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Ovarian Tumor Domain-Containing Proteases-Deubiquitylation Enzyme Gene SsCI33130 Involved in the Regulation of Mating/Filamentation and Pathogenicity in Sporisorium scitamineum

Sugarcane is an important sugar crop. Sugarcane smut, caused by Sporisorium scitamineum, is a worldwide sugarcane disease with serious economic losses and lack of effective control measures. Revealing the molecular pathogenesis of S. scitamineum is very helpful to the development of effective preven...

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Autores principales: Li, Huizhong, Cai, Yichang, Deng, Quanqing, Bao, Han, Chen, Jianwen, Shen, Wankuan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8523855/
https://www.ncbi.nlm.nih.gov/pubmed/34675909
http://dx.doi.org/10.3389/fmicb.2021.746550
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author Li, Huizhong
Cai, Yichang
Deng, Quanqing
Bao, Han
Chen, Jianwen
Shen, Wankuan
author_facet Li, Huizhong
Cai, Yichang
Deng, Quanqing
Bao, Han
Chen, Jianwen
Shen, Wankuan
author_sort Li, Huizhong
collection PubMed
description Sugarcane is an important sugar crop. Sugarcane smut, caused by Sporisorium scitamineum, is a worldwide sugarcane disease with serious economic losses and lack of effective control measures. Revealing the molecular pathogenesis of S. scitamineum is very helpful to the development of effective prevention and control technology. Deubiquitinase removes ubiquitin molecules from their binding substrates and participates in a variety of physiological activities in eukaryotes. Based on the transcriptome sequencing data of two isolates (Ss16 and Ss47) of S. scitamineum with different pathogenicities, SsCI33130, a gene encoding an OTU1-deubiquitin enzyme, was identified. The positive knockout mutants and complementary mutants of the SsCI33130 gene were successfully obtained through polyethylene glycol-mediated protoplast transformation technology. In order to study the possible function of this gene in pathogenicity, phenotypic comparison of the growth, morphology, abiotic stress, sexual mating, pathogenicity, and gene expression levels of the knockout mutants, complementary mutants, and their wild type strains were conducted. The results demonstrated that the gene had almost no effect on abiotic stress, cell wall integrity, growth, and morphology, but was related to the sexual mating and pathogenicity of S. scitamineum. The sexual mating ability and pathogenicity between the knockout mutants or between the knockout mutant and wild type were more significantly reduced than between the wild types, the complementary mutants, or the wild types and complementary mutants. The sexual mating between the knockout mutants or between the knockout mutant and wild type could be restored by the exogenous addition of small-molecule signaling substances such as 5 mM cyclic adenosine monophosphate (cAMP) or 0.02 mM tryptophol. In addition, during sexual mating, the expression levels of tryptophol and cAMP synthesis-related genes in the knockout mutant combinations were significantly lower than those in the wild type combinations, while the expression levels in the complementary mutant combinations were restored to the level of the wild type. It is speculated that the SsCI33130 gene may be involved in the development of sexual mating and pathogenicity in S. scitamineum by regulating the synthesis of the small-molecule signaling substances (cAMP or tryptophol) required during the sexual mating of S. scitamineum, thereby providing a molecular basis for the study of the pathogenic mechanisms of S. scitamineum.
