Giovanni Beccari
Francesco Tini
Hans J. L. Jørgensen- 1Department of Agricultural, Food and Environmental Sciences, University of Perugia, Perugia, Italy
- 2Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Frederiksberg, Denmark
Editorial on the Research Topic
Current advances in the metabolism of mycotoxins in plants
Mycotoxins are toxic secondary metabolites (SM) produced by various genera of filamentous fungi. They can induce a wide variety of harmful effects in humans and animals. Often, mycotoxin accumulation begins in plants when they are attacked by mycotoxigenic fungi. However, plants have the ability to transform and detoxify phytotoxic chemical compounds such as mycotoxins (Berthiller et al., 2007; Berthiller et al., 2013). Thus, plants can transform mycotoxins, and in some cases, the resulting compounds may be harmless, while in others, they may be toxic, being considered as “masked mycotoxins” (Freire and Sant’Ana, 2018; Zhang et al., 2020). For some mycotoxins, the host’s ability to metabolize these compounds is well-known, while for others, limited data are available. Conversely, SM produced by non-pathogenic fungal microorganisms could have an antifungal role against pathogenic fungi (Rodrigo et al., 2022). SM can also interact with plant metabolism, enhancing the plant’s defence to counteract pathogens (Elhamouly et al., 2022).
For all these reasons, understanding the metabolism of mycotoxins in plants is a key aspect of counterbalancing their spread in food/feed products and adopting mitigation tactics to reduce human and animal health hazards. In this context, the objective of this Research Topic was to collect articles relative to the current advances in the metabolism of mycotoxins. This Research Topic contains five manuscripts that cover significant aspects of this field.
The paper written by Meng et al. highlights introductory elements showing the presence of mycotoxigenic fungi in cereal grain. They reported the presence of Aspergillus, Fusarium and Alternaria, as well as their abilities to produce mycotoxins, in wheat and paddy grains (fresh and stored samples) collected in 2021 from Shanghai (China). Fusarium sambucinum and species within Aspergillus section flavi were more frequently found in paddy grains, whereas Alternaria was the predominant genus in wheat. Fusarium spp. were the main species in fresh grains and Aspergillus was predominant in stored grains. In vitro assessments on potato dextrose agar demonstrated that Fusarium isolates were mainly capable of producing deoxynivalenol and zearalenone. Aflatoxins were exclusively produced by Aspergillus section flavi. Alternaria species predominantly synthesized alternariol, together with other mycotoxins like alternariol monomethyl ether, altenuene, tenuazonic acid, tentoxin, and altenusin. A combined analysis of the mycobiota and their mycotoxin-producing potential provides valuable insights into mycotoxin-production mechanisms, thereby facilitating the development of effective prevention and control strategies for wheat and paddy in a specific geographic region.
In addition to paddy and wheat grains, Aspergillus section flavi is also often associated with maize grains causing aflatoxins contaminations (Smith et al., 2019). In this context, the paper by Castano-Duque et al. provides interesting discoveries on the modulation by flavonoids of aflatoxins accumulation from Aspergillus flavus in maize kernels. To understand the molecular mechanisms of maize resistance to A. flavus colonization and aflatoxin accumulation better, they performed a transcriptomic study in maize kernels infected by the fungus. They found a significant association between flavonoid biosynthetic pathway genes and infection by A. flavus. This suggests that flavonoids can contribute to host resistance mechanisms against aflatoxin contamination through the modulation of toxin accumulation in maize kernels.
Maize grains can also be colonized by other mycotoxigenic species such as those belonging to the genus Fusarium (Bryła et al., 2022). In this context, Cao et al. investigated the resistance of maize kernels to Fusarium ear rot (FER), caused by Fusarium verticillioides as well as fumonisin accumulation. For this, quantitative trait loci (QTLs) and bulk-segregant RNA-seq techniques were utilized. Genetic regions within genetic bins 4.07-4.1, 6-6.01, 6.04-6.05, and 8.05-8.08 were linked to FER resistance and reduced fumonisin levels. Transcriptome comparisons between resistant and susceptible inbred bulks at 10 days post-inoculation with F. verticillioides identified 364 differentially expressed genes (DEGs). In resistant bulks, genes associated with fatty acid and starch biosynthesis, cell division and phytosulfokine signalling were downregulated. Conversely, genes tied to secondary metabolism, cell wall biosynthesis/rearrangement and flavonoid production were upregulated, reflecting a growth-defence trade-off. Several DEGs, located within QTL confidence intervals and showing significant expression differences between resistant and susceptible bulks, were identified as candidate genes for FER resistance and fumonisin reduction.
