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Mitochondrial FgEch1 is responsible for conidiation and full virulence in Fusarium graminearum

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Abstract

Enoyl-CoA hydratase (Ech) is an important and well-recognized enzyme that functions in the degradation of fatty acids by β-oxidation. However, its functions in plant pathogenic fungi are not well known. We characterized an Ech1 orthologue, FgEch1, in Fusarium graminearum. The FgEch1 deletion mutant was defective in the utilization of short-chain fatty acids and conidiation, but not in hyphal growth on glucose-rich media or in perithecium formation. The FgEch1 deletion mutant showed reduced deoxynivalenol (DON) production and virulence in plants. Deletion of FgEch1 also led to increased production of lipid droplets and autophagy. FgEch1, which was localized in the mitochondrion, required the MTS domain for mitochondrial localization and function in F. graminearum. Taken together, these data indicate that mitochondrial FgEch1 is important for conidiation, DON production, and plant infection.

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References

  • Alexander NJ, Proctor RH, McCormick SP (2009) Genes, gene clusters, and biosynthesis of trichothecenes and fumonisins in Fusarium. Toxin Rev 28:198–215

    Article  CAS  Google Scholar 

  • Aliyu SR, Lin LL, Chen XM, Abdul W, Lin YH, Otieno FJ, Shabbir A, Batool W, Zhang YQ, Tang W, Wang ZH, Norvienyeku J (2019) Disruption of putative short-chain acyl-CoA dehydrogenases compromised free radical scavenging, conidiogenesis, and pathogenesis of Magnaporthe oryzae. Fungal Genet Biol 127:23–34

    Article  CAS  Google Scholar 

  • Arunachalam C, Doohan FM (2013) Trichothecene toxicity in eukaryotes: cellular and molecular mechanisms in plants and animals. Toxicol Lett 217:149–158

    Article  CAS  Google Scholar 

  • Bai GH, Shaner G (2004) Management and resistance in wheat and barley to Fusarium head blight. Annu Rev Phytopathol 42:135–161

    Article  CAS  Google Scholar 

  • Bruno KS, Tenjo F, Li L, Hamer JE, Xu JR (2004) Cellular localization and role of kinase activity of PMK1 in Magnaporthe grisea. Eukaryot Cell 3:1525–1532

    Article  CAS  Google Scholar 

  • Catlett NL, Lee BN, Yoder OC, Turgeon BG (2003) Split-marker recombination for efficient targeted deletion of fungal genes. Fungal Genet Newsl 50:9–11

    Google Scholar 

  • Cavinder B, Sikhakolli U, Fellows KM, Trail F (2012) Sexual development and ascospore discharge in Fusarium graminearum. J Vis Exp 61:5407

    Google Scholar 

  • Dean R, van Kan JA, Pretorius ZA, Hammond-kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430

    Article  Google Scholar 

  • Desjardins AE, Hohn TM, McCormick SP (1993) Trichothecene biosynthesis in Fusarium species: chemistry, genetics, and significance. Microbiol Rev 57:595–604

    Article  CAS  Google Scholar 

  • Desjardins AE, Proctor RH, Bai H, McCormick SP, Shaner G, Buechley G, Hohn TM (1996) Reduced virulence of trichothecene-nonproducing mutants of Gibberella zeae in wheat field tests. Mol Plant Microbe Interact 9:775–781

    Article  CAS  Google Scholar 

  • Feron G, Blin-Perrin C, Krasniewski I, Mauvais G, Lherminier J (2005) Metabolism of fatty acid in yeast: characterisation of oxidation and ultrastructural changes in the genus Sporidiobolus sp. cultivated on ricinoleic acid methyl ester. FEMS Microbiol Lett 250:63–69

    Article  CAS  Google Scholar 

  • Gardiner DM, Kazan K, Manners JM (2009) Nutrient profiling reveals potent inducers of trichothecene biosynthesis in Fusarium graminearum. Fungal Genet Biol 46:604–613

