Evolution of a novel chimeric maltotriose transporter in Saccharomyces eubayanus from parent proteins unable to perform this function
Abstract
At the molecular level, the evolution of new traits can be broadly divided between changes in gene expression and changes in protein-coding sequence. For proteins, the evolution of novel functions is generally thought to proceed through sequential point mutations or recombination of whole functional units. In Saccharomyces, the uptake of the sugar maltotriose into the cell is the primary limiting factor in its utilization, but maltotriose transporters are relatively rare, except in brewing strains. No known wild strains of Saccharomyces eubayanus, the cold-tolerant parent of hybrid lager-brewing yeasts (Saccharomyces cerevisiae x S. eubayanus), are able to consume maltotriose, which limits their ability to fully ferment malt extract. In one strain of S. eubayanus, we found a gene closely related to a known maltotriose transporter and were able to confer maltotriose consumption by overexpressing this gene or by passaging the strain on maltose. Even so, most wild strains of S. eubayanus lack native maltotriose transporters. To determine how this rare trait could evolve in naive genetic backgrounds, we performed an adaptive evolution experiment for maltotriose consumption, which yielded a single strain of S. eubayanus able to grow on maltotriose. We mapped the causative locus to a gene encoding a novel chimericmore »
- Publication Date:
- Research Org.:
- Univ. of Wisconsin, Madison, WI (United States). Great Lakes Bioenergy Research Center
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); USDA
- OSTI Identifier:
- 1546688
- Grant/Contract Number:
- SC0018409; DEB-1253634
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Genetics
- Additional Journal Information:
- Journal Volume: 15; Journal Issue: 4; Journal ID: ISSN 1553-7404
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Baker, EmilyClare P., Hittinger, Chris Todd, and Zhang, Jianzhi. Evolution of a novel chimeric maltotriose transporter in Saccharomyces eubayanus from parent proteins unable to perform this function. United States: N. p., 2019.
Web. doi:10.1371/journal.pgen.1007786.
Baker, EmilyClare P., Hittinger, Chris Todd, & Zhang, Jianzhi. Evolution of a novel chimeric maltotriose transporter in Saccharomyces eubayanus from parent proteins unable to perform this function. United States. doi:10.1371/journal.pgen.1007786.
Baker, EmilyClare P., Hittinger, Chris Todd, and Zhang, Jianzhi. Thu .
"Evolution of a novel chimeric maltotriose transporter in Saccharomyces eubayanus from parent proteins unable to perform this function". United States. doi:10.1371/journal.pgen.1007786. https://www.osti.gov/servlets/purl/1546688.
@article{osti_1546688,
title = {Evolution of a novel chimeric maltotriose transporter in Saccharomyces eubayanus from parent proteins unable to perform this function},
author = {Baker, EmilyClare P. and Hittinger, Chris Todd and Zhang, Jianzhi},
abstractNote = {At the molecular level, the evolution of new traits can be broadly divided between changes in gene expression and changes in protein-coding sequence. For proteins, the evolution of novel functions is generally thought to proceed through sequential point mutations or recombination of whole functional units. In Saccharomyces, the uptake of the sugar maltotriose into the cell is the primary limiting factor in its utilization, but maltotriose transporters are relatively rare, except in brewing strains. No known wild strains of Saccharomyces eubayanus, the cold-tolerant parent of hybrid lager-brewing yeasts (Saccharomyces cerevisiae x S. eubayanus), are able to consume maltotriose, which limits their ability to fully ferment malt extract. In one strain of S. eubayanus, we found a gene closely related to a known maltotriose transporter and were able to confer maltotriose consumption by overexpressing this gene or by passaging the strain on maltose. Even so, most wild strains of S. eubayanus lack native maltotriose transporters. To determine how this rare trait could evolve in naive genetic backgrounds, we performed an adaptive evolution experiment for maltotriose consumption, which yielded a single strain of S. eubayanus able to grow on maltotriose. We mapped the causative locus to a gene encoding a novel chimeric transporter that was formed by an ectopic recombination event between two genes encoding transporters that are unable to import maltotriose. In contrast to classic models of the evolution of novel protein functions, the recombination breakpoints occurred within a single functional domain. Thus, the ability of the new protein to carry maltotriose was likely acquired through epistatic interactions between independently evolved substitutions. By acquiring multiple mutations at once, the transporter rapidly gained a novel function, while bypassing potentially deleterious intermediate steps. This study provides an illuminating example of how recombination between paralogs can establish novel interactions among substitutions to create adaptive functions.},
doi = {10.1371/journal.pgen.1007786},
journal = {PLoS Genetics},
number = 4,
volume = 15,
place = {United States},
year = {2019},
month = {4}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 8 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Beer brewing using a fusant between a sake yeast and a brewer's yeast
journal, January 2001
- Mukai, Nobuhiko; Nishimori, Chiharu; Fujishige, Ikuko Wilson
- Journal of Bioscience and Bioengineering, Vol. 91, Issue 5
Structure and function of facultative sugar transporters
journal, August 1999
- Barrett, Michael P.; Walmsleyt, Adrian R.; Gould, Gwyn W.
