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Advances in Trichoderma-Plant Beneficial Interactions

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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 (31 July 2022) | Viewed by 34543

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Special Issue Editors

Prof. Dr. Rosa Hermosa

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Guest Editor

Spanish-Portuguese Institute for Agricultural Research (CIALE), University of Salamanca, Salamanca, Spain
Interests: Trichoderma–plant interactions

Prof. Dr. Enrique Monte

E-Mail Website
Guest Editor

Spanish-Portuguese Institute for Agricultural Research (CIALE), University of Salamanca, Salamanca, Spain
Interests: Trichoderma–plant interactions

Special Issue Information

Dear Colleagues,

Trichoderma is one of the most important fungal genera, and its study falls into a wide variety of research fields. The mycoparasitic and antibiotic activities of different species of Trichoderma have been exploited in the biocontrol of plant diseases, although many strains are proving to have beneficial effects on plants in terms of growth promotion and activation of defenses against biotic and abiotic stresses. Deciphering the signaling and metabolic pathways that allow us to understand how plants respond to Trichoderma in the presence of pathogens or environmental stresses and how this fungus proliferates in very diverse habitats, including the plant rhizosphere, is of paramount importance to achieve effective applications on plants and crops. The topics covered by this Special Issue include genes, proteins, or metabolites involved in Trichoderma–plant interactions; metagenomics and ecological approaches; cross-kingdom communications; and research papers and reviews dealing with other important challenges in Trichoderma biology.

Prof. Dr. Rosa Hermosa
Prof. Dr. Enrique Monte
Guest Editors

Manuscript Submission Information

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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

plant defense
endophyte
biostimulant
plant colonization
priming
genomics
transcriptomics
metabolomics
ecological distribution

Published Papers (11 papers)

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Research

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25 pages, 10272 KiB

Open AccessArticle

Containment of Fusarium culmorum and Its Mycotoxins in Various Biological Systems by Antagonistic Trichoderma and Clonostachys Strains

by Lidia Błaszczyk, Hanna Ćwiek-Kupczyńska, Karolina Hoppe Gromadzka, Aneta Basińska-Barczak, Łukasz Stępień, Joanna Kaczmarek and Leszek Lenc

J. Fungi 2023, 9(3), 289; https://0-doi-org.brum.beds.ac.uk/10.3390/jof9030289 - 22 Feb 2023

Cited by 2 | Viewed by 1687

Abstract

Prevention of fungal diseases caused by Fusarium species, including F. culmorum, and thus the accumulation of mycotoxins in wheat ears, is a constant challenge focused on the development of new, effective crop management solutions. One of the currently most ecologically attractive approaches is biological control using natural antagonistic microorganisms. With this in mind, the antagonistic potential of thirty-three Clonostachys and Trichoderma strains was assessed in this work. Screening tests were carried out in in vitro cultures, and the observed potential of selected Trichoderma and Clonostachys strains was verified in field and semi-field experiments with two forms of wheat: winter cv. Legenda and spring cv. Bombona. Three strains, namely C. rosea AN291, T. atroviride AN240 and T. viride AN430 were reported to be most effective in inhibiting the growth of F. culmorum KF846 and the synthesis of DON, 3AcDON and ZEN under both laboratory and semi-controlled field conditions. Observations of the contact zones of the tested fungi in dual cultures exposed their mycoparasitic abilities against KF846. In addition, studies on liquid cultures have demonstrated the ability of these strains to eliminate F. culmorum toxins. Meanwhile, the strains of T. atroviride AN35 and T. cremeum AN392 used as soil inoculants in the field experiment showed a different effect on the content of toxins in ears (grains and chaffs), while improved wheat yield parameters, mainly grain health in both wheat cultivars. It is concluded that the selected Trichoderma and Clonostachys strains have a high potential to reduce the adverse effects of F. culmorum ear infection; therefore, they can be further considered in the context of potential biocontrol factors and as wheat crop improvers. Full article

(This article belongs to the Special Issue Advances in Trichoderma-Plant Beneficial Interactions)

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13 pages, 1808 KiB

Open AccessArticle

Testing the Biocontrol Ability of a Trichoderma-Streptomycetes Consortium against Pyrrhoderma noxium (Corner) L.W. Zhou and Y.C. Dai in Soil

by Harrchun Panchalingam, Nina Ashfield-Crook, Vatsal Naik, Richard Frenken, Keith Foster, Russell Tomlin, Alison Shapcott and D. İpek Kurtböke

