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Metabolites
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Secondary Metabolites in Fungi-Plant Interactions
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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 14771

Special Issue Editors

Prof. Dr. Jolanta Jaroszuk-Ściseł

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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
Special Issues, Collections and Topics in MDPI journals
Dr. Artur Nowak

E-Mail Website
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

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

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. Metabolites 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 2700 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

  • 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

Published Papers (5 papers)

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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 1723
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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Graphical abstract

Graphical abstract
Full article ">Figure 1
<p>Dynamics of EPS (g/L) synthesis by <span class="html-italic">Plenodomus lingam</span> (PLIGR1, PLIGR2, PLIGR3) and <span class="html-italic">Plenodomus biglobosus</span> (PBIGR1, PBIGR2, PBIGR3) strains during the culture growth period of 4–17 days. Statistical data analysis: one-way ANOVA with post hoc Tukey’s HSD test, <span class="html-italic">p</span> &lt; 0.05. Bars with the different letter are statistically significantly different from each other. Standard deviations are shown as deviation bars (<span class="html-italic">n</span> = 3).</p> Full article ">Figure 2
<p>Heat map presenting the differences in the EPS synthesis dynamics between <span class="html-italic">Plenodomus lingam</span> (PLIGR1, PLIGR2, PLIGR3) and <span class="html-italic">Plenodomus biglobosus</span> (PBIGR1, PBIGR2, PBIGR3) species during the 4–14-day culture growth. The colour intensity on the heat map corresponds to the EPS g/L synthesis efficiency.</p> Full article ">Figure 3
<p>Dynamics of fungal biomass growth and changes in the pH value in <span class="html-italic">Plenodomus lingam</span> (PLIGR1, PLIGR2, PLIGR3) and <span class="html-italic">Plenodomus biglobosus</span> (PBIGR1, PBIGR2, PBIGR3) strains during culture growth for 4–17 days. Statistical data analysis: one-way ANOVA with post hoc Tukey’s HSD test, <span class="html-italic">p</span> &lt; 0.05. Bars with the different letter are statistically significantly different from each other. Bars with the different letter are statistically significantly different from each other. Standard deviations are shown as deviation bars (<span class="html-italic">n</span> = 3).</p> Full article ">Figure 4
<p>Heat map presenting the differences in the EPS yield and the biomass growth rate (mg/g) between <span class="html-italic">Plenodomus lingam</span> (PLIGR1, PLIGR2, PLIGR3) and <span class="html-italic">Plenodomus biglobosus</span> (PBIGR1, PBIGR2, PBIGR3) species during the 4–14-day culture growth. The colour intensity on the heat map corresponds to the EPS mg/g synthesis efficiency.</p> Full article ">Figure 5
<p>β-Glucanase activity in cultures of (<b>A</b>) <span class="html-italic">Plenodomus lingam</span> (PLIGR1, PLIGR2, PLIGR3) and (<b>B</b>) <span class="html-italic">Plenodomus biglobosus</span> (PBIGR1, PBIGR2, PBIGR3) strains. Statistical data analysis: one-way ANOVA with post hoc Tukey’s HSD test, <span class="html-italic">p</span> &lt; 0.05. Bars with the different letter are statistically significantly different from each other. Standard deviations are shown as deviation bars (<span class="html-italic">n</span> = 3).</p> Full article ">Figure 6
<p>Invertase activity in cultures of (<b>A</b>) <span class="html-italic">Plenodomus lingam</span> (PLIGR1, PLIGR2, PLIGR3) and (<b>B</b>) <span class="html-italic">Plenodomus biglobosus</span> (PBIGR1, PBIGR2, PBIGR3) strains. Statistical data analysis: one-way ANOVA with post hoc Tukey’s HSD test, <span class="html-italic">p</span> &lt; 0.05. Bars with the different letter are statistically significantly different from each other. Standard deviations are shown as deviation bars (<span class="html-italic">n</span> = 3).</p> Full article ">Figure 7
<p>Ability to synthesise the IAA phytohormone by (<b>A</b>) <span class="html-italic">Plenodomus lingam</span> (PLIGR1, PLIGR2, PLIGR3) and (<b>B</b>) <span class="html-italic">Plenodomus biglobosus</span> (PBIGR1, PBIGR2, PBIGR3) strains. Bars with the different letter are statistically significantly different from each other. Statistical data analysis: one-way ANOVA with post hoc Tukey’s HSD test, <span class="html-italic">p</span> &lt; 0.05. Standard deviations are shown as deviation bars (<span class="html-italic">n</span> = 3).</p> Full article ">Figure 8
<p>Correlation between EPS synthesis efficiency (g/L) and β-glucanase and invertase activity in PLIGR1 (<b>A</b>,<b>D</b>), PLIGR2 (<b>B</b>,<b>E</b>), and PLIGR3 (<b>C</b>,<b>F</b>), and in PBIGR1 (<b>G</b>,<b>J</b>), PBIGR2 (<b>H</b>,<b>K</b>) and PBIGR3 (<b>I</b>,<b>L</b>). The correlations were analysed based on Pearson’s correlation coefficient <span class="html-italic">R</span> and the statistical significance <span class="html-italic">p</span> of this coefficient.</p> Full article ">Figure 9
<p>Correlation matrices between day, pH, biomass, EPS yield, β-glucanase, and invertase activity obtained in cultures of PLIGR1 (<b>A</b>), PLIGR2 (<b>B</b>) and PLIGR3 (<b>C</b>), and PBIGR1 (<b>D</b>), PBIGR2 (<b>E</b>) and PBIGR3 (<b>F</b>). The results are presented as Pearson’s correlation coefficient <span class="html-italic">R</span>.</p> Full article ">Figure 10
<p>Scree plot (<b>A</b>), biplot (<b>B</b>) and plot of points by day (<b>C</b>) of the Principal Component Analysis (PCA) describing the pH, amount of biomass, day of the culture, IAA and EPS yields, and β-glucanase and invertase activities in <span class="html-italic">Plenodomus</span> species.</p> Full article ">
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 2208
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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Figure 1