- Current Opinion in Cell Biology, Vol. 11, Issue 4
Repeated batch fermentation from raw starch using a maltose transporter and amylase expressing diploid yeast strain
journal, February 2010
- Yamakawa, Syun-ichi; Yamada, Ryosuke; Tanaka, Tsutomu
- Applied Microbiology and Biotechnology, Vol. 87, Issue 1
Alternative Saccharomyces interspecies hybrid combinations and their potential for low-temperature wort fermentation : Alternative Saccharomyces interspecies hybrids for brewing
journal, August 2017
- Nikulin, Jarkko; Krogerus, Kristoffer; Gibson, Brian
- Yeast, Vol. 35, Issue 1
I-TASSER: a unified platform for automated protein structure and function prediction
journal, March 2010
- Roy, Ambrish; Kucukural, Alper; Zhang, Yang
- Nature Protocols, Vol. 5, Issue 4
Structural Biology of the Major Facilitator Superfamily Transporters
journal, June 2015
- Yan, Nieng
- Annual Review of Biophysics, Vol. 44, Issue 1
Chimeric Genes as a Source of Rapid Evolution in Drosophila melanogaster
journal, July 2011
- Rogers, R. L.; Hartl, D. L.
- Molecular Biology and Evolution, Vol. 29, Issue 2
The temperature dependence of maltose transport in ale and lager strains of brewer's yeast: The temperature dependence of maltose transport into yeasts
journal, March 2010
- Vidgren, Virve; Multanen, Jyri-Pekka; Ruohonen, Laura
- FEMS Yeast Research, Vol. 10, Issue 4
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
journal, September 1997
- Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A.
- Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402
Protein evolution by molecular breeding
journal, June 1999
- Minshull, Jeremy; Willem Stemmer, P. C.
- Current Opinion in Chemical Biology, Vol. 3, Issue 3, p. 284-290
Improved Fermentation Performance of a Lager Yeast after Repair of Its AGT1 Maltose and Maltotriose Transporter Genes
journal, January 2009
- Vidgren, V.; Huuskonen, A.; Virtanen, H.
- Applied and Environmental Microbiology, Vol. 75, Issue 8
Birth, decay, and reconstruction of an ancient TRIMCyp gene fusion in primate genomes
journal, January 2013
- Malfavon-Borja, R.; Wu, L. I.; Emerman, M.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 7
The I-TASSER Suite: protein structure and function prediction
journal, December 2014
- Yang, Jianyi; Yan, Renxiang; Roy, Ambrish
- Nature Methods, Vol. 12, Issue 1
Resistance to malaria through structural variation of red blood cell invasion receptors
journal, May 2017
- Leffler, Ellen M.; Band, Gavin; Busby, George B. J.
