Editorial: Fusarium species as plant and human pathogens, mycotoxin producers, and biotechnological importance
Sofia N. Chulze
Sheryl Tittlemier
Adriana M. Torres- 1Research Institute on Mycology and Mycotoxicology (IMICO) National University of Rio Cuarto(UNRC) National Technological and Research Council from Argentina (CONICET), Rio Cuarto, Córdoba, Argentina
- 2Canadian Grain Commission, Grain Research Laboratory, Winnipeg, MB, Canada
Editorial on the Research Topic
Fusarium species as plant and human pathogens, mycotoxin producers, and biotechnological importance
The fungal genus Fusarium Link includes many plant pathogens of agricultural crops, human pathogens, and species with biotechnological applications (Leslie and Summerell, 2006; Aoki et al., 2014; Meyer et al., 2020; Geiser et al., 2021). The main concern in the last decades has been devoted to those species that infect staple crops and produce secondary metabolites known as mycotoxins. Mycotoxins produced by Fusarium species have been shown to occur worldwide. Among these, fumonisins and trichothecenes are of great concern for their impact on human and animal health (Munkvold et al., 2021). Under a scenario of climate change, the situation can worsen due to changes in fungal biodiversity, in the resistance/resilience of crops, and in the strong impact of the environmental factors affecting both global food security and safety (Singh et al., 2023).
This Research Topic describes recent advances in the field of plant pathogens and toxigenic Fusarium species and strategies to reduce their impact.
In this Research Topic, four works (three original research articles and one hypothesis and theory article) were published on Fusarium species that are important as plant pathogens in maize, wheat, and tobacco and the recent advances in their biodiversity and control.
Environmentally friendly strategies are explored to reduce the impact of mycotoxins produced by Fusarium species on cereals (Petrucci et al., 2023). The manuscript of Satterlee et al., on the transcriptomic response of Fusarium verticillioides to variably inhibitory environmental isolates of Streptomyces, described the evaluation of Streptomyces strains to control F. verticillioides. The strains that showed more impact on F. verticillioides growth also caused more impact in the transcriptomic response. Variation in time response was observed. Among the genes involved, one was related to nitrogen assimilation and others to the gene cluster of fusaric acid. This metabolite is important in the interaction of F. verticillioides with potential antagonists. Other genes affected were those related to β lactamases produced by F. verticillioides; these enzymes were induced under the confrontation of the pathogen with Streptomyces strains. The potential of Streptomyces species as biocontrol agents against F. verticillioides was highlighted.
Wheat (Triticum aestivum L and T. durum L) is a global staple food that is susceptible to infection by various Fusarium species. Under certain conditions, Fusarium infection can lead to Fusarium head blight (FHB), one of the most critical fungal diseases of wheat. In epidemic years, FHB decreases grain yield and quality and impacts the safety of wheat due to the production of mycotoxins. The trichothecene mycotoxin deoxynivalenol (DON) is of particular concern due to its potential health impacts and regulated status in many jurisdictions. The occurrence and severity of FHB are governed by several factors, including the aggressiveness and mycotoxin production potential of the infecting Fusarium species.
The work done by Bamforth et al. surveyed the presence of various Fusarium species in Canadian wheat harvest samples. They examined the relationships of Fusarium species, including the trichothecene chemotype, present on visually identified Fusarium-damaged kernels with growing location, harvest year, and wheat species (i.e., hexaploid and durum wheat). They noted some biodiversity of Fusarium species across Canada in wheat grain, the most common species and genotype isolated being F. graminearum and 3-ADON, respectively. The occurrence of the 3-ADON genotype increased, particularly in the western Prairie regions, over the time period of the survey (2014-2020). The researchers also noted higher severity of FHB and DON accumulation in durum wheat compared to hexaploid wheat.
Tobacco (Nicotiana tabacum L.) is one of the most widely cultivated crops, produced in more than 125 countries worldwide, and it can be infected by Fusarium species within the Fusarium oxysporum and F. solani complexes, causing root rot (Food and Agriculture Organization-FAO, 2022).
Li et al. described the interactions between Fusarium and other members of the soil microbial community. The authors used high-throughput sequencing technology and found that infected soil had higher levels of soil nutrients but lower observed richness within the different microbial groups compared to healthy soil. The infection by F. solani had a significant impact on the microbial community structure and interactions in soil. Moreover, F. solani had a higher number of connecting nodes in infected soils. The study highlighted the importance of understanding the interactions among microorganisms in the soil ecosystem and the vulnerability of soil microbial communities to pathogen invasion.
