Ady2p is essential for the acetate permease activity in the yeast Saccharomyces cerevisiae
Open accessAbstract
To identify new genes involved in acetate uptake in Saccharomyces cerevisiae, an analysis of the gene expression profiles of cells shifted from glucose to acetic acid was performed. The gene expression reprogramming of yeast adapting to a poor non-fermentable carbon source was observed, including dramatic metabolic changes, global activation of translation machinery, mitochondria biogenesis and the induction of known or putative transporters. Among them, the gene ADY2/YCR010c was identified as a new key element for acetate transport, being homologous to the Yarrowia lipolytica GPR1 gene, which has a role in acetic acid sensitivity. Disruption of ADY2 in S. cerevisiae abolished the active transport of acetate. Microarray analyses of ady2Delta strains showed that this gene is not a critical regulator of acetate response and that its role is directly connected to acetate transport. Ady2p is predicted to be a membrane protein and is a valuable acetate transporter candidate.
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In S. cerevisiae, ADY2 (also called ATO1) encodes a permease-mediating uptake of acetate-propionate-formate present in ethanol or acetate-grown cells.
“In S. cerevisiae, ADY2 (also called ATO1) encodes a permease-mediating uptake of acetate–propionate–formate present in ethanol or acetate-grown cells (Casal et al., 1996; Paiva et al., 2004; Pacheco et al., 2012).”
From Candida glabrata susceptibility to antifungals and phagocytosis is modulated by acetate (2015) · cites this paper as Paiva et al., 2004
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“In S. cerevisiae, ADY2 (also called ATO1) encodes a permeasemediating uptake of acetate–propionate–formate present in ethanol or acetate-grown cells (Casal et al., 1996; Paiva et al., 2004; Pacheco et al., 2012).”
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“2), which display 53% and 50% identity to the yeast acetate transporter Ady2p, which was shown to be essential for the active uptake of acetate (Paiva et al., 2004) and may also be able to transport propionate.”
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Ždralević, M., Guaragnella, N., Antonacci, L., Marra, E., & Giannattasio, S. (2012) · The Scientific World JOURNAL · doi:10.1100/2012/912147 · Cited by 38 · see citing works
“…such as phosphatidylserine externalization to the outer layer of the cytoplasmic membrane, DNA fragmentation, chromatin condensation, ROS production, and involvement of specific pro-apoptotic proteins, including cyt c, Aif1p, and Bcl-2 homology domain 3- (BH3-) containing protein [31–33].”
Robellet, X., Flipphi, M. J. A., Pégot, S., MacCabe, A., & Vélot, C. (2008) · Biochemical Journal · doi:10.1042/bj20080124 · Cited by 38 · see citing works
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“In S. cerevisiae, export of carboxylic acids remains a poorly understood subject, as exemplified by the fact that even export of simple organic acids such as acetic acid and lactic acid remain incompletely understood (Casal et al., 2008; Paiva et al., 2004; van Maris et al., 2004b).”
BackgroundHeit, C., Martin, S., Yang, F., & Inglis, D. L. (2018) · Journal of Applied Microbiology · doi:10.1111/jam.13733 · Cited by 35 · see citing works
“ADY2 encodes for a protein that has been proposed to function as an acetate permease (Paiva et al. 2004).”
BackgroundNoar, R. D., & Daub, M. E. (2016) · BMC Genomics · doi:10.1186/s12864-016-3031-5 · Cited by 35 · see citing works
“in the environment was determined and is indicated in the bar chart [112–123].”
BackgroundXu, Q. L., Bai, C., Liu, Y., Song, L., Tian, L., Yan, Y., Zhou, J., Zhou, X., Zhang, Y., & Cai, M. (2019) · Biotechnology for Biofuels · doi:10.1186/s13068-019-1404-0 · Cited by 33 · see citing works
Mans, R., Hassing, E.-J., Wijsman, M., Giezekamp, A., Pronk, J. T., Daran, J.-M. G., & van Maris, A. J. A. (2017) · FEMS Yeast Research · doi:10.1093/femsyr/fox085 · Cited by 32 · see citing works
“…major facilitator superfamily (MFS) lactate transporter Jen1 and the acetate transporter Ady2 (Cássio, Leao and Van Uden 1987; Casal et al. 1999; Paiva et al. 2004; Ramos, Sychrová and Kschischo 2016) and combined deletion of JEN1 and ADY2 eliminates growth on lactate as the sole carbon source…”
BackgroundSoares‐Silva, I., Sá‐Pessoa, J., Myrianthopoulos, V., Mikros, E., Casal, M., & Diallinas, G. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2011.07729.x · Cited by 32 · see citing works
“, 1999) and another by the ADY2 gene (Paiva et al., 2004).”
