Extensive Intra-Kingdom Horizontal Gene Transfer Converging on a Fungal Fructose Transporter Gene

Coelho, Marco A.; Gonçalves, Carla; Sampaio, José Paulo; Gonçalves, Paula

doi:10.1371/journal.pgen.1003587

Extensive Intra-Kingdom Horizontal Gene Transfer Converging on a Fungal Fructose Transporter Gene

Journal Article · Thu Jun 20 00:00:00 EDT 2013 · PLoS Genetics

DOI:https://doi.org/10.1371/journal.pgen.1003587· OSTI ID:1627301

Coelho, Marco A. ^[1]; Gonçalves, Carla ^[2]; Sampaio, José Paulo ^[2]; Gonçalves, Paula ^[2]

Universidade Nova de Lisboa, Caparica (Portugal); DOE/OSTI
Universidade Nova de Lisboa, Caparica (Portugal)

Comparative genomics revealed in the last decade a scenario of rampant horizontal gene transfer (HGT) among prokaryotes, but for fungi a clearly dominant pattern of vertical inheritance still stands, punctuated however by an increasing number of exceptions. In the present work, we studied the phylogenetic distribution and pattern of inheritance of a fungal gene encoding a fructose transporter (FSY1) with unique substrate selectivity. 109 FSY1 homologues were identified in two sub-phyla of the Ascomycota, in a survey that included 241 available fungal genomes. At least 10 independent inter-species instances of horizontal gene transfer (HGT) involving FSY1 were identified, supported by strong phylogenetic evidence and synteny analyses. The acquisition of FSY1 through HGT was sometimes suggestive of xenolog gene displacement, but several cases of pseudoparalogy were also uncovered. Moreover, evidence was found for successive HGT events, possibly including those responsible for transmission of the gene among yeast lineages. These occurrences do not seem to be driven by functional diversification of the Fsy1 proteins because Fsy1 homologues from widely distant lineages, including at least one acquired by HGT, appear to have similar biochemical properties. In summary, retracing the evolutionary path of the FSY1 gene brought to light an unparalleled number of independent HGT events involving a single fungal gene. We propose that the turbulent evolutionary history of the gene may be linked to the unique biochemical properties of the encoded transporter, whose predictable effect on fitness may be highly variable. In general, our results support the most recent views suggesting that inter-species HGT may have contributed much more substantially to shape fungal genomes than heretofore assumed.

Research Organization:: Universidade Nova de Lisboa, Caparica (Portugal)

Sponsoring Organization:: Fundação para a Ciência e a Tecnologia

OSTI ID:: 1627301

Journal Information:: PLoS Genetics, Journal Name: PLoS Genetics Journal Issue: 6 Vol. 9; ISSN 1553-7404

Publisher:: Public Library of Science

Country of Publication:: United States

Language:: English

References (94)

