Fungal Endophytes of Grasses

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

Deadline for manuscript submissions: closed (30 November 2022) | Viewed by 33394

Special Issue Editors


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Guest Editor
Department of Biology, Wilfrid Laurier University, Waterloo, ON N2L 3C5, Canada
Interests: ecology, physiology and evolution of Epichlöe–grass–herbivore interactions; climate change ecology; invasion ecology

E-Mail Website
Guest Editor
Innovation Centre of Excellence Leader, Resilient Agriculture, AgResearch, New Zealand
Interests: the use of molecular genetic techniques, including gene editing and “omic” technologies to manipulate secondary metabolite pathways and to understand the molecular complexity of endophyte/host interactions

Special Issue Information

Dear Colleagues,

Endophytic fungi in the genus Epichlöe form symbiotic relationships with cool-season grasses. The interaction is of fundamental interest to ecologists, evolutionary biologists, and plant physiologists. These fungi also play important roles in both pasture and turfgrass applications. 

In 1990, researchers organized the 1st International Symposium on Fungal Endophytes of Grasses (ISFEG) in Louisiana, which attracted >100 researchers from 22 countries. It has been more than three years since the last (10th) ISFEG in Salamanca, Spain (June 2018). Unfortunately, the global pandemic has forced further delays in plans for the next ISFEG (New Zealand, November 2023). In lieu of getting together in person, we would like to invite you to share some of your work in this area in an upcoming Special Issue of the Journal of Fungi (2021 Impact Factor 5.816). We welcome submissions covering all aspects of Epichlöe biology, including but not limited to ecology, evolution, physiology and agronomic applications. Submissions may be original research or a critical review. For reviews, please discuss ideas with the editors to ensure no duplication of topics.

Dr. Jonathan Newman
Dr. Linda Johnson
Guest Editors

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Published Papers (20 papers)

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18 pages, 2209 KiB  
Article
Comparative Transcriptomics Profiling of Perennial Ryegrass Infected with Wild Type or a ΔvelA Epichloë festucae Mutant Reveals Host Processes Underlying Mutualistic versus Antagonistic Interactions
by Mostafa Rahnama, Paul Maclean, Damien J. Fleetwood and Richard D. Johnson
J. Fungi 2023, 9(2), 190; https://doi.org/10.3390/jof9020190 - 01 Feb 2023
Cited by 2 | Viewed by 1372
Abstract
Epichloë species form bioprotective endophytic symbioses with many cool-season grasses, including agriculturally important forage grasses. Despite its importance, relatively little is known about the molecular details of the interaction and the regulatory genes involved. VelA is a key global regulator in fungal secondary [...] Read more.
Epichloë species form bioprotective endophytic symbioses with many cool-season grasses, including agriculturally important forage grasses. Despite its importance, relatively little is known about the molecular details of the interaction and the regulatory genes involved. VelA is a key global regulator in fungal secondary metabolism and development. In previous studies, we showed the requirement of velA for E. festucae to form a mutualistic interaction with Lolium perenne. We showed that VelA regulates the expression of genes encoding proteins involved in membrane transport, fungal cell wall biosynthesis, host cell wall degradation, and secondary metabolism, along with several small-secreted proteins in Epichloë festucae. Here, by a comparative transcriptomics analysis on perennial ryegrass seedlings and mature plants, which are endophyte free or infected with wild type (mutualistic interaction) or mutant ΔvelA E. festucae (antagonistic or incompatible interaction), regulatory effects of the endophytic interaction on perennial ryegrass development was studied. We show that ΔvelA mutant associations influence the expression of genes involved in primary metabolism, secondary metabolism, and response to biotic and abiotic stresses compared with wild type associations, providing an insight into processes defining mutualistic versus antagonistic interactions. Full article
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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11 pages, 1008 KiB  
Article
Translocation of Loline Alkaloids in Epichloë-Infected Cereal and Pasture Grasses: What the Insects Tell Us
by Alison J. Popay, Joanne G. Jensen, Wayne R. Simpson, Wade J. Mace and Chanatda Somchit
J. Fungi 2023, 9(1), 96; https://doi.org/10.3390/jof9010096 - 10 Jan 2023
Viewed by 1244
Abstract
Aphids are major pests of cereal and pasture grasses throughout the world, vectoring disease and reducing plant production. There are few control options other than insecticides. Epichloë endophytes that produce loline alkaloids in their hosts provide a possible mechanism of control, with both [...] Read more.