BackgroundVilela, A. (2017) · Fermentation · doi:10.3390/fermentation3040051 · Cited by 31 · see citing works
“Later, it was found that the protein Ady2p was vital for acetate transport in acetic acid-grown cells [63].”
BackgroundThe physiological effect of heavy metals and volatile fatty acids on Methanococcus maripaludis S2
Abdel Azim, A., Rittmann, S. K.-M. R., Fino, D., & Bochmann, G. (2018) · Biotechnology for Biofuels · doi:10.1186/s13068-018-1302-x · Cited by 30 · see citing works
Welte, C. U., Kröninger, L., & Deppenmeier, U. (2014) · FEMS Microbiology Letters · doi:10.1111/1574-6968.12550 · Cited by 30 · see citing works
Carboxylic Acid Transporters in Candida Pathogenesis
Alves, R. M. A., Sousa-Silva, M., Vieira, D., Soares, P. A., Chebaro, Y., Lorenz, M. C., Casal, M., Soares‐Silva, I., & Paiva, S. (2020) · mBio · doi:10.1128/mbio.00156-20 · Cited by 28 · see citing works
“cerevisiae, Ady2 has been identified as an acetate permease with the ability to transport other monocarboxylates, such as propionate, formate, and lactate (18, 36).”
BackgroundExpression and specificity profile of the major acetate transporter AcpA in Aspergillus nidulans
Sá‐Pessoa, J., Amillis, S., Casal, M., & Diallinas, G. (2015) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2015.02.010 · Cited by 26 · see citing works
“The orthologue of AcpA in the yeast Saccharomyces cerevisiae is Ady2p, which is responsible for the uptake of acetate, propionate and formate in symport with protons (Casal et al., 1996; Paiva et al., 2004; Pacheco et al., 2012).”
BackgroundFailure to Maintain Acetate Homeostasis by Acetate-Activating Enzymes Impacts Plant Development
Fu, X., Yang, H., Pangestu, F., & Nikolau, B. J. (2019) · PLANT PHYSIOLOGY · doi:10.1104/pp.19.01162 · Cited by 28 · see citing works
“Monocarboxylate transporters that can facilitate the translocation of acetate have been commonly found in bacteria, yeast, and mammals (Paiva et al., 2004; Moschen et al., 2012; Sun et al., 2018), and the Arabidopsis ABC transporter COMATOSE (CTS) has been invoked in the transport of acetate into…”
BackgroundHlynialuk, C. J. W., Schierholtz, R., Vernooy, A., & van der Merwe, G. K. (2008) · Microbiology · doi:10.1099/mic.0.2008/019976-0 · Cited by 28 · see citing works
“We further analysed the effect of NSF1 deletion on the transcription of ADY2, which encodes the acetate permease of S. cerevisiae and is transcriptionally repressed by glucose, but activated by non-fermentable carbon sources, specifically acetate (Paiva et al., 2004).”
BackgroundMagnesium ions in yeast: setting free the metabolism from glucose catabolite repression
de Souza, R. B., Silva, R. K., Ferreira, D. S., Paiva, S. D. S. L., Pita, W. D. B., & de Morais, M. A. (2016) · Metallomics · doi:10.1039/c6mt00157b · Cited by 27 · see citing works
The acetate uptake transporter family motif “NPAPLGL(M/S)” is essential for substrate uptake
Ribas, D. M. N., Soares‐Silva, I., Vieira, D., Sousa-Silva, M., Sá‐Pessoa, J., Azevedo‐Silva, J., Viegas, S. C., Arraiano, C. M., Diallinas, G., Paiva, S., et al. (2018) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2018.10.001 · Cited by 27 · see citing works
Dolpatcha, S., Phong, H. X., Thanonkeo, P., Klanrit, P., Yamada, M. C., & Thanonkeo, P. (2023) · Scientific Reports · doi:10.1038/s41598-023-48408-7 · Cited by 26 · see citing works
“In S. cerevisiae , tolerance to acetic acid is also correlated with the expression of these three genes 97,98 as well as other genes, including ASG1 (encoding transcriptional regulator), ADH3 (encoding alcohol dehydrogenase), SKS1 (encoding protein kinase), and GIS4 (encoding a protein involved in…”
BackgroundMota, S. M. D. S., Vieira, N., Barbosa, S., Delaveau, T., Torchet, C., Saux, A. L., Garcia, M., Pereira, A. M. M. B., Lemoine, S., Coulpier, F., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0111589 · Cited by 26 · see citing works
Řičicová, M., Kučerová, H., Váchová, L., & Palková, Z. (2007) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2007.02.011 · Cited by 25 · see citing works
Durante, L., Hübner, W., Lauersen, K. J., & Remacle, C. (2019) · Plant Direct · doi:10.1002/pld3.148 · Cited by 25 · see citing works
Ianiri, G., Dagotto, G., Sun, S., & Heitman, J. (2019) · Genetics · doi:10.1534/genetics.119.302329 · Cited by 25 · see citing works
de Kok, S., Nijkamp, J. F., Oud, B., Roque, F. C., de Ridder, D., Daran, J.-M. G., Pronk, J. T., & van Maris, A. J. A. (2012) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2012.00787.x · Cited by 25 · see citing works
Turner, T. L., Lane, S., Jayakody, L. N., Zhang, G.-C., Kim, H., Cho, W., & Jin, Y. (2019) · FEMS Yeast Research · doi:10.1093/femsyr/foz050 · Cited by 23 · see citing works
Queirós, O., Pereira, L., Paiva, S., Moradas‐Ferreira, P., & Casal, M. (2006) · Current Genetics · doi:10.1007/s00294-006-0107-9 · Cited by 24 · see citing works
“Recently, the gene ADY2 was reported as a new key element in the mechanism of transport of acetic acid in S. cerevisiae (Paiva et al. 2004).”
