Cargando…

Aminotransferase SsAro8 Regulates Tryptophan Metabolism Essential for Filamentous Growth of Sugarcane Smut Fungus Sporisorium scitamineum

Sugarcane smut caused by the basidiomycetous fungus Sporisorium scitamineum leads to severe economic losses globally. Sexual mating/filamentation of S. scitamineum is critical for its pathogenicity, as only the dikaryotic hyphae formed after sexual mating are capable of invading the host cane. Our c...

Descripción completa

Detalles Bibliográficos
Autores principales: Cui, Guobing, Huang, Chengwei, Bi, Xinping, Wang, Yixu, Yin, Kai, Zhu, Luyuan, Jiang, Zide, Chen, Baoshan, Deng, Yi Zhen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9431617/
https://www.ncbi.nlm.nih.gov/pubmed/35862944
http://dx.doi.org/10.1128/spectrum.00570-22
_version_ 1784780104838152192
author Cui, Guobing
Huang, Chengwei
Bi, Xinping
Wang, Yixu
Yin, Kai
Zhu, Luyuan
Jiang, Zide
Chen, Baoshan
Deng, Yi Zhen
author_facet Cui, Guobing
Huang, Chengwei
Bi, Xinping
Wang, Yixu
Yin, Kai
Zhu, Luyuan
Jiang, Zide
Chen, Baoshan
Deng, Yi Zhen
author_sort Cui, Guobing
collection PubMed
description Sugarcane smut caused by the basidiomycetous fungus Sporisorium scitamineum leads to severe economic losses globally. Sexual mating/filamentation of S. scitamineum is critical for its pathogenicity, as only the dikaryotic hyphae formed after sexual mating are capable of invading the host cane. Our comparative transcriptome analysis showed that the mitogen-activated protein kinase (MAPK) pathway and the AGC kinase Agc1 (orthologous to yeast Rim15), both governing S. scitamineum mating/filamentation, were induced by elevated tryptophol level, supporting a positive regulation of S. scitamineum mating/filamentation by tryptophol. However, the biosynthesis pathway of tryptophol remains unknown in S. scitamineum. Here, we identified an aminotransferase orthologous to the established tryptophan aminotransferase Tam1/Aro8, catalyzing the first step of tryptophan-dependent indole-3-acetic acid (IAA) production as well as that of the Ehrlich pathway for tryptophol production. We designated this S. scitamineum aminotransferase as SsAro8 and found that it was essential for mating/filamentation. Comparative metabolomics analysis revealed that SsAro8 was involved in tryptophan metabolism, likely for producing important intermediate products, including tryptophol. Exogenous addition of tryptophan or tryptophol could differentially restore mating/filamentation in the ssaro8Δ mutant, indicating that in addition to tryptophol, other product(s) of tryptophan catabolism may also be involved in S. scitamineum mating/filamentation regulation. S. scitamineum could also produce IAA, partially dependent on SsAro8 function. Surprisingly, photodestruction of IAA produced the compound(s) able to suppress S. scitamineum growth/differentiation. Lastly, we found that SsAro8 was required for proper biofilm formation, oxidative stress tolerance, and full pathogenicity in S. scitamineum. Overall, our study establishes the aminotransferase SsAro8 as an essential regulator of S. scitamineum pathogenic differentiation, as well as fungus-host interaction, and therefore of great potential as a molecular target for sugarcane smut disease control. IMPORTANCE Sugarcane smut caused by the basidiomycete fungus S. scitamineum leads to massive economic losses in sugarcane plantation globally. Dikaryotic hyphae formation (filamentous growth) and biofilm formation are two important aspects in S. scitamineum pathogenesis, yet the molecular regulation of these two processes was not as extensively investigated as that in the model pathogenic fungi, e.g., Candida albicans, Ustilago maydis, or Cryptococcus neoformans. In this study, a tryptophan aminotransferase ortholog was identified in S. scitamineum, designated SsAro8. Functional characterization showed that SsAro8 positively regulates both filamentous growth and biofilm formation, respectively, via tryptophol-dependent and -independent manners. Furthermore, SsAro8 is required for full pathogenicity and, thus, is a promising molecular target for designing anti-smut strategy.
format Online
Article
Text
id pubmed-9431617
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher American Society for Microbiology
record_format MEDLINE/PubMed
spelling pubmed-94316172022-09-01 Aminotransferase SsAro8 Regulates Tryptophan Metabolism Essential for Filamentous Growth of Sugarcane Smut Fungus Sporisorium scitamineum Cui, Guobing Huang, Chengwei Bi, Xinping Wang, Yixu Yin, Kai Zhu, Luyuan Jiang, Zide Chen, Baoshan Deng, Yi Zhen Microbiol Spectr Research Article Sugarcane smut caused by the basidiomycetous fungus Sporisorium scitamineum leads to severe economic losses globally. Sexual mating/filamentation of S. scitamineum is critical for its pathogenicity, as only the dikaryotic hyphae formed after sexual mating are capable of invading the host cane. Our comparative transcriptome analysis showed that the mitogen-activated protein kinase (MAPK) pathway and the AGC kinase Agc1 (orthologous to yeast Rim15), both governing S. scitamineum mating/filamentation, were induced by elevated tryptophol level, supporting a positive regulation of