krutmuang
J. Fungi 2020, 6(4), 196; https://doi.org/10.3390/jof6040196 - 29 Sep 2020
Cited by 27 | Viewed by 3028
Abstract
The present investigation aimed to determine the fungal toxicity of Isaria tenuipes (My-It) against the dengue mosquito vector Aedes aegypti L. and its non-target impact against the aquatic predator Toxorhynchitessplendens. Lethal concentrations (LC50 and LC90) of My-It were [...] Read more.
The present investigation aimed to determine the fungal toxicity of Isaria tenuipes (My-It) against the dengue mosquito vector Aedes aegypti L. and its non-target impact against the aquatic predator Toxorhynchitessplendens. Lethal concentrations (LC50 and LC90) of My-It were observed in 2.27 and 2.93 log ppm dosages, respectively. The sub-lethal dosage (My-It-1 × 104 conidia/mL) displayed a significant oviposition deterrence index and also blocked the fecundity rate of dengue mosquitos in a dose-dependent manner. The level of major detoxifying enzymes, such as carboxylesterase (α-and β-) and SOD, significantly declined in both third and fourth instar larvae at the maximum dosage of My-It 1 × 105 conidia/mL. However, the level of glutathione S-transferase (GST) and cytochrome P-450 (CYP450) declined steadily when the sub-lethal dosage was increased and attained maximum reduction in the enzyme level at the dosage of My-It (1 × 105 conidia/mL). Correspondingly, the gut-histology and photomicrography results made evident that My-It (1 × 105 conidia/mL) heavily damaged the internal gut cells and external physiology of the dengue larvae compared to the control. Moreover, the non-target toxicity against the beneficial predator revealed that My-It at the maximum dosage (1 × 1020 conidia/mL) was found to be less toxic with <45% larval toxicity against Tx.splendens. Thus, the present toxicological research on Isaria tenuipes showed that it is target-specific and a potential agent for managing medically threatening arthropods. Full article
(This article belongs to the Special Issue Host-Pathogen Interactions: Insects vs Fungi)
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14 pages, 7578 KiB  
Article
MrHex1 is Required for Woronin Body Formation, Fungal Development and Virulence in Metarhizium robertsii
by Guirong Tang, Yanfang Shang, Shiqing Li and Chengshu Wang
J. Fungi 2020, 6(3), 172; https://doi.org/10.3390/jof6030172 - 14 Sep 2020
Cited by 17 | Viewed by 3473
Abstract
The Woronin body (WB) is a peroxisome-derived dense-core vesicle, a self-assembling hexagonal crystal of a single protein Hex1. This organelle is specific to the ascomycete fungi belonging to the Pezizomycotina subphylum by functioning in sealing septal pores in response to mycelium damage and [...] Read more.
The Woronin body (WB) is a peroxisome-derived dense-core vesicle, a self-assembling hexagonal crystal of a single protein Hex1. This organelle is specific to the ascomycete fungi belonging to the Pezizomycotina subphylum by functioning in sealing septal pores in response to mycelium damage and the control of cell heterogeneity. We retrieved all available Hex1-domain containing proteins of different fungi from the GenBank database and found considerable length variations among 460 obtained Hex1 proteins. However, a highly conserved Hex1 domain containing 75 amino acid residues with a specific S/A-R/S-L consensus motif for targeting peroxisome is present at the carboxy-terminus of each protein. A homologous Hex1 gene, named MrHex1, was deleted in the entomopathogenic fungus Metarhizium robertsii. It was found that MrHex1 was responsible for WB formation in M. robertsii and involved in sealing septal pores to maintain cell integrity and heterogeneity. Different assays indicated that, relative to the wild-type (WT) strain, ∆Mrhex1 demonstrated a growth defect on a solid medium and substantial reductions of conidiation, appressorium formation and topical infectivity against insect hosts. However, there was no obvious virulence difference between WT and mutants during injection of insects. We also found that ∆MrHex1 could tolerate different stress conditions like the WT and the gene-rescued mutant of M. robertsii, which is in contrast to the reports of the stress-response defects of the Hex1 null mutants of other fungal species. In addition to revealing the phenotypic/functional alterations of the Hex1 deletion mutants between different pathotype fungi, the results of this study may benefit the understanding of the evolution and WB-control of fungal entomopathogenicity. Full article
(This article belongs to the Special Issue Host-Pathogen Interactions: Insects vs Fungi)
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20 pages, 4063 KiB  
Article
Interplay between Fungal Infection and Bacterial Associates in the Wax Moth Galleria mellonella under Different Temperature Conditions
by Vadim Yu Kryukov, Elena Kosman, Oksana Tomilova, Olga Polenogova, Ulyana Rotskaya, Maksim Tyurin, Tatyana Alikina, Olga Yaroslavtseva, Marsel Kabilov and Viktor Glupov
J. Fungi 2020, 6(3), 170; https://doi.org/10.3390/jof6030170 - 10 Sep 2020
Cited by 19 | Viewed by 4087
Abstract
Various insect bacterial associates are involved in pathogeneses caused by entomopathogenic fungi. The outcome of infection (fungal growth or decomposition) may depend on environmental factors such as temperature. The aim of this study was to analyze the bacterial communities and immune response of [...] Read more.