- Science, Vol. 356, Issue 6343
Comparative physiology and fermentation performance of Saaz and Frohberg lager yeast strains and the parental species Saccharomyces eubayanus : Fermentaton performance of Saaz and Frohberg yeast
journal, June 2013
- Gibson, Brian R.; Storgårds, Erna; Krogerus, Kristoffer
- Yeast, Vol. 30, Issue 7
I-TASSER server for protein 3D structure prediction
journal, January 2008
- Zhang, Yang
- BMC Bioinformatics, Vol. 9, Issue 1
Formation of Chimeric Genes by Copy-Number Variation as a Mutational Mechanism in Schizophrenia
journal, October 2013
- Rippey, Caitlin; Walsh, Tom; Gulsuner, Suleyman
- The American Journal of Human Genetics, Vol. 93, Issue 4
Characterization of the Saccharomyces bayanus-type AGT1 transporter of lager yeast: Saccharomyces bayanus-type AGT1 transporter of lager yeast
journal, July 2012
- Vidgren, Virve; Londesborough, John
- Journal of the Institute of Brewing, Vol. 118, Issue 2
Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus
journal, July 2016
- Peris, David; Langdon, Quinn K.; Moriarty, Ryan V.
- PLOS Genetics, Vol. 12, Issue 7
Characterization of the putative maltose transporters encoded by YDL247w and YJR160c
journal, January 2002
- Day, Rachel E.; Higgins, Vincent J.; Rogers, Peter J.
- Yeast, Vol. 19, Issue 12
SIFT: predicting amino acid changes that affect protein function
journal, July 2003
- Ng, P. C.
- Nucleic Acids Research, Vol. 31, Issue 13
The impact of translocations and gene fusions on cancer causation
journal, March 2007
- Mitelman, Felix; Johansson, Bertil; Mertens, Fredrik
- Nature Reviews Cancer, Vol. 7, Issue 4
STRUM: structure-based prediction of protein stability changes upon single-point mutation
journal, June 2016
- Quan, Lijun; Lv, Qiang; Zhang, Yang
- Bioinformatics, Vol. 32, Issue 19
Inheritance of brewing-relevant phenotypes in constructed Saccharomyces cerevisiae × Saccharomyces eubayanus hybrids
journal, April 2017
- Krogerus, Kristoffer; Seppänen-Laakso, Tuulikki; Castillo, Sandra
- Microbial Cell Factories, Vol. 16, Issue 1
Transposable Elements, Epigenetics, and Genome Evolution
journal, November 2012
- Fedoroff, N. V.
- Science, Vol. 338, Issue 6108
Concerted Evolution of Two Novel Protein Families in Caenorhabditis Species
journal, January 2006
- Thomas, James H.
- Genetics, Vol. 172, Issue 4
Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae
journal, November 2002
- Dunham, M. J.; Badrane, H.; Ferea, T.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 25
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing
journal, May 2012
- Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry
- Journal of Computational Biology, Vol. 19, Issue 5
On the conservative nature of intragenic recombination
journal, April 2005
- Drummond, D. A.; Silberg, J. J.; Meyer, M. M.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 15
Characterization of AGT1 encoding a general alpha-glucoside transporter from Saccharomyces
journal, September 1995
- Han, Eun-Kyoung; Cotty, Francis; Sottas, Chantal
- Molecular Microbiology, Vol. 17, Issue 6
The 100-genomes strains, an S. cerevisiae resource that illuminates its natural phenotypic and genotypic variation and emergence as an opportunistic pathogen
journal, April 2015
- Strope, Pooja K.; Skelly, Daniel A.; Kozmin, Stanislav G.
- Genome Research, Vol. 25, Issue 5
S. cerevisiae × S. eubayanus interspecific hybrid, the best of both worlds and beyond
journal, March 2015
- Hebly, Marit; Brickwedde, Anja; Bolat, Irina
- FEMS Yeast Research, Vol. 15, Issue 3
Yeast Evolution and Comparative Genomics
journal, October 2005
- Liti, Gianni; Louis, Edward J.
