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. 2021 Nov 7;10(11):1448. doi: 10.3390/pathogens10111448

Metabolic Profile and Mycoherbicidal Activity of Three Alternaria alternata Isolates for the Control of Convolvulus arvensis, Sonchus oleraceus, and Xanthium strumarium

Nesma Abdessemed 1, Alessia Staropoli 2,3, Nadjia Zermane 4, Francesco Vinale 3,5,*
Editors: Lawrence S Young, Susanne Zeilinger-Migsich
PMCID: PMC8620798  PMID: 34832604

Abstract

Alternaria alternata isolates C1, S1, and X3 were isolated respectively from the weeds Convolvulus arvensis, Sonchus oleraceus, and Xanthium strumarium in Algiers during 2016 and identified by morphological and molecular analyses. The aim of this investigation was to chemically characterize the exometabolome of these fungi and to evaluate the myco-herbicidal potential of their culture filtrates, crude extracts, or fractions towards target weeds. Results revealed a great heterogeneity in the biochemical profiles of the exometabolome with the remarkable presence of two compounds: tenuazonic acid (TeA) and triprenyl phenol-7 (SMTP-7). To the best of our knowledge, SMTP-7—found in all the isolates—as well as 12-methoxycitromycin detected in the culture filtrate of isolate C1, have never been reported to be produced by A. alternata. Some fractions of isolates C1 and S1 showed symptoms (necrosis and chlorosis) on the detached leaves of C. arvensis and S. oleraceus, respectively with up to 100% phytotoxic effect at low concentration. In conclusion, biochemical characterization revealed great difference of C1, S1, and X3 exometabolome that is likely to explain the difference in their phytotoxic activity. Some fractions (d1, e1, h1, i1, a2, and f2) of isolates C1 and S1 of A. alternata caused severe necrosis and chlorosis on the injured detached leaves of C. arvensis and S. oleraceus, respectively.

Keywords: metabolomics, mass spectrometry, tenuazonicacid, SMTP-7

1. Introduction

Alternaria is a cosmopolitan fungal genus with 275 species [1], widely distributed in soil and organic matter. It includes saprophytic, endophytic, and pathogenic species [2,3]. Alternaria spp.can produce a variety of secondary metabolites [4]. In particular, at least 268 compounds have been reported in the past few decades that can be grouped into several categories, including nitrogen-containing compounds, steroids, terpenoids, pyranones (pyrones), quinones, and phenolics [2]. Many of these secondary metabolites are either mycotoxins or phytotoxins [5]. Alternaria spp. produces more than 70 mycotoxins [6], several species produce also various phytotoxins that are host-specific (HSTs) and non-host-specific (nHSTs) depending upon their physiological and morphological stages [6,7]. On the other hand, several studies demonstrated that metabolite profiling is a reliable tool to characterize and differentiate plant pathogenic fungi [8]. Microbial metabolites can be exploited as natural herbicides [9,10] and their use might be a promising alternative approach to designing bio formulates [11,12]. Their exploitation can also solve the problems of restrictions of living microorganisms such as: limitation of marketing, storage, difficulty of application, time of action, viability, influence of environmental conditions, etc. [13,14]. Several studies have been conducted to assess the herbicidal activity of fungal metabolites on weeds [15,16]. In this contest, some A. alternata compounds showed herbicidal potential against different weeds [17,18] and the target of these phytotoxins on plant cells are mitochondria, chloroplast, plasma membrane, Golgi complex and nucleus, etc. [3]. Tenuazonic acid (TeA) is one of the major toxic compounds produced by Alternaria species [19,20]. TeA shows also other biological properties including antitumor, antibacterial, antiviral, and phytotoxic activities [21,22]. It is also known for its broad-spectrum herbicidal activity to diverse speciessuch as Digitariasanguinalis, Amaranthus retroflexus, Ageratina adenophora, Acalypha australis, Alopecurus japonicus, Ambrosia artemisiifolia, Commelina communis, Cyperus iria, C. difformis, Echinochloa crus-galli, Eclipta prostrata, Erigeron annuus, Geranium carolinianum, Leptochloa chinensis, Sonchus asper, Trifolium repens, and Vicia sativa [23,24].

In our previous investigations, A. alternata (isolates X3, S1, C1) used in the present study were evaluated for their herbicidal potential towards their target weed hosts under controlled and field conditions [25,26]. Disease severity following application of the isolates on their targets reached up to 99% in the detached leaf assay, 80% in pot trial, and 43% in field experiments. The rapeseed-oil-based liquid formulation of isolate X3 reduced cocklebur (Xanthium strumarium L.) height, root length and dry weight by up to 50%, 27%, and 58%, respectively in pot trial and 40%, 51%, and 45%, respectively in the field experiment. Similarly, the liquid formulation of isolate S1 reduced sow thistle (Sonchus oleraceus L.) height, root length, and dry weight by up to 80%, 65%, and 80%, respectively in pot trial and 39%, 50%, and 44%, respectively in the field experiment [27] unpublished data. None of the crops tested for host specificity including tomato (Solanum lycopersicum cv. Saint Pierre, Solanaceae), wheat (Triticum durum cv. Vitron, Poaceae), faba bean (Vicia faba cv. Aquadulce, Fabaceae), and zucchini (Cucurbita pepo cv. Quarantaine, Cucurbitaceae) was susceptible to the three A. alternata isolates.

