Secondary Metabolites in Fungi-Plant Interactions

A special issue of Metabolites (ISSN 2218-1989). This special issue belongs to the section "Plant Metabolism".

Deadline for manuscript submissions: closed (15 April 2023) | Viewed by 16594

Special Issue Editors


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Guest Editor
Department of Industrial and Environmental Microbiology, Faculty of Biology and Biotechnology, Maria Curie-Sklodowska University in Lublin, Lublin, Poland
Interests: plant biocontrol; bio-fertilization and protection; biotic and abiotic factors of plant resistance; inhibition of phytopathogen growth; soil bioremediation by microorganisms; cell wall-degrading enzymes and microbiological metabolites; siderophores; phytohormones
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Guest Editor
Department of Industrial and Environmental Microbiology, Institute of Biological Science, Maria Curie-Skłodowska University, Akademicka 19, 20-033 Lublin, Poland
Interests: biochemical and microbial soil activity; soil filamentous fungi and their metabolites; extracellular and wall fungal polymers; stimulation of plant resistance with fungal elicitors

Special Issue Information

Dear Colleagues,

This Special Issue is dedicated to increasing the knowledge of the role of secondary metabolites (SMs) of fungi playing an essential role in establishing and stabilizing plant–fungal interactions. Plant–fungal interactions are extremely complex and varied as the fungi involved in these interactions can combine different lifestyles—saprophytic, symbiotic (e.g., mycorrhizal), or pathogenic; necrotrophic, hemibiotrophic, and biotrophic—and the plant can trigger numerous defense reactions. A result of many plant–fungal interactions is the promotion of plant growth and development by improving the plant uptake of nutrients and water and stress tolerance. Fungal SMs mimicking such plant hormonal substances as auxins, gibberellins, and jasmonic, salicylic, and abscisic acids may be responsible for such effects. SMs significantly contribute to the ability of fungi to colonize and penetrate plants and play important roles in the virulence and lifestyle of fungal plant pathogens. The loss of SM biosynthetic pathways is most likely associated with biotrophy. Chemically diverse fungal SMs, i.e., polyketides (e.g., aflatoxin and fumonisins), terpenes, and nonribosomal peptides (e.g., sirodesmin, peramine and siderophores such as ferricrocin), are the major components of filamentous fungi. Despite their chemical diversity, fungal SMs are synthesized in only a few biosynthetic pathways. The production of SMs is strain-specific and depends on the specific stages of fungal growth and development, growing conditions, the availability of the precursors of respective SMs, the presence or absence of other organisms, and abiotic and biotic environmental stresses. Mycotoxins, i.e., relatively low-molecular weight nonvolatile fungal products that may affect exposed vertebrates in a variety of ways, include both well-known compounds and less abundant compounds that are poorly understood in terms of structure and interaction. In contrast, fungal phytotoxins include host-selective toxins that are active only toward host plants, with unique modes of action and toxicity and non-host selective toxins. The pathogenicity or tolerance of fungi to environmental factors can be influenced by such SMs as pigments, polyols, and mycosporines. Gene clusters encoding fungal SMs in individual fungi are recognized thanks to the availability of the latest genome sequences and next-generation genomic tools. An important aspect of this Special Issue will be the presentation of the latest modern techniques for obtaining and analyzing the structure, functions, and studies of the interaction of fungal SMs with plant host metabolites. The aim of this Special Issue is to collect the latest data and systematize the knowledge of the diversity of secondary metabolites (SMs) produced by fungi interacting with plants and to elucidate the role of these metabolites in the types of fungus–plant interaction. There is a need to describe the results of intensive genomic, transcriptomic, and metabolomic research on genes encoding fungal SMs, the expression of these genes in various environmental conditions, SM biosynthesis pathways, and possibilities of using fungal SMs in many fields of science (e.g., agriculture, medicine, pharmacy, etc.).

Prof. Dr. Jolanta Jaroszuk-Ściseł
Dr. Artur Nowak
Guest Editors

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Keywords

  • endophytes
  • epiphytes
  • symbionts
  • mycorrhizal fungi
  • phytopathogens (necrotrophs, hemibiotrophs, and biotrophs)
  • siderophores
  • toxins
  • mycotoxin
  • host-selective and non-host selective phytotoxins
  • hormonal substances (auxins, gibberellins, jasmonic, salicylic, and abscisic acids)
  • pigments
  • polyols
  • mycosporines

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Published Papers (5 papers)