Figure 1
<p>Schematic of the enzymatic reaction resulting in the formation of a mixture containing synthesised lactobionic acid (sLBA).</p> Full article ">Figure 2
<p>Enzymatic oxidation of lactose and qualitative analysis of the resulting product (lactobionic acid) using HPLC chromatography at 0.5 h, 1 h, 3 h, 6 h, 8 h, and 24 h. (<b>a</b>) Enzymatic system of PlCDH and lactose as a substrate at 30 °C. (<b>b</b>) Enzymatic system of PlCDH, CuLAC, and lactose as a substrate at 30 °C. (<b>c</b>) Enzymatic system of PlCDH and lactose as a substrate at 50 °C. (<b>d</b>) Enzymatic system of PlCDH, CuLAC, and lactose as a substrate at 50 °C.</p> Full article ">Figure 3
<p>Enzymatic oxidation of lactose. (<b>A</b>) Enzymatic system of PlCDH and lactose as a substrate in two temperature conditions over 24 h. (<b>B</b>) Enzymatic system of PlCDH, CuLAC, and lactose as a substrate in two temperature conditions at 24 h. Error bars represent the standard deviation of the three experiments.</p> Full article ">Figure 4
<p>Scheme of the lactobionic acid synthesis process performed using the cellobiose dehydrogenase/lactose system in the presence of a redox mediator (ABTS or DCPIP). The reaction was carried out in two temperature conditions in parallel: 30 °C and 50 °C. PlCDH is able to catalyse the oxidation reaction of disaccharides linked by β-1-4-glycosidic bonds such as lactose. As a result of this process, lactobiono-δ-lactone is formed and spontaneously hydrolysed in an aqueous solution to aldonic acid (lactobionic acid) [<a href="#B20-metabolites-13-00469" class="html-bibr">20</a>]. The reaction is catalysed by a redox mediator; when reduced in a lactose oxidation reaction, it can return to its oxidised form thanks to the presence of CuLAC. With the use of redox mediators, this process can proceed continuously [<a href="#B17-metabolites-13-00469" class="html-bibr">17</a>].</p> Full article ">Figure 5
<p>Qualitative study of lactobionic acid using the TLC method. Samples containing a redox mediator (ABTS (<b>A</b>) or DCPIP (<b>B</b>)) incubated at two different temperatures (30 °C or 50 °C) were used for the analysis. Lane 3 (30 °C) and 4 (50 °C) were samples with ABTS (<b>A</b>), while lane 7 (30 °C) and 8 (50 °C) represented those with DCPIP (<b>B</b>). Control samples were cLBA at a concentration of 20 mM (lanes 2 and 6) and 25 mM lactose in acetate buffer (lanes 1 and 5). After the stain analysis, the presence of both lactose (the oxidized substrate) and lactobionic acid (the product of the enzymatic reaction) was confirmed in the control samples.</p> Full article ">Figure 6
<p>Enzymatic oxidation of lactose and qualitative analysis of the resulting product (lactobionic acid) using HPLC chromatography after 24-h enzymatic reaction. The synthesised acid was labelled as sLBA, while the commercial acid was labelled as cLBA. The reaction conditions are shown in brackets.</p> Full article ">Figure 7
<p>FTIR spectra of lactose (<b>A</b>), acetate buffer (<b>B</b>) and lactobionic acid (<b>C</b>). (<b>D</b>) Comparison of FTIR spectra of A30 (d), A50 (e), D30 (f), and D50 (g) samples after enzymatic reaction. An asterisk marks 1735 cm<sup>−1</sup> band of the C=O<sub>acid</sub> bond.</p> Full article ">Figure 8
<p>Comparison of sample-lactose differential spectra of A30 (a), A50 (b), D30 (c), D50 (d) and pure LBA (e). An asterisk * marks 1735 cm<sup>−1</sup> band of the C=O<sub>acid</sub> bond.</p> Full article ">Figure 9
<p>Results of the 2,2-diphenylpicrylhydrazyl (DPPH) antioxidant test. (<b>A</b>) Antioxidant properties of a reaction mixture containing 12 mM LBA derived from the oxidation of lactose in the presence of ABTS at 30 °C and commercial LBA with the same concentration, (<b>B</b>) 21 mM LBA derived from the oxidation of lactose in the presence of ABTS at 50 °C and commercial LBA with the same concentration, (<b>C</b>) 10 mM LBA extracted via lactose oxidation in the presence of DCPIP at 30 °C and commercial LBA with the same concentration, and (<b>D</b>) 13 mM LBA extracted via lactose oxidation in the presence of DCPIP at 50 °C and commercial LBA with the same concentration. Error bars represent the standard deviation of the three experiments.</p> Full article ">
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 4 | Viewed by 2328
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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Graphical abstract