The aim of this study was to characterize, with a metabolomic approach, three different strains of Alternaria alternata (isolates X3, S1, C1) recovered from their target weeds—namely Xanthium strumarium L., Sonchus oleraceus L., and Convolvulus arvensis L.—and to evaluate their myco-herbicidal potential on detached leaves of their host weeds.

2. Results

2.1. Chemical Characterization of Alternaria alternata Isolates C1, S1, and X3

Organic crude extracts, obtained from A. alternata culture filtrates, showed differences in terms of biochemical profile. Hence, the number of compounds detected in the organic extracts was 27, 29, 20 compounds (identified and unidentified), respectively in A. alternata C1, S1, and X3. LC-MS qTOF analysis allowed the identification of 15 compounds differently occurring in the isolates. In Table 1 and (Supplementary Materials) Table S1 are reported the main compounds detected on the crude extract of C1, S1, and X3.

Table 1.

Main secondary metabolites identified in organic extracts of Alternaria alternata C1, S1, and X3 by LC-MSqTOF analysis.

Compounds Alternaria alternata Isolates
C1 S1 X3
Cyclo-l-prolylglycine + + +
12-Methoxycitromycin + − −
Erythroglaucin + − −
Alternarian acid + − −
TAN 913 + − −
Verrol + + +
Tenuazonicacid + + +
Brassicicene F + + +
Rezishanone C + + +
Brassicicene D + + −
Chaetoquadrin E + − −
Tanzawaicacid F + − −
Cytosporin C − + −
Striatisporin − + −
Cyclo-(Pro-Ala) − − +
Triprenyl phenol-7 (SMTP-7) + + +
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+ = presence of the specific compound;− = absence of the specific compound.

Figure 1 shows total ion chromatograms (TIC) for the three isolates. It can be seen that tenuazonic acid (TeA) represents the major compound in organic extracts of all the three isolates in an isolate-dependent concentration (relative concentration).

Figure 1.

Figure 1

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Total ion chromatograms (TIC) LC-MS qTOF chromatograms of Alternaria alternata organic extracts of isolates X3, S1, and C1.

Cyclo-L-prolylglycine, verrol, brassicene F, and rezishanone C were also detected in all samples at a lower concentration compared to TeA. Brassicicene D is another common compound, produced by A. alternata isolates C1 and S1. The compounds 12-methoxycitromycin, erythroglaucin, alternarian acid, TAN 913, chaetoquadrin E, and tanzawaic acid F are compounds only found in the culture filtrate of isolate C1, whereas cytosporin C and striatisporin A are only found in the culture filtrate of A. alternata isolate S1. Similarly, Cyclo-(Pro-Ala) is only found in the culture filtrate of A. alternata isolate X3 (Table 1).

The analysis of the samples obtained after fractionating the crude extract of C1 showed that all fractions contain the Stachybotrys microspora metabolite named triprenylphenol-7 (SMTP-7). The fractions from C1 contained also tenuazonic acid, decarestrictin N that was less abundant, and only one fraction contained tricycloalternarene (ACTG) toxin A.

Regarding A. alternata isolate S1, 2 out of 7 fractions—obtained from the crude extract—contain SMTP-7 and tenuazonic acid; while ACTG toxin A (low abundance), virescenoside M and phoenistatin (high abundance) were detected in one fraction.

As for the composition of A. alternata isolate X3, 6 out of 8 fractions contain decarestrictin N, while all the fractions contain SMTP-7. Five out of the 8 fractions contain tenuazonic acid and benzoic acid is detected in two fractions in small amounts. Cyclo-(L-Phe-L-Pro) is found exclusively in one fraction of isolate X3 (Supplementary Materials: Table S2).

2.2. Herbicidal Activity (Detached Leaf Assay)

2.2.1. Effect of C1 Metabolites on Detached Leaves of Convolvulus arvensis

Fractions d1, e1, h1, and i1 were able to cause symptoms on injured detached leaves. Analysis of variance showed a significant effect of the crude extract and the fractions d1, e1, and i1 on the severity of phytotoxicity on injured leaves (p ≤ 0.001, df = 12, MS = 5782.59, F = 346.95) (Figure 2).

Figure 2.

Figure 2

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Effect of exometabolites of Alternaria alternata isolate C1 on injured detached leaves of Convolvulus arvensis. C. extract: crude extract; F.a1–j1: Fractions a1–j1; Ctrl. Meth.: methanol control; Ctrl. SDW: sterile distilled water control; a, b, c: represent the homogeneous groups.