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Research

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25 pages, 3139 KiB  
Article
Differences in the Production of Extracellular Polymeric Substances (EPS) and Other Metabolites of Plenodomus (Leptosphaeria) Infecting Winter Oilseed Rape (Brassica napus L.)
by Artur Nowak, Mateusz Kutyła, Joanna Kaczmarek, Jolanta Jaroszuk-Ściseł and Małgorzata Jędryczka
Metabolites 2023, 13(6), 759; https://doi.org/10.3390/metabo13060759 - 17 Jun 2023
Cited by 1 | Viewed by 1983
Abstract
Species of the genus Plenodomus (Leptosphaeria) are phytopathogens of the Brassicaceae family, which includes oilseed rape. The spores of these fungi spread by airborne transmission, infect plants, and cause crop losses. The secondary metabolism of P. lingam and P. biglobosus was [...] Read more.
Species of the genus Plenodomus (Leptosphaeria) are phytopathogens of the Brassicaceae family, which includes oilseed rape. The spores of these fungi spread by airborne transmission, infect plants, and cause crop losses. The secondary metabolism of P. lingam and P. biglobosus was studied and compared, with the main focus being on the ability to produce Extracellular Polymeric Substances (EPS). In spite of the 1.5–2-fold faster growth rate of P. biglobosus on Czapek-Dox and other screening media, the average yield of EPS in this fungus was only 0.29 g/L, compared to that of P. lingam (0.43 g/L). In turn, P. biglobosus showed a higher capacity to synthesise IAA, i.e., 14 µg/mL, in contrast to <1.5 µg/mL produced by P. lingam. On the other hand, the P. lingam strains showed higher β-glucanase activity (350–400 mU/mL), compared to 50–100 mU/mL in P. biglobosus. Invertase levels were similar in both species (250 mU/mL). The positive correlation between invertase activity and EPS yield contrasted with the absence of a correlation of EPS with β-glucanase. Plenodomus neither solubilised phosphate nor used proteins from milk. All strains showed the ability to synthesise siderophores on CAS agar. P. biglobosus exhibited the highest efficiency of amylolytic and cellulolytic activity. Full article
(This article belongs to the Special Issue Secondary Metabolites in Fungi-Plant Interactions)
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17 pages, 3691 KiB  
Article
Multi-Enzymatic Synthesis of Lactobionic Acid Using Wood-Degrading Enzymes Produced by White Rot Fungi
by Wiktoria Piątek-Gołda, Justyna Sulej, Marcin Grąz, Piotr Waśko, Ewa Janik-Zabrotowicz and Monika Osińska-Jaroszuk
Metabolites 2023, 13(4), 469; https://doi.org/10.3390/metabo13040469 - 24 Mar 2023
Cited by 2 | Viewed by 2555
Abstract
Enzymes produced by white rot fungi are involved in the synthesis of secondary metabolites with valuable biotechnological properties. One of these metabolites is lactobionic acid (LBA). The aim of this study was to characterize a novel enzyme system consisting of a cellobiose dehydrogenase [...] Read more.
Enzymes produced by white rot fungi are involved in the synthesis of secondary metabolites with valuable biotechnological properties. One of these metabolites is lactobionic acid (LBA). The aim of this study was to characterize a novel enzyme system consisting of a cellobiose dehydrogenase from Phlebia lindtneri (PlCDH), a laccase from Cerrena unicolor (CuLAC), a redox mediator (ABTS or DCPIP), and lactose as a substrate. We used quantitative (HPLC) and qualitative methods (TLC, FTIR) to characterise the obtained LBA. The free radical scavenging effect of the synthesised LBA was assessed with the DPPH method. Bactericidal properties were tested against Gram-negative and Gram-positive bacteria. We obtained LBA in all the systems tested; however, the study showed that the temperature of 50 °C with the addition of ABTS was the most advantageous condition for the synthesis of lactobionic acid. A mixture with 13 mM LBA synthesised at 50 °C with DCPIP showed the best antioxidant properties (40% higher compared with the commercial reagent). Furthermore, LBA had an inhibitory effect on all the bacteria tested, but the effect was better against Gram-negative bacteria with growth inhibition no lower than 70%. Summarizing the obtained data, lactobionic acid derived in a multienzymatic system is a compound with great biotechnological potential. Full article
(This article belongs to the Special Issue Secondary Metabolites in Fungi-Plant Interactions)
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13 pages, 15660 KiB  
Article
Report on Vincristine-Producing Endophytic Fungus Nigrospora zimmermanii from Leaves of Catharanthus roseus
by Kanchan Birat, Reem Binsuwaidan, Tariq Omar Siddiqi, Showkat Rasool Mir, Nawaf Alshammari, Mohd Adnan, Rahila Nazir, Bushra Ejaz, Moien Qadir Malik, Rikeshwer Prasad Dewangan, Syed Amir Ashraf and Bibhu Prasad Panda
Metabolites 2022, 12(11), 1119; https://doi.org/10.3390/metabo12111119 - 15 Nov 2022
Cited by 8 | Viewed by 2641
Abstract
Vincristine is an anti-cancer compound and one of the most crucial vinca alkaloids produced by the medicinal plant Catharanthus roseus (L.) G. Don. (Apocynaceae). This plant is home to hundreds of endophytic microbes, which produce a variety of bioactive secondary metabolites that are [...] Read more.
Vincristine is an anti-cancer compound and one of the most crucial vinca alkaloids produced by the medicinal plant Catharanthus roseus (L.) G. Don. (Apocynaceae). This plant is home to hundreds of endophytic microbes, which produce a variety of bioactive secondary metabolites that are known for their medicinal properties. In this study, we focused on isolating an endophytic fungus that could increase the yield of vincristine under laboratory conditions as an alternative to plant-mediated extraction of vincristine. The endophytic fungus Nigrospora zimmermanii (Apiosporaceae) was isolated from Catharanthus roseus and it was found to be producing the anticancer compound vincristine. It was identified using high-performance thin-layer chromatography by matching the Rf value and spectral data with the vincristine standard and mass spectrometry data and the reference molecule from the PubChem database. The generation study of this microbe showed that the production of vincristine in the parent fungus was at its maximum, i.e., 5.344 µg/mL, while it was slightly reduced in subsequent generations. A colonization study was also performed and it showed that the fungus N. zimmermanii was able to re-infect the plant Catharanthus roseus after 20 days of inoculation. The colonization study showed that N. zimmernanii could infect the plant after isolation. This method is an efficient and easy way to obtain a high yield of vincristine, as compared to plant-mediated production. Full article
(This article belongs to the Special Issue Secondary Metabolites in Fungi-Plant Interactions)
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22 pages, 3577 KiB  
Article
The Metabolic Profile of Anchusa officinalis L. Differs According to Its Associated Arbuscular Mycorrhizal Fungi
by Evangelia Tsiokanos, Annalisa Cartabia, Nikolaos Tsafantakis, Ismahen Lalaymia, Aikaterini Termentzi, Maria Miguel, Stéphane Declerck and Nikolas Fokialakis
Metabolites 2022, 12(7), 573; https://doi.org/10.3390/metabo12070573 - 22 Jun 2022
Cited by 10 | Viewed by 2532
Abstract
Anchusa officinalis (L.) interacts with various microorganisms including arbuscular mycorrhizal fungi (AMF). Recently, the AMF Rhizophagus irregularis MUCL 41833 has been shown to modulate the metabolome of A. officinalis. However, little information is available on the impact that different AMF species may [...] Read more.
Anchusa officinalis (L.) interacts with various microorganisms including arbuscular mycorrhizal fungi (AMF). Recently, the AMF Rhizophagus irregularis MUCL 41833 has been shown to modulate the metabolome of A. officinalis. However, little information is available on the impact that different AMF species may have on primary and secondary plant metabolites. In this study, four AMF species belonging to the genus Rhizophagus (R. irregularis MUCL 41833, R. intraradices MUCL 49410, R. clarus MUCL 46238, R. aggregatus MUCL 49408), were evaluated for their potential to modulate A. officinalis metabolome under controlled semi-hydroponic cultivation conditions. An untargeted metabolomic analysis was performed using UHPLC-HRMS followed by a multivariate data analysis. Forty-two compounds were reported to be highly modulated in relation to the different AMF associations. Among them, six new secondary metabolites were tentatively identified including two acetyl- and four malonyl- phenylpropanoid and saponin derivatives, all presenting a common substitution at position C-6 of the glycosidic moiety. In addition, an enhanced accumulation of primary and secondary metabolites was observed for R. irregularis and R. intraradices, showing a stronger effect on A. officinalis metabolome compared to R. clarus and R. aggregatus. Therefore, our data suggest that different AMF species may specifically modulate A. officinalis metabolite production. Full article
(This article belongs to the Special Issue Secondary Metabolites in Fungi-Plant Interactions)
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Review