Aphids are major pests of cereal and pasture grasses throughout the world, vectoring disease and reducing plant production. There are few control options other than insecticides. Epichloë endophytes that produce loline alkaloids in their hosts provide a possible mechanism of control, with both meadow fescue and tall fescue naturally infected with loline-producing endophytes showing a resistance to Rhopalosiphum padi. We screened Elymus spp. naturally infected with endophytes that produced loline alkaloids at concentrations known to affect aphids on fescue but found no effect on these insects infesting Elymus. A synthetic loline-producing endophyte association with rye also had no effect on the aphids. After hypothesizing that the lolines were being translocated in the xylem in Elymus and rye rather than the phloem, we tested the rye and meadow fescue infected with loline-producing endophytes against a xylem feeding spittlebug. The endophyte in rye inhibited the feeding of the insect and reduced its survival, whereas the endophyte-infected meadow fescue had no effect on the spittlebug but reduced the number of aphids. Lolines applied to the potting medium of endophyte-free and endophyte-infected rye, ryegrass, and tall fescue resulted in a decrease in the aphid populations on the endophyte-free pasture grasses relative to the untreated controls but had no effect on aphid numbers on the rye. We tentatively conclude that lolines, produced in both natural and synthetic association with Elymus and rye, are partitioned in the xylem rather than the phloem, where they are inaccessible to aphids. Full article
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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16 pages, 5263 KiB  
Article
Epichloë Endophytes Shape the Foliar Endophytic Fungal Microbiome and Alter the Auxin and Salicylic Acid Phytohormone Levels in Two Meadow Fescue Cultivars
by Suni Anie Mathew, Marjo Helander, Kari Saikkonen, Radomira Vankova, Petre I. Dobrev, Serdar Dirihan and Benjamin Fuchs
J. Fungi 2023, 9(1), 90; https://doi.org/10.3390/jof9010090 - 06 Jan 2023
Cited by 6 | Viewed by 1765
Abstract
Plants harbor a large diversity of endophytic microbes. Meadow fescue (Festuca pratensis) is a cool-season grass known for its symbiotic relationship with the systemic and vertically—via seeds—transmitted fungal endophyte Epichloë uncinata, yet its effects on plant hormones and the microbial community [...] Read more.
Plants harbor a large diversity of endophytic microbes. Meadow fescue (Festuca pratensis) is a cool-season grass known for its symbiotic relationship with the systemic and vertically—via seeds—transmitted fungal endophyte Epichloë uncinata, yet its effects on plant hormones and the microbial community is largely unexplored. Here, we sequenced the endophytic bacterial and fungal communities in the leaves and roots, analyzing phytohormone concentrations and plant performance parameters in Epichloë-symbiotic (E+) and Epichloë-free (E-) individuals of two meadow fescue cultivars. The endophytic microbial community differed between leaf and root tissues independent of Epichloë symbiosis, while the fungal community was different in the leaves of Epichloë-symbiotic and Epichloë-free plants in both cultivars. At the same time, Epichloë symbiosis decreased salicylic acid and increased auxin concentrations in leaves. Epichloë-symbiotic plants showed higher biomass and higher seed mass at the end of the season. Our results demonstrate that Epichloë symbiosis alters the leaf fungal microbiota, which coincides with changes in phytohormone concentrations, indicating that Epichloë endophytes affect both plant immune responses and other fungal endophytes. Whether the effect of Epichloë endophytes on other fungal endophytes is connected to changes in phytohormone concentrations remains to be elucidated. Full article
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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11 pages, 5886 KiB  
Article
Endophytic Fungus Negatively Affects Salt Tolerance of Tall Fescue
by Aino Kalske, Kari Saikkonen and Marjo Helander
J. Fungi 2023, 9(1), 14; https://doi.org/10.3390/jof9010014 - 21 Dec 2022
Cited by 1 | Viewed by 1223
Abstract
Vertically transmitted endophytic fungi can mitigate the negative effects of salinity encountered by their host grass and alter the competitive interactions between plant individuals. To experimentally study the interactive effects of the fungal endophyte Epichloë coenophiala on salt tolerance and intraspecific competition of [...] Read more.
Vertically transmitted endophytic fungi can mitigate the negative effects of salinity encountered by their host grass and alter the competitive interactions between plant individuals. To experimentally study the interactive effects of the fungal endophyte Epichloë coenophiala on salt tolerance and intraspecific competition of its host plant, tall fescue Festuca arundinacea, we subjected 15 maternal lines of each Epichloë associated (E+) and Epichloë free (E−) tall fescue to salt treatment and competition in the greenhouse and common garden. Then, to explore variation in endophyte incidence in natural populations of tall fescue, we surveyed 23 natural populations occurring on or near the Baltic Sea coast in Aland islands in southwestern Finland for endophyte incidence, distance to shore, and competitive environment. Under salinity in the greenhouse, E− plants grew larger than E+ plants, but there was no size difference in the control treatment. E− plants grew taller and were more likely to flower than E+ plants when grown in benign conditions in the common garden but not with salinity or competition. The frequency of Epichloë incidence was high (90%) in natural populations, and it decreased towards the shore and risk of salt exposure. These results demonstrate a negative effect of Epichloë endophyte on the salt tolerance of its host. The high incidence of Epichloë in natural populations of tall fescue in the northern part of the species distribution range is likely due to factors other than salinity. Full article
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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17 pages, 2461 KiB  
Article
Transcriptomic Analyses Reveals Molecular Regulation of Photosynthesis by Epichloë endophyte in Achnatherum inebrians under Blumeria graminis Infection
by Yue Zhu, Shibo Zhu, Fang Zhang, Zhenrui Zhao, Michael J. Christensen, Zhibiao Nan and Xingxu Zhang
J. Fungi 2022, 8(11), 1201; https://doi.org/10.3390/jof8111201 - 14 Nov 2022
Cited by 3 | Viewed by 1563
Abstract
Photosynthesis is essential for the growth of all green plants, and the presence of an Epichloë endophyte enhances the photosynthesis of Achnatherum inebrians (drunken horse grass, DHG), including when it is under attack by fungal pathogens. However, few studies have examined the mechanism [...] Read more.