Various insect bacterial associates are involved in pathogeneses caused by entomopathogenic fungi. The outcome of infection (fungal growth or decomposition) may depend on environmental factors such as temperature. The aim of this study was to analyze the bacterial communities and immune response of Galleria mellonella larvae injected with Cordyceps militaris and incubated at 15 °C and 25 °C. We examined changes in the bacterial CFUs, bacterial communities (Illumina MiSeq 16S rRNA gene sequencing) and expression of immune, apoptosis, ROS and stress-related genes (qPCR) in larval tissues in response to fungal infection at the mentioned temperatures. Increased survival of larvae after C. militaris injection was observed at 25 °C, although more frequent episodes of spontaneous bacteriosis were observed at this temperature compared to 15 °C. We revealed an increase in the abundance of enterococci and enterobacteria in the midgut and hemolymph in response to infection at 25 °C, which was not observed at 15 °C. Antifungal peptide genes showed the highest expression at 25 °C, while antibacterial peptides and inhibitor of apoptosis genes were strongly expressed at 15 °C. Cultivable bacteria significantly suppressed the growth of C. militaris. We suggest that fungi such as C. militaris may need low temperatures to avoid competition with host bacterial associates. Full article
(This article belongs to the Special Issue Host-Pathogen Interactions: Insects vs Fungi)
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16 pages, 11429 KiB  
Article
Effectiveness of the Entomopathogenic Fungal Species Metarhizium anisopliae Strain NCAIM 362 Treatments against Soil Inhabiting Melolontha melolontha Larvae in Sweet Potato (Ipomoea batatas L.)
by Barna Putnoky-Csicsó, Szende Tonk, Attila Szabó, Zsuzsanna Márton, Franciska Tóthné Bogdányi, Ferenc Tóth, Éva Abod, János Bálint and Adalbert Balog
J. Fungi 2020, 6(3), 116; https://doi.org/10.3390/jof6030116 - 22 Jul 2020
Cited by 10 | Viewed by 3084
Abstract
The effect of fungal entomopathogen M. anisopliae strain NCAIM 362 against M. melolontha larvae in sweet potato was tested under open field conditions when crop management included compost supply and soil cover (agro-foil or agro-textile). Additionally, the effect of M. anisopliae same strain [...] Read more.
The effect of fungal entomopathogen M. anisopliae strain NCAIM 362 against M. melolontha larvae in sweet potato was tested under open field conditions when crop management included compost supply and soil cover (agro-foil or agro-textile). Additionally, the effect of M. anisopliae same strain against M. melolontha was compared with the effect of α-cypermethrin under greenhouse conditions. Soil microbial community using Illumina sequencing and soil biological activity were tested as possible parameter influencing M. anisopliae effect. According to the results, compost supply and textile cover may enhance the effectiveness of M. anisopliae under open field conditions, while no effect of fungal treatment was detected under greenhouse conditions. Even if soil parameters (chemical composition, bacterial, and biological activity) were identical, the effect of α-cypermethrin against M. melolontha larvae was significant: lower ratio of larval survival and less damaged tubers were detected after the chemical treatment. Our results suggest that M. anisopliae strain NCAIM 362 is not effective to control M. melolontha larvae, further pieces of research are needed to test other species of the Metarhizium genus to find an effective agent for sustainable pest control in sweet potato. Full article
(This article belongs to the Special Issue Host-Pathogen Interactions: Insects vs Fungi)
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Review

Jump to: Editorial, Research

24 pages, 708 KiB  
Review
Fungi–Nematode Interactions: Diversity, Ecology, and Biocontrol Prospects in Agriculture
by Ying Zhang, Shuoshuo Li, Haixia Li, Ruirui Wang, Ke-Qin Zhang and Jianping Xu
J. Fungi 2020, 6(4), 206; https://doi.org/10.3390/jof6040206 - 4 Oct 2020
Cited by 97 | Viewed by 10384
Abstract
Fungi and nematodes are among the most abundant organisms in soil habitats. They provide essential ecosystem services and play crucial roles for maintaining the stability of food-webs and for facilitating nutrient cycling. As two of the very abundant groups of organisms, fungi and [...] Read more.
Fungi and nematodes are among the most abundant organisms in soil habitats. They provide essential ecosystem services and play crucial roles for maintaining the stability of food-webs and for facilitating nutrient cycling. As two of the very abundant groups of organisms, fungi and nematodes interact with each other in multiple ways. Here in this review, we provide a broad framework of interactions between fungi and nematodes with an emphasis on those that impact crops and agriculture ecosystems. We describe the diversity and evolution of fungi that closely interact with nematodes, including food fungi for nematodes as well as fungi that feed on nematodes. Among the nematophagous fungi, those that produce specialized nematode-trapping devices are especially interesting, and a great deal is known about their diversity, evolution, and molecular mechanisms of interactions with nematodes. Some of the fungi and nematodes are significant pathogens and pests to crops. We summarize the ecological and molecular mechanisms identified so far that impact, either directly or indirectly, the interactions among phytopathogenic fungi, phytopathogenic nematodes, and crop plants. The potential applications of our understanding to controlling phytophagous nematodes and soilborne fungal pathogens in agricultural fields are discussed. Full article
(This article belongs to the Special Issue Host-Pathogen Interactions: Insects vs Fungi)
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