- Annual Review of Microbiology, Vol. 59, Issue 1
Prolonged Maltose-Limited Cultivation of Saccharomyces cerevisiae Selects for Cells with Improved Maltose Affinity and Hypersensitivity
journal, April 2004
- Jansen, M. L. A.; Daran-Lapujade, P.; de Winde, J. H.
- Applied and Environmental Microbiology, Vol. 70, Issue 4
Movement of DNA sequence recognition domains between non-orthologous proteins
journal, July 2012
- Furuta, Yoshikazu; Kobayashi, Ichizo
- Nucleic Acids Research, Vol. 40, Issue 18
The Genome Sequence of Saccharomyces eubayanus and the Domestication of Lager-Brewing Yeasts
journal, August 2015
- Baker, EmilyClare; Wang, Bing; Bellora, Nicolas
- Molecular Biology and Evolution, Vol. 32, Issue 11
Characterization of maltotriose transporters from the Saccharomyces eubayanus subgenome of the hybrid Saccharomyces pastorianus lager brewing yeast strain Weihenstephan 34/70
journal, November 2012
- Cousseau, F. E. M.; Alves, S. L.; Trichez, D.
- Letters in Applied Microbiology, Vol. 56, Issue 1
The Multiplicity of Domains in Proteins
journal, June 1995
- Doolittle, Russell F.
- Annual Review of Biochemistry, Vol. 64, Issue 1
Dissection of genetically complex traits with extremely large pools of yeast segregants
journal, April 2010
- Ehrenreich, Ian M.; Torabi, Noorossadat; Jia, Yue
- Nature, Vol. 464, Issue 7291
Evidence for a Far East Asian origin of lager beer yeast
journal, May 2014
- Bing, Jian; Han, Pei-Jie; Liu, Wan-Qiu
- Current Biology, Vol. 24, Issue 10
MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004
- Edgar, R. C.
- Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
Predicting the Effects of Amino Acid Substitutions on Protein Function
journal, September 2006
- Ng, Pauline C.; Henikoff, Steven
- Annual Review of Genomics and Human Genetics, Vol. 7, Issue 1
Accounting for Human Polymorphisms Predicted to Affect Protein Function
journal, March 2002
- Ng, P. C.
- Genome Research, Vol. 12, Issue 3
Predicting Deleterious Amino Acid Substitutions
journal, May 2001
- Ng, P. C.; Henikoff, S.
- Genome Research, Vol. 11, Issue 5
The origin of new genes: glimpses from the young and old
journal, November 2003
- Long, Manyuan; Betrán, Esther; Thornton, Kevin
- Nature Reviews Genetics, Vol. 4, Issue 11
Population structure and reticulate evolution of Saccharomyces eubayanus and its lager-brewing hybrids
journal, April 2014
- Peris, David; Sylvester, Kayla; Libkind, Diego
- Molecular Ecology, Vol. 23, Issue 8
Genome evolution and the evolution of exon-shuffling — a review
journal, September 1999
- Patthy, László
- Gene, Vol. 238, Issue 1
The Generation of New Protein Functions by the Combination of Domains
journal, January 2007
- Bashton, Matthew; Chothia, Cyrus
- Structure, Vol. 15, Issue 1
Mapping Novel Traits by Array-Assisted Bulk Segregant Analysis in Saccharomyces cerevisiae
journal, April 2006
- Brauer, Matthew J.; Christianson, Cheryl M.; Pai, Dave A.
- Genetics, Vol. 173, Issue 3
The genetic manipulation of industrial yeast strains
journal, October 1981
- Stewart, G. G.
- Canadian Journal of Microbiology, Vol. 27, Issue 10
High-Resolution Mutation Mapping Reveals Parallel Experimental Evolution in Yeast
journal, July 2006
- Segrè, Ayellet V.; Murray, Andrew W.; Leu, Jun-Yi
- PLoS Biology, Vol. 4, Issue 8
Regulations of sugar transporters: insights from yeast
journal, March 2013
- Horák, J.
