Rapamycin induces morphological and physiological changes without increase in lipid content in Ustilago maydis

Romero-Aguilar, Lucero; Guerra-Sánchez, Guadalupe; Tenorio, Eda Patricia; Tapia-Rodríguez, Miguel; Matus-Ortega, Genaro; Flores-Herrera, Óscar; González, Jesús Salvador; Pardo, Juan Pablo

doi:10.1007/s00203-020-01833-y

Cited by 6 publications

(7 citation statements)

References 59 publications

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“…However, this morphology defect was not found in RUT-C30 grown on glucose or lactose, and strain KU70 or ΔtrFKBP12 propagated on cellulose, indicating that it is a very specific phenotype for RUT-C30 cultured on cellulose. Similar hyphal morphology alterations with the treatment of rapamycin were previously reported in other filamentous fungi like P. anserina [40] and U. maydis [83].…”

Section: Discussionsupporting

confidence: 86%

“…It has been reported that rapamycin treatment led to an increase in the number and size of lipid droplets in the fungus S. cerevisiae [38], Podospora anserina [39,40], and Ustilago maydis [41]. Therefore, to see whether the lipid content of T. reesei RUT-C30 was altered by rapamycin, the lipid content of T. reesei RUT-C30 grown on cellulose, lactose or glucose was stained by Nile Red and checked under CLSM (Fig.…”

Section: Rapamycin Hinders Cell Growth and Sporulation Of T Reesei Rmentioning

confidence: 99%

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High-dose rapamycin exerts a temporary impact on T. reesei RUT-C30 through gene trFKBP12

Pang

Wang

Zhang

et al. 2021

Biotechnol Biofuels

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Background Knowledge with respect to regulatory systems for cellulase production is prerequisite for exploitation of such regulatory networks to increase cellulase production, improve fermentation efficiency and reduce the relevant production cost. The target of rapamycin (TOR) signaling pathway is considered as a central signaling hub coordinating eukaryotic cell growth and metabolism with environmental inputs. However, how and to what extent the TOR signaling pathway and rapamycin are involved in cellulase production remain elusive. Result At the early fermentation stage, high-dose rapamycin (100 μM) caused a temporary inhibition effect on cellulase production, cell growth and sporulation of Trichoderma reesei RUT-C30 independently of the carbon sources, and specifically caused a tentative morphology defect in RUT-C30 grown on cellulose. On the contrary, the lipid content of T. reesei RUT-C30 was not affected by rapamycin. Accordingly, the transcriptional levels of genes involved in the cellulase production were downregulated notably with the addition of rapamycin. Although the mRNA levels of the putative rapamycin receptor trFKBP12 was upregulated significantly by rapamycin, gene trTOR (the downstream effector of the rapamycin–FKBP12 complex) and genes associated with the TOR signaling pathways were not changed markedly. With the deletion of gene trFKBP12, there is no impact of rapamycin on cellulase production, indicating that trFKBP12 mediates the observed temporary inhibition effect of rapamycin. Conclusion Our study shows for the first time that only high-concentration rapamycin induced a transient impact on T. reesei RUT-C30 at its early cultivation stage, demonstrating T. reesei RUT-C30 is highly resistant to rapamycin, probably due to that trTOR and its related signaling pathways were not that sensitive to rapamycin. This temporary influence of rapamycin was facilitated by gene trFKBP12. These findings add to our knowledge on the roles of rapamycin and the TOR signaling pathways play in T. reesei.

show abstract

Section: Discussionsupporting

confidence: 86%

Section: Rapamycin Hinders Cell Growth and Sporulation Of T Reesei Rmentioning

confidence: 99%

High-dose rapamycin exerts a temporary impact on T. reesei RUT-C30 through gene trFKBP12

Pang

Wang

Zhang

et al. 2021

Biotechnol Biofuels

View full text Add to dashboard Cite

show abstract

“…However, this morphology defect was not found in RUT-C30 grown on glucose or lactose, and strain KU70 or ΔtrFKBP12 propagated on cellulose, indicating that it is a very speci c phenotype for RUT-C30 cultured on cellulose. Similar hyphal morphology alterations with the treatment of rapamycin were previously reported in other lamentous fungi like P. anserine (23) and U. maydis (54).…”

Section: Discussionsupporting

confidence: 86%

“…It has been reported that rapamycin treatment led to an increase in the number and size of lipid droplets in the fungus S. cerevisiae (21), Podospora anserine (22,23), and Ustilago maydis (24). Therefore, to see whether the lipid content of T. reesei was altered by rapamycin, the lipid content of T. reesei grown on cellulose, lactose or glucose was stained by Nile Red and checked under CLSM ( Fig.…”

Section: Rapamycin Hinders Cell Growth and Sporulation Of T Reesei Tmentioning

confidence: 99%

High-dose rapamycin excerts a temporary impact on T. reesei through gene trFKBP12