J. Fungi 2023, 9(1), 67; https://0-doi-org.brum.beds.ac.uk/10.3390/jof9010067 - 31 Dec 2022

Cited by 7 | Viewed by 1583

Abstract

The Brown root rot pathogen Pyrrhoderma noxium (Corner) L.W. Zhou and Y.C. Dai is known to infect a large number of culturally and economically important plant species across the world. Although chemical control measures have been effective in managing this pathogen, their adverse effects on the ecosystem have limited their use. The use of biological control agents (BCAs) thus is generally accepted as an environmentally friendly way of managing various pathogens. Testing various consortia of the BCAs with different antagonistic mechanisms may even provide better disease protection than the use of a single BCA against aggressive plant pathogens such as the P. noxium. In the presented study, the wood decay experiment and the pot trial confirmed that the consortium of Trichoderma strains (#5029 and 5001) and streptomycetes (#USC−6914 and #USC−595-B) used was effective in protecting wood decay and plant disease caused by P. noxium. Among the treatments, complete elimination of the pathogen was observed when the BCAs were applied as a consortium. In addition, the BCAs used in this study promoted the plant growth. Therefore, Trichoderma and streptomycetes consortium could be used as a potential biocontrol measure to manage P. noxium infections in the field over the application of hazardous chemical control measures. Full article

(This article belongs to the Special Issue Advances in Trichoderma-Plant Beneficial Interactions)

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25 pages, 3122 KiB

Open AccessArticle

Assessing the Various Antagonistic Mechanisms of Trichoderma Strains against the Brown Root Rot Pathogen Pyrrhoderma noxium Infecting Heritage Fig Trees

by Harrchun Panchalingam, Daniel Powell, Cherrihan Adra, Keith Foster, Russell Tomlin, Bonnie L. Quigley, Sharon Nyari, R. Andrew Hayes, Alison Shapcott and D. İpek Kurtböke

J. Fungi 2022, 8(10), 1105; https://doi.org/10.3390/jof8101105 - 19 Oct 2022

Cited by 11 | Viewed by 2510

Abstract

A wide range of phytopathogenic fungi exist causing various plant diseases, which can lead to devastating economic, environmental, and social impacts on a global scale. One such fungus is Pyrrhoderma noxium, causing brown root rot disease in over 200 plant species of a variety of life forms mostly in the tropical and subtropical regions of the globe. The aim of this study was to discover the antagonistic abilities of two Trichoderma strains (#5001 and #5029) found to be closely related to Trichoderma reesei against P. noxium. The mycoparasitic mechanism of these Trichoderma strains against P. noxium involved coiling around the hyphae of the pathogen and producing appressorium like structures. Furthermore, a gene expression study identified an induced expression of the biological control activity associated genes in Trichoderma strains during the interaction with the pathogen. In addition, volatile and diffusible antifungal compounds produced by the Trichoderma strains were also effective in inhibiting the growth of the pathogen. The ability to produce Indole-3-acetic acid (IAA), siderophores and the volatile compounds related to plant growth promotion were also identified as added benefits to the performance of these Trichoderma strains as biological control agents. Overall, these results show promise for the possibility of using the Trichoderma strains as potential biological control agents to protect P. noxium infected trees as well as preventing new infections. Full article

(This article belongs to the Special Issue Advances in Trichoderma-Plant Beneficial Interactions)

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15 pages, 3037 KiB

Open AccessArticle

Volatile Organic Compound (VOC) Profiles of Different Trichoderma Species and Their Potential Application

by Liberata Gualtieri, Maurilia Maria Monti, Francesca Mele, Assunta Russo, Paolo Alfonso Pedata and Michelina Ruocco

J. Fungi 2022, 8(10), 989; https://0-doi-org.brum.beds.ac.uk/10.3390/jof8100989 - 21 Sep 2022

Cited by 6 | Viewed by 2556

Abstract

Fungi emit a broad spectrum of volatile organic compounds (VOCs), sometimes producing species-specific volatile profiles. Volatilomes have received over the last decade increasing attention in ecological, environmental and agricultural studies due to their potential to be used in the biocontrol of plant pathogens and pests and as plant growth-promoting factors. In the present study, we characterised and compared the volatilomes from four different Trichoderma species: T. asperellum B6; T. atroviride P1; T. afroharzianum T22; and T. longibrachiatum MK1. VOCs were collected from each strain grown both on PDA and in soil and analysed using proton transfer reaction quadrupole interface time-of-flight mass spectrometry (PTR-Qi-TOF-MS). Analysis of the detected volatiles highlighted a clear separation of the volatilomes of all the four species grown on PDA whereas the volatilomes of the soil-grown fungi could be only partially separated. Moreover, a limited number of species-specific peaks were found and putatively identified. In particular, each of the four Trichoderma species over-emitted somevolatiles involved in resistance induction, promotion of plant seed germination and seedling development and antimicrobial activity, as 2-pentyl-furan, 6PP, acetophenone and p-cymene by T. asperellum B6, T. atroviride P1, T. afroharzianum T22 and T. longibrachiatum MK1, respectively. Their potential role in interspecific interactions from the perspective of biological control is briefly discussed. Full article

