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Fungal Endophytes in Agriculture and Ecosystems

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A special issue of Journal of Fungi (ISSN 2309-608X). This special issue belongs to the section "Environmental and Ecological Interactions of Fungi".

Deadline for manuscript submissions: closed (30 September 2020) | Viewed by 40881

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Special Issue Editors

Prof. Dr. Trevor R. Hodkinson

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Guest Editor

Botany, School of Natural Sciences, Trinity College Dublin, The University of Dublin, Dublin D2, Ireland
Interests: fungal endophytes; grasses; systematics; agriculture; genetic resources; forest trees

Dr. Brian R. Murphy

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Guest Editor

Special Issue Information

Dear Colleagues,

This Special Issue will explore the diversity and role of fungal endophytes in ecosystems and how such knowledge can be applied to agriculture, forestry, and the environment. Endophytic fungi include any fungus living within any part of the plant, including mycorrhizal symbionts. Topics relating to agriculture will include production, sustainability, biocontrol, integrated pest management, and stress resistance. Wider environmental roles of fungal endophytes in ecosystems will also be explored, including applications in phytoremediation and forestry. Interactions of endophytic fungi with other microorganisms in the phytobiome will be covered, including bacterial, protist and soil microfauna.

Prof. Dr. Trevor R. Hodkinson
Dr. Brian R. Murphy
Guest Editors

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Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Journal of Fungi is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2600 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

agriculture
biocontrol
ecosystems
endophyte
environment
forestry
mycorrhizae
paleobiology
phytoremediation
phytobiome

Published Papers (14 papers)

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16 pages, 904 KiB

Open AccessArticle

Assessing Genotypic and Environmental Effects on Endophyte Communities of Fraxinus (Ash) Using Culture Dependent and Independent DNA Sequencing

by Anindita Lahiri, Brian R. Murphy and Trevor R. Hodkinson

J. Fungi 2021, 7(7), 565; https://doi.org/10.3390/jof7070565 - 15 Jul 2021

Cited by 8 | Viewed by 2616

Abstract

Fraxinus excelsior populations are in decline due to the ash dieback disease Hymenoscyphus fraxineus. It is important to understand genotypic and environmental effects on its fungal microbiome to develop disease management strategies. To do this, we used culture dependent and culture independent approaches to characterize endophyte material from contrasting ash provenances, environments, and tissues (leaves, roots, seeds). Endophytes were isolated and identified using nrITS, LSU, or tef DNA loci in the culture dependent assessments, which were mostly Ascomycota and assigned to 37 families. Few taxa were shared between roots and leaves. The culture independent approach used high throughput sequencing (HTS) of nrITS amplicons directly from plant DNA and detected 35 families. Large differences were found in OTU diversity and community composition estimated by the contrasting approaches and these data need to be combined for estimations of the core endophyte communities. Species richness and Shannon index values were highest for the leaf material and the French population. Few species were shared between seed and leaf tissue. PCoA and NMDS of the HTS data showed that seed and leaf microbiome communities were highly distinct and that there was a strong influence of Fraxinus species identity on their fungal community composition. The results will facilitate a better understanding of ash fungal ecology and are a step toward identifying microbial biocontrol systems to minimize the impact of the disease. Full article

(This article belongs to the Special Issue Fungal Endophytes in Agriculture and Ecosystems)

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15 pages, 1026 KiB

Open AccessArticle

Hidden Fungi: Combining Culture-Dependent and -Independent DNA Barcoding Reveals Inter-Plant Variation in Species Richness of Endophytic Root Fungi in Elymus repens

by Anna K. Høyer and Trevor R. Hodkinson

J. Fungi 2021, 7(6), 466; https://doi.org/10.3390/jof7060466 - 09 Jun 2021

Cited by 7 | Viewed by 2739

Abstract

The root endophyte community of the grass species Elymus repens was investigated using both a culture-dependent approach and a direct amplicon sequencing method across five sites and from individual plants. There was much heterogeneity across the five sites and among individual plants. Focusing on one site, 349 OTUs were identified by direct amplicon sequencing but only 66 OTUs were cultured. The two approaches shared ten OTUs and the majority of cultured endophytes do not overlap with the amplicon dataset. Media influenced the cultured species richness and without the inclusion of 2% MEA and full-strength MEA, approximately half of the unique OTUs would not have been isolated using only PDA. Combining both culture-dependent and -independent methods for the most accurate determination of root fungal species richness is therefore recommended. High inter-plant variation in fungal species richness was demonstrated, which highlights the need to rethink the scale at which we describe endophyte communities. Full article