BackgroundJungbluth, M., Mösch, H., & Taxis, C. (2012) · Eukaryotic Cell · doi:10.1128/ec.05240-11 · Cited by 24 · see citing works
“Ady1 is important for the localization of Mpc54 to SPBs and the formation of MPs (11), whereas Ady2 is important for acetate uptake (44) and MP component production (57).”
BackgroundLack of Ach1 CoA-Transferase Triggers Apoptosis and Decreases Chronological Lifespan in Yeast
Orlandi, I., Casatta, N., & Vai, M. (2012) · Frontiers in Oncology · doi:10.3389/fonc.2012.00067 · Cited by 23 · see citing works
“This work was supported by FAR 2010 to Marina Vai.”
BackgroundMethodKuanyshev, N., Ami, D., Signori, L., Porro, D., Morrissey, J. P., & Branduardi, P. (2016) · FEMS Yeast Research · doi:10.1093/femsyr/fow058 · Cited by 23 · see citing works
“The mechanism of acetic acid toxicity, model organic acid for stress response studies, has been extensively studied in the yeast S. cerevisiae (Paiva et al. 2004; Mira, Teixeira and Sa 2010; Nygård et al. 2014).”
BackgroundPattanakittivorakul, S., Tsuzuno, T., Kosaka, T., Murata, M., Kanesaki, Y., Yoshikawa, H., Limtong, S., & Yamada, M. C. (2022) · Microorganisms · doi:10.3390/microorganisms10040798 · Cited by 22 · see citing works
Acetate provokes mitochondrial stress and cell death inUstilago maydis
Kretschmer, M., Lambie, S. C., Croll, D., & Kronstad, J. W. (2017) · Molecular Microbiology · doi:10.1111/mmi.13894 · Cited by 22 · see citing works
“cerevisiae, for example, acetate is not used as a carbon source if fermentable sugars are available, but it is taken up passively by the aquaporin Fps1 in the presence of glucose at low pH (Paiva et al., 2004; Mollapour and Piper, 2007).”
BackgroundEngineering Flocculation for Improved Tolerance and Production of d-Lactic Acid in Pichia pastoris
Sae-Tang, K., Bumrungtham, P., Mhuantong, W., Champreda, V., Tanapongpipat, S., Zhao, X., Liu, C., & Runguphan, W. (2023) · Journal of Fungi · doi:10.3390/jof9040409 · Cited by 19 · see citing works
Mathematical Modeling and Validation of the Ergosterol Pathway in Saccharomyces cerevisiae
Alvarez‐Vasquez, F., Riezman, H., Hannun, Y. A., & Voit, E. O. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028344 · Cited by 21 · see citing works
“cerevisiae represses expression of acetyl energy dependent transporters [117,118]; under these conditions, the uptake of acetate is proportional to the external acetate concentration [119,120].”