(This article belongs to the Special Issue Advances in Trichoderma-Plant Beneficial Interactions)

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23 pages, 5427 KiB

Open AccessArticle

The Multilateral Efficacy of Chitosan and Trichoderma on Sugar Beet

by Lisa Kappel, Nicole Kosa and Sabine Gruber

J. Fungi 2022, 8(2), 137; https://0-doi-org.brum.beds.ac.uk/10.3390/jof8020137 - 29 Jan 2022

Cited by 14 | Viewed by 3675

Abstract

The majority of all fungal formulations contain Trichoderma spp., making them effective biological control agents for agriculture. Chitosan, one of the most effective natural biopolymers, was also reported as a plant resistance enhancer and as a biocide against a variety of plant pathogens. An in vitro three-way interaction assay of T. atroviride, chitosan, and important plant pathogens (such as Cercospora beticola and Fusarium oxysporum) revealed a synergistic effect on fungistasis. Furthermore, chitosan coating on Beta vulgaris ssp. vulgaris seeds positively affected the onset and efficiency of germination. We show that priming with T. atroviride spores or chitosan leads to the induced expression of a pathogenesis-related gene (PR-3), but only supplementation of chitosan led to significant upregulation of phytoalexin synthesis (PAL) and oxidative stress-related genes (GST) as a defense response. Repeated foliar application of either agent promoted growth, triggered defense reactions, and reduced incidence of Cercospora leaf spot (CLS) disease in B. vulgaris. Our data suggest that both agents are excellent candidates to replace or assist common fungicides in use. Chitosan triggered the systemic resistance and had a biocidal effect, while T. atroviride mainly induced stress-related defense genes in B. vulgaris. We assume that both agents act synergistically across different signaling pathways, which could be of high relevance for their combinatorial and thus beneficial application on field. Full article

(This article belongs to the Special Issue Advances in Trichoderma-Plant Beneficial Interactions)

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14 pages, 6497 KiB

Open AccessArticle

Effects of Trichoderma strigosellum in Eucalyptus urophylla Development and Leaf-Cutting Ant Behavior

by Kamilla Otoni Marques Batista, Dayara Vieira Silva, Vitor L. Nascimento and Danival José de Souza

J. Fungi 2022, 8(1), 15; https://0-doi-org.brum.beds.ac.uk/10.3390/jof8010015 - 27 Dec 2021

Cited by 5 | Viewed by 2346

Abstract

Fungal endophytes can protect plants against herbivory and be used to control leaf-cutting ants. In this study, we aimed to evaluate the potential of endophytic colonization of Eucalyptus urophylla by three filamentous fungal species and their influence on the plant development and foraging behavior of Atta sexdens. The study design was completely randomized and comprised a factorial scheme of 4 × 3, three antagonistic fungal species (Escovopsis sp., Metarhizium anisopliae, and Trichoderma strigosellum) of the leaf-cutting ant, and one control and three inoculation methods (conidial suspension via foliar spray [FS] and soil drench [SD] inoculation, and seedlings inoculated with mycelium [SWM]). The SWM method allowed T. strigosellum to colonize all plant organs, and these plants exhibited higher height, leaf number, shoot dry mass, and total dry mass than the ones subjected to the other inoculation methods. The SWM method increased the plant height than the control plants and those inoculated with Escovopsis sp. and M. anisopliae. Trichoderma strigosellum, previously isolated from soil, colonized E. urophylla plants and positively influenced their development, as demonstrated by the SWM method. Trichoderma strigosellum promoted the increase in E. urophylla height compared with when the FS and SD methods were used (by 19.62% and 18.52%, respectively). Our results reveal that A. sexdens workers preferentially began cutting the leaves from plants not previously colonized by T. strigosellum. This behavior can be explained by modifications in the phenotypic traits of the eucalyptus leaves. Full article

(This article belongs to the Special Issue Advances in Trichoderma-Plant Beneficial Interactions)

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21 pages, 3204 KiB

Open AccessArticle

Why Is the Correct Selection of Trichoderma Strains Important? The Case of Wheat Endophytic Strains of T. harzianum and T. simmonsii

by Alberto Pedrero-Méndez, H. Camilo Insuasti, Theodora Neagu, María Illescas, M. Belén Rubio, Enrique Monte and Rosa Hermosa