Maize (Zea mays L) is grown in different regions and can also be contaminated with Fusarium species, including the trichothecene producers associated with red ear rot (Fusarium graminearum and related species) and the fumonisin producers associated with pink ear rot (Fusarium verticillioides and other species within the Fusarium fujikuroi complex). The contamination with these trichothecene and fumonisin mycotoxins causes toxic effects both to humans and animals and economic losses in the maize food and feed chains (Logrieco et al., 2021).
Cereals including maize, wheat, and rice contain compounds such as 2-benzoxazolinone that have shown antifungal activity. Gao et al. reported the ability of Fusarium verticillioides to degrade compounds that contain lactam and/or lactone moieties. Using transcriptome analysis, it was observed that besides the two previously identified gene clusters, FDB1 and FDB2, this fungal species degrades 2-benzoxazolinone when it is exposed to 2-benzoxazolinone and three related chemical compounds, 2-oxindole, 2-coumaranone, and chlorzoxazone. This degradation is mediated when other gene clusters are activated, including a cluster responsible for pyridoxine (vitamin B6) biosynthesis and the gene cluster for fusaric acid, among others. This study provides more data on the ability of Fusarium verticillioides to respond to stress conditions due to the presence of phytochemicals with antifungal activity.
There is still a variety of research being performed on Fusarium species, highlighting the relevance of the species within the genus as significant pathogens for agricultural crops. A better understanding of the roles of Fusarium species within their environment and their varied internal functions will help to manage this genus’s impact on the yield, quality, and safety of crops. Furthermore, more studies on the biotechnological potential of Fusarium species are encouraged.
Author contributions
SC: Conceptualization, Writing – original draft. ST: Writing – review & editing. AT: Writing – review & editing.
Funding
The author(s) declare that no financial support was received for the research, authorship, and/or publication of this article.
Acknowledgments
The editors would like to acknowledge and thank the authors for their contributions and all the reviewers for their effort, expertise, and constructive suggestions that significantly contributed to the quality 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.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
References
Aoki T., O’Donnell K., Geiser D. M. (2014). Systematics of key phytopathogenic Fusarium species: current status and future challenges. J. Gen. Plant Pathol. 80, 189–201. doi: 10.1007/s10327-014-0509-3
Food and Agriculture Organization-FAO (2022) Statistical Year Book Statistical Year Book World Food and Agriculture 2022. Available at: http://www.fao.org/.
Geiser D. M., Al-Hatmi A. M. S., Aoki T., Arie T., Balmas V., Barnes I., et al. (2021). Phylogenomic analysis of a 55.1-kb 19-gene dataset resolves a monophyletic Fusarium that includes the Fusarium solani species complex. Phytopathology 111 (7), 1064–1079. doi: 10.1094/PHYTO-08-20-0330-LE
Logrieco A., Battilani P., Leggieri M. C., Jiang Y., Haesaert G., Lanubile A., et al. (2021). Perspectives on global mycotoxin issues and management from the mycoKey maize working group. Plant Dis. 105 (3), 525–537. doi: 10.1094/PDIS-06-20-1322-FE
Meyer V., Basenko E. Y., Benz J. P., Braus G. H., Caddick M. X., Csukai M., et al. (2020). Growing a circular economy with fungal biotechnology: a white paper. Fungal Biol. Biotechnol. 7, 5. doi: 10.1186/s40694-020-00095-z
Munkvold G. P., Proctor R. H., Moretti A. (2021). Mycotoxin production in Fusarium according to contemporary species concepts. Ann. Rev. Phytopathol. 59, 373–402. doi: 10.1146/annurev-phyto-020620-102825
Petrucci A., Khairullina A., Sarrocco ,. S., Funck Jensen D., Jensen B., Lyngs Jørgensen H. J., et al. (2023). Understanding the mechanisms underlying biological control of Fusarium diseases in cereals. Eur. J. Plant Pathol. doi: 10.1007/s10658-023-02753-5
Keywords: antifungal compounds, Fusarium, biocontrol, fusarium head blight, mycotoxins, maize, tobacco
Citation: Chulze SN, Tittlemier S and Torres AM (2023) Editorial: Fusarium species as plant and human pathogens, mycotoxin producers, and biotechnological importance. Front. Fungal Biol. 4:1320198. doi: 10.3389/ffunb.2023.1320198
Received: 11 October 2023; Accepted: 06 November 2023;
Published: 14 November 2023.
Edited and Reviewed by:
N. Louise Glass, University of California, Berkeley, United StatesCopyright © 2023 Chulze, Tittlemier and Torres. 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: Sofia N. Chulze, schulze@exa.unrc.edu.ar