Photosynthesis is essential for the growth of all green plants, and the presence of an Epichloë endophyte enhances the photosynthesis of Achnatherum inebrians (drunken horse grass, DHG), including when it is under attack by fungal pathogens. However, few studies have examined the mechanism of the increased photosynthetic activity at the molecular level of A. inebrians when it is under pathogen stress. The present study investigated the effects of the presence of the Epichloë endophyte on the net photosynthetic rate, intercellular CO2 concentration, stomatal conductance, and transpiration rate of DHG plants under a Blumeria graminis infection condition, and we compared the transcriptomes using RNA sequencing. The results showed that the photosynthetic rate of Epichloë endophyte-infected (E+) plants was higher under the B. graminis infection condition, and also without this pathogen, when it was compared with Epichloë endophyte-free (E-) plants. The E+ plants uninfected with B. graminis had 15 up-regulated unigenes that are involved in photosynthesis which were compared to the E- plants that were uninfected with this pathogen. This suggests that the presence of an Epichloë endophyte up-regulates the genes that are involved in the process of photosynthesis. Full article
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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11 pages, 842 KiB  
Article
Epichloë Increases Root Fungal Endophyte Richness and Alters Root Fungal Endophyte Composition in a Changing World
by Kylea R. Garces, Haley E. Sage, Natalie Christian and Sarah M. Emery
J. Fungi 2022, 8(11), 1142; https://doi.org/10.3390/jof8111142 - 28 Oct 2022
Cited by 1 | Viewed by 1679
Abstract
Plants harbor a variety of fungal symbionts both above- and belowground, yet little is known about how these fungi interact within hosts, especially in a world where resource availability is changing due to human activities. Systemic vertically transmitted endophytes such as Epichloë spp. [...] Read more.
Plants harbor a variety of fungal symbionts both above- and belowground, yet little is known about how these fungi interact within hosts, especially in a world where resource availability is changing due to human activities. Systemic vertically transmitted endophytes such as Epichloë spp. may have particularly strong effects on the diversity and composition of later-colonizing symbionts such as root fungal endophytes, especially in primary successional systems. We made use of a long-term field experiment in Great Lakes sand dunes to test whether Epichloë colonization of the dune-building grass, Ammophila breviligulata, could alter fungal root endophyte species richness or community composition in host plants. We also tested whether nitrogen addition intensified the effects of Epichlöe on the root endophyte community. We found that Epichloë increased richness of root endophytes in Ammophila by 17% overall, but only shifted community composition of root endophytes under nitrogen-enriched conditions. These results indicate that Epichlöe acts as a key species within Ammophila, changing richness and composition of the root mycobiome and integrating above- and belowground mycobiome interactions. Further, effects of Epichloë on root endophyte communities were enhanced by N addition, indicating that this fungal species may become even more important in future environments. Full article
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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15 pages, 1931 KiB  
Article
Abscisic Acid May Play a Critical Role in the Moderating Effect of Epichloë Endophyte on Achnatherum inebrians under Drought Stress
by Xuelian Cui, Wen He, Michael John. Christensen, Jinfeng Yue, Fanbin Zeng, Xingxu Zhang, Zhibiao Nan and Chao Xia
J. Fungi 2022, 8(11), 1140; https://doi.org/10.3390/jof8111140 - 28 Oct 2022
Cited by 5 | Viewed by 1416
Abstract
Water scarcity is a major constraint that adversely affects plant development and growth. Abscisic acid (ABA) is a plant stress hormone that is rapidly synthesized and can induce stomatal closure to conserve water, thereby alleviating the drought stress of plants. The Epichloë endophyte [...] Read more.