C1 crude extract and d1–e1 fractions resulted in small necroses surrounded by chlorosis; both fractions caused total leaf destruction at the end of the experiment (4 days). The h1 fraction caused larger necrosis compared to d1 and e1 but did not result in total leaf destruction; the i1 fraction caused black spots that subsequently occupied the entire leaf surface. Both controls remained symptomless (Figure 3).

Figure 3.

Figure 3

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Appearance of the injured detached leaves of Convolvulus arvensis after treatment with the crude extract and fractions d1, e1, h1, and i1 of Alternaria alternata isolate C1. d.a.a.: days after application (1 or 4 days). C. extract: crude extract; F.a1–j1: Fractions a1–j1; Ctrl. Meth.: methanol control; Ctrl. SDW: sterile distilled water control.

2.2.2. Effect of S1 Metabolites on Detached Leaves of Sonchus oleraceus

Fractions a2 and f2 caused symptoms on the injured detached leaves. The analysis of variance showed a significant phytotoxic effect of fraction a2 on the injured detached leaves (p = 0.001, df = 9, MS = 124.44, F = 14.93). However, severity level of both fractions was not high (Figure 4).

Figure 4.

Figure 4

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Effect of crude extract and fractions of Alternaria alternata isolate S1 on injured detached leaves of Sonchus oleraceus. C. extract: crude extract; F. a2–g2: Fractions a2–g2; Ctrl. Meth.: methanol control, Ctrl. SDW: sterile distilled water control; a, b: represent the homogeneous groups.

Symptoms caused by both fractions were in the form of brown areas (Figure 5). The crude extract did not cause any symptoms.

Figure 5.

Figure 5

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Appearance of the injured detached leaves of Sonchus oleraceus after treatment with the fractions a2 and f2 of Alternaria alternata isolate S1. d.a.a.: days after application. F.a2–f2: Fractions a2–f2; Ctrl. Meth.: methanol control, Ctrl. SDW: sterile distilled water control.

2.2.3. Effect of X3 Metabolites on Detached Leaves of Xanthium strumarium

The crude extract and the eight fractions recovered from A. alternata isolate X3 did not show any effect on either injured or uninjured detached leaves of the target weed.

Table 2 shows the active fractions and their corresponding exometabolites identified by LC-MS analysis. The main compounds common in all the active fractions are SMTP-7 and tenuazonic acid.

Table 2.

Active fractions and corresponding exometabolites identified.

Alternaria alternataIsolates Active Fractions Compounds
A. alternata C1 d1 SMTP-7
(+)-Phomopsidin
Tenuazonic acid
e1 Decarestrictin N
SMTP-7
Tenuazonic acid
h1 SMTP-7
Tenuazonic acid
i1 Decarestrictin N
SMTP-7
Tenuazonic acid
A. alternata S1 a2 SMTP-7
f2 Decarestrictin N
SMTP-7
Tenuazonic acid
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3. Discussion

The biochemical profile of organic extracts of the three isolates of A. alternata showed different composition, but with some common compounds—i.e., tenuazonic acid and SMT7 that were found in almost all fractions from the three crude extracts. These results are in agreement with those reported by Sottoret al. [28]. Their work showed that Streptomyces strains, closely related through the 16S rRNA gene marker, produced a common set of natural compounds and another set that is unique for each strain (SN25_8.1 and DSM 40236T); they considered the common secondary metabolites as core molecules and the strain-specific compounds as accessory natural products. Ukaet al. [29] also found that Aspergillus flavus has a high intraspecies diversity of secondary metabolites. Llorenset al. [30] studied the influence of incubation temperature, water activity (aw), and type of isolate on the production of deoxynivalenol (DON), nivalenol (NIV), and 3-acetyldeoxynivalenol (3-AcDON) by three isolates of Fusarium graminearum and three isolates of Fusarium culmorum from different hosts (wheat, corn, banana, and leek) in different regions of Spain. They found that the production of these toxins differs (present, absent, and trace) between isolates of the same species grown in the same conditions.

Davis et al. [17], found that isolates 582 and 584 of Alternaria alternata produced tenuazonic acid but not isolate 938 of the same fungal species when grown on cottonseed and yeast-sucrose extract broth.

Schumacher et al. [31] also found a difference in biochemical composition of seven strains of A. alternata isolated from plant litter from different regions in Australia.

This difference among strains can be explained by morphological and cultural characteristics Schumacher et al. [31], the horizontal genes transfer (HGT) of entire biosynthetic pathways [32,33], the environmental competition, the survival needs of the strain, the need to adapt and specialize in their ecological niche, and host differences [28,29].