Graphical abstract
Full article ">Figure 1
<p>Isolated fungus <span class="html-italic">Nigrospora zimmermanii</span> on PDA media, showing (<b>a</b>) top view; (<b>b</b>) back view, microscopy of the isolated fungus <span class="html-italic">Nigrospora zimmermanii</span>; (<b>c</b>) hypha with conidiophores; (<b>d</b>) conidia.</p> Full article ">Figure 2
<p>Re-infection of endophytic fungus in a healthy <span class="html-italic">Catharanthus roseus</span> plant, showing (<b>a</b>) chosen site for infection; (<b>b</b>) creation of wound; (<b>c</b>) inoculation of desired endophytic fungus; (<b>d</b>) site of infection covered with a muslin cloth.</p> Full article ">Figure 3
<p>Phylogenetic tree with most recent common ancestor (green dot and green highlights) and the ultimate common ancestor (gray dot) of the desired isolated fungus <span class="html-italic">Nigrospora zimmermanii</span> (blue dot and yellow highlights).</p> Full article ">Figure 4
<p>HPTLC peaks for vincristine, showing (<b>a</b>) standard at 200 ng/mL; (<b>b</b>) standard at 1 mg/mL; (<b>c</b>) generation 1 at 300 ng/mL; (<b>d</b>) generation 2 at 300 ng/mL; (<b>e</b>) generation 3 at 300 ng/mL; (<b>f</b>) generation 4 at 300 ng/mL; (<b>g</b>) generation 5 at 300 ng/mL; and (<b>h</b>) generation 6 at 300 ng/mL.</p> Full article ">Figure 5
<p>LC–MS chromatogram for vincristine in sample and vincristine standard.</p> Full article ">Figure 6
<p>Mass spectrometry for vincristine in sample and vincristine standard showing m/z [M+2H]<sup>2+</sup> = 413.2458.</p> Full article ">Figure 7
<p>Spectral data for vincristine, showing (<b>a</b>) λ max at 300 nm in standard; (<b>b</b>) λ max at 300 nm in samples.</p> Full article ">
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 9 | Viewed by 2324
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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Graphical abstract