Water scarcity is a major constraint that adversely affects plant development and growth. Abscisic acid (ABA) is a plant stress hormone that is rapidly synthesized and can induce stomatal closure to conserve water, thereby alleviating the drought stress of plants. The Epichloë endophyte enhances the drought tolerance of Achnatherum inebrians (drunken horse grass, DHG). To better understand how the Epichloë endophyte enhances drought tolerance, DHG plants without (EF) and with (EI), an Epichloë endophyte, were grown under 20% and 60% soil water conditions (SWC), and the leaves of the three treatments of EF and EI plants were sprayed with ABA solution (1 mg/L); fluridone (FLU), the ABA biosynthesis inhibitor solution (1 mg/L); and distilled water, respectively. Four-weeks later, the results indicated that the exogenous ABA application promoted plant growth, stomatal conductance, and photosynthetic rate, while the opposite effect occurred with plants sprayed with FLU. The differences between EI and EF plants in tiller number, height, chlorophyll content, stomata conductance, and photosynthetic rate were highest when sprayed with ABA. Thus, it is concluded that ABA might be involved in the moderating effect of Epichloë endophytes on DHG plants exposed to drought by maintaining growth and improving photosynthetic efficiency. Full article
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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18 pages, 2589 KiB  
Article
Toxicological Assessment of Pure Lolitrem B and Ryegrass Seed Infected with the AR37 Endophyte Using Mice
by Sarah C. Finch, Allan D. Hawkes, Joan M. Fitzgerald, Ric B. Broadhurst, Maryann R. Staincliffe and John S. Munday
J. Fungi 2022, 8(11), 1139; https://doi.org/10.3390/jof8111139 - 28 Oct 2022
Viewed by 1227
Abstract
Fungal endophytes in perennial ryegrass are essential to New Zealand’s pastoral system due to anti-insect effects. However, endophytes also produce compounds which can be detrimental to animals. Furthermore, as these toxins have been detected in the milk and fat of animals grazing common-toxic [...] Read more.
Fungal endophytes in perennial ryegrass are essential to New Zealand’s pastoral system due to anti-insect effects. However, endophytes also produce compounds which can be detrimental to animals. Furthermore, as these toxins have been detected in the milk and fat of animals grazing common-toxic (containing lolitrem B) or AR37 endophyte-infected herbage they could enter the human food chain. To assess the risk to human health mice were fed for 90 days with three dose rates of lolitrem B and of AR37. Parameters indicative of animal health were measured as well as chemical, hematological and histological analysis of samples collected on day 90. Since endophyte toxin residues have been detected in milk, they could be transferred from mother to offspring via breast milk. To evaluate possible effects on reproduction two complete generations of mice were fed lolitrem B or AR37. At the dose rates given no adverse effects were observed in either study. The 100-fold safety factor to allow the use of animal data in human health assessments was applied and by considering the concentrations of lolitrem B or AR37 metabolites which could be ingested by a consumer it is highly unlikely that they pose any risk to human health. Full article
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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29 pages, 6682 KiB  
Article
The Epichloë festucae Antifungal Protein Efe-AfpA Protects Creeping Bentgrass (Agrostis stolonifera) from the Plant Pathogen Clarireedia jacksonii, the Causal Agent of Dollar Spot Disease
by Patrick A. Fardella, Zipeng Tian, Bruce B. Clarke and Faith C. Belanger
J. Fungi 2022, 8(10), 1097; https://doi.org/10.3390/jof8101097 - 18 Oct 2022
Cited by 3 | Viewed by 1690
Abstract
Dollar spot disease, caused by the fungal pathogen Clarireedia jacksonii, is a major problem in many turfgrass species, particularly creeping bentgrass (Agrostis stolonifera). It is well-established that strong creeping red fescue (Festuca rubra subsp. rubra) exhibits good dollar [...] Read more.
Dollar spot disease, caused by the fungal pathogen Clarireedia jacksonii, is a major problem in many turfgrass species, particularly creeping bentgrass (Agrostis stolonifera). It is well-established that strong creeping red fescue (Festuca rubra subsp. rubra) exhibits good dollar spot resistance when infected by the fungal endophyte Epichloë festucae. This endophyte-mediated disease resistance is unique to the fine fescues and has not been observed in other grass species infected with other Epichloë spp. The mechanism underlying the unique endophyte-mediated disease resistance in strong creeping red fescue has not yet been established. We pursued the possibility that it may be due to the presence of an abundant secreted antifungal protein produced by E. festucae. Here, we compare the activity of the antifungal protein expressed in Escherichia coli, Pichia pastoris, and Penicillium chrysogenum. Active protein was recovered from all systems, with the best activity being from Pe. chrysogenum. In greenhouse assays, topical application of the purified antifungal protein to creeping bentgrass and endophyte-free strong creeping red fescue protected the plants from developing severe symptoms caused by C. jacksonii. These results support the hypothesis that Efe-AfpA is a major contributor to the dollar spot resistance observed with E. festucae-infected strong creeping red fescue in the field, and that this protein could be developed as an alternative or complement to fungicides for the management of this disease on turfgrasses. Full article
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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21 pages, 2882 KiB  
Article
Comprehensive Analysis of Transcriptome and Metabolome Elucidates the Molecular Regulatory Mechanism of Salt Resistance in Roots of Achnatherum inebrians Mediated by Epichloë gansuensis
by Chao Wang, Rong Huang, Jianfeng Wang, Jie Jin, Kamran Malik, Xueli Niu, Rong Tang, Wenpeng Hou, Chen Cheng, Yinglong Liu and Jie Liu
J. Fungi 2022, 8(10), 1092; https://doi.org/10.3390/jof8101092 - 17 Oct 2022
Cited by 3 | Viewed by 1848
Abstract
Salinization of soil is a major environmental risk factor to plant functions, leading to a reduction of productivity of crops and forage. Epichloë gansuensis, seed-borne endophytic fungi, establishes a mutualistic symbiotic relationship with Achnatherum inebrians and confers salt tolerance in the host [...] Read more.