In our study, tenuazonic acid was found to be the major compound of the three culture filtrates and was detected in most of the fractions. This finding agrees with results of Meronucket al. and Davis et al. [17,34] that found this metabolite in their selected strains at different concentrations. Tenuazonic acid was first isolated from Alternaria tenuis by Rosettet al. [35]. It was detected in culture filtrates of several species of Alternaria genus: A. longiceps, A. kikuchiana, A. mali, A. alternata, and A. tenuissima [19,36]. Tenuazonic acid is known as a natural potential herbicide for which different bioassays (such as cut shoot, seedling, and detached leaf bioassays) have been used [16,18].

The second important exometabolite detected was SMTP-7 (Stachybotrys microspora triprenyl phenol-7) which is a low molecular weight compound that has a thrombolytic, anti-inflammatory, and antioxidant effects. This molecule is usually secreted by the fungal species Stachybotrys microspora and is known for its therapeutic activity against cerebral infarction in several rodent models [36,37]. To the best of our knowledge, neither SMTP-7 nor 12-methoxycitromycin detected in the culture filtrate of isolate C1 (Table 2) have been reported to be produced by Alternaria spp.

Some fractions from isolates C1 and S1 (d1, e1, h1, i1, a2, and f2) caused symptoms (necrosis and chlorosis) on injured detached leaves of S. oleraceus and C. arvensis. The four fractions (d1, e1, h1, and i1) that gave an effect on injured detached leaves of C. arvensis all contain SMTP-7 and tenuazonic acid. These compounds are also present in two other fractions (g1 and j1) that did not give an effect. Fractions a2 and f2, that showed an effect on injured detached leaves of S. oleraceus, contain SMTP-7, whereas the fraction f2 contains tenuazonic acid and decarestrictin N. These identified compounds are also present in other fractions that did not give an effect. Therefore, phytotoxic activity might eventually be also explained by the synergistic effect of the different molecules identified in the fractions.

Our findings regarding the herbicidal effect agree with the results of several studies that showed the efficiency of secondary metabolites from Alternaria towards different weeds (Xanthium occidentale, Parthenium hysterophorus, and Lantana camara) [15,16,18]. Such effects may be due to the presence of phytotoxic substances with herbicidal potential [10,38,39].

The crude extract and its fractions from isolate X3 did not show any effect on the injured detached leaves of X. strumarium. This result could be explained if we consider that this weed is less sensitive to the tested compounds than the other two weeds. On the other hand, the toxicogenic potency of Alternaria species and the effect of each toxic component vary between different isolates [40,41]. Zhou et al. [24] found that the effect of secondary metabolites of A. alternata on plants increases with increasing concentration of secondary metabolites and that this effect differs between the plant species.

Secondary metabolites cannot penetrate the leaf, and for this reason several authors [15,38] recommended the combination of secondary metabolites with the pathogen itself (the pathogen could be assisted by the toxin during the penetration and colonization phase to increase the level of disease on the weed without any effect on the non-host plant), as well as with other control methods in integrated weed management.

4. Materials and Methods

4.1. Fungal Isolates

Three isolates of Alternaria alternata (Fries.) Kiessler (X3, S1, C1) were previously recovered from Xanthium strumarium, Sonchus oleraceus and Convolvulus arvensis, respectively and documented [25,42]. These isolates showed morphological and cultural differences. Sequences of internal transcribed spacer (ITS) of the isolates X3, S1, and C1 were deposited in the NCBI Genebank (accession numbers MH827056, MH879766, and MH828350) and showed 99% homology with the sequences of the holotype of A. alternata CBS 916.96 (accession no. KF465761).

The fungal isolates were cultured on Potato Dextrose Agar medium (PDA; 200 g potato, 20 g dextrose, and 20 g agar in 1000 mL distilled water) in Petri dishes (9 cm in diameter) and incubated at 25 °C in the dark for 7 days, then stored at 4 °C until use.

4.2. Metabolites Production and Extraction

Small plugs (3 mm in diameter) from 7-day-old cultures of each of the fungal isolates were used to inoculate individually 2000 mL of Potato Dextrose Broth (PDB) liquid medium in 5000 mL capacity Erlenmeyer flasks. The fungal cultures were incubated statically under laboratory conditions for 21 days. Afterwards, mycelium-free culture filtrates were recovered by filtration through two-layer muslin cloth. The culture filtrates were subsequently extracted three times with equal volumes of ethyl acetate using a separating funnel and the resulting organic extracts were dehydrated with anhydrous sodium sulfate (Na2SO4). The extracts were concentrated using a rotary evaporator (IKA®-Werke GmbH & CO. KG, Staufen, Germany) under vacuum and at 40 °C [43].

4.3. Metabolite Fractionation

The crude extracts of isolates X3, S1, and C1 of A. alternata were fractionated by direct phase column chromatography (CC) eluted with different solvents (Supplementary Materials: Table S3) yielding different groups of homogeneous fractions.