S. scitamineum mating/filamentation by tryptophol. However, the biosynthesis pathway of tryptophol remains unknown in S. scitamineum. Here, we identified an aminotransferase orthologous to the established tryptophan aminotransferase Tam1/Aro8, catalyzing the first step of tryptophan-dependent indole-3-acetic acid (IAA) production as well as that of the Ehrlich pathway for tryptophol production. We designated this S. scitamineum aminotransferase as SsAro8 and found that it was essential for mating/filamentation. Comparative metabolomics analysis revealed that SsAro8 was involved in tryptophan metabolism, likely for producing important intermediate products, including tryptophol. Exogenous addition of tryptophan or tryptophol could differentially restore mating/filamentation in the ssaro8Δ mutant, indicating that in addition to tryptophol, other product(s) of tryptophan catabolism may also be involved in S. scitamineum mating/filamentation regulation. S. scitamineum could also produce IAA, partially dependent on SsAro8 function. Surprisingly, photodestruction of IAA produced the compound(s) able to suppress S. scitamineum growth/differentiation. Lastly, we found that SsAro8 was required for proper biofilm formation, oxidative stress tolerance, and full pathogenicity in S. scitamineum. Overall, our study establishes the aminotransferase SsAro8 as an essential regulator of S. scitamineum pathogenic differentiation, as well as fungus-host interaction, and therefore of great potential as a molecular target for sugarcane smut disease control. IMPORTANCE Sugarcane smut caused by the basidiomycete fungus S. scitamineum leads to massive economic losses in sugarcane plantation globally. Dikaryotic hyphae formation (filamentous growth) and biofilm formation are two important aspects in S. scitamineum pathogenesis, yet the molecular regulation of these two processes was not as extensively investigated as that in the model pathogenic fungi, e.g., Candida albicans, Ustilago maydis, or Cryptococcus neoformans. In this study, a tryptophan aminotransferase ortholog was identified in S. scitamineum, designated SsAro8. Functional characterization showed that SsAro8 positively regulates both filamentous growth and biofilm formation, respectively, via tryptophol-dependent and -independent manners. Furthermore, SsAro8 is required for full pathogenicity and, thus, is a promising molecular target for designing anti-smut strategy. American Society for Microbiology 2022-07-06 /pmc/articles/PMC9431617/ /pubmed/35862944 http://dx.doi.org/10.1128/spectrum.00570-22 Text en Copyright © 2022 Cui et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Cui, Guobing
Huang, Chengwei
Bi, Xinping
Wang, Yixu
Yin, Kai
Zhu, Luyuan
Jiang, Zide
Chen, Baoshan
Deng, Yi Zhen
Aminotransferase SsAro8 Regulates Tryptophan Metabolism Essential for Filamentous Growth of Sugarcane Smut Fungus Sporisorium scitamineum
title Aminotransferase SsAro8 Regulates Tryptophan Metabolism Essential for Filamentous Growth of Sugarcane Smut Fungus Sporisorium scitamineum
title_full Aminotransferase SsAro8 Regulates Tryptophan Metabolism Essential for Filamentous Growth of Sugarcane Smut Fungus Sporisorium scitamineum
title_fullStr Aminotransferase SsAro8 Regulates Tryptophan Metabolism Essential for Filamentous Growth of Sugarcane Smut Fungus Sporisorium scitamineum
title_full_unstemmed Aminotransferase SsAro8 Regulates Tryptophan Metabolism Essential for Filamentous Growth of Sugarcane Smut Fungus Sporisorium scitamineum
title_short Aminotransferase SsAro8 Regulates Tryptophan Metabolism Essential for Filamentous Growth of Sugarcane Smut Fungus Sporisorium scitamineum
title_sort aminotransferase ssaro8 regulates tryptophan metabolism essential for filamentous growth of sugarcane smut fungus sporisorium scitamineum
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9431617/
https://www.ncbi.nlm.nih.gov/pubmed/35862944
http://dx.doi.org/10.1128/spectrum.00570-22
work_keys_str_mv AT cuiguobing aminotransferasessaro8regulatestryptophanmetabolismessentialforfilamentousgrowthofsugarcanesmutfungussporisoriumscitamineum
AT huangchengwei aminotransferasessaro8regulatestryptophanmetabolismessentialforfilamentousgrowthofsugarcanesmutfungussporisoriumscitamineum
AT bixinping aminotransferasessaro8regulatestryptophanmetabolismessentialforfilamentousgrowthofsugarcanesmutfungussporisoriumscitamineum
AT wangyixu aminotransferasessaro8regulatestryptophanmetabolismessentialforfilamentousgrowthofsugarcanesmutfungussporisoriumscitamineum
AT yinkai aminotransferasessaro8regulatestryptophanmetabolismessentialforfilamentousgrowthofsugarcanesmutfungussporisoriumscitamineum
AT zhuluyuan aminotransferasessaro8regulatestryptophanmetabolismessentialforfilamentousgrowthofsugarcanesmutfungussporisoriumscitamineum
AT jiangzide aminotransferasessaro8regulatestryptophanmetabolismessentialforfilamentousgrowthofsugarcanesmutfungussporisoriumscitamineum
AT chenbaoshan aminotransferasessaro8regulatestryptophanmetabolismessentialforfilamentousgrowthofsugarcanesmutfungussporisoriumscitamineum
AT dengyizhen aminotransferasessaro8regulatestryptophanmetabolismessentialforfilamentousgrowthofsugarcanesmutfungussporisoriumscitamineum