- Current Genetics, Vol. 59, Issue 1-2
The Origin of the Jingwei Gene and the Complex Modular Structure of Its Parental Gene, Yellow Emperor, in Drosophila melanogaster
journal, September 2000
- Wang, Wen; Zhang, Jianming; Alvarez, Carlos
- Molecular Biology and Evolution, Vol. 17, Issue 9
In vivo recombination of Saccharomyces eubayanus maltose-transporter genes yields a chimeric transporter that enables maltotriose fermentation
journal, April 2019
- Brouwers, Nick; Gorter de Vries, Arthur R.; van den Broek, Marcel
- PLOS Genetics, Vol. 15, Issue 4
PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments
journal, July 2006
- Suyama, M.; Torrents, D.; Bork, P.
- Nucleic Acids Research, Vol. 34, Issue Web Server
Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data
journal, April 2012
- Kearse, M.; Moir, R.; Wilson, A.
- Bioinformatics, Vol. 28, Issue 12
Comprehensive variation discovery in single human genomes
journal, October 2014
- Weisenfeld, Neil I.; Yin, Shuangye; Sharpe, Ted
- Nature Genetics, Vol. 46, Issue 12
Efficient engineering of marker-free synthetic allotetraploids of Saccharomyces
journal, April 2016
- Alexander, William G.; Peris, David; Pfannenstiel, Brandon T.
- Fungal Genetics and Biology, Vol. 89
New lager yeast strains generated by interspecific hybridization
journal, February 2015
- Krogerus, Kristoffer; Magalhães, Frederico; Vidgren, Virve
- Journal of Industrial Microbiology & Biotechnology, Vol. 42, Issue 5
Molecular Analysis of Maltotriose Transport and Utilization by Saccharomycescerevisiae
journal, November 2002
- Day, R. E.; Rogers, P. J.; Dawes, I. W.
- Applied and Environmental Microbiology, Vol. 68, Issue 11
Combinatorial protein design by in vitro recombination
journal, June 1998
- Giver, Lori; Arnold, Frances H.
- Current Opinion in Chemical Biology, Vol. 2, Issue 3
Improvement of maltotriose fermentation by Saccharomyces cerevisiae
journal, October 2006
- Stambuk, B. U.; Alves, S. L.; Hollatz, C.
- Letters in Applied Microbiology, Vol. 43, Issue 4
Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm
journal, June 2009
- Kumar, Prateek; Henikoff, Steven; Ng, Pauline C.
- Nature Protocols, Vol. 4, Issue 7
The Repertoire and Dynamics of Evolutionary Adaptations to Controlled Nutrient-Limited Environments in Yeast
journal, December 2008
- Gresham, David; Desai, Michael M.; Tucker, Cheryl M.
- PLoS Genetics, Vol. 4, Issue 12
Structural, Physiological and Regulatory Analysis of Maltose Transporter Genes in Saccharomyces eubayanus CBS 12357T
journal, August 2018
- Brickwedde, Anja; Brouwers, Nick; van den Broek, Marcel
- Frontiers in Microbiology, Vol. 9
Gene Families: The Taxonomy of Protein Paralogs and Chimeras
journal, October 1997
- Henikoff, S.
- Science, Vol. 278, Issue 5338
Utilizing natural diversity to evolve protein function: applications towards thermostability
journal, June 2011
- Cole, Megan F.; Gaucher, Eric A.
- Current Opinion in Chemical Biology, Vol. 15, Issue 3
Increased xylose affinity of Hxt2 through gene shuffling of hexose transporters in Saccharomyces cerevisiae
journal, January 2018
- Nijland, J. G.; Shin, H. Y.; de Waal, P. P.
- Journal of Applied Microbiology, Vol. 124, Issue 2
A hierarchical approach to protein molecular evolution
journal, March 1999
- Bogarad, L. D.; Deem, M. W.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 6
Genome Sequence of the Lager Brewing Yeast, an Interspecies Hybrid
journal, January 2009
- Nakao, Y.; Kanamori, T.; Itoh, T.
