Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2022 Jun 20:3:923112.
doi: 10.3389/ffunb.2022.923112. eCollection 2022.

Transcriptomic Responses of Fusarium verticillioides to Lactam and Lactone Xenobiotics

Affiliations

Transcriptomic Responses of Fusarium verticillioides to Lactam and Lactone Xenobiotics

Minglu Gao et al. Front Fungal Biol. .

Abstract

The important cereal crops of maize, rye, and wheat constitutively produce precursors to 2-benzoxazolinone, a phytochemical having antifungal effects towards many Fusarium species. However, Fusarium verticillioides can tolerate 2-benzoxazolinone by converting it into non-toxic metabolites through the synergism of two previously identified gene clusters, FDB1 and FDB2. Inspired by the induction of these two clusters upon exposure to 2-benzoxazolinone, RNA sequencing experiments were carried out by challenging F. verticillioides individually with 2-benzoxazolinone and three related chemical compounds, 2-oxindole, 2-coumaranone, and chlorzoxazone. These compounds all contain lactam and/or lactone moieties, and transcriptional analysis provided inferences regarding the degradation of such lactams and lactones. Besides induction of FDB1 and FDB2 gene clusters, four additional clusters were identified as induced by 2-benzoxazolinone exposure, including a cluster thought to be responsible for biosynthesis of pyridoxine (vitamin B6), a known antioxidant providing tolerance to reactive oxygen species. Three putative gene clusters were identified as induced by challenging F. verticillioides with 2-oxindole, two with 2-coumaranone, and two with chlorzoxazone. Interestingly, 2-benzoxazolinone and 2-oxindole each induced two specific gene clusters with similar composition of enzymatic functions. Exposure to 2-coumranone elicited the expression of the fusaric acid biosynthetic gene cluster. Another gene cluster that may encode enzymes responsible for degrading intermediate catabolic metabolites with carboxylic ester bonds was induced by 2-benzoxazolinone, 2-oxindole, and chlorzoxazone. Also, the induction of a dehalogenase encoding gene during chlorzoxazone exposure suggested its role in the removal of the chlorine atom. Together, this work identifies genes and putative gene clusters responsive to the 2-benzoxazolinone-like compounds with metabolic inferences. Potential targets for future functional analyses are discussed.

Keywords: 2-benzoxazolinone; 2-coumaranone; 2-oxindole; BOA; RNA-Seq; chlorzoxazone; gene clusters.

PubMed Disclaimer

Conflict of interest statement

Authors MG and XG are employed by Bayer R&D Services LLC. The remaining 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.

Figures

Figure 1
Figure 1
Chemical structures of BOA, OXD, CMN, and CZX. Lactam bonds are shown in blue and lactone bonds in red.
Figure 2
Figure 2
BOA, OXD, CMN, and CZX elicit differential gene expression. Heatmaps showing transcription levels of differentially expressed genes upon exposure to BOA (A), OXD (B), CMN (C), and CZX (D). The Y-axis represents genes that are clustered and colored by z-score. See the colored key. The X-axis shows the three biological replicates of each treatment.
Figure 3
Figure 3
Co-upregulated genes were observed among BOA, OXD, CMN, and CZX treatments. Venn diagram shows the number of genes with altered expression due to BOA, OXD, CMN, or CZX exposure. Each circle represents one chemical treatment. Overlaps represent up-regulated genes shared between corresponding treatments.

References

    1. Awata H., Endo F., Tanoue A., Kitano A., Nakano Y., Matsuda I. (1994). Structural Organization and Analysis of the Human Fumarylacetoacetate Hydrolase Gene in Tyrosinemia Type I. Biochim. Biophys. Acta. 1226 (2), 168–172. doi: 10.1016/0925-4439(94)90025-6 - DOI - PubMed
    1. Anders S., Pyl P. T., Huber W. (2015). HTSeq-a Python Framework to Work With High-Throughput Sequencing Data. Bioinformatics 31, 166–169. doi: 10.1093/bioinformatics/btu638 - DOI - PMC - PubMed
    1. Andrews S. (2010). FastQC: A Quality Control Tool for High Throughput Sequence Data. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc
    1. Bilski P., Li M. Y., Ehrenshaft M., Daub M. E., Chignell C. F. (2000). Vitamin B6 (Pyridoxine) and its Derivatives are Efficient Singlet Oxygen Quenchers and Potential Fungal Antioxidants. Photochem. Photobiol. 71 (2), 129–134. doi: 10.1562/0031-8655(2000)071<0129:sipvbp>2.0.co;2 - DOI - PubMed
    1. Blacutt A. A., Gold S. E., Voss K. A., Gao M., Glenn A. E. (2018). Fusarium Verticillioides: Advancements in Understanding the Toxicity, Virulence, and Niche Adaptations of a Model Mycotoxigenic Pathogen of Maize. Phytopathology 108, 312–326. doi: 10.1094/PHYTO-06-17-0203-RVW - DOI - PubMed