4.4. HPLC-MS Analysis

A high-performance liquid chromatography-mass spectrometry (HPLC-MS) method was developed using an HPLC coupled to a quadrupole time-of-flight (Q-TOF) mass spectrometer with a dual electrospray ionization (ESI) source and equipped with a diode array detector (DAD) system (Agilent Technologies, Santa Clara, CA). Flow rate was set at 0.40 mL min−1. Metabolites were eluted at constant temperature of 37 °C, using a linear gradient composed by A: 0.1% (v/v) formic acid (FA) in H2O and, B: 0.1% (v/v) FA in acetonitrile (ACN). The gradient was as follows: starting condition 5% B, 0 min, 100% B in 6 min and held for8 min, 5% B for 9 and 10 min. UV spectra were collected by DAD every 0.4 s from 190 to 750 nm with a resolution of 2 nm. MS parameters were set with Agilent Mass Hunter Data Acquisition Software, rev. B.05.01. The instrument operated in positive mode, as [M + H]+ions; MS spectra were recorded in centroid mode, with an m/z 100–1700 mass range. The injected sample volume was 7 μL. In order to perform real-time lock mass correction, an isocratic pump (1260 Infinity Series, Agilent Technologies) was used to infuse a standard solution consisting of two reference mass compounds: purine (C5H4N4, m/z 121.050873, 10 μmolL−1) and hexakis (1H,1H,3H-tetrafluoropentoxy)-phosphazene(C18H18O6N3P3F24, m/z 922.009798, 2 μmolL−1). Flow rate was set at 0.06 mL min−1 while the detection window and the minimum height were set at 1000 ppm and 10,000 counts, respectively, for reference mass correction.

4.5. Detached Leaf Assay

Healthy leaves detached from the three weed hosts were surface sterilized in 2% sodium hypochlorite for 5 min, rinsed three times with sterile distilled water (SDW) and blotted dry in sterile paper sheets. Half of the leaves were injured using fine sterile needles (10small wounds were practiced over the entire surface of the leaf blade). Injured and uninjured leaves were then placed adaxial side up on wet filter paper in glass sterile Petri dishes (9 cm diameter, 2 leaves per dish).

Leaves were then treated each with 50 µL of the crude extract solutions and their fractions applied separately all over the limb. To distinguish between fractions, the numbers 1, 2, and 3 were assigned, respectively to fractions from isolates C1, S1, and X3. The fractions; c1, e2, e3, and d3 were not tested because of insufficient amounts. In the injured leaves, 5 µL of each diluted fraction were deposited on the wounds. Control leaves were treated with the same volume of SDW or with methanol at 2% [15,18]. Crude extracts and fractions were used at a concentration of 0.1 mg mL−1. All leaves were incubated at 25 °C and 60% relative humidity (RH) under laboratory conditions. Phytotoxic effect was monitored daily starting from the first day after treatment. At the end of the experiment which lasted 4, 7, and 9 days for the detached leaves of C. arvensis, S. oleraceus, and X. strumarium respectively, the severity of phytotoxicity of crude extracts and fractions tested was recorded for each treatment using a 0–5 rating scale of [16] as follows:0: 0–4%: no effect, 1: 2–19%: slight chlorosis; 2: 20–49%: marked chlorosis and slight necrosis; 3: 50–79%: acute chlorosis and marked necrosis; 4: 80–94%: high chlorosis and high necrosis; 5: 95–100%: acute chlorosis and necrosis.

4.6. Data Analysis

Detached leaf experiment was conducted in a randomized complete block design and was repeated twice with 2 replicates per treatment in the first experiment and 3 replicates in the second one. Data were subjected to analysis of variance (One-way ANOVA). Means were compared using HSD of Tukey at p ≤ 0.05 using the STATISTICA software (Statistica version 8.5, year 2014).

5. Conclusions

It can be concluded from our findings that the biochemical composition of the organic extracts showed great biochemical heterogeneity within the three isolates (C1, S1, and X3) of A. alternata with the remarkable presence of tenuazonic acid and SMTP-7. Only the crude extract of isolate C1 and some fractions (d1, e1, h1, i1, a2, and f2) of the two isolates (C1 and S1) of A. alternata showed symptoms (necrosis and chlorosis) on the injured detached leaves of C. arvensis and S. oleraceus, respectively. Therefore, it would be interesting to broaden the spectrum of research to highlight the whole biochemical active composition of these fungi and their effects on other weeds.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/pathogens10111448/s1, Table S1: Putatively identified metabolites in cultural filtrates of A. Alternata isolates C1. S1 and X3 obtained by LC-MS analysis. Data include retention time, experimental and theoretical mono-isotopic mass and molecular formula, Table S2: Chemical characterization of Alternaria alternata fractions (isolates C1. S1 and X3).(+ indicate the presence of a single compound; − indicate the absence of the single compound), Table S3: Solvent proportions used as eluents in the fractionation of crude extracts of Alternaria alternata isolates X3 S1 and C1 by column chromatography.