- DNA Research, Vol. 16, Issue 2
Genomic analysis of a key innovation in an experimental Escherichia coli population
journal, September 2012
- Blount, Zachary D.; Barrick, Jeffrey E.; Davidson, Carla J.
- Nature, Vol. 489, Issue 7417
Rapid Expansion and Functional Divergence of Subtelomeric Gene Families in Yeasts
journal, May 2010
- Brown, Chris A.; Murray, Andrew W.; Verstrepen, Kevin J.
- Current Biology, Vol. 20, Issue 10
A Large Set of Newly Created Interspecific Saccharomyces Hybrids Increases Aromatic Diversity in Lager Beers
journal, September 2015
- Mertens, Stijn; Steensels, Jan; Saels, Veerle
- Applied and Environmental Microbiology, Vol. 81, Issue 23
Maltotriose utilization in lager yeast strains:MTT1 encodes a maltotriose transporter
journal, January 2005
- Dietvorst, J.; Londesborough, J.; Steensma, H. Y.
- Yeast, Vol. 22, Issue 10
Identification of interdomain sequences promoting the intronless evolution of a bacterial protein family.
journal, August 1996
- de Chateau, M.; Bjorck, L.
- Proceedings of the National Academy of Sciences, Vol. 93, Issue 16
Novel brewing yeast hybrids: creation and application
journal, November 2016
- Krogerus, Kristoffer; Magalhães, Frederico; Vidgren, Virve
- Applied Microbiology and Biotechnology, Vol. 101, Issue 1
Recombinatoric exploration of novel folded structures: A heteropolymer-based model of protein evolutionary landscapes
journal, January 2002
- Cui, Y.; Wong, W. H.; Bornberg-Bauer, E.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 2
In Silico Whole Genome Sequencer and Analyzer (iWGS): a Computational Pipeline to Guide the Design and Analysis of de novo Genome Sequencing Studies
journal, September 2016
- Zhou, Xiaofan; Peris, David; Kominek, Jacek
- G3: Genes|Genomes|Genetics, Vol. 6, Issue 11
Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast
journal, August 2011
- Libkind, D.; Hittinger, C. T.; Valerio, E.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 35
Characterization and Functional Analysis of the MAL and MPH Loci for Maltose Utilization in Some Ale and Lager Yeast Strains
journal, December 2005
- Vidgren, V.; Ruohonen, L.; Londesborough, J.
- Applied and Environmental Microbiology, Vol. 71, Issue 12
Empirical fitness landscapes reveal accessible evolutionary paths
journal, January 2007
- Poelwijk, Frank J.; Kiviet, Daniel J.; Weinreich, Daniel M.
- Nature, Vol. 445, Issue 7126
A High-Definition View of Functional Genetic Variation from Natural Yeast Genomes
journal, January 2014
- Bergström, Anders; Simpson, Jared T.; Salinas, Francisco
- Molecular Biology and Evolution, Vol. 31, Issue 4
Amino acid substitution matrices from protein blocks.
journal, November 1992
- Henikoff, S.; Henikoff, J. G.
- Proceedings of the National Academy of Sciences, Vol. 89, Issue 22, p. 10915-10919
Evolutionary Engineering in Chemostat Cultures for Improved Maltotriose Fermentation Kinetics in Saccharomyces pastorianus Lager Brewing Yeast
journal, September 2017
- Brickwedde, Anja; van den Broek, Marcel; Geertman, Jan-Maarten A.
- Frontiers in Microbiology, Vol. 8
Modularity of MAP kinases allows deformation of their signalling pathways
journal, March 2009
- Mody, Areez; Weiner, Joan; Ramanathan, Sharad
- Nature Cell Biology, Vol. 11, Issue 4
Molecular Analysis of Maltotriose Active Transport and Fermentation by Saccharomyces cerevisiae Reveals a Determinant Role for the AGT1 Permease
journal, January 2008
- Alves, S. L.; Herberts, R. A.; Hollatz, C.