J. Fungi 2021, 7(12), 1087; https://0-doi-org.brum.beds.ac.uk/10.3390/jof7121087 - 17 Dec 2021

Cited by 21 | Viewed by 3671

Abstract

The search for endophytic fungi in the roots of healthy wheat plants from a non-irrigation field trial allowed us to select 4 out of a total of 54 cultivable isolates belonging to the genus Trichoderma, identified as T. harzianum T136 and T139, T. simmonsii T137, and T. afroharzianum T138. In vitro assays against the phytopathogenic fungus Fusarium graminearum showed that the T. harzianum strains had the highest biocontrol potential and that T136 exhibited the highest cellulase and chitinase activities. Production patterns of eight phytohormones varied among the Trichoderma strains. All four, when applied alone or in combination, colonized roots of other wheat cultivars and promoted seed germination, tillering, and plant growth under optimal irrigation conditions in the greenhouse. Apart from T136, the endophytic Trichoderma strains showed plant protection capacity against drought as they activated the antioxidant enzyme machinery of the wheat plants. However, T. simmonsii T137 gave the best plant size and spike weight performance in water-stressed plants at the end of the crop. This trait correlated with significantly increased production of indole acetic acid and abscisic acid and increased 1-aminocyclopropane-1-carboxylic acid deaminase activity by T137. This study shows the potential of Trichoderma endophytes and that their success in agricultural systems requires careful selection of suitable strains. Full article

(This article belongs to the Special Issue Advances in Trichoderma-Plant Beneficial Interactions)

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18 pages, 1455 KiB

Open AccessArticle

Effect of a Wood-Based Carrier of Trichoderma atroviride SC1 on the Microorganisms of the Soil

by Hamza Chammem, Livio Antonielli, Andrea Nesler, Massimo Pindo and Ilaria Pertot

J. Fungi 2021, 7(9), 751; https://0-doi-org.brum.beds.ac.uk/10.3390/jof7090751 - 13 Sep 2021

Cited by 4 | Viewed by 2617

Abstract

Wood pellets can sustain the growth of Trichoderma spp. in soil; however, little is known about their side effects on the microbiota. The aims of this study were to evaluate the effect of wood pellets on the growth of Trichoderma spp. in bulk soil and on the soil microbial population’s composition and diversity. Trichoderma atroviride SC1 coated wood pellets and non-coated pellets were applied at the level of 10 g∙kg⁻¹ of soil and at the final concentration of 5 × 10³ conidia∙g⁻¹ of soil and compared to a conidial suspension applied at the same concentration without the wood carrier. Untreated bulk soil served as a control. The non-coated wood pellets increased the total Trichoderma spp. population throughout the experiment (estimated as colony-forming unit g⁻¹ of soil), while wood pellets coated with T. atroviride SC1 did not. The wood carrier increased the richness, and temporarily decreased the diversity, of the bacterial population, with Massilia being the most abundant bacterial genus, while it decreased both the richness and diversity of the fungal community. Wood pellets selectively increased fungal species having biocontrol potential, such as Mortierella, Cladorrhinum, and Stachybotrys, which confirms the suitability of such carriers of Trichoderma spp. for soil application. Full article

(This article belongs to the Special Issue Advances in Trichoderma-Plant Beneficial Interactions)

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19 pages, 4586 KiB

Open AccessArticle

Trichoderma Biological Control to Protect Sensitive Maize Hybrids against Late Wilt Disease in the Field