Salinization of soil is a major environmental risk factor to plant functions, leading to a reduction of productivity of crops and forage. Epichloë gansuensis, seed-borne endophytic fungi, establishes a mutualistic symbiotic relationship with Achnatherum inebrians and confers salt tolerance in the host plants. In this study, analysis of transcriptome and metabolome was used to explore the potential molecular mechanism underlying the salt-adaptation of A. inebrians roots mediated by E. gansuensis. We found that E. gansuensis played an important role in the gene expression of the host’s roots and regulated multiple pathways involved in amino acid metabolism, carbohydrate metabolism, TCA cycle, secondary metabolism, and lipid metabolism in the roots of A. inebrians. Importantly, E. gansuensis significantly induced the biological processes, including exocytosis, glycolytic process, fructose metabolic process, and potassium ion transport in roots of host plants at transcriptional levels, and altered the pathways, including inositol phosphate metabolism, galactose metabolism, starch, and sucrose metabolism at metabolite levels under NaCl stress. These findings provided insight into the molecular mechanism of salt resistance in roots of A. inebrians mediated by E. gansuensis and could drive progress in the cultivation of new salt-resistance breeds with endophytes. Full article
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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19 pages, 2260 KiB  
Article
Genetic Diversity of Epichloë Endophytes Associated with Brachypodium and Calamagrostis Host Grass Genera including Two New Species
by Adrian Leuchtmann and Christopher L. Schardl
J. Fungi 2022, 8(10), 1086; https://doi.org/10.3390/jof8101086 - 15 Oct 2022
Cited by 1 | Viewed by 1602
Abstract
Fungi of genus Epichloë (Ascomycota, Clavicipitaceae) are common endophytic symbionts of Poaceae, including wild and agronomically important cool-season grass species (subfam. Poöideae). Here, we examined the genetic diversity of Epichloë from three European species of Brachypodium (B. sylvaticum, B. pinnatum and B. [...] Read more.
Fungi of genus Epichloë (Ascomycota, Clavicipitaceae) are common endophytic symbionts of Poaceae, including wild and agronomically important cool-season grass species (subfam. Poöideae). Here, we examined the genetic diversity of Epichloë from three European species of Brachypodium (B. sylvaticum, B. pinnatum and B. phoenicoides) and three species of Calamagrostis (C. arundinacea, C. purpurea and C. villosa), using DNA sequences of tubB and tefA genes. In addition, microsatellite markers were obtained from a larger set of isolates from B. sylvaticum sampled across Europe. Based on phylogenetic analyses the isolates from Brachypodium hosts were placed in three different subclades within the Epichloë typhina complex (ETC) but did not strictly group according to host grass species, suggesting that the host does not always select for particular endophyte genotypes. Analysis of microsatellite markers confirmed the presence of genetically distinct lineages of Epichloësylvatica on B. sylvaticum, which appeared to be tied to different modes of reproduction (sexual or asexual). Among isolates from Calamagrostis hosts, two subclades were detected which were placed outside ETC. These endophyte lineages are recognized as distinct species for which we propose the names E. calamagrostidis Leuchtm. & Schardl, sp. nov. and E. ftanensis Leuchtm. & A.D. Treindl, sp. nov. This study extends knowledge of the phylogeny and evolutionary diversification of Epichloë endophytes that are symbionts of wild Brachypodium and Calamagrostis host grasses. Full article
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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21 pages, 9457 KiB  
Article
A First Draft of the Core Fungal Microbiome of Schedonorus arundinaceus with and without Its Fungal Mutualist Epichloë coenophiala
by Jenna C. M. Dale and Jonathan A. Newman
J. Fungi 2022, 8(10), 1026; https://doi.org/10.3390/jof8101026 - 28 Sep 2022
Cited by 2 | Viewed by 1468
Abstract
Tall fescue (Schedonorus arundinaceus) is a cool-season grass which is commonly infected with the fungal endophyte Epichloë coenophiala. Although the relationship between tall fescue and E. coenophiala is well-studied, less is known about its broader fungal communities. We used next-generation [...] Read more.