Pang¹,

Wang²,

Zhang³

et al. 2020

Preprint

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Background: Knowledge with respect to regulatory systems for cellulase production is prerequisite for exploitation of such regulatory networks to increase cellulase production, improve fermentation efficiency and reduce the relevant production cost. The TOR (Target of Rapamycin) signaling pathway is considered as a central signaling hub coordinating eukaryotic cell growth and metabolism with environmental inputs. However, how and to what extent the TOR signaling pathway and rapamycin are involved in cellulase production remains elusive. Result: At the early fermentation stage, high-dose rapamycin (100 μM) caused a temporary inhibition effect on cellulase production, cell growth and sporulation of Trichoderma reesei independently of the carbon sources, and specifically caused a tentative morphology defect in RUT-C30 grown on cellulose. On the contrary, the lipid content of T. reesei was not affected by rapamycin. Accordingly, the transcriptional levels of genes involved in the cellulase production were downregulated notably with the addition of rapamycin. Although the mRNA levels of the putative rapamycin receptor trFKBP12 was upregulated significantly by rapamycin, gene trTOR (the downstream effector of the rapamycin-FKBP12 complex) and genes associated with the TOR signaling pathways were not changed markedly. With the deletion of gene trFKBP12, there is no impact of rapamycin on cellulase production, indicating that trFKBP12 mediates the observed temporary inhibition effect of rapamycin. Conclusion: Our study shows for the first time that only high-concentration rapamycin induced a transient impact on T. reesei at its early cultivation stage, demonstrating T. reesei is highly resistant to rapamycin, probably due to that trTOR and its related signaling pathways were not that sensitive to rapamycin. This temporary influence of rapamycin was facilitated by gene trFKBP12. These findings add to our knowledge on the roles of rapamycin and the TOR signaling pathways play in T. reesei.

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“…All of these genes, except for rlm1, ald4, and tdh3 [isoform A], are related to processes of programmed cell death, as SIN3, that is involved in the regulation of mitophagy receptor protein Atg32 in yeast (Aihara et al, 2014). ATG8 is an autophagic protein that plays a key role in autophagosome formation (Dufresne et al, 1998;Nadal and Gold, 2010;Khan et al, 2012); mca1 plays a dual role in the induction of programmed cell death and intracellular protein quality control on exposure to stress conditions (Mukherjee et al, 2017); aif1 is a conserved flavoprotein that causes chromatin condensation and DNA fragmentation, two hallmarks of apoptosis (Susin et al, 1999;Cande et al, 2004;Elguindy and Nakamaru-Ogiso, 2015;Ma et al, 2016); NUC1 causes apoptosis in yeast without the involvement of metacaspase or of apoptosisinducing factor (Büttner et al, 2007); TOR kinase controls the initiation of autophagy, which results in the development of a single membrane structure known as the phagophore (Yorimitsu et al, 2007;Aguilar et al, 2017;Romero-Aguilar et al, 2020).…”

Section: Gene Expression Analysismentioning

confidence: 99%

Identifying Genes Devoted to the Cell Death Process in the Gene Regulatory Network of Ustilago maydis

et al. 2021

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Cell death is a process that can be divided into three morphological patterns: apoptosis, autophagy and necrosis. In fungi, cell death is induced in response to intracellular and extracellular perturbations, such as plant defense molecules, toxins and fungicides, among others. Ustilago maydis is a dimorphic fungus used as a model for pathogenic fungi of animals, including humans, and plants. Here, we reconstructed the transcriptional regulatory network of U. maydis, through homology inferences by using as templates the well-known gene regulatory networks (GRNs) of Saccharomyces cerevisiae, Aspergillus nidulans and Neurospora crassa. Based on this GRN, we identified transcription factors (TFs) as hubs and functional modules and calculated diverse topological metrics. In addition, we analyzed exhaustively the module related to cell death, with 60 TFs and 108 genes, where diverse cell proliferation, mating-type switching and meiosis, among other functions, were identified. To determine the role of some of these genes, we selected a set of 11 genes for expression analysis by qRT-PCR (sin3, rlm1, aif1, tdh3 [isoform A], tdh3 [isoform B], ald4, mca1, nuc1, tor1, ras1, and atg8) whose homologues in other fungi have been described as central in cell death. These genes were identified as downregulated at 72 h, in agreement with the beginning of the cell death process. Our results can serve as the basis for the study of transcriptional regulation, not only of the cell death process but also of all the cellular processes of U. maydis.

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Rapamycin induces morphological and physiological changes without increase in lipid content in Ustilago maydis

Cited by 6 publications

References 59 publications

High-dose rapamycin exerts a temporary impact on T. reesei RUT-C30 through gene trFKBP12

High-dose rapamycin exerts a temporary impact on T. reesei RUT-C30 through gene trFKBP12

High-dose rapamycin excerts a temporary impact on T. reesei through gene trFKBP12

Identifying Genes Devoted to the Cell Death Process in the Gene Regulatory Network of Ustilago maydis

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