(This article belongs to the Special Issue Fungal Endophytes in Agriculture and Ecosystems)

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12 pages, 502 KiB

Open AccessArticle

Investigating Host Preference of Root Endophytes of Three European Tree Species, with a Focus on Members of the Phialocephala fortinii—Acephala applanata Species Complex (PAC)

by Sophie Stroheker, Vivanne Dubach, Irina Vögtli and Thomas N. Sieber

J. Fungi 2021, 7(4), 317; https://doi.org/10.3390/jof7040317 - 19 Apr 2021

Cited by 9 | Viewed by 2182

Abstract

Host preference of root endophytes of the three European tree species of Norway spruce (Picea abies), common ash (Fraxinus excelsior), and sycamore maple (Acer pseudoplatanus) were investigated in two forest stands near Zurich, Switzerland. The focus was placed on members of the Phialocephala fortinii s.l. (sensu lato)—Acephala applanata species complex (PAC), as well as other dark septate endopyhtes (DSE). PAC species were identified based on 13 microsatellite loci. Eleven PAC species were found, with Phialocephala helvetica, P. europaea being the most frequent. All but cryptic species 12 (CSP12) preferred Norway spruce as a host. Though very rare in general, CSP12 was most frequently isolated from maple roots. Regarding the abundant PAC species, P. helvetica and P. europaea, the preference of spruce as a host was least pronounced in P. europaea, as it was also often isolated from ash and maple. It is the first record of PAC found on common ash (Fraxinus excelsior). Cadophora orchidicola, a close relative of PAC, has frequently been isolated from ash. Various species of the Nectriaceae (Cylindrocarpon spp.) have often been isolated, particularly from maple roots. By comparison, Pezicula spp. (Cryptosporiopsis spp.) was found to be abundant on all three hosts. Phomopsis phaseoli exhibits a clear preference for spruce. Full article

(This article belongs to the Special Issue Fungal Endophytes in Agriculture and Ecosystems)

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14 pages, 1278 KiB

Open AccessArticle

Beauveria bassiana Endophytic Strain as Plant Growth Promoter: The Case of the Grape Vine Vitis vinifera

by Spiridon Mantzoukas, Ioannis Lagogiannis, Dionusia Mpousia, Aristeidis Ntoukas, Katerina Karmakolia, Panagiotis A. Eliopoulos and Konstantinos Poulas

J. Fungi 2021, 7(2), 142; https://doi.org/10.3390/jof7020142 - 16 Feb 2021

Cited by 21 | Viewed by 3591

Abstract

The common grape vine, Vitis vinifera, is a widely known plant with commercial and pharmacological value. The plant hosts a variety of microorganisms known as endophytes that can live within the tissues of the plant for a considerable time period, or even their whole life cycle. The fungus Beauveria bassiana is a well-studied endophyte which can colonize a variety of plants in many ways and in different parts of the plant. In this study, we examined the effect of the endophytic fungus B. bassiana on the growth of V. vinifera. The results demonstrated not only a successful colonization of the endophyte, but also a noteworthy impact on the growth of the V. vinifera root without harming the plant in any way. The fungus was also re-isolated from the parts of the plant using inst bait method. Overall, the study demonstrates the capability of B. bassiana to colonize V. vinifera plants, adding to the already existing knowledge of its endophytic activity, and highlighting its beneficial impact on the root growth. Full article

(This article belongs to the Special Issue Fungal Endophytes in Agriculture and Ecosystems)

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11 pages, 801 KiB

Open AccessArticle

Bioactive Metabolites from the Endophytic Fungus Aspergillus sp. SPH2

by Viridiana Morales-Sánchez, Carmen E. Díaz, Elena Trujillo, Sonia A. Olmeda, Felix Valcarcel, Rubén Muñoz, María Fe Andrés and Azucena González-Coloma