Graphical abstract
Full article ">Figure 1
<p>Principal component analysis (PCA)—Comparison of UHPLC-HRMS metabolic profiles from <span class="html-italic">A. officinalis</span> root (<b>a</b>) and shoot (<b>b</b>) samples associated with <span class="html-italic">R. irregularis</span>, <span class="html-italic">R. intraradices</span>, <span class="html-italic">R. clarus</span> and <span class="html-italic">R. aggregatus</span>, after 9 days of growth in the semi-hydroponic cultivation system. (<span class="html-italic">R. irregularis</span> MUCL 41833: blue dots; <span class="html-italic">R. intraradices</span> MUCL 49410: green dots; <span class="html-italic">R. clarus</span> MUCL 46238: red dots; <span class="html-italic">R. aggregatus</span> MUCL 49408: yellow dots).</p> Full article ">Figure 2
<p>Volcano-plot analysis—Identification of up- and down-regulated compounds (<span class="html-italic">p</span>-value &lt; 0.05 and fold change &gt; 1.5) between <span class="html-italic">A. officinalis</span> root samples associated with four AMF species (<span class="html-italic">R. irregularis</span>, <span class="html-italic">R. intraradices</span>, <span class="html-italic">R. clarus</span> and <span class="html-italic">R. aggregatus</span>) after 9 days of growth in the semi-hydroponic cultivation system. Comparison of metabolic profiles from root samples associated with (<b>a</b>) <span class="html-italic">R. irregularis</span> MUCL 41833 and <span class="html-italic">R. clarus</span> MUCL 46238; (<b>b</b>) <span class="html-italic">R. irregularis</span> MUCL 41833 and <span class="html-italic">R. aggregatus</span> MUCL 49408; (<b>c</b>) <span class="html-italic">R. intraradices</span> MUCL 49410 and <span class="html-italic">R. clarus</span> MUCL 46238; (<b>d</b>) <span class="html-italic">R. intraradices</span> MUCL 49410 and <span class="html-italic">R. aggregatus</span> MUCL 49408. Significant up-regulated compounds are represented in blue (right side of the plots) and down-regulated in magenta (left side of the plots). Blue and magenta arrows represent the amount of up- and down-regulated compounds, respectively, in the specific AMF-plants treatment.</p> Full article ">Figure 3
<p>Volcano-plot analysis—Identification of up- and down-regulated compounds (<span class="html-italic">p</span>-value &lt; 0.05 and fold change &gt; 1.5) between <span class="html-italic">A. officinalis</span> shoot samples associated with four AMF species (<span class="html-italic">R. irregularis</span>, <span class="html-italic">R. intraradices</span>, <span class="html-italic">R. clarus</span> and <span class="html-italic">R. aggregatus</span>) after 9 days of growth in the semi-hydroponic cultivation system. Comparison of metabolic profiles from shoot samples associated with (<b>a</b>) <span class="html-italic">R. irregularis</span> MUCL 41833 and <span class="html-italic">R. clarus</span> MUCL 46238; (<b>b</b>) <span class="html-italic">R. irregularis</span> MUCL 41833 and <span class="html-italic">R. aggregatus</span> MUCL 49408; (<b>c</b>) <span class="html-italic">R. intraradices</span> MUCL 49410 and <span class="html-italic">R. clarus</span> MUCL 46238; (<b>d</b>) <span class="html-italic">R. intraradices</span> MUCL 49410 and <span class="html-italic">R. aggregatus</span> MUCL 49408. Significant up-regulated compounds are represented in blue (right side of the plots) and down-regulated in magenta (left side of the plots). Blue and magenta arrows represent the amount of up- and down-regulated compounds, respectively, in specific AMF-plants treatment.</p> Full article ">Figure 4