BackgroundPhi, Q., Oh, S.-H., Park, Y.-M., Park, S., Ryu, C., & Ghim, S. (2008) · Current Microbiology · doi:10.1007/s00284-008-9118-8 · Cited by 20 · see citing works
“These proteins are predicted to be localized in the bacterial membrane involving transport and their function remains to be elucidated [4], whereas in yeasts and fungi this novel protein family has been demonstrated to be involved in ammonia secretion, acetate uptake, and the adaptation process to acetic acid [1, 4, 1…”
BackgroundStojiljković, M., Foulquié-Moreno, M. R., & Thevelein, J. M. (2020) · Biotechnology for Biofuels · doi:10.1186/s13068-020-01761-5 · Cited by 19 · see citing works
Dijk, M., Rugbjerg, P., Nygård, Y., & Lisbeth Olsson, A. (2021) · Biotechnology for Biofuels · doi:10.1186/s13068-021-02049-y · Cited by 19 · see citing works
Characterization of the Metabolic Requirements in Yeast Meiosis
Ray, D., & Ye, P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0063707 · Cited by 19 · see citing works
“Reactions are compartmentalized in either the cytoplasm or the mitochondria, based on the sub-cellular localization of enzymes determined by experimental evidence [33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54].”
Mechanism and improvement of yeast tolerance to biomass-derived inhibitors: A review
Yu, J., Li, C., Cheng, Y. W., Guo, S., Lu, H., Xie, X., Ji, H., & Qiao, Y. (2025) · Biotechnology Advances · doi:10.1016/j.biotechadv.2025.108562 · Cited by 18 · see citing works
Kozak, B. U., van Rossum, H. M., Niemeijer, M. S., Dijk, M., Benjamin, K. R., Wu, L., Daran, J.-M. G., Pronk, J. T., & van Maris, A. J. A. (2016) · FEMS Yeast Research · doi:10.1093/femsyr/fow006 · Cited by 18 · see citing works
“ADY2, which encodes an acetic acid importer localized in the plasma-membrane (Paiva et al. 2004), was among the 14 genes on this region (Table S3, Supporting Information).”
BackgroundGentsch, M., Kuschel, M., Schlegel, S., & Barth, G. (2007) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2006.00191.x · Cited by 18 · see citing works
“Data indicate that Ycr010cp (Ady2p) is essential for the mediated acetate uptake in S. cerevisiae (Paiva et al., 2004).”
BackgroundFunctional analysis of alcS, a gene of the alc cluster in Aspergillus nidulans
Flipphi, M. J. A., Robellet, X., Dequier, E., Leschelle, X., Felenbok, B., & Vélot, C. (2006) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2005.12.008 · Cited by 18 · see citing works
Shepherd, A., & Piper, P. W. (2010) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2010.00636.x · Cited by 17 · see citing works
“Loss of Fps1p elevates acetic acid resistance in Z. rouxii In its glucose-repressed state, S. cerevisiae cannot assimilate acetate as a carbon source (Casal et al., 1996; Paiva et al., 2004).”
BackgroundGenome-wide overexpression screen for sodium acetate resistance in Saccharomyces cerevisiae
Peña, P. V., Glasker, S., & Srienc, F. (2012) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2012.12.005 · Cited by 16 · see citing works
Yeast as a tool to express sugar acid transporters with biotechnological interest
Ribas, D. M. N., Sá‐Pessoa, J., Soares‐Silva, I., Paiva, S., Nygård, Y., Ruohonen, L., Penttilä, M. E., & Casal, M. (2017) · FEMS Yeast Research · doi:10.1093/femsyr/fox005 · Cited by 15 · see citing works
- Authors
- Paiva, S., Devaux, F., Barbosa, S., Jacq, C., & Casal, M.
- Affiliations
- University of Minho (PT)
- Centre National de la Recherche Scientifique (FR)
- Venue
- Yeast
- Publisher
- Wiley
- Published
- 2004-02
- Volume
- 21
- Issue
- 3
- Pages
- 201-210
- ISSN
- 0749-503X (ISSN-L)
- 1097-0061
- OpenAlex
- W2000461833
- Cited by
- 154
- References
- 23
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 3 · 2023: 5 · 2022: 8 · 2021: 17 · 2020: 5 · 2019: 11 · 2018: 8 · 2017: 7 · 2016: 7 · 2015: 9 · 2014: 5 · 2013: 6 · 2012: 14
- FWCI
- 2.13
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- Locations
- Yeast (publishedVersion)
- PubMed (publishedVersion)
- Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT) (submittedVersion, other-oa)
- Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT) (submittedVersion, cc-by-nc-nd)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Keywords
- acetate uptake, acetate transport, Saccharomyces cerevisiae, non-fermentable carbon sources, gene expression reprogramming, mitochondrial biogenesis, translation activation, membrane transporters
- MeSH terms
- Biological Transport, DNA, Fungal, Saccharomyces cerevisiae, Gene Expression Regulation, Fungal, Mutagenesis, Insertional, Acetic Acid, Oligonucleotide Array Sequence Analysis, Membrane Transport Proteins, Monocarboxylic Acid Transporters, Saccharomyces cerevisiae Proteins
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