    Article  CAS  Google Scholar 

  • Goswami RS, Kistler HC (2004) Heading for disaster: Fusarium graminearum on cereal crops. Mol Plant Pathol 5:515–525

    Article  CAS  Google Scholar 

  • Goswami RS, Kistler HC (2005) Pathogenicity and in planta mycotoxin accumulation among members of the Fusarium graminearum species complex on wheat and rice. Phytopathology 95:1397–1404

    Article  CAS  Google Scholar 

  • Hiltunen JK, Mursula AM, Rottensteiner H, Wierenga RK, Kastaniotis AJ, Gurvitz A (2003) The biochemistry of peroxisomal β-oxidation in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 27:35–64

    Article  CAS  Google Scholar 

  • Hou Z, Xue C, Peng Y, Katan T, Kistler HC, Xu JR (2002) A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol Plant Microbe Interact 15:1119–1127

    Article  CAS  Google Scholar 

  • Houten SM, Wanders RJ (2010) A general introduction to the biochemistry of mitochondrial fatty acid-oxidation. J Inherit Metab Dis 33:469–477

    Article  CAS  Google Scholar 

  • Hsu TH, Chen RH, Cheng YH, Wang CW (2017) Lipid droplets are central organelles for meiosis II progression during yeast sporulation. Mol Biol Cell 128:440–451

    Article  Google Scholar 

  • Hynes MJ, Murray SL, Duncan A, Khew GS, Davis MA (2006) Regulation genes controlling fatty acid catabolism and peroxisomal functions in the filamentous fungus Aspergillus nidulans. Eukaryot Cell 5:794–805

    Article  CAS  Google Scholar 

  • Kretschmer M, Wang J, Kronstad JW (2012) Peroxisomal and mitochondrial-oxidation pathways influence the virulence of the pathogenic fungus Cryptococcus neoformans. Eukaryot Cell 11:1041–1054

    Google Scholar 

  • Leslie JF, Summerell BA (2006) The Fusarium laboratory manual. Blackwell Pub Professional, Hoboken

    Book  Google Scholar 

  • Liu XH, Lu JP, Zhang L, Dong B, Min H, Lin FC (2007) Involvement of a Magnaporthe oryzae serine/threonine kinase gene, MgATG1, in appressorium turgor and pathogenesis. Eukaryot Cell 6:997–1005

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    CAS  Google Scholar 

  • Maggio-Hall LA, Keller NP (2004) Mitochondrial β-oxidation in Aspergillus nidulans. Mol Microbiol 54:1173–1185

    Article  CAS  Google Scholar 

  • McMullen M, Jones R, Gallenberg D (2007) Scab of wheat and barley: a re-emerging disease of devastating impact. Plant Dis 81:1340–1348

    Article  Google Scholar 

  • Mirocha CJ, Kolaczkowski E, Xie WP, Yu H, Jelen H (1998) Analysis of deoxynivalenol and its derivatives (batch and single kernel) using gas chromatography/mass spectrometry. J Agric Food Chem 46:1414–1418

    Article  CAS  Google Scholar 

  • Ohneda M, Arioka M, Nakajima H, Kitamoto K (2002) Visualization of vacuoles in Aspergillus oryzae by expression of CPY-EGFP. Fungal Genet Biol 37:29–38

    Article  CAS  Google Scholar 

  • Patkar RN, Ramos-Pamplona M, Gupta AP, Fan Y, Naqvi N (2012) Mitochondrial β-oxidation regulates organellar integrity and is necessary for conidial germination and invasive growth in Magnaporthe oryzae. Mol Microbiol 86:1345–1363

    Article  CAS  Google Scholar 

  • Pestka JJ, Smolinski AT (2005) Deoxynivalenol: toxicology and potential effects on humans. J Toxicol Environ Health Part B 8:39–69