J. Fungi 2021, 7(2), 109; https://doi.org/10.3390/jof7020109 - 02 Feb 2021

Cited by 15 | Viewed by 3421

Abstract

In the current study, an ethyl acetate extract from the endophytic fungus Aspergillus sp. SPH2 isolated from the stem parts of the endemic plant Bethencourtia palmensis was screened for its biocontrol properties against plant pathogens (Fusarium moniliforme, Alternaria alternata, and Botrytis cinerea), insect pests (Spodoptera littoralis, Myzus persicae, Rhopalosiphum padi), plant parasites (Meloidogyne javanica), and ticks (Hyalomma lusitanicum). SPH2 gave extracts with strong fungicidal and ixodicidal effects at different fermentation times. The bioguided isolation of these extracts gave compounds 1–3. Mellein (1) showed strong ixodicidal effects and was also fungicidal. This is the first report on the ixodicidal effects of 1. Neoaspergillic acid (2) showed potent antifungal effects. Compound 2 appeared during the exponential phase of the fungal growth while neohydroxyaspergillic acid (3) appeared during the stationary phase, suggesting that 2 is the biosynthetic precursor of 3. The mycotoxin ochratoxin A was not detected under the fermentation conditions used in this work. Therefore, SPH2 could be a potential biotechnological tool for the production of ixodicidal extracts rich in mellein. Full article

(This article belongs to the Special Issue Fungal Endophytes in Agriculture and Ecosystems)

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18 pages, 1261 KiB

Open AccessArticle

Space and Vine Cultivar Interact to Determine the Arbuscular Mycorrhizal Fungal Community Composition

by Álvaro López-García, José A. Jurado-Rivera, Josefina Bota, Josep Cifre and Elena Baraza

J. Fungi 2020, 6(4), 317; https://doi.org/10.3390/jof6040317 - 27 Nov 2020

Cited by 4 | Viewed by 2512

Abstract

The interest in the use of microbes as biofertilizers is increasing in recent years as the demands for sustainable cropping systems become more pressing. Although very widely used as biofertilizers, arbuscular mycorrhizal (AM) fungal associations with specific crops have received little attention and knowledge is limited, especially in the case of vineyards. In this study, the AM fungal community associated with soil and roots of a vineyard on Mallorca Island, Spain was characterized by DNA sequencing to resolve the relative importance of grape variety on their diversity and composition. Overall, soil contained a wider AM fungal diversity than plant roots, and this was found at both taxonomic and phylogenetic levels. The major effect on community composition was associated with sample type, either root or soil material, with a significant effect for the variety of the grape. This effect interacted with the spatial distribution of the plants. Such an interaction revealed a hierarchical effect of abiotic and biotic factors in shaping the composition of AM fungal communities. Our results have direct implications for the understanding of plant-fungal assemblages and the potential functional differences across plants in vineyard cropping. Full article

(This article belongs to the Special Issue Fungal Endophytes in Agriculture and Ecosystems)

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15 pages, 2746 KiB

Open AccessArticle

Fungal Endophytes for Grass Based Bioremediation: An Endophytic Consortium Isolated from Agrostis stolonifera Stimulates the Growth of Festuca arundinacea in Lead Contaminated Soil

by Erika Soldi, Catelyn Casey, Brian R. Murphy and Trevor R. Hodkinson

J. Fungi 2020, 6(4), 254; https://doi.org/10.3390/jof6040254 - 29 Oct 2020

Cited by 19 | Viewed by 3475

Abstract

Bioremediation is an ecologically-friendly approach for the restoration of heavy metal-contaminated sites and can exploit environmental microorganisms such as bacteria and fungi. These microorganisms are capable of removing and/or deactivating pollutants from contaminated substrates through biological and chemical reactions. Moreover, they interact with the natural flora, protecting and stimulating plant growth in these harsh conditions. In this study, we isolated a group of endophytic fungi from Agrostis stolonifera grasses growing on toxic waste from an abandoned lead mine (up to 47,990 Pb mg/kg) and identified them using DNA sequencing (nrITS barcoding). The endophytes were then tested as a consortium of eight strains in a growth chamber experiment in association with the grass Festuca arundinacea at increasing concentrations of lead in the soil to investigate how they influenced several growth parameters. As a general trend, plants treated with endophytes performed better compared to the controls at each concentration of heavy metal, with significant improvements in growth recorded at the highest concentration of lead (800 galena mg/kg). Indeed, this set of plants germinated and tillered significantly earlier compared to the control, with greater production of foliar fresh and dry biomass. Compared with the control, endophyte treated plants germinated more than 1-day earlier and produced 35.91% more plant tillers at 35 days-after-sowing. Our results demonstrate the potential of these fungal endophytes used in a consortium for establishing grassy plant species on lead contaminated soils, which may result in practical applications for heavy metal bioremediation. Full article