<p>Graphical representation of metabolome profile variations in shoots of <span class="html-italic">Anchusa officinalis</span> associated with four different AMF species (<span class="html-italic">R. irregularis</span> MUCL 41883, <span class="html-italic">R. intraradices</span> MUCL 49410, <span class="html-italic">R. clarus</span> MUCL 46238 and <span class="html-italic">R. aggregatus</span> MUCL 49408). The AMF treatment means followed by the same lowercase letters are not significantly different according to HSD Tukey’s test (<span class="html-italic">p</span>-value &lt; 0.05).</p> Full article ">Figure 5
<p>Graphical representation of metabolome profile variations in roots of <span class="html-italic">Anchusa officinalis</span> associated with four different AMF species (<span class="html-italic">R. irregularis</span> MUCL 41883, <span class="html-italic">R. intraradices</span> MUCL 49410, <span class="html-italic">R. clarus</span> MUCL 46238 and <span class="html-italic">R. aggregatus</span> MUCL 49408). The AMF treatment means followed by the same lowercase letters are not significantly different according to HSD Tukey’s test (<span class="html-italic">p</span>-value &lt; 0.05).</p> Full article ">Figure 6
<p>Schematic representation of the circulatory semi-hydroponic cultivation system. The Hoagland solution circulated through the containers supporting <span class="html-italic">Anchusa officinalis</span> plants associated with four different AMF species (<span class="html-italic">R. irregularis</span> MUCL 41833; <span class="html-italic">R. intraradices</span> MUCL 49410; <span class="html-italic">R. clarus</span> MUCL 46238; <span class="html-italic">R. aggregatus</span> MUCL 49408). The nutrient solution in the glass bottle (1) is pumped using a peristaltic pump (2) via silicon tubes (3) to the upper part of the plant container (4) containing <span class="html-italic">A. officinalis</span> plants (5). The solution percolates through the plant container back into the glass bottle. The black arrows indicate the flow direction of the nutrient solution in the tubing. The roots-stained images represent the plant-AMF colonization of the four different AMF species applied in this study.</p> Full article ">

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 19 | Viewed by 4976
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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Figure 1

Figure 1
<p>Multidimensional network of interactions between plants and PGPM, between plants and pathogens, and between PGPM and pathogens.</p> Full article ">Figure 2
<p>Colonization of root by a fungus belonging to <span class="html-italic">Trichoderma</span>. Adhesion and protection of hyphae are mediated by the layer of hydrophobins, whereas lytic enzymes enable penetration of the epidermis. Swollenins facilitate penetration of apoplast through an expansion-like effect on plant cell walls. Recognition of <span class="html-italic">Trichoderma</span>-derived MAMP molecules (swollenins, hydrophobins, cellulolytic enzymes, and chitin) triggers plant responses to infection, i.e., synthesis of antimicrobial compounds (defensins and phytoanticipins), synthesis of the callose wall in order to physically inhibit further penetration, and overproduction of ROS and possibly also alarmones. See text for more details.</p> Full article ">
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