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47 pages, 1402 KiB  
Review
The Importance of Microorganisms for Sustainable Agriculture—A Review
by Marcel Antoszewski, Agnieszka Mierek-Adamska and Grażyna B. Dąbrowska
Metabolites 2022, 12(11), 1100; https://doi.org/10.3390/metabo12111100 - 11 Nov 2022
Cited by 21 | Viewed by 5617
Abstract
In the face of climate change, progressive degradation of the environment, including agricultural land negatively affecting plant growth and development, endangers plant productivity. Seeking efficient and sustainable agricultural techniques to replace agricultural chemicals is one of the most important challenges nowadays. The use [...] Read more.
In the face of climate change, progressive degradation of the environment, including agricultural land negatively affecting plant growth and development, endangers plant productivity. Seeking efficient and sustainable agricultural techniques to replace agricultural chemicals is one of the most important challenges nowadays. The use of plant growth-promoting microorganisms is among the most promising approaches; however, molecular mechanisms underneath plant–microbe interactions are still poorly understood. In this review, we summarized the knowledge on plant–microbe interactions, highlighting the role of microbial and plant proteins and metabolites in the formation of symbiotic relationships. This review covers rhizosphere and phyllosphere microbiomes, the role of root exudates in plant–microorganism interactions, the functioning of the plant’s immune system during the plant–microorganism interactions. We also emphasized the possible role of the stringent response and the evolutionarily conserved mechanism during the established interaction between plants and microorganisms. As a case study, we discussed fungi belonging to the genus Trichoderma. Our review aims to summarize the existing knowledge about plant–microorganism interactions and to highlight molecular pathways that need further investigation. Full article
(This article belongs to the Special Issue Secondary Metabolites in Fungi-Plant Interactions)
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