Tall fescue (Schedonorus arundinaceus) is a cool-season grass which is commonly infected with the fungal endophyte Epichloë coenophiala. Although the relationship between tall fescue and E. coenophiala is well-studied, less is known about its broader fungal communities. We used next-generation sequencing of the ITS2 region to describe the complete foliar fungal microbiomes in a set of field-grown tall fescue plants over two years, and whether these fungal communities were affected by the presence of Epichloë. We used the Georgia 5 cultivar of tall fescue, grown in the field for six years prior to sampling. Plants were either uninfected with E. coenophiala, or they were infected with one of two E. coenophiala strains: The common toxic strain or the AR542 strain (sold commerically as MaxQ). We observed 3487 amplicon sequence variants (ASVs) across all plants and identified 43 ASVs which may make up a potential core microbiome. Fungal communities did not differ strongly between Epichloë treatments, but did show a great deal of variation between the two years. Plant fitness also changed over time but was not influenced by E. coenophiala infection. Full article
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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19 pages, 3548 KiB  
Article
Identification of Three Epichloë Endophytes from Hordeum bogdanii Wilensky in China
by Tian Wang, Taixiang Chen, James F. White and Chunjie Li
J. Fungi 2022, 8(9), 928; https://doi.org/10.3390/jof8090928 - 31 Aug 2022
Cited by 2 | Viewed by 1415
Abstract
Cool season grasses often form reciprocal symbiotic relationships with endophytic fungal species in genus Epichloë. In this study, we characterized three fungal endophytes isolated from the grass Hordeum bogdanii native to northwest China. Based on morphological characteristics and phylogenetic analyses of tefA [...] Read more.
Cool season grasses often form reciprocal symbiotic relationships with endophytic fungal species in genus Epichloë. In this study, we characterized three fungal endophytes isolated from the grass Hordeum bogdanii native to northwest China. Based on morphological characteristics and phylogenetic analyses of tefA, tubB, and actG sequences, we identified them as Epichloë sp. HboTG-2 (H. bogdanii Taxonomic Group 2: E. bromicola × E. typhina). Alkaloid synthesis related genes analysis showed that Epichloë sp. HboTG-2 may have the ability only to produce peramine which is toxic to insects but not to animals. In the process of this study, we did not observe sexual structures or epiphyllous growth on leaves of infected plants. Full article
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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12 pages, 1255 KiB  
Article
Cuticular Wax Modification by Epichloë Endophyte in Achnatherum inebrians under Different Soil Moisture Availability
by Zhenrui Zhao, Yawen Ju, Mingzhu Kou, Mei Tian, Michael John Christensen, Xingxu Zhang and Zhibiao Nan
J. Fungi 2022, 8(7), 725; https://doi.org/10.3390/jof8070725 - 12 Jul 2022
Cited by 1 | Viewed by 1772
Abstract
The cuticular wax serves as the outermost hydrophobic barrier of plants against nonstomatal water loss and various environmental stresses. An objective of this study was to investigate the contribution of the mutualistic fungal endophyte Epichloë gansuensis to leaf cuticular wax of Achnatherum inebrians [...] Read more.
The cuticular wax serves as the outermost hydrophobic barrier of plants against nonstomatal water loss and various environmental stresses. An objective of this study was to investigate the contribution of the mutualistic fungal endophyte Epichloë gansuensis to leaf cuticular wax of Achnatherum inebrians under different soil moisture availability. Through a pot experiment and gas chromatography−mass spectrometry (GC−MS) analysis, our results indicated that the hydrocarbons were the dominant components of leaf cuticular wax, and the proportion of alcohols, aldehydes, amines, and ethers varied with the presence or absence of E. gansuensis and different soil moisture availability. Amines and ethers are unique in endophyte-free (EF) A. inebrians plants and endophyte-infected (EI) A. inebrians plants, respectively. By transcriptome analysis, we found a total of 13 differentially expressed genes (DEGs) related to cuticular biosynthesis, including FabG, desB, SSI2, fadD, BiP, KCS, KAR, FAR, and ABCB1. A model is proposed which provides insights for understanding cuticular wax biosynthesis in the association of A. inebrians plants with E. gansuensis. These results may help guide the functional analyses of candidate genes important for improving the protective layer of cuticular wax of endophyte-symbiotic plants. Full article
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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13 pages, 1262 KiB  
Article
Telomere-to-Telomere Genome Sequences across a Single Genus Reveal Highly Variable Chromosome Rearrangement Rates but Absolute Stasis of Chromosome Number
by Mathieu Quenu, Artemis D. Treindl, Kate Lee, Daigo Takemoto, Torsten Thünen, Samad Ashrafi, David Winter, Austen R. D. Ganley, Adrian Leuchtmann, Carolyn A. Young and Murray P. Cox
J. Fungi 2022, 8(7), 670; https://doi.org/10.3390/jof8070670 - 25 Jun 2022
Viewed by 1878
Abstract
Genome rearrangements in filamentous fungi are prevalent but little is known about the modalities of their evolution, in part because few complete genomes are available within a single genus. To address this, we have generated and compared 15 complete telomere-to-telomere genomes across the [...] Read more.
