Plant Protect. Sci., 2023, 59(4):337-347 | DOI: 10.17221/52/2023-PPS
Identification and functional analysis of glyoxal oxidase gene from rubber tree anthracnoseOriginal Paper
- 1 Sanya Nanfan Research Institute of Hainan University, College of Plant Protection, Hainan University, Sanya and Haikou, China
- 2 Hainan Key Laboratory for Cultivation and Physiology, Key Laboratory of Biology and Genetic Resources of Rubber Tree, Ministry of Agriculture and Rural Affairs, Rubber Research Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, China
- 3 College of Tropical Crops, Yunnan Agricultural University, Puer, China
Glyoxal oxidase (GLOX, EC 1.2.3.15) is a class of hydrogen peroxide synthases involved in lignin degradation. Several GLOX genes of biotrophic and necrotrophic phytopathogenic fungi have been confirmed to contribute to fungal growth, development, and pathogenicity. However, the composition, sequence characteristics and functions of genes in the GLOX family of hemi-biotrophic phytopathogenic fungi remain poorly understood. This study identified a GLOX-encoding gene CsGLOX in the hemi-biotrophic phytopathogenic fungus Colletotrichum siamense by bioinformatics analysis and PCR cloning. The encoded protein contains a signal peptide and five cell wall stress-responsive component (WSC) domains at the N terminus, followed by a catalytic structural domain (AA5_1). CsGLOX-deficient mutants were constructed by homologous replacement, which significantly increased the formation of conidia and reduced the pathogenicity and the high-osmotic stress tolerance of the fungus. However, the deletions did not influence fungal filamentous growth. This study proposes that the CsGLOX gene is involved in pathogen conidial formation, pathogenicity, and osmotic stress response, which deepens our understanding of the pathogenic mechanism of hemi-biotrophic phytopathogenic fungus C. siamense.
Keywords: glyoxal oxidase; Colletotrichum siamense; pathogenicity; stress responses; pathogenic mechanism
Received: May 9, 2023; Revised: September 19, 2023; Accepted: October 4, 2023; Prepublished online: November 10, 2023; Published: November 28, 2023 Show citation
References
- Bak J.S., Ko J.K., Choi I.G., Park Y.C., Seo J.H., Kim K.H. (2009): Fungal pretreatment of lignocellulose by Phanerochaete chrysosporium to produce ethanol from rice straw. Biotechnology and Bioengineering, 104: 471-482.
Go to original source...
Go to PubMed...
- Cao X.R., Xu X.M., Che H.Y., West J.S., Luo D.Q. (2017): Distribution and fungicide sensitivity of Colletotrichum species complexes from rubber tree in Hainan, China. Plant Disease, 101: 1774-1780.
Go to original source...
Go to PubMed...
- Chandrasekar B., Wanke A., Wawra S., Saake Pia., Mahdi L., Charura N., Neidert M., Poschmann G., et al. (2022): Fungi hijack a ubiquitous plant apoplastic endoglucanase to release a ROS scavenging β-glucan decasaccharide to subvert immune responses. Plant Cell, 34: 2765-2784.
Go to original source...
Go to PubMed...
- Crutcher F.K., Moran-Diez M.E., Krieger I.V., Kenerley C.M. (2019): Effects on hyphal morphology and development by the putative copper radical oxidase glx1 in Trichoderma virens suggest a novel role as a cell wall associated enzyme. Fungal Genetics and Biology, 131: 103245. doi: 10.1016/j.fgb.2019.103245
Go to original source...
Go to PubMed...
- Daou M., Faulds C.B. (2017): Glyoxal oxidases: their nature and properties. World journal of Microbiology and Biotechnology, 33: 87.
Go to original source...
Go to PubMed...
- Eloy Y.R.G., Vasconcelos I.M., Barreto A.L.H., Freire-Filho F.R., Oliveira J.T.A. (2015): H2O2 plays an important role in the lifestyle of Colletotrichum gloeosporioides during interaction with cowpea [Vigna unguiculata (L.) Walp]. Fungal biology, 119: 747-757.
Go to original source...
Go to PubMed...
- Fong J.K., Brumer H. (2023): Copper radical oxidases: galactose oxidase, glyoxal oxidase, and beyond. Essays in Biochemistry, 67: 597-613.
Go to original source...
Go to PubMed...
- Futagami T., Nakao S., Kido Y., Oka T., Kajiwara Y., Takashita H., Omori T., Furukawa K., et al. (2011): Putative stress sensors WscA and WscB are involved in hypo-osmotic and acidic pH stress tolerance in Aspergillus nidulans. Eukaryotic cell, 10: 1504-1515.
Go to original source...
Go to PubMed...
