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      MFS Transporters and GABA Metabolism Are Involved in the Self-Defense Against DON in Fusarium graminearum

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          Abstract

          Trichothecene mycotoxins, such as deoxynivalenol (DON) produced by the fungal pathogen, Fusarium graminearum, are not only important for plant infection but are also harmful to human and animal health. Trichothecene targets the ribosomal protein Rpl3 that is conserved in eukaryotes. Hence, a self-defense mechanism must exist in DON-producing fungi. It is reported that TRI (trichothecene biosynthesis) 101 and TRI12 are two genes responsible for self-defense against trichothecene toxins in Fusarium. In this study, however, we found that simultaneous disruption of TRI101 and TRI12 has no obvious influence on DON resistance upon exogenous DON treatment in F. graminearum, suggesting that other mechanisms may be involved in self-defense. By using RNA-seq, we identified 253 genes specifically induced in DON-treated cultures compared with samples from cultures treated or untreated with cycloheximide, a commonly used inhibitor of eukaryotic protein synthesis. We found that transporter genes are significantly enriched in this group of DON-induced genes. Of those genes, 15 encode major facilitator superfamily transporters likely involved in mycotoxin efflux. Significantly, we found that genes involved in the metabolism of gamma-aminobutyric acid (GABA), a known inducer of DON production in F. graminearum, are significantly enriched among the DON-induced genes. The GABA biosynthesis gene PROLINE UTILIZATION 2-2 ( PUT2-2) is downregulated, while GABA degradation genes are upregulated at least twofold upon treatment with DON, resulting in decreased levels of GABA. Taken together, our results suggest that transporters influencing DON efflux are important for self-defense and that GABA mediates the balance of DON production and self-defense in F. graminearum.

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          Most cited references36

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          A review of worldwide contamination of cereal grains and animal feed with Fusarium mycotoxins

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            Effects of trichothecene mycotoxins on eukaryotic cells: a review.

            The major products of the trichothecene mycotoxin biosynthetic pathway produced in a species- and sometimes isolate-specific manner by cereal-pathogenic Fusarium fungi include T-2 toxin, diacetoxyscirpenol, deoxynivalenol and nivalenol. This paper briefly reviews the major effects of such trichothecenes on the gross morphology, cytology and molecular signalling within eukaryotic cells. The gross toxic effects of select trichothecenes on animals include growth retardation, reduced ovarian function and reproductive disorders, immuno-compromization, feed refusal and vomiting. The phytotoxic effects of deoxynivalenol on plants can be summarized as growth retardation, inhibition of seedling and green plant regeneration. Trichothecenes are now recognized as having multiple inhibitory effects on eukaryote cells, including inhibition of protein, DNA and RNA synthesis, inhibition of mitochondrial function, effects on cell division and membrane effects. In animal cells, they induce apoptosis, a programmed cell death response. Current knowledge about the eukaryotic signal transduction cascades and downstream gene products activated by trichothecenes is limited, especially in plants. In mammalian cells, certain trichothecenes trigger a ribotoxic stress response and activate mitogen-activated protein kinases. DON mediates the inflammatory response by modulating the binding activities of specific transcription factors and subsequently inducing cytokine gene expression. Several genes are up-regulated in wheat in response to trichothecene mycotoxins; the significance, if any, of these genes in the host response to trichothecenes has yet to be elucidated.
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              Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene.

              The production of trichothecene mycotoxins by some plant pathogenic species of Fusarium is thought to contribute to their virulence. Gibberella zeae (F. graminearum) is an important cereal pathogen that produces the trichothecene deoxynivalenol. To determine if trichothecene production contributes to the virulence of G. zeae, we generated trichothecene-deficient mutants of the fungus by gene disruption. The disrupted gene, Tri5, encodes the enzyme trichodiene synthase, which catalyzes the first step in trichothecene biosynthesis. To disrupt Tri5, G. zeae was transformed with a plasmid carrying a doubly truncated copy of the Tri5 coding region interrupted by a hygromycin B resistance gene. Tri5- transformants were selected by screening for the inability to produce trichothecenes and by Southern blot analysis. Tri5- strains exhibited reduced virulence on seedlings of Wheaton wheat and common winter rye, but wild-type virulence on seedlings of Golden Bantam maize. On Caldwell and Marshall wheat and Porter oat seedlings, Tri5- strains were inconsistent in causing less disease than their wild-type progenitor strain. Head blight developed more slowly on Wheaton when inoculated with Tri5- mutants than when inoculated with wild-type strains. These results suggest that trichothecene production contributes to the virulence of G. zeae on some hosts.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                13 April 2018
                2018
                : 9
                : 438
                Affiliations
                [1] 1State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F University , Yangling, China
                [2] 2Department of Botany and Plant Pathology, Purdue University , West Lafayette, IN, United States
                [3] 3Innovation Experimental College, Northwest A&F University , Yangling, China
                Author notes

                Edited by: Brigitte Mauch-Mani, University of Neuchâtel, Switzerland

                Reviewed by: Javier Plasencia, Universidad Nacional Autónoma de México, Mexico; Mostafa Abdelwahed Abdelrahman, Tohoku University, Japan

                *Correspondence: Huiquan Liu, liuhuiquan@ 123456nwsuaf.edu.cn

                These authors have contributed equally to this work.

                This article was submitted to Plant Microbe Interactions, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2018.00438
                5908970
                29706976
                a94c65ca-20b8-4c26-a843-100eea32a50c
                Copyright © 2018 Wang, Chen, Wu, Zhu, Jiang, Xu and Liu.

                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 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.

                History
                : 30 November 2017
                : 21 March 2018
                Page count
                Figures: 7, Tables: 2, Equations: 0, References: 50, Pages: 10, Words: 0
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                fusarium head blight,fusarium graminearum,don resistance,mfs transporter,gamma-aminobutyric acid

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