(This article belongs to the Special Issue Fungal Endophytes in Agriculture and Ecosystems)

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13 pages, 1382 KiB

Open AccessArticle

Effect of Host, Environment and Fungal Growth on Fungal Leaf Endophyte Communities in Taiwan

by Yu-Ling Huang

J. Fungi 2020, 6(4), 244; https://doi.org/10.3390/jof6040244 - 23 Oct 2020

Cited by 7 | Viewed by 2387

Abstract

Fungal endophytes inhabit plant tissues without causing disease symptoms. They are highly diverse and distributed globally in all plants that have been investigated. Host, geographic, and environmental effects on endophyte communities have been reported in several studies, but the direct effect of fungal growth rate on endophyte composition has not been tested. To understand the relationship between foliar endophyte composition and fungal growth and to examine the effect of host, elevation, and climatic factors on the foliar endophyte communities, this study examined the foliar endophyte communities of representative gymnosperms and Rhododendron spp. across different elevations of Hehuanshan and Taipingshan forests in Taiwan. The isolation frequency and diversity of foliar endophytes were higher at low elevations than at high elevations. The foliar endophyte community structure differed as a function of host family and forest vegetation type. Elevation, mean annual temperature, and precipitation were significantly correlated with the community structure. Fungal growth rate was correlated with the endophyte abundance, which indicates that fast-growing fungi might have a competitive advantage when coexisting with other fungi in a plant host. Full article

(This article belongs to the Special Issue Fungal Endophytes in Agriculture and Ecosystems)

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17 pages, 2363 KiB

Open AccessArticle

The Fungal Endophyte Serendipita williamsii Does Not Affect Phosphorus Status But Carbon and Nitrogen Dynamics in Arbuscular Mycorrhizal Tomato Plants

by Anna M. Hallasgo, Bernhard Spangl, Siegrid Steinkellner and Karin Hage-Ahmed

J. Fungi 2020, 6(4), 233; https://doi.org/10.3390/jof6040233 - 19 Oct 2020

Cited by 11 | Viewed by 2772

Abstract

Some members of the root endophytic Serendipitaceae were observed to frequently coexist with arbuscular mycorrhizal fungi (AMF), but their interactions and potential synergistic effects in plants have not yet been well elucidated. Here, we inoculated three-week-old tomato seedlings with Serendipita indica or Serendipita williamsii alone or in combination with the arbuscular mycorrhizal fungus Funneliformis mosseae and cultivated the plants in a greenhouse until the late vegetative stage. Our data show that the simultaneous presence of Serendipita spp. did not affect root colonization by AMF, proving the feasibility of their combination for future agronomic uses. The photosynthetic performance was enhanced in AM tomato plants, although growth remained unresponsive following single or dual inoculation with Serendipita spp. and AMF. With regard to nutrient status under dual inoculation, AMF-induced phosphorus increases remained unaffected, but nitrogen and carbon dynamics were highly altered. Specifically, the application of S. williamsii to mycorrhizal tomato plants significantly enhanced nitrogen concentration in the shoots, but this effect was also compensated with a carbon cost. Our findings indicate that S. williamsii performs differently from S. indica when co-inoculated with AMF, and this suggests an unknown mechanism that needs more detailed investigation. Full article

(This article belongs to the Special Issue Fungal Endophytes in Agriculture and Ecosystems)

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13 pages, 1686 KiB

Open AccessArticle

Genetic Response of Common Bean to the Inoculation with Indigenous Fusarium Isolates

by Alejandra J. Porteous-Álvarez, Sara Mayo-Prieto, Samuel Álvarez-García, Bonifacio Reinoso and Pedro A. Casquero