Click here for additional data file. (131.8KB, zip)

Author Contributions

Conceptualization, F.V., N.A., and N.Z.; Methodology, F.V., A.S., N.A., and N.Z.; Writing—original draft preparation, N.A.; Review and editing, N.Z. and F.V.; Supervision F.V. and N.Z.; Funding acquisition, F.V. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by MISE CRESO grant number protection no. F/050421/01-03/X32; Viabio no. F/200095/01-03/X45; and Regione Campania (Project Dioniso, no. B98H19005010009).The first author’s (A.N.) mobility within a PhD program was supported by a grant from the Algerian Ministry of Higher Education and Scientific Research (MESRS—Algeria).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The datasets generated during and/or analysed during the current study can be find in the main text and the supplementary materials.

Conflicts of Interest

The authors declare no conflict of interest.

Footnotes

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  • 1.Simmons E.G. Alternaria: An Identification Manual. 2nd ed. CBS Biodiversity; Utrecht, The Netherlands: 2007. p. 775. [Google Scholar]
  • 2.Lou J., Fu L., Peng Y., Zhou L. Metabolites from Alternaria fungi and their bioactivities. Molecules. 2013;18:5891–5935. doi: 10.3390/molecules18055891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Meena M., Gupta S.K., Swapnil P., Zehra A., Dubey M.K., Upadhyay R.S. Alternaria toxins: Potential virulence factors and genes related to pathogenesis. Front. Microbiol. 2017;8:1–14. doi: 10.3389/fmicb.2017.01451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Andersen B., Nielsen K.F., Pinto V.F., Patriarca A. Characterization of Alternaria strains from Argentinean blueberry, tomato, walnut and wheat. Int. J. Food Microbiol. 2015;196:1–10. doi: 10.1016/j.ijfoodmicro.2014.11.029. [DOI] [PubMed] [Google Scholar]
  • 5.Patriarcaa A., Cabrala L.D.C., Pavicicha M.A., Nielsen K.F., Andersen B. Secondary metabolite profiles of small-spored Alternaria support the new phylogenetic organization of the genus. Int. J. Food Microbiol. 2019;29:135–143. doi: 10.1016/j.ijfoodmicro.2018.11.022. [DOI] [PubMed] [Google Scholar]
  • 6.Meenaa M., Samal S. Alternaria host-specific (HSTs) toxins: An overview of chemical characterization, target sites, regulation and their toxic effects. Toxicol. Rep. 2019;6:745–758. doi: 10.1016/j.toxrep.2019.06.021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Thomma B.H.J. Alternaria spp.: From general saprophyte to specific parasite. Mol. Plant Pathol. 2003;4:225–236. doi: 10.1046/j.1364-3703.2003.00173.x. [DOI] [PubMed] [Google Scholar]
  • 8.Siciliano I., Ortega S.F., Gilardi G., Bosio P., Garibaldi A., Gullino M.L. Molecular phylogeny and characterization of secondary metabolite profile of plant pathogenic Alternaria species isolated from basil. Food Microbiol. 2018;73:264–274. doi: 10.1016/j.fm.2018.02.001. [DOI] [PubMed] [Google Scholar]
  • 9.Kenfield D., Bunkers G., Strobel G.A., Sugawara F. Potential new herbicides—Phytotoxins from plant pathogens. Weed Technol. 1988;2:519–524. doi: 10.1017/S0890037X00032383. [DOI] [Google Scholar]
  • 10.Evidente A., Cimmino A., Andolfi A., Berestetskiy A., Motta A. Phomachalasins A-D, 26-oxa [16] and [15] cytochalasans produced by Phomaexigua var. exigua, a potential mycoherbicide for Cirsium arvense biocontrol. Tetrahedron. 2011;67:1557–1563. doi: 10.1016/j.tet.2010.12.058. [DOI] [Google Scholar]
  • 11.Vinale F., Sivasithamparam K. Beneficial effects of Trichoderma secondary metabolites on crops. Phytother. Res. 2020;34:2835–2842. doi: 10.1002/ptr.6728. [DOI] [PubMed] [Google Scholar]
  • 12.Woo S.L., Pepe O. Microbial consortia: Promising probiotics as plant biostimulants for sustainable agriculture. Front. Plant Sci. 2018;9:1801. doi: 10.3389/fpls.2018.01801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Glare T., Caradus J., Gelernter W., Jackson T., Keyhani N., Köhl J., Marrone P., Morin L., Stewart A. Have biopesticides come of age? Trends Biotechnol. 2012;30:250–258. doi: 10.1016/j.tibtech.2012.01.003. [DOI] [PubMed] [Google Scholar]
  • 14.Charudattan R., Dinoor A. Biological control of weeds using plant pathogens: Accomplishments and limitations. Crop Prot. 2000;19:691–695. doi: 10.1016/S0261-2194(00)00092-2. [DOI] [Google Scholar]