Genome rearrangements in filamentous fungi are prevalent but little is known about the modalities of their evolution, in part because few complete genomes are available within a single genus. To address this, we have generated and compared 15 complete telomere-to-telomere genomes across the phylogeny of a single genus of filamentous fungi, Epichloë. We find that the striking distinction between gene-rich and repeat-rich regions previously reported for isolated species is ubiquitous across the Epichloë genus. We built a species phylogeny from single-copy gene orthologs to provide a comparative framing to study chromosome composition and structural change through evolutionary time. All Epichloë genomes have exactly seven nuclear chromosomes, but despite this conserved ploidy, analyses reveal low synteny and substantial rearrangement of gene content across the genus. These rearrangements are highly lineage-dependent, with most occurring over short evolutionary distances, with long periods of structural stasis. Quantification of chromosomal rearrangements shows they are uncorrelated with numbers of substitutions and evolutionary distances, suggesting that different modes of evolution are acting to create nucleotide and chromosome-scale changes. Full article
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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12 pages, 2765 KiB  
Article
Comparative Research on Metabolites of Different Species of Epichloë Endophytes and Their Host Achnatherum sibiricum
by Yongkang Deng, Yuan Gao, Chenxi Li, Junzhen Zhang, Xiaowen Fan, Nianxi Zhao, Yubao Gao and Anzhi Ren
J. Fungi 2022, 8(6), 619; https://doi.org/10.3390/jof8060619 - 10 Jun 2022
Cited by 1 | Viewed by 2065
Abstract
Achnatherum sibiricum can be infected by two species of fungal endophytes, Epichloë gansuensis (Eg) and Epichloë sibirica (Es). In this study, the metabolites of Eg, Es, and their infected plants were studied by GC–MS analysis. The results showed that the metabolic [...] Read more.
Achnatherum sibiricum can be infected by two species of fungal endophytes, Epichloë gansuensis (Eg) and Epichloë sibirica (Es). In this study, the metabolites of Eg, Es, and their infected plants were studied by GC–MS analysis. The results showed that the metabolic profiles of Eg and Es were similar in general, and only six differential metabolites were detected. The direct effect of endophyte infection on the metabolites in A. sibiricum was that endophyte-infected plants could produce mannitol, which was not present in uninfected plants. Epichloë infection indirectly caused an increase in the soluble sugars in A. sibiricum related to growth and metabolites related to the defense against pathogens and herbivores, such as α-tocopherol, α-linolenic acid and aromatic amino acids. Epichloë infection could regulate galactose metabolism, starch and sucrose metabolism, tyrosine metabolism and phenylalanine metabolism of host grass. In addition, there was a significant positive correlation in the metabolite contents between the endophyte and the host. Full article
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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14 pages, 2272 KiB  
Article
Vertically Transmitted Epichloë Systemic Endophyte Enhances Drought Tolerance of Achnatherum inebrians Host Plants through Promoting Photosynthesis and Biomass Accumulation
by Rui Zhong, Daniel A. Bastías, Xingxu Zhang, Chunjie Li and Zhibiao Nan
J. Fungi 2022, 8(5), 512; https://doi.org/10.3390/jof8050512 - 16 May 2022
Cited by 6 | Viewed by 1707
Abstract
Achnatherum inebrians (drunken horse grass, DHG) plants, a dominant grass species in the arid and semi-arid regions of northwest China, symbiotic with an Epichloë fungal endophyte, is well adapted to drought. However, little is known about how the presence of the foliar Epichloë [...] Read more.
Achnatherum inebrians (drunken horse grass, DHG) plants, a dominant grass species in the arid and semi-arid regions of northwest China, symbiotic with an Epichloë fungal endophyte, is well adapted to drought. However, little is known about how the presence of the foliar Epichloë endophyte enhances the tolerance of DHG to drought at the molecular level. This study explored the positive effects of the presence of the Epichloë endophyte on plant growth, biomass, and photosynthetic efficiency and processes of DHG under non-drought and two drought (moderate and severe) treatments, using RNA sequencing to compare transcriptomes. The transcriptome results showed that 32 selected unigenes involved in the photosynthesis processes within Epichloë symbiotic plants were differently expressed (DEGs) versus non-symbiotic plants. The majority of these selected DEGs were upregulated in Epichloë symbiotic plants versus non-symbiotic plants, such as upregulated unigenes (c51525.graph_c1, c47798.graph_c0 & c64087.graph_c0) under drought conditions. In line with the transcriptomes data, the presence of the Epichloë endophyte promoted the photosynthetic rate and biomass accumulation of DHG plants, and the relationship between the photosynthetic rate and biomass is linear and significant. The presence of the endophyte only increased the biomass per tiller of DHG plants under drought. This study provides further insights into the molecular mechanisms that underlie the enhanced plant growth and drought tolerance of Epichloë-symbiotic DHG plants. Full article
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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Review

Jump to: Research

13 pages, 671 KiB  
Review
The Interaction between Arbuscular Mycorrhizal Fungi (AMF) and Grass Endophyte (Epichloë) on Host Plants: A Review
by Youlei Shen and Tingyu Duan
J. Fungi 2024, 10(3), 174; https://doi.org/10.3390/jof10030174 - 26 Feb 2024
Viewed by 1196
Abstract
In nature, plants frequently experience concurrent colonization with arbuscular mycorrhizal fungi (AMF) and grass endophytes (Epichloë). These two fungi assist in mineral uptake and stress tolerance by the host. Despite the abundance of recent studies exploring the individual functions of these [...] Read more.