by Ofir Degani and Shlomit Dor

J. Fungi 2021, 7(4), 315; https://0-doi-org.brum.beds.ac.uk/10.3390/jof7040315 - 18 Apr 2021

Cited by 43 | Viewed by 4528

Abstract

Late wilt, a disease severely affecting maize fields throughout Israel, is characterized by the relatively rapid wilting of maize plants from the tasseling stage to maturity. The disease is caused by the fungus Magnaporthiopsis maydis, a soil and seed-borne pathogen. The pathogen is controlled traditionally through the use of maize cultivars having reduced sensitivity to the disease. Nevertheless, such cultivars may lose their immunity after several years of intensive growth due to the presence of high virulent isolates of M. maydis. Alternative effective and economical chemical treatment to the disease was recently established but is dependent on the use of a dripline assigned for two adjacent rows and exposes the risk of fungicide resistance. In the current work, eight marine and soil isolates of Trichoderma spp., known for high mycoparasitic potential, were tested as biocontrol agents against M. maydis. An in vitro confront plate assay revealed strong antagonistic activity against the pathogen of two T. longibrachiatum isolates and of T. asperelloides. These species produce soluble metabolites that can inhibit or kill the maize pathogen in submerged and solid media culture growth assays. In greenhouse experiments accompanied by real-time PCR tracking of the pathogen, the Trichoderma species or their metabolites managed to improve the seedlings’ wet biomass and reduced the pathogen DNA in the maize roots. A follow-up experiment carried out through a whole growth session, under field conditions, provided important support to the Trichoderma species’ beneficial impact. The direct addition of T. longibrachiatum and even more T. asperelloides to the seeds, with the sowing, resulted in a yield improvement, a significant increase in the growth parameters and crops, to the degree of noninfected plants. These bioprotective treatments also restricted the pathogen DNA in the host tissues (up to 98%) and prevented the disease symptoms. The results encourage more in-depth research to uncover such biological agents’ potential and the methods to implement them in commercial fields. If adequately developed into final products and combined with other control methods, the biological control could play an important role in maize crop protection against Late wilt. Full article

(This article belongs to the Special Issue Advances in Trichoderma-Plant Beneficial Interactions)

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Review

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13 pages, 2587 KiB

Open AccessReview

Adhesion as a Focus in Trichoderma–Root Interactions

by James T. Taylor, Rebekka Harting, Samer Shalaby, Charles M. Kenerley, Gerhard H. Braus and Benjamin A. Horwitz

J. Fungi 2022, 8(4), 372; https://0-doi-org.brum.beds.ac.uk/10.3390/jof8040372 - 06 Apr 2022

Cited by 6 | Viewed by 2532

Abstract

Fungal spores, germlings, and mycelia adhere to substrates, including host tissues. The adhesive forces depend on the substrate and on the adhesins, the fungal cell surface proteins. Attachment is often a prerequisite for the invasion of the host, hence its importance. Adhesion visibly precedes colonization of root surfaces and outer cortex layers, but little is known about the molecular details. We propose that by starting from what is already known from other fungi, including yeast and other filamentous pathogens and symbionts, the mechanism and function of Trichoderma adhesion will become accessible. There is a sequence, and perhaps functional, homology to other rhizosphere-competent Sordariomycetes. Specifically, Verticillium dahliae is a soil-borne pathogen that establishes itself in the xylem and causes destructive wilt disease. Metarhizium species are best-known as insect pathogens with biocontrol potential, but they also colonize roots. Verticillium orthologs of the yeast Flo8 transcription factor, Som1, and several other relevant genes are already under study for their roles in adhesion. Metarhizium encodes relevant adhesins. Trichoderma virens encodes homologs of Som1, as well as adhesin candidates. These genes should provide exciting leads toward the first step in the establishment of beneficial interactions with roots in the rhizosphere. Full article

(This article belongs to the Special Issue Advances in Trichoderma-Plant Beneficial Interactions)

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23 pages, 7244 KiB

Open AccessReview

Trichoderma and the Plant Heritable Priming Responses

by María E. Morán-Diez, Ángel Emilio Martínez de Alba, M. Belén Rubio, Rosa Hermosa and Enrique Monte

J. Fungi 2021, 7(4), 318; https://0-doi-org.brum.beds.ac.uk/10.3390/jof7040318 - 19 Apr 2021

Cited by 58 | Viewed by 4941

Abstract

There is no doubt that Trichoderma is an inhabitant of the rhizosphere that plays an important role in how plants interact with the environment. Beyond the production of cell wall degrading enzymes and metabolites, Trichoderma spp. can protect plants by inducing faster and stronger immune responses, a mechanism known as priming, which involves enhanced accumulation of dormant cellular proteins that function in intracellular signal amplification. One example of these proteins is the mitogen-activated protein kinases (MAPK) that are triggered by the rise of cytosolic calcium levels and cellular redox changes following a stressful challenge. Transcription factors such as WRKYs, MYBs, and MYCs, play important roles in priming as they act as regulatory nodes in the transcriptional network of systemic defence after stress recognition. In terms of long-lasting priming, Trichoderma spp. may be involved in plants epigenetic regulation through histone modifications and replacements, DNA (hypo)methylation, and RNA-directed DNA methylation (RdDM). Inheritance of these epigenetic marks for enhanced resistance and growth promotion, without compromising the level of resistance of the plant’s offspring to abiotic or biotic stresses, seems to be an interesting path to be fully explored. Full article

(This article belongs to the Special Issue Advances in Trichoderma-Plant Beneficial Interactions)

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