  • 15.Vurro M., Evidente A., Andolfi A., Zonno M.C., Giordano F., Motta A. Brefeldin A and a,b-dehydrocurvularin, two phytotoxins from Alternaria zinniae, a biocontrol agent of Xanthium occidentale. Plant Sci. 1998;138:67–79. doi: 10.1016/S0168-9452(98)00131-9. [DOI] [Google Scholar]
  • 16.Sanodiya B.S., Thakur G.S., Baghel R.K., Pandey A.K., Prasad G.B.K.S., Bisen P.S. Isolation and characterization of tenuazonic acid produced by Alternaria alternata, a potential bioherbicidal agent for control of Lantana camara. J. Plant Prot. Res. 2010;50:133–139. doi: 10.2478/v10045-010-0023-3. [DOI] [Google Scholar]
  • 17.Davis N.D., Diener U.L., Morgan-Jones G. Tenuazonic Acid Production by Alternaria alternata and Alternaria tenuissima Isolated from Cotton, Appl. Environ. Microbiol. 1977;34:155–157. doi: 10.1128/aem.34.2.155-157.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Sanodiya B.S., Thakur G.S., Debnath M., Pandey A.K., Prasadd G.B.K.S., Bisen P.S. Characterization of herbicidal potential of tenuazonic acid isolated from Alternaria alternata for the management of Parthenium hysterophorus. Rom. J. Plant Prot. 2009;2:49–61. [Google Scholar]
  • 19.Alexander J., Benford D., Boobis A., Ceccatelli S., Cottrill B., Cravedi J., Farmer P. Scientific opinion on the risks for animal and public health related to the presence of Alternaria toxins in feed and food. EFSA J. 2011;9:2407–2504. [Google Scholar]
  • 20.Yun C.S., Motoyama T., Osada H. Biosynthesis of the mycotoxin tenuazonic acid by a fungal NRPS–PKS hybrid enzyme. Nat. Commun. 2015;6:1–9. doi: 10.1038/ncomms9758. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Miller F.A., Rightsel W.A., Sloan B.J., Ehrlich J., French J.C., Bartz Q.R., Dixon G.J. Antiviral activity of tenuazonic acid. Nature. 1963;200:1338–1339. doi: 10.1038/2001338a0. [DOI] [PubMed] [Google Scholar]
  • 22.Lebrun M.H., Nicolas L., Boutar M., Gaudemer F., Ranomenjanahary S., Gaudemer A. Relationships between the structure and the phytotoxicity of the fungal toxin tenuazonic acid. Phytochemistry. 1988;27:77–84. doi: 10.1016/0031-9422(88)80594-6. [DOI] [Google Scholar]
  • 23.Chen S., Qiang S. Recent advances in tenuazonic acid as a potential herbicide. Pestic. Biochem. Physiol. 2017;143:252–257. doi: 10.1016/j.pestbp.2017.01.003. [DOI] [PubMed] [Google Scholar]
  • 24.Zhou B., Wang H., Meng B., Wei R., Wang L., An C., Chen S., Yang C., Qiang S. An evaluation of tenuazonic acid, a potential biobased herbicide in cotton. Pest Manag. Sci. 2019;75:2482–2489. doi: 10.1002/ps.5402. [DOI] [PubMed] [Google Scholar]
  • 25.Abdessemed N., Kerroum A., Bahet Y.A., Talbi N., Zermane N. First report of Alternaria leaf spot caused by Alternaria alternata (Fries.) Kiessler on Sonchusoleraceus L. and Convolvulus arvensis L. in Algeria. J. Phytopathol. 2019;167:321–325. doi: 10.1111/jph.12800. [DOI] [Google Scholar]
  • 26.Abdessemed N., Bahet Y.A., Zermane N. Mycoherbicide potential of Alternaria alternata (Fries.) Kiessler and its formulations on the host weed Xanthium strumarium L. Biocontrol Sci. Technol. 2020;30:1300–1315. doi: 10.1080/09583157.2020.1814692. [DOI] [Google Scholar]
  • 27.Abdessemed N. Ph.D. Thesis. Ecole Nationale Supérieure Agronomique; El-Harrach, Algeria: Jan 7, 2021. Champignons À Potentiel Mycoherbicide. [Google Scholar]
  • 28.Sottor I., Wiese J., Lipfert M., Preußke N., Sönnichsen F.D., Imho J.F. Different Secondary Metabolite Profiles of Phylogenetically almost Identical Streptomyces griseus Strains Originating from Geographically Remote Locations. Microorganisms. 2019;7:166. doi: 10.3390/microorganisms7060166. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Uka V., Moore G.G., Arroyo-Manzanares N., Dashnor N., De Saeger S., Di Mavungu J.D. Secondary Metabolite Dereplication and Phylogenetic Analysis Identify Various Emerging Mycotoxins and Reveal the High Intra-Species Diversity in Aspergillus flavus. Front. Microbiol. 2019;10:667. doi: 10.3389/fmicb.2019.00667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Llorens A., Mateo R., Hinojo M.J., Valle-Algarra F.M., Jiménez M. Influence of environmental factors on the biosynthesis of type B trichothecenes by isolates of Fusarium spp. from Spanish crops. Int. J. Food Microbiol. 2004;94:43–54. doi: 10.1016/j.ijfoodmicro.2003.12.017. [DOI] [PubMed] [Google Scholar]
