KAE1 Allelic Variants Affect TORC1 Activation and Fermentation Kinetics in Saccharomyces cerevisiae
The eukaryotic domain-conserved TORC1 signalling pathway connects growth with nutrient sufficiency, promoting anabolic processes such as ribosomal biogenesis and protein synthesis. In Saccharomyces cerevisiae, TORC1 is activated mainly by the nitrogen sources. Recently, this pathway has gotten renew...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-07-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2019.01686/full |
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| author | Eduardo I. Kessi-Pérez Eduardo I. Kessi-Pérez Francisco Salinas Francisco Salinas Francisco Salinas Asier González Ying Su José M. Guillamón Michael N. Hall Luis F. Larrondo Luis F. Larrondo Claudio Martínez Claudio Martínez |
| author_facet | Eduardo I. Kessi-Pérez Eduardo I. Kessi-Pérez Francisco Salinas Francisco Salinas Francisco Salinas Asier González Ying Su José M. Guillamón Michael N. Hall Luis F. Larrondo Luis F. Larrondo Claudio Martínez Claudio Martínez |
| author_sort | Eduardo I. Kessi-Pérez |
| collection | DOAJ |
| description | The eukaryotic domain-conserved TORC1 signalling pathway connects growth with nutrient sufficiency, promoting anabolic processes such as ribosomal biogenesis and protein synthesis. In Saccharomyces cerevisiae, TORC1 is activated mainly by the nitrogen sources. Recently, this pathway has gotten renewed attention but now in the context of the alcoholic fermentation, due to its key role in nitrogen metabolism regulation. Although the distal and proximal effectors downstream TORC1 are well characterised in yeast, the mechanism by which TORC1 is activated by nitrogen sources is not fully understood. In this work, we took advantage of a previously developed microculture-based methodology, which indirectly evaluates TORC1 activation in a nitrogen upshift experiment, to identify genetic variants affecting the activation of this pathway. We used this method to phenotype a recombinant population derived from two strains (SA and WE) with different geographic origins, which show opposite phenotypes for TORC1 activation by glutamine. Using this phenotypic information, we performed a QTL mapping that allowed us to identify several QTLs for TORC1 activation. Using a reciprocal hemizygous analysis, we validated GUS1, KAE1, PIB2, and UTH1 as genes responsible for the natural variation in the TORC1 activation. We observed that reciprocal hemizygous strains for KAE1 (ATPase required for t6A tRNA modification) gene showed the greatest phenotypic differences for TORC1 activation, with the hemizygous strain carrying the SA allele (KAE1SA) showing the higher TORC1 activation. In addition, we evaluated the fermentative capacities of the hemizygous strains under low nitrogen conditions, observing an antagonistic effect for KAE1SA allele, where the hemizygous strain containing this allele presented the lower fermentation rate. Altogether, these results highlight the importance of the tRNA processing in TORC1 activation and connects this pathway with the yeasts fermentation kinetics under nitrogen-limited conditions. |
| first_indexed | 2024-04-12T07:16:19Z |
| format | Article |
| id | doaj.art-a14a4b4a9ffe47009404e6004f95d0c0 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-12T07:16:19Z |
| publishDate | 2019-07-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Microbiology |
| spelling | doaj.art-a14a4b4a9ffe47009404e6004f95d0c02022-12-22T03:42:27ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-07-011010.3389/fmicb.2019.01686458293KAE1 Allelic Variants Affect TORC1 Activation and Fermentation Kinetics in Saccharomyces cerevisiaeEduardo I. Kessi-Pérez0Eduardo I. Kessi-Pérez1Francisco Salinas2Francisco Salinas3Francisco Salinas4Asier González5Ying Su6José M. Guillamón7Michael N. Hall8Luis F. Larrondo9Luis F. Larrondo10Claudio Martínez11Claudio Martínez12Departamento de Ciencia y Tecnología de los Alimentos, Universidad de Santiago de Chile (USACH), Santiago, ChileCentro de Estudios en Ciencia y Tecnología de Alimentos (CECTA), Universidad de Santiago de Chile (USACH), Santiago, ChileCentro de Estudios en Ciencia y Tecnología de Alimentos (CECTA), Universidad de Santiago de Chile (USACH), Santiago, ChileMillennium Institute for Integrative Biology (iBio), Santiago, ChileInstituto de Bioquímica y Microbiología, Facultad de Ciencias, Universidad Austral de Chile (UACH), Valdivia, ChileBiozentrum, University of Basel, Basel, SwitzerlandDepartamento de Biotecnología de los Alimentos, Instituto de Agroquímica y Tecnología de Alimentos (IATA), Consejo Superior de Investigaciones Científicas (CSIC), Valencia, SpainDepartamento de Biotecnología de los Alimentos, Instituto de Agroquímica y Tecnología de Alimentos (IATA), Consejo Superior de Investigaciones Científicas (CSIC), Valencia, SpainBiozentrum, University of Basel, Basel, SwitzerlandMillennium Institute for Integrative Biology (iBio), Santiago, ChileDepartamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, ChileDepartamento de Ciencia y Tecnología de los Alimentos, Universidad de Santiago de Chile (USACH), Santiago, ChileCentro de Estudios en Ciencia y Tecnología de Alimentos (CECTA), Universidad de Santiago de Chile (USACH), Santiago, ChileThe eukaryotic domain-conserved TORC1 signalling pathway connects growth with nutrient sufficiency, promoting anabolic processes such as ribosomal biogenesis and protein synthesis. In Saccharomyces cerevisiae, TORC1 is activated mainly by the nitrogen sources. Recently, this pathway has gotten renewed attention but now in the context of the alcoholic fermentation, due to its key role in nitrogen metabolism regulation. Although the distal and proximal effectors downstream TORC1 are well characterised in yeast, the mechanism by which TORC1 is activated by nitrogen sources is not fully understood. In this work, we took advantage of a previously developed microculture-based methodology, which indirectly evaluates TORC1 activation in a nitrogen upshift experiment, to identify genetic variants affecting the activation of this pathway. We used this method to phenotype a recombinant population derived from two strains (SA and WE) with different geographic origins, which show opposite phenotypes for TORC1 activation by glutamine. Using this phenotypic information, we performed a QTL mapping that allowed us to identify several QTLs for TORC1 activation. Using a reciprocal hemizygous analysis, we validated GUS1, KAE1, PIB2, and UTH1 as genes responsible for the natural variation in the TORC1 activation. We observed that reciprocal hemizygous strains for KAE1 (ATPase required for t6A tRNA modification) gene showed the greatest phenotypic differences for TORC1 activation, with the hemizygous strain carrying the SA allele (KAE1SA) showing the higher TORC1 activation. In addition, we evaluated the fermentative capacities of the hemizygous strains under low nitrogen conditions, observing an antagonistic effect for KAE1SA allele, where the hemizygous strain containing this allele presented the lower fermentation rate. Altogether, these results highlight the importance of the tRNA processing in TORC1 activation and connects this pathway with the yeasts fermentation kinetics under nitrogen-limited conditions.https://www.frontiersin.org/article/10.3389/fmicb.2019.01686/fullSaccharomyces cerevisiaeTORC1 pathwaynatural variationmicroculturefermentationtRNA modification |
| spellingShingle | Eduardo I. Kessi-Pérez Eduardo I. Kessi-Pérez Francisco Salinas Francisco Salinas Francisco Salinas Asier González Ying Su José M. Guillamón Michael N. Hall Luis F. Larrondo Luis F. Larrondo Claudio Martínez Claudio Martínez KAE1 Allelic Variants Affect TORC1 Activation and Fermentation Kinetics in Saccharomyces cerevisiae Frontiers in Microbiology Saccharomyces cerevisiae TORC1 pathway natural variation microculture fermentation tRNA modification |
| title | KAE1 Allelic Variants Affect TORC1 Activation and Fermentation Kinetics in Saccharomyces cerevisiae |
| title_full | KAE1 Allelic Variants Affect TORC1 Activation and Fermentation Kinetics in Saccharomyces cerevisiae |
| title_fullStr | KAE1 Allelic Variants Affect TORC1 Activation and Fermentation Kinetics in Saccharomyces cerevisiae |
| title_full_unstemmed | KAE1 Allelic Variants Affect TORC1 Activation and Fermentation Kinetics in Saccharomyces cerevisiae |
| title_short | KAE1 Allelic Variants Affect TORC1 Activation and Fermentation Kinetics in Saccharomyces cerevisiae |
| title_sort | kae1 allelic variants affect torc1 activation and fermentation kinetics in saccharomyces cerevisiae |
| topic | Saccharomyces cerevisiae TORC1 pathway natural variation microculture fermentation tRNA modification |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2019.01686/full |
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