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The arabinose transporter MtLat-1 is involved in hemicellulase repression as a pentose transceptor in Myceliophthora thermophila

BACKGROUND: Filamentous fungi possess an array of secreted enzymes to depolymerize the structural polysaccharide components of plant biomass. Sugar transporters play an essential role in nutrient uptake and sensing of extracellular signal molecules to inhibit or trigger the induction of lignocellulo...

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Autores principales: Gu, Shuying, Zhao, Zhen, Xue, Fanglei, Liu, Defei, Liu, Qian, Li, Jingen, Tian, Chaoguang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10040116/
https://www.ncbi.nlm.nih.gov/pubmed/36966330
http://dx.doi.org/10.1186/s13068-023-02305-3
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author Gu, Shuying
Zhao, Zhen
Xue, Fanglei
Liu, Defei
Liu, Qian
Li, Jingen
Tian, Chaoguang
author_facet Gu, Shuying
Zhao, Zhen
Xue, Fanglei
Liu, Defei
Liu, Qian
Li, Jingen
Tian, Chaoguang
author_sort Gu, Shuying
collection PubMed
description BACKGROUND: Filamentous fungi possess an array of secreted enzymes to depolymerize the structural polysaccharide components of plant biomass. Sugar transporters play an essential role in nutrient uptake and sensing of extracellular signal molecules to inhibit or trigger the induction of lignocellulolytic enzymes. However, the identities and functions of transceptors associated with the induction of hemicellulase genes remain elusive. RESULTS: In this study, we reveal that the l-arabinose transporter MtLat-1 is associated with repression of hemicellulase gene expression in the filamentous fungus Myceliophthora thermophila. The absence of Mtlat-1 caused a decrease in l-arabinose uptake and consumption rates. However, mycelium growth, protein production, and hemicellulolytic activities were markedly increased in a ΔMtlat-1 mutant compared with the wild-type (WT) when grown on arabinan. Comparative transcriptomic analysis showed a different expression profile in the ΔMtlat-1 strain from that in the WT in response to arabinan, and demonstrated that MtLat-1 was involved in the repression of the main hemicellulase-encoding genes. A point mutation that abolished the l-arabinose transport activity of MtLat-1 did not impact the repression of hemicellulase gene expression when the mutant protein was expressed in the ΔMtlat-1 strain. Thus, the involvement of MtLat-1 in the expression of hemicellulase genes is independent of its transport activity. The data suggested that MtLat-1 is a transceptor that senses and transduces the molecular signal, resulting in downstream repression of hemicellulolytic gene expression. MtAra-1 protein directly regulated the expression of Mtlat-1 by binding to its promoter region. Transcriptomic profiling indicated that the transcription factor MtAra-1 also plays an important role in expression of arabinanolytic enzyme genes and l-arabinose catabolism. CONCLUSIONS: M. thermophila MtLat-1 functions as a transceptor that is involved in l-arabinose transport and signal transduction associated with suppression of the expression of hemicellulolytic enzyme-encoding genes. The data presented in this study add to the models of the regulation of hemicellulases in filamentous fungi. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13068-023-02305-3.
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spelling pubmed-100401162023-03-27 The arabinose transporter MtLat-1 is involved in hemicellulase repression as a pentose transceptor in Myceliophthora thermophila Gu, Shuying Zhao, Zhen Xue, Fanglei Liu, Defei Liu, Qian Li, Jingen Tian, Chaoguang Biotechnol Biofuels Bioprod Research BACKGROUND: Filamentous fungi possess an array of secreted enzymes to depolymerize the structural polysaccharide components of plant biomass. Sugar transporters play an essential role in nutrient uptake and sensing of extracellular signal molecules to inhibit or trigger the induction of lignocellulolytic enzymes. However, the identities and functions of transceptors associated with the induction of hemicellulase genes remain elusive. RESULTS: In this study, we reveal that the l-arabinose transporter MtLat-1 is associated with repression of hemicellulase gene expression in the filamentous fungus Myceliophthora thermophila. The absence of Mtlat-1 caused a decrease in l-arabinose uptake and consumption rates. However, mycelium growth, protein production, and hemicellulolytic activities were markedly increased in a ΔMtlat-1 mutant compared with the wild-type (WT) when grown on arabinan. Comparative transcriptomic analysis showed a different expression profile in the ΔMtlat-1 strain from that in the WT in response to arabinan, and demonstrated that MtLat-1 was involved in the repression of the main hemicellulase-encoding genes. A point mutation that abolished the l-arabinose transport activity of MtLat-1 did not impact the repression of hemicellulase gene expression when the mutant protein was expressed in the ΔMtlat-1 strain. Thus, the involvement of MtLat-1 in the expression of hemicellulase genes is independent of its transport activity. The data suggested that MtLat-1 is a transceptor that senses and transduces the molecular signal, resulting in downstream repression of hemicellulolytic gene expression. MtAra-1 protein directly regulated the expression of Mtlat-1 by binding to its promoter region. Transcriptomic profiling indicated that the transcription factor MtAra-1 also plays an important role in expression of arabinanolytic enzyme genes and l-arabinose catabolism. CONCLUSIONS: M. thermophila MtLat-1 functions as a transceptor that is involved in l-arabinose transport and signal transduction associated with suppression of the expression of hemicellulolytic enzyme-encoding genes. The data presented in this study add to the models of the regulation of hemicellulases in filamentous fungi. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13068-023-02305-3. BioMed Central 2023-03-25 /pmc/articles/PMC10040116/ /pubmed/36966330 http://dx.doi.org/10.1186/s13068-023-02305-3 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Gu, Shuying
Zhao, Zhen
Xue, Fanglei
Liu, Defei
Liu, Qian
Li, Jingen
Tian, Chaoguang
The arabinose transporter MtLat-1 is involved in hemicellulase repression as a pentose transceptor in Myceliophthora thermophila
title The arabinose transporter MtLat-1 is involved in hemicellulase repression as a pentose transceptor in Myceliophthora thermophila
title_full The arabinose transporter MtLat-1 is involved in hemicellulase repression as a pentose transceptor in Myceliophthora thermophila
title_fullStr The arabinose transporter MtLat-1 is involved in hemicellulase repression as a pentose transceptor in Myceliophthora thermophila
title_full_unstemmed The arabinose transporter MtLat-1 is involved in hemicellulase repression as a pentose transceptor in Myceliophthora thermophila
title_short The arabinose transporter MtLat-1 is involved in hemicellulase repression as a pentose transceptor in Myceliophthora thermophila
title_sort arabinose transporter mtlat-1 is involved in hemicellulase repression as a pentose transceptor in myceliophthora thermophila
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10040116/
https://www.ncbi.nlm.nih.gov/pubmed/36966330
http://dx.doi.org/10.1186/s13068-023-02305-3
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