J. Fungi 2020, 6(4), 228; https://doi.org/10.3390/jof6040228 - 16 Oct 2020

Cited by 4 | Viewed by 1894

Abstract

Fungal species from the genus Fusarium are important soil-borne pathogens worldwide, causing significant economic losses in diverse crops. The need to find sustainable solutions against this disease has led to the development of new strategies—for instance, the use of biocontrol agents. In this regard, non-pathogenic Fusarium isolates have demonstrated their ability to help other plants withstand subsequent pathogen attacks. In the present work, several Fusarium isolates were evaluated in climatic chambers to identify those presenting low or non-pathogenic behavior. The inoculation with a low-pathogenic isolate of the fungus did not affect the development of the plant, contrary to the results observed in plants inoculated with pathogenic isolates. The expression of defense-related genes was evaluated and compared between plants inoculated with pathogenic and low-pathogenic Fusarium isolates. Low-pathogenic isolates caused a general downregulation of several plant defense-related genes, while pathogenic ones produced an upregulation of these genes. This kind of response to low-pathogenic fungal isolates has been already described for other plant species and fungal pathogens, being related to enhanced tolerance to later pathogen attacks. The results here presented suggest that low-pathogenic F. oxysporum and F. solani isolates may have potential biocontrol activity against bean pathogens via induced and systemic responses in the plant. Full article

(This article belongs to the Special Issue Fungal Endophytes in Agriculture and Ecosystems)

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20 pages, 3626 KiB

Open AccessArticle

Stem Endophytic Mycobiota in Wild and Domesticated Wheat: Structural Differences and Hidden Resources for Wheat Improvement

by Xiang Sun, Evsey Kosman and Amir Sharon

J. Fungi 2020, 6(3), 180; https://doi.org/10.3390/jof6030180 - 18 Sep 2020

Cited by 16 | Viewed by 2393

Abstract

Towards the identification of entophytic fungal taxa with potential for crop improvement, we characterized and compared fungal endophyte communities (FECs) from domesticated bread wheat and two wheat ancestors, Aegilopssharonensis and Triticumdicoccoides. Data generated by next generation sequencing identified a total of 1666 taxa. The FECs in the three plant species contained high proportions of random taxa with low abundance. At plant species level, the majority of abundant taxa were common to all host plants, and the collective FECs of each of the three plant species had similar diversity. However, FECs from the wild plants in specific sites were more diverse and had greater richness than wheat FECs from corresponding specific fields. The wild plants also had higher numbers of differentially abundant fungal taxa than wheat, with Alternaria infectoria being the most abundant species in wild plants and Candida sake the most abundant in wheat. Network analysis on co-occurrence association revealed a small number of taxa with a relatively high number of co-occurrence associations, which might be important in community assembly. Our results show that the actual endophytic cargo in cultivated wheat plants is limited relative to wild plants, and highlight putative functional and hub fungal taxa with potential for wheat improvement. Full article

(This article belongs to the Special Issue Fungal Endophytes in Agriculture and Ecosystems)

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17 pages, 1194 KiB

Open AccessArticle

Alkaloid Concentrations of Lolium perenne Infected with Epichloë festucae var. lolii with Different Detection Methods—A Re-Evaluation of Intoxication Risk in Germany?

by Veronika Vikuk, Benjamin Fuchs, Markus Krischke, Martin J. Mueller, Selina Rueb and Jochen Krauss

J. Fungi 2020, 6(3), 177; https://doi.org/10.3390/jof6030177 - 18 Sep 2020

Cited by 2 | Viewed by 2684

Abstract

Mycotoxins in agriculturally used plants can cause intoxication in animals and can lead to severe financial losses for farmers. The endophytic fungus Epichloë festucae var. lolii living symbiotically within the cool season grass species Lolium perenne can produce vertebrate and invertebrate toxic alkaloids. Hence, an exact quantitation of alkaloid concentrations is essential to determine intoxication risk for animals. Many studies use different methods to detect alkaloid concentrations, which complicates the comparability. In this study, we showed that alkaloid concentrations of individual plants exceeded toxicity thresholds on real world grasslands in Germany, but not on the population level. Alkaloid concentrations on five German grasslands with high alkaloid levels peaked in summer but were also below toxicity thresholds on population level. Furthermore, we showed that alkaloid concentrations follow the same seasonal trend, regardless of whether plant fresh or dry weight was used, in the field and in a common garden study. However, alkaloid concentrations were around three times higher when detected with dry weight. Finally, we showed that alkaloid concentrations can additionally be biased to different alkaloid detection methods. We highlight that toxicity risks should be analyzed using plant dry weight, but concentration trends of fresh weight are reliable. Full article