    Article  CAS  Google Scholar 

  • Piekarska K, Mol E, van den Berg M, Hardy G, van den Burg J, van Roermund C, MacCallum D, Odds F, Distel B (2006) Peroxisomal fatty acid-oxidation is not essential for virulence of Candida albicans. Eukaryot Cell 5:1847–1856

    Article  CAS  Google Scholar 

  • Proctor RH, Hohn TM, McCormick SP (1995) Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Mol Plant Microbe Interact 8:593–601

    Article  CAS  Google Scholar 

  • Reiser K, Davis MA, Mj Hynes (2010) AoxA is a major peroxisomal long chain fatty acyl-CoA oxidase required for β-oxidation in A. nidulans. Curr Genet 56:139–150

    Article  CAS  Google Scholar 

  • Ren WC, Zhang ZH, Shao WY, Yang YL, Zhou MG, Chen CJ (2017) The autophagy-related gene BcATG1 is involved in fungal development and pathogenicity in Botrytis cinerea. Mol Plant Pathol 18:238–248

    Article  CAS  Google Scholar 

  • Ren WC, Liu N, Sang CW, Shi DY, Zhou MG, Chen CJ, Qin QM, Chen WC (2018) The autophagy gene BcATG8 regulates the vegetative differentiation and pathogenicity of Botrytis cinerea. Appl Environ Microbiol 84:1–14

    Article  Google Scholar 

  • Seong KY, Zhao XH, Xu JR, Guldener U, Kistler CH (2008) Conidial germination in the filamentous fungus Fusarium graminearum. Fungal Genet Biol 45:389–399

    Article  CAS  Google Scholar 

  • Shi L, Tu BP (2015) Acetyl-CoA and the regulation of metabolism: metabolisms and consequences. Curr Opin Cell Biol 33:125–131

    Article  CAS  Google Scholar 

  • Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, Tanaka K, Cuervo AM, Czaja MJ (2009) Autophagy regulates lipid metabolism. Nature 458:1131–1135

    Article  CAS  Google Scholar 

  • Trotter PJ (2001) The genetics of fatty acid metabolism in Saccharomyces cerevisiae. Annu Rev Nutr 21:97–119

    Article  CAS  Google Scholar 

  • Walther TC, Chung J, Farese RV Jr (2017) Lipid droplet biogenesis. Ann Rev Cell Dev Biol 33:491–510

    Article  CAS  Google Scholar 

  • Zhang H, Van der Lee T, Waalwijk C, Chen WQ, Xu J, Xu JS, Zhang Y, Feng J (2011) Population analysis of the Fusarium graminearum species complex from wheat in China show a shift to more aggressive isolates. PLoS One 7:e31722

    Article  Google Scholar 

  • Zhang L, Wang L, Liang YC, Yu JF (2019) FgPEX4 is involved in development, pathogenicity, and cell wall integrity in Fusarium graminearum. Curr Genet 65:747–758

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Natural Science Foundation of Shandong Province (ZR2017MC020), Shandong Province Key Research and Development Plan (2019NC106094), the Wheat Innovation Team of Shandong Province Modern Agricultural Industry Technology System (SDAIT-01-09), and Funds of Shandong “Double Tops” Program (SYL2017XTTD11).

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  1. Lin Tang and Xiaoyang Yu contributed equally to this work.

Authors and Affiliations

  1. Shandong Province Key Laboratory of Agricultural Microbiology, College of Plant Protection, Shandong Agricultural University, Tai’an, 271018, China

    Lin Tang, Xiaoyang Yu, Li Zhang, Liyuan Zhang, Lei Chen, Shenshen Zou, Yuancun Liang, Jinfeng Yu & Hansong Dong

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  1. Lin Tang
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  2. Xiaoyang Yu
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  3. Li Zhang
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Tang, L., Yu, X., Zhang, L. et al. Mitochondrial FgEch1 is responsible for conidiation and full virulence in Fusarium graminearum. Curr Genet 66, 361–371 (2020). https://doi.org/10.1007/s00294-019-01028-z

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