Studying the same host-pathogen interaction, Cao et al. performed a metabolome study in maize, comparing recombinant inbred lines with and without inoculation with F. verticillioides. The maize lines varied in resistance to the pathogen and the aim was to elucidate pathways involved in resistance and find markers for FER and fumonisin contamination in maize kernels. Data obtained 10 days after inoculation explained differences between resistance and susceptibility better than data from 3 days. It was found that differences in membrane lipid homeostasis, methionine metabolism and modulation of indolacetic acid conjugation appeared relevant when distinguishing between resistant and susceptible lines. Furthermore, specific metabolites, such as polyamine spermidine and the alkaloid isoquinoline appeared to be interesting when looking for improvement of resistance to FER and reduction of fumonisin levels.
SM produced by microorganisms may have an antifungal role against phytopathogenic fungi. Among different microorganisms, the species of the genus Trichoderma are the most potent biocontrol agents in use today, among others because they produce a diverse range of antimicrobial SM (Khan et al., 2020). Cardoza et al. studied the biocontrol fungus Trichoderma arundinaceum, which has the potential as a biological control agent, but also can produce trichothecene toxins. Three Trichoderma arundinaceum isolates from bean fields produced trichothecene harzianum A (HA) and trichodermol (an intermediate in the HA-biosynthesis). The three isolates showed antifungal activity against the bean pathogens Rhizoctonia solani and Sclerotinia sclerotiorum in vitro and this was ascribed to HA production. Furthermore, seed treatment with the Trichoderma-isolates gave faster germination and, in some cases, increased growth of aerial parts of bean plants. Transcriptomics of bean plants inoculated with the T. arundinaceum isolates indicated that HA production increased the expression of plant defence-related genes, especially chitinase-encoding genes. Collectively, the study indicated that Trichoderma species can induce resistance in plants without negative effects on plant growth.
The collection of articles on this Research Topic provides interesting information on the presence of mycotoxins in plants, the plant’s activity to reduce the accumulation of mycotoxins, as well as the interaction of some SM with the host, enhancing its ability to counteract pathogens.
Author contributions
GB: Conceptualization, Writing – original draft, Writing – review & editing. FT: Conceptualization, Writing – original draft, Writing – review & editing. HJ: Conceptualization, Writing – original draft, Writing – review & editing.
Acknowledgments
The editors would like to thank all editors and reviewers who evaluated manuscripts of this Research Topic.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision
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References
Berthiller, F., Crews, C., Dall’Asta, C., De Saeger, S., Haesaert, G., Karlovsky, P., et al. (2013). Masked mycotoxins: a review. Mol. Nutr. Food Res. 57, 165–186. doi: 10.1002/mnfr.201100764
Berthiller, F., Lemmens, M., Werner, U., Krska, R., Hauser, M. T., Adam, G., et al. (2007). Short review: metabolism of the Fusarium mycotoxins deoxynivalenol and zearalenone in plants. Mycotoxin Res. 23, 68–72. doi: 10.1007/BF02946028
Bryła, M., Pierzgalski, A., Zapaśnik, A., Uwineza, P. A., Ksieniewicz-Woźniak, E., Modrzewska, M., et al. (2022). Recent research on fusarium mycotoxins in maize—A review. Foods 11, 3465. doi: 10.3390/foods11213465
Elhamouly, N. A., Hewedy, O. A., Zaitoon, A., Miraples, A., Elshorbagy, O. T., Hussien, S., et al. (2022). The hidden power of secondary metabolites in plant-fungi interactions and sustainable phytoremediation. Front. Plant Sci. 13. doi: 10.3389/fpls.2022.1044896
Freire, L., Sant’Ana, A. (2018). Modified mycotoxins: an updated review on their formation, detection, occurrence, and toxic effects. Food Chem. Toxicol. 111, 189–205. doi: 10.1016/j.fct.2017.11.021
Khan, R. A. A., Najeeb, S., Hussain, S., Xie, B., Li, Y. (2020). Bioactive secondary metabolites from Trichoderma spp. against phytopathogenic fungi. Microorganisms 8, 817. doi: 10.3390/microorganisms8060817
Rodrigo, S., García-Latorre, C., Santamaria, O. (2022). Metabolites produced by fungi against fungal phytopathogens: review, implementation and perspectives. Plants 11, 81. doi: 10.3390/plants11010081
Smith, J. S., Williams, W. P., Windham, G. L. (2019). Aflatoxin in maize: a review of the early literature from “moldy-corn toxicosis”. to Genet. aflatoxin accumulation resistance Mycotoxin Res. 35, 11–128. doi: 10.1007/s12550-018-00340-w
Keywords: secondary metabolites, fungi, cereals, bean, Fusarium, Aspergillus, Trichoderma
Citation: Beccari G, Tini F and Jørgensen HJL (2023) Editorial: Current advances in the metabolism of mycotoxins in plants. Front. Plant Sci. 14:1343855. doi: 10.3389/fpls.2023.1343855
Received: 24 November 2023; Accepted: 27 November 2023;
Published: 04 December 2023.
Edited and Reviewed by:
Brigitte Mauch-Mani, Université de Neuchâtel, SwitzerlandCopyright © 2023 Beccari, Tini and Jørgensen. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Francesco Tini, francesco.tini@unipg.it