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spelling pubmed-85238552021-10-20 Ovarian Tumor Domain-Containing Proteases-Deubiquitylation Enzyme Gene SsCI33130 Involved in the Regulation of Mating/Filamentation and Pathogenicity in Sporisorium scitamineum Li, Huizhong Cai, Yichang Deng, Quanqing Bao, Han Chen, Jianwen Shen, Wankuan Front Microbiol Microbiology Sugarcane is an important sugar crop. Sugarcane smut, caused by Sporisorium scitamineum, is a worldwide sugarcane disease with serious economic losses and lack of effective control measures. Revealing the molecular pathogenesis of S. scitamineum is very helpful to the development of effective prevention and control technology. Deubiquitinase removes ubiquitin molecules from their binding substrates and participates in a variety of physiological activities in eukaryotes. Based on the transcriptome sequencing data of two isolates (Ss16 and Ss47) of S. scitamineum with different pathogenicities, SsCI33130, a gene encoding an OTU1-deubiquitin enzyme, was identified. The positive knockout mutants and complementary mutants of the SsCI33130 gene were successfully obtained through polyethylene glycol-mediated protoplast transformation technology. In order to study the possible function of this gene in pathogenicity, phenotypic comparison of the growth, morphology, abiotic stress, sexual mating, pathogenicity, and gene expression levels of the knockout mutants, complementary mutants, and their wild type strains were conducted. The results demonstrated that the gene had almost no effect on abiotic stress, cell wall integrity, growth, and morphology, but was related to the sexual mating and pathogenicity of S. scitamineum. The sexual mating ability and pathogenicity between the knockout mutants or between the knockout mutant and wild type were more significantly reduced than between the wild types, the complementary mutants, or the wild types and complementary mutants. The sexual mating between the knockout mutants or between the knockout mutant and wild type could be restored by the exogenous addition of small-molecule signaling substances such as 5 mM cyclic adenosine monophosphate (cAMP) or 0.02 mM tryptophol. In addition, during sexual mating, the expression levels of tryptophol and cAMP synthesis-related genes in the knockout mutant combinations were significantly lower than those in the wild type combinations, while the expression levels in the complementary mutant combinations were restored to the level of the wild type. It is speculated that the SsCI33130 gene may be involved in the development of sexual mating and pathogenicity in S. scitamineum by regulating the synthesis of the small-molecule signaling substances (cAMP or tryptophol) required during the sexual mating of S. scitamineum, thereby providing a molecular basis for the study of the pathogenic mechanisms of S. scitamineum. Frontiers Media S.A. 2021-10-05 /pmc/articles/PMC8523855/ /pubmed/34675909 http://dx.doi.org/10.3389/fmicb.2021.746550 Text en Copyright © 2021 Li, Cai, Deng, Bao, Chen and Shen. https://creativecommons.org/licenses/by/4.0/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.
spellingShingle Microbiology
Li, Huizhong
Cai, Yichang
Deng, Quanqing
Bao, Han
Chen, Jianwen
Shen, Wankuan
Ovarian Tumor Domain-Containing Proteases-Deubiquitylation Enzyme Gene SsCI33130 Involved in the Regulation of Mating/Filamentation and Pathogenicity in Sporisorium scitamineum
title Ovarian Tumor Domain-Containing Proteases-Deubiquitylation Enzyme Gene SsCI33130 Involved in the Regulation of Mating/Filamentation and Pathogenicity in Sporisorium scitamineum
title_full Ovarian Tumor Domain-Containing Proteases-Deubiquitylation Enzyme Gene SsCI33130 Involved in the Regulation of Mating/Filamentation and Pathogenicity in Sporisorium scitamineum
title_fullStr Ovarian Tumor Domain-Containing Proteases-Deubiquitylation Enzyme Gene SsCI33130 Involved in the Regulation of Mating/Filamentation and Pathogenicity in Sporisorium scitamineum
title_full_unstemmed Ovarian Tumor Domain-Containing Proteases-Deubiquitylation Enzyme Gene SsCI33130 Involved in the Regulation of Mating/Filamentation and Pathogenicity in Sporisorium scitamineum
title_short Ovarian Tumor Domain-Containing Proteases-Deubiquitylation Enzyme Gene SsCI33130 Involved in the Regulation of Mating/Filamentation and Pathogenicity in Sporisorium scitamineum
title_sort ovarian tumor domain-containing proteases-deubiquitylation enzyme gene ssci33130 involved in the regulation of mating/filamentation and pathogenicity in sporisorium scitamineum
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8523855/
https://www.ncbi.nlm.nih.gov/pubmed/34675909
http://dx.doi.org/10.3389/fmicb.2021.746550
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