(This article belongs to the Special Issue Fungal Endophytes in Agriculture and Ecosystems)

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10 pages, 3697 KiB

Open AccessArticle

Self-Inhibitory Activity of Trichoderma Soluble Metabolites and Their Antifungal Effects on Fusarium oxysporum

by Samuel Álvarez-García, Sara Mayo-Prieto, Santiago Gutiérrez and Pedro Antonio Casquero

J. Fungi 2020, 6(3), 176; https://doi.org/10.3390/jof6030176 - 17 Sep 2020

Cited by 6 | Viewed by 3057

Abstract

Self-inhibitory processes are a common feature shared by different organisms. One of the main mechanisms involved in these interactions regarding microorganisms is the release of toxic diffusible substances into the environment. These metabolites can exert both antimicrobial effects against other organisms as well as self-inhibitory ones. The in vitro evaluation of these effects against other organisms has been widely used to identify potential biocontrol agents against phytopathogenic microorganisms. In the present study, we performed membrane assays to compare the self-inhibitory effects of soluble metabolites produced by several Trichoderma isolates and their antifungal activity against a phytopathogenic strain of Fusarium oxysporum. The results demonstrated that Trichoderma spp. present a high self-inhibitory activity in vitro, being affected in both their growth rate and the macroscopic structure of their colonies. These effects were highly similar to those exerted against F. oxysporum in the same conditions, showing no significant differences in most cases. Consequently, membrane assays may not be very informative by themselves to assess putative biocontrol capabilities. Therefore, different methods, or a combination of antifungal and self-inhibitory experiments, could be a better approach to evaluate the potential biocontrol activity of microbial strains in order to pre-select them for further in vivo trials. Full article

(This article belongs to the Special Issue Fungal Endophytes in Agriculture and Ecosystems)

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Review

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44 pages, 658 KiB

Open AccessReview

Epichloë Fungal Endophytes—From a Biological Curiosity in Wild Grasses to an Essential Component of Resilient High Performing Ryegrass and Fescue Pastures

by John R. Caradus and Linda J. Johnson

J. Fungi 2020, 6(4), 322; https://doi.org/10.3390/jof6040322 - 27 Nov 2020

Cited by 20 | Viewed by 3730

Abstract

The relationship between Epichloë endophytes found in a wide range of temperate grasses spans the continuum from antagonistic to mutualistic. The diversity of asexual mutualistic types can be characterised by the types of alkaloids they produce in planta. Some of these are responsible for detrimental health and welfare issues of ruminants when consumed, while others protect the host plant from insect pests and pathogens. In many temperate regions they are an essential component of high producing resilient tall fescue and ryegrass swards. This obligate mutualism between fungus and host is a seed-borne technology that has resulted in several commercial products being used with high uptake rates by end-user farmers, particularly in New Zealand and to a lesser extent Australia and USA. However, this has not happened by chance. It has been reliant on multi-disciplinary research teams undertaking excellent science to understand the taxonomic relationships of these endophytes, their life cycle, symbiosis regulation at both the cellular and molecular level, and the impact of secondary metabolites, including an understanding of their mammalian toxicity and bioactivity against insects and pathogens. Additionally, agronomic trials and seed biology studies of these microbes have all contributed to the delivery of robust and efficacious products. The supply chain from science, through seed companies and retailers to the end-user farmer needs to be well resourced providing convincing information on the efficacy and ensuring effective quality control to result in a strong uptake of these Epichloë endophyte technologies in pastoral agriculture. Full article

(This article belongs to the Special Issue Fungal Endophytes in Agriculture and Ecosystems)

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