- González-Fernández R., Valero-Galván J., Gómez-Gálvez F.J., orrín-Novo Jesús V.J. (2015): Unraveling the in vitro secretome of the phytopathogen Botrytis cinerea to understand the interaction with its hosts. Frontiers in Plant Science, 6: 839.
Go to original source...
Go to PubMed...
- Haile Z.M., Malacarne G., Pilati S., Sonego P., Moretto M., Masuero D., Vrhovsek U., Engelen K., et al. (2020): Dual transcriptome and metabolic analysis of Vitis vinifera cv. pinot noir berry and Botrytis cinerea during quiescence and egressed infection. Frontiers in Plant Science, 10: 1704.
Go to original source...
Go to PubMed...
- Kadowaki M.A.S., Godoy M.O.D., Kumagai P.S., Costa-Filho A.J.D., Mort A., Prade R.A., Polikarpov I. (2018): Characterization of a new glyoxal oxidase from the thermophilic fungus Myceliophthora thermophila M77: Hydrogen peroxide production retained in 5-hydroxymethylfurfural oxidation. Catalysts, 8: 476.
Go to original source...
- Kan J.A.L.V., Stefanato F., Raats E.M. (2004): A mysterious, pleiotropic growth defect caused by deletion of a glyoxal oxidase gene in Botrytis cinerea. In: Book of Abstracts 7th European Conference on Fungal Genetics, April 17-20, 2004, Copenhagen, Denmark: 168-168.
- Kersten P., Cullen D. (2014): Copper radical oxidases and related extracellular oxidoreductases of wood-decay Agaricomycetes. Fungal Genetics and Biology, 72: 124-130.
Go to original source...
Go to PubMed...
- Kersten P.J., Kirk T.K. (1987): Involvement of a new enzyme, glyoxal oxidase, in extracellular H2O2 production by Phanerochaete chrysosporium. Journal of Bacteriology, 169: 2195-2201.
Go to original source...
Go to PubMed...
- Kersten P.J., Witek C., Wymelenberg A.V., Cullen D. (1995): Phanerochaete chrysosporium glyoxal oxidase is encoded by two allelic variants: structure, genomic organization, and heterologous expression of glx1 and glx2. Journal of Bacteriology, 17: 6106-6110.
Go to original source...
Go to PubMed...
- Koschorreck K., Alpdagtas S., Urlacher V.B. (2022): Copper-radical oxidases: A diverse group of biocatalysts with distinct properties and a broad range of biotechnological applications. Engineering Microbiology, 2: 100037. doi: 10.1016/j.engmic.2022.100037
Go to original source...
- Leuthner B., Aichinger C., Oehmen E., Koopmann E., Müller O., Müller P., Kahmann R., Bölker M., et al. (2005): A H2O2-producing glyoxal oxidase is required for filamentous growth and pathogenicity in Ustilago maydis. Molecular Genetics and Genomics, 272: 639-650.
Go to original source...
Go to PubMed...
- Lima D.M.C.G., Costa T.P.C., Emri T., Pócsi I., Pupin B., Rangel D.E.N. (2021): Fungal tolerance to Congo red, a cell wall integrity stress, as a promising indicator of ecological niche. Fungal Biology, 125: 646-657.
Go to original source...
Go to PubMed...
- Lin C.H., Huang G.X., Zheng F.C., Miao W.G. (2018): Functional characterization of CgPBS2, a MAP kinase in Colletotrichum gloeosporioides, using osmotic stress sensitivity as a selection marker. Eeuropean Journal Plant Pathology, 152: 801-813.
Go to original source...
- Liu X.B., Li B.X., Cai J.M., Zheng Z.L., Feng Y.L., Huang G.X. (2018): Colletotrichum species causing anthracnose of rubber trees in China. Scientific Reports, 8: 10435.
Go to original source...
Go to PubMed...
- Liu X.B, Li B.X., Yang Y., Cai J.M., Shi T., Zheng X.L., Huang G.X. (2020): Pathogenic adaptations revealed by comparative genome analyses of two Colletotrichum spp., the causal agent of anthracnose in rubber tree. Frontiers in Microbiology, 11: 1484.
Go to original source...
Go to PubMed...
- Lodder A.L., Lee T.K., Ballester R. (1999): Characterization of the Wsc1 protein, a putative receptor in the stress response of Saccharomyces cerevisiae. Genetics, 152: 1487-1499.
Go to original source...
Go to PubMed...
- Lopez D., Ribeiro S., Label P., Fumanal B., Venisse J.S., Kohler A., Oliveira R.R.D., Labutti K., et al. (2018): Genome-wide analysis of Corynespora cassiicola leaf fall disease putative effectors. Frontiers in Microbiology, 9: 276.
Go to original source...
Go to PubMed...