  • 31.Schumacher M.J., Sandra E.J. Variability of Alternaria alternata: Biochemical and immunological characteristics of culture filtrates from seven isolates. J. Allergy Clin. Immunol. 1976;58:263–277. doi: 10.1016/0091-6749(76)90131-7. [DOI] [PubMed] [Google Scholar]
  • 32.Khaldi N., Collemare J., Lebrun M.H., Wolfe K.H. Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi. Genome Boil. 2008;9:1–10. doi: 10.1186/gb-2008-9-1-r18. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Ziemert N., Lechner A., Wietz M., Millán-Aguiñaga N., Chavarria K.L., Jensen P.R. Diversity and evolution of secondary metabolism in the marine actinomycete genus Salinispora. Proc. Natl. Acad. Sci. USA. 2014;111:E1130–E1139. doi: 10.1073/pnas.1324161111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Meronuck R.A., Steele J.A., Mirocha C.J., Christensen C.M. Tenuazonic Acid, a Toxin Produced by Alternaria alternata. Appl. Microbiol. 1972;23:613–617. doi: 10.1128/am.23.3.613-617.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Rosett T., Sankhala R.H., Stickings C.E., Taylor M.E.U., Thomas R. Studies in the biochemistry of micro-organisms. 103. Metabolites of Alternaria tenuis Auct.: Culture filtrate products. Biochem. J. 1957;67:390–400. doi: 10.1042/bj0670390. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Hashimoto T., Shibata K., Nobe K., Hasumi K., Honda K. A Novel Embolic Model of Cerebral Infarction and Evaluation of Stachybotrys microspora Triprenyl Phenol-7 (SMTP-7), a Novel Fungal Triprenyl Phenol Metabolite. J. Pharmacol. Sci. 2010;114:41–49. doi: 10.1254/jphs.10131FP. [DOI] [PubMed] [Google Scholar]
  • 37.Sawada H., Nishimura N., Suzuki E., Zhuang J., Hasegawa K., Takamatsu H., Honda K., Hasumi K. SMTP-7, a novel small-molecule thrombolytic for ischemic stroke: A study in rodents and primates. J. Cereb. Blood Flow Metab. 2014;34:235–241. doi: 10.1038/jcbfm.2013.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Evidente A., Capasso R., Cutignano A., Taglialatela-Scafati O., Vurro M., Zonno M.C., Motta A. Ascaulitoxin, a phytotoxique bis-amino acid N-glucoside from Ascochytacaulina. Phytochemistry. 1998;48:1131–1137. doi: 10.1016/S0031-9422(97)01072-8. [DOI] [Google Scholar]
  • 39.Cimmino A., Andolfi A., Zonno M.C., Avolio F., Berestetskiy A., Vurro M., Evidente A. Chenopodolans A–C: Phytotoxic furopyrans produced by Phoma chenopodiicola, a fungal pathogen of Chenopodium album. Phytochemistry. 2013;96:208–213. doi: 10.1016/j.phytochem.2013.10.007. [DOI] [PubMed] [Google Scholar]
  • 40.Meena M., Zehra A., Dubey M.K., Aamir M., Gupta V.K., Upadhyay R.S. Comparative evaluation of biochemical changes in tomato (Lycopersicon esculentum Mill.) infected by Alternaria alternata and its toxic metabolites (TeA, AOH, and AME) Front. Plant Sci. 2016;7:1408. doi: 10.3389/fpls.2016.01408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Meena M., Swapnil P., Upadhyay R.S. Isolation, characterization and toxicological potential of Alternaria-mycotoxins (TeA, AOH and AME) in different Alternaria species from various regions of India. Sci. Rep. 2017;7:1–19. doi: 10.1038/s41598-017-09138-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Abdessemed N., Kerroum A., Bahet Y.A., Zermane N. First report of Alternaria alternata leaf spot on Xanthium strumarium L. in Algeria. Plant Pathol. J. 2019;101:781. doi: 10.1007/s42161-019-00245-2. [DOI] [Google Scholar]
  • 43.Qiang S., Wang L., Wei R., Zhou B., Chen S., Zhu Y., Dong Y., An C. Bioassay of the Herbicidal Activity of AAC-Toxin Produced by Alternaría alternata isolated from Ageratina adenophora. Weed Technol. 2010;24:197–201. doi: 10.1614/WT-D-09-00016.1. [DOI] [Google Scholar]

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Supplementary Materials

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Data Availability Statement

The datasets generated during and/or analysed during the current study can be find in the main text and the supplementary materials.

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