In nature, plants frequently experience concurrent colonization with arbuscular mycorrhizal fungi (AMF) and grass endophytes (Epichloë). These two fungi assist in mineral uptake and stress tolerance by the host. Despite the abundance of recent studies exploring the individual functions of these fungi in diverse ecosystems, research on the effects of the interaction between these two symbiotic fungi on the host, particularly in agricultural production and ecological conservation. This review provides an overview of the current knowledge regarding the interaction between AMF and grass endophytes and their synergistic effects on host plants in response to abiotic and biotic stress, while also outlining prospects for future research in this field. This knowledge not only enhances our comprehension of complex interaction effects between the two fungi, but also facilitates the optimal utilization of fungal resources, contributing to ecological construction and higher agricultural production. Full article
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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15 pages, 1226 KiB  
Review
Global Change Factors Influence Plant-Epichloë Associations
by Daniel A. Bastías, Andrea C. Ueno and Pedro E. Gundel
J. Fungi 2023, 9(4), 446; https://doi.org/10.3390/jof9040446 - 06 Apr 2023
Cited by 3 | Viewed by 1443
Abstract
There is an increasing interest in determining the influence of global change on plant–microorganism interactions. We review the results of experiments that evaluated the effects of the global change factors carbon dioxide, ozone, temperature, drought, flooding, and salinity on plant symbioses with beneficial [...] Read more.
There is an increasing interest in determining the influence of global change on plant–microorganism interactions. We review the results of experiments that evaluated the effects of the global change factors carbon dioxide, ozone, temperature, drought, flooding, and salinity on plant symbioses with beneficial Epichloë endophytes. The factors affected the performance of both plants and endophytes as well as the frequency of plants symbiotic with the fungus. Elevated carbon dioxide levels and low temperatures differentially influenced the growth of plants and endophytes, which could compromise the symbioses. Furthermore, we summarise the plant stage in which the effects of the factors were quantified (vegetative, reproductive, or progeny). The factors ozone and drought were studied at all plant stages, but flooding and carbon dioxide were studied in just a few of them. While only studied in response to ozone and drought, evidence showed that the effects of these factors on symbiotic plants persisted trans-generationally. We also identified the putative mechanisms that would explain the effects of the factors on plant–endophyte associations. These mechanisms included the increased contents of reactive oxygen species and defence-related phytohormones, reduced photosynthesis, and altered levels of plant primary metabolites. Finally, we describe the counteracting mechanisms by which endophytes would mitigate the detrimental effects of the factors on plants. In presence of the factors, endophytes increased the contents of antioxidants, reduced the levels of defence-related phytohormones, and enhanced the plant uptake of nutrients and photosynthesis levels. Knowledge gaps regarding the effects of global change on plant–endophyte associations were identified and discussed. Full article
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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9 pages, 258 KiB  
Review
Does the Degree of Mutualism between Epichloë Fungi and Botanophila Flies Depend upon the Reproductive Mode of the Fungi?
by Thomas L. Bultman, Marlena Lembicz and Adrian Leuchtmann
J. Fungi 2022, 8(12), 1270; https://doi.org/10.3390/jof8121270 - 01 Dec 2022
Cited by 1 | Viewed by 1124
Abstract
Epichloë (Ascomycota: Clavicipitaceae) fungi can form an intriguing interaction with Botanophila flies. The fungi live within above-ground shoots of grasses. Some species (type I) only reproduce sexually by forming stromata on all host culms (choke disease). Stromata produce haploid spores (spermatia) that fertilize [...] Read more.
Epichloë (Ascomycota: Clavicipitaceae) fungi can form an intriguing interaction with Botanophila flies. The fungi live within above-ground shoots of grasses. Some species (type I) only reproduce sexually by forming stromata on all host culms (choke disease). Stromata produce haploid spores (spermatia) that fertilize stromata of opposite mating type to form dikaryotic cells. A second category of Epichloë species (type II) produces stromata on only some of the host culms; culms without choke produce flowers and seeds. These Epichloë can reproduce asexually by invading host seed, as well as sexually. Female Botanophila flies visit stromata for feeding and oviposition. Spermatia pass through the gut of Botanophila intact and viable. Flies can cross-fertilize the fungus during defecation after egg laying. Hence, we described the interaction as a mutualism similar to pollination. Yet, subsequent work by others and ourselves showed that visitation by Botanophila flies was not necessary for cross fertilization of Epichloë. We believe these contradictory results can be reconciled from an evolutionary perspective, if one takes into account the reproductive mode of the fungus. We explore a novel hypothesis to reconcile this contradiction, its predictions and discuss ways in which to test them. Full article
(This article belongs to the Special Issue Fungal Endophytes of Grasses)
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