- MacDonald J., Doering M., Canam T., Gong Y.C., Guttman D.S., Campbell M.M., Master E.R. (2011): Transcriptomic responses of the softwood-degrading whiterot fungus Phanerochaete carnosa during growth on coniferous and deciduous wood. Applied and Environmental Microbiology, 77: 3211-3218.
Go to original source...
Go to PubMed...
- Matityahu Avi., Sitruk A., Hadar Y., Belinky P.A. (2015): Factors affecting the induction of lignin peroxidase in manganese-deficient cultures of the white rot fungus Phanerochaete chrysosporium. Advances in Microbiology, 5: 83-92.
Go to original source...
- Meinhardt L.W., Costa G.G.L., Thomazella D.P., Teixeira P.J.P., Carazzolle M.F., Schuster S.C., Carlson J.E., Guiltinan M.J., et al. (2014): Genome and secretome analysis of the hemibiotrophic fungal pathogen, Moniliophthora roreri, which causes frosty pod rot disease of cacao: mechanisms of the biotrophic and necrotrophic phases. BMC Genomics, 15: 164.
Go to original source...
Go to PubMed...
- Oide S., Tanakaa Y., Watanabea A., Inui M. (2019): Carbohydrate-binding property of a cell wall integrity and stress response component (WSC) domain of an alcohol oxidase from the rice blast pathogen Pyricularia oryzae. Enzyme and Microbial Technology, 125: 13-20.
Go to original source...
Go to PubMed...
- Ribeaucourt D., Saker S., Navarro D., Bissaro B., Drula E., Correia L.O., Haon M., Grisel S., et al. (2021): Identification of copper-containing oxidoreductases in the secretomes of three Colletotrichum species with a focus on copper radical oxidases for the biocatalytic production of fatty aldehydes. Applied and Environmental Microbiology, 87: e01526-21. doi: 10.1128/AEM.01526-21
Go to original source...
Go to PubMed...
- Robert X., Gouet P. (2014): Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Rresearch, 42: 320-324.
Go to original source...
Go to PubMed...
- Song M., Fang S.Q., Li Z.G., Wang N., Li X., Liu W.B., Zhang Y., Lin C.H., et al. (2022): CsAtf1, a bZIP transcription factor, is involved in fludioxonil sensitivity and virulence in the rubber tree anthracnose fungus Colletotrichum siamense. Fungal Genetics and Biology, 158: 103649.
Go to original source...
Go to PubMed...
- Song X.S., Xing S., Li H.P., Zhang J.B., Qu B., Jiang J.H., Fan C., Yang P., et al. (2016): An antibody that confers plant disease resistance targets a membrane-bound glyoxal oxidase in Fusarium. New Phytologist, 210: 997-1010.
Go to original source...
Go to PubMed...
- Takano M., Nakamura M., Yamaguchi M. (2010): Glyoxal oxidase supplies hydrogen peroxide at hyphal tips and on hyphal wall to manganese peroxidase of white-rot fungus Phanerochaete crassa WD1694. Journal of Wood Science, 56: 307-313.
Go to original source...
- Tong S.M., Chen Y., Zhu J., Ying S.H., Feng M.G. (2016): Subcellular localization of five singular WSC domain-containing proteins and their roles in Beauveria bassiana responses to stress cues and metal ions. Environmental Microbiology Reports, 8: 295-304.
Go to original source...
Go to PubMed...
- Tong S.M., Wang D.Y., Gao B.J., Ying S.H., Feng M.G. (2019): The DUF1996 and WSC domain-containing protein Wsc1I acts as a novel sensor of multiple stress cues in Beauveria bassiana. Cellular Microbiology, 21: e13100. doi: 10.1111/cmi.13100
Go to original source...
Go to PubMed...
- Vela-Corcía D., Bautista R., Vicente A.D., Spanu P.D., Pérez-García A. (2016): De novo analysis of the epiphytic transcriptome of the cucurbit powdery mildew fungus Podosphaera xanthii and identification of candidate secreted effector proteins. Plos One, 11: e0163379. doi: 10.1371/journal.pone.0163379
Go to original source...
Go to PubMed...
- Wohlschlager L., Kracher D., Scheiblbrandner S., Csarman F., Ludwig R. (2021): Spectroelectrochemical investigation of the glyoxal oxidase activation mechanism. Bioelectrochemistry, 141: 107845. doi: 10.1016/j.bioelechem.2021.107845
Go to original source...
Go to PubMed...
- Yin D.T., Urresti S., Lafond M., Johnston E.M., Derikvand F., Ciano L., Berrin J.G., Henrissat B., et al. (2015): Structure-function characterization reveals new catalytic diversity in the galactose oxidase and glyoxal oxidase family. Nature Communications, 6: 10197.
Go to original source...
Go to PubMed...
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