- Applied and Environmental Microbiology, Vol. 74, Issue 5
Engineering and Two-Stage Evolution of a Lignocellulosic Hydrolysate-Tolerant Saccharomyces cerevisiae Strain for Anaerobic Fermentation of Xylose from AFEX Pretreated Corn Stover
journal, September 2014
- Parreiras, Lucas S.; Breuer, Rebecca J.; Avanasi Narasimhan, Ragothaman
- PLoS ONE, Vol. 9, Issue 9
Identification of loci that cause phenotypic variation in diverse species with the reciprocal hemizygosity test
journal, December 2014
- Stern, David L.
- Trends in Genetics, Vol. 30, Issue 12
Structure, function and evolution of multidomain proteins
journal, April 2004
- Vogel, Christine; Bashton, Matthew; Kerrison, Nicola D.
- Current Opinion in Structural Biology, Vol. 14, Issue 2
Ploidy influences the functional attributes of de novo lager yeast hybrids
journal, May 2016
- Krogerus, Kristoffer; Arvas, Mikko; De Chiara, Matteo
- Applied Microbiology and Biotechnology, Vol. 100, Issue 16
Enzyme Promiscuity: A Mechanistic and Evolutionary Perspective
journal, June 2010
- Khersonsky, Olga; Tawfik, Dan S.
- Annual Review of Biochemistry, Vol. 79, Issue 1, p. 471-505
Maltotriose Utilization by Industrial Saccharomyces Strains: Characterization of a New Member of the -Glucoside Transporter Family
journal, September 2005
- Salema-Oom, M.; Valadao Pinto, V.; Goncalves, P.
- Applied and Environmental Microbiology, Vol. 71, Issue 9
The Thr 505 and Ser 557 residues of the AGT1-encoded α-glucoside transporter are critical for maltotriose transport in Saccharomyces cerevisiae
journal, April 2008
- Smit, A.; Moses, S. G.; Pretorius, I. S.
- Journal of Applied Microbiology, Vol. 104, Issue 4
Diverse yeasts for diverse fermented beverages and foods
journal, February 2018
- Hittinger, Chris Todd; Steele, James L.; Ryder, David S.
- Current Opinion in Biotechnology, Vol. 49
Dynamic New World: Refining Our View of Protein Structure, Function and Evolution
journal, March 2014
- Mannige, Ranjan
- Proteomes, Vol. 2, Issue 1
Works referencing / citing this record:
A deletion in the STA1 promoter determines maltotriose and starch utilization in STA1+ Saccharomyces cerevisiae strains
journal, July 2019
- Krogerus, Kristoffer; Magalhães, Frederico; Kuivanen, Joosu
- Applied Microbiology and Biotechnology, Vol. 103, Issue 18
A deletion in the STA1 promoter determines maltotriose and starch utilization in STA1+ Saccharomyces cerevisiae strains
journal, July 2019
- Krogerus, Kristoffer; Magalhães, Frederico; Kuivanen, Joosu
- Applied Microbiology and Biotechnology, Vol. 103, Issue 18
Fermentation innovation through complex hybridization of wild and domesticated yeasts
journal, October 2019
- Langdon, Quinn K.; Peris, David; Baker, EmilyClare P.
- Nature Ecology & Evolution, Vol. 3, Issue 11
Lager-brewing yeasts in the era of modern genetics
journal, September 2019
- Gorter de Vries, Arthur R.; Pronk, Jack T.; Daran, Jean-Marc G.
- FEMS Yeast Research, Vol. 19, Issue 7
Himalayan Saccharomyces eubayanus Genome Sequences Reveal Genetic Markers Explaining Heterotic Maltotriose Consumption by Saccharomyces pastorianus Hybrids
journal, September 2019
- Brouwers, Nick; Brickwedde, Anja; Gorter de Vries, Arthur R.
- Applied and Environmental Microbiology, Vol. 85, Issue 22