You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes Ford Doolittle, W. Trends in Genetics, Vol. 14, Issue 8 https://doi.org/10.1016/S0168-9525(98)01494-2	journal	December 1998
Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes Richards, T. A.; Soanes, D. M.; Jones, M. D. M. Proceedings of the National Academy of Sciences, Vol. 108, Issue 37 https://doi.org/10.1073/pnas.1105100108	journal	August 2011
Friend or foe? Evolutionary history of glycoside hydrolase family 32 genes encoding for sucrolytic activity in fungi and its implications for plant-fungal symbioses Parrent, Jeri; James, Timothy Y.; Vasaitis, Rimvydas BMC Evolutionary Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2148-9-148	journal	January 2009
concatenator: sequence data matrices handling made easy Pina-Martins, F.; Paulo, O. S. Molecular Ecology Resources, Vol. 8, Issue 6 https://doi.org/10.1111/j.1755-0998.2008.02164.x	journal	November 2008
A Likelihood Approach to Estimating Phylogeny from Discrete Morphological Character Data Lewis, Paul O. Systematic Biology, Vol. 50, Issue 6 https://doi.org/10.1080/106351501753462876	journal	November 2001
Characterization of a carbohydrate transporter from symbiotic glomeromycotan fungi Schüßler, Arthur; Martin, Holger; Cohen, David Nature, Vol. 444, Issue 7121 https://doi.org/10.1038/nature05364	journal	December 2006
Genomic Islands in the Pathogenic Filamentous Fungus Aspergillus fumigatus Fedorova, Natalie D.; Khaldi, Nora; Joardar, Vinita S. PLoS Genetics, Vol. 4, Issue 4, Article No. e1000046 https://doi.org/10.1371/journal.pgen.1000046	journal	April 2008
Functional properties and differential mode of regulation of the nitrate transporter from a plant symbiotic ascomycete Montanini, Barbara; Viscomi, Arturo R.; Bolchi, Angelo Biochemical Journal, Vol. 394, Issue 1 https://doi.org/10.1042/BJ20051199	journal	January 2006
Catabolite interconversion of glucose transport systems in the yeast Candida wickerhamii Spencer-Martins, I.; Van Uden, N. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 812, Issue 1 https://doi.org/10.1016/0005-2736(85)90535-8	journal	January 1985
Composition-based statistics and translated nucleotide searches: Improving the TBLASTN module of BLAST Gertz, E. Michael; Yu, Yi-Kuo; Agarwala, Richa BMC Biology, Vol. 4, Issue 1 https://doi.org/10.1186/1741-7007-4-41	journal	December 2006
The Maximum Likelihood Approach to Reconstructing Ancestral Character States of Discrete Characters on Phylogenies Pagel, Mark Systematic Biology, Vol. 48, Issue 3 https://doi.org/10.1080/106351599260184	journal	July 1999
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae Galagan, James E.; Calvo, Sarah E.; Cuomo, Christina Nature, Vol. 438, Issue 7071 https://doi.org/10.1038/nature04341	journal	December 2005
Complex evolution of the DAL5 transporter family Hellborg, Linda; Woolfit, Megan; Arthursson-Hellborg, Mattias BMC Genomics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2164-9-164	journal	January 2008
SplitsTree: analyzing and visualizing evolutionary data Huson, D. H. Bioinformatics, Vol. 14, Issue 1 https://doi.org/10.1093/bioinformatics/14.1.68	journal	February 1998
Functional characterization of the Frt1 sugar transporter and of fructose uptake in Kluyveromyces lactis Diezemann, Anja; Boles, Eckhard Current Genetics, Vol. 43, Issue 4 https://doi.org/10.1007/s00294-003-0392-5	journal	July 2003
Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast Libkind, D.; Hittinger, C. T.; Valerio, E. Proceedings of the National Academy of Sciences, Vol. 108, Issue 35 https://doi.org/10.1073/pnas.1105430108	journal	August 2011
Differential regulation by glucose and fructose of a gene encoding a specific fructose/H+ symporter inSaccharomyces sensu stricto yeasts de Sousa, Helena Rodrigues; Spencer-Martins, Isabel; Gonçalves, Paula Yeast, Vol. 21, Issue 6 https://doi.org/10.1002/yea.1118	journal	April 2004
FSY1, a Novel Gene Encoding a Specific Fructose/H+ Symporter in the Type Strain of Saccharomyces carlsbergensis Goncalves, P.; Rodrigues de Sousa, H.; Spencer-Martins, I. Journal of Bacteriology, Vol. 182, Issue 19 https://doi.org/10.1128/JB.182.19.5628-5630.2000	journal	October 2000
Using native and syntenically mapped cDNA alignments to improve de novo gene finding Stanke, Mario; Diekhans, Mark; Baertsch, Robert Bioinformatics, Vol. 24, Issue 5 https://doi.org/10.1093/bioinformatics/btn013	journal	January 2008
Horizontal Transfer of a Large and Highly Toxic Secondary Metabolic Gene Cluster between Fungi Slot, Jason C.; Rokas, Antonis Current Biology, Vol. 21, Issue 2 https://doi.org/10.1016/j.cub.2010.12.020	journal	January 2011
Multiple Horizontal Gene Transfers of Ammonium Transporters/Ammonia Permeases from Prokaryotes to Eukaryotes: Toward a New Functional and Evolutionary Classification McDonald, T. R.; Dietrich, F. S.; Lutzoni, F. Molecular Biology and Evolution, Vol. 29, Issue 1 https://doi.org/10.1093/molbev/msr123	journal	June 2011
Incidence of SUC-RTM telomeric repeated genes in brewing and wild wine strains of Saccharomyces Denayrolles, Muriel; de Villechenon, Edouard Pinot; Lonvaud-Funel, Aline Current Genetics, Vol. 31, Issue 6 https://doi.org/10.1007/s002940050230	journal	July 1997
FSY1, a horizontally transferred gene in the Saccharomyces cerevisiae EC1118 wine yeast strain, encodes a high-affinity fructose/H+ symporter Galeote, V.; Novo, M.; Salema-Oom, M. Microbiology, Vol. 156, Issue 12 https://doi.org/10.1099/mic.0.041673-0	journal	August 2010
Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium Ma, Li-Jun; van der Does, H. Charlotte; Borkovich, Katherine A. Nature, Vol. 464, Issue 7287 https://doi.org/10.1038/nature08850	journal	March 2010
Hexose Transporters of a Hemibiotrophic Plant Pathogen Lingner, Ulrike; Münch, Steffen; Deising, Holger B. Journal of Biological Chemistry, Vol. 286, Issue 23 https://doi.org/10.1074/jbc.M110.213678	journal	June 2011
Sugar transporters in plants and in their interactions with fungi Doidy, Joan; Grace, Emily; Kühn, Christina Trends in Plant Science, Vol. 17, Issue 7 https://doi.org/10.1016/j.tplants.2012.03.009	journal	July 2012
Population genetics of filamentous fungi Hoekstra, Rolf F. Antonie van Leeuwenhoek, Vol. 65, Issue 3 https://doi.org/10.1007/BF00871947	journal	January 1994
Horizontal gene transfer in eukaryotic evolution Keeling, Patrick J.; Palmer, Jeffrey D. Nature Reviews Genetics, Vol. 9, Issue 8 https://doi.org/10.1038/nrg2386	journal	August 2008
Structure of Kluyveromyces lactis subtelomeres: duplications and gene content Fairhead, CÃ©cile; Dujon, Bernard FEMS Yeast Research, Vol. 6, Issue 3 https://doi.org/10.1111/j.1567-1364.2006.00033.x	journal	May 2006
Application of Phylogenetic Networks in Evolutionary Studies Huson, Daniel H.; Bryant, David Molecular Biology and Evolution, Vol. 23, Issue 2 https://doi.org/10.1093/molbev/msj030	journal	October 2005
The Yeast Gene Order Browser: Combining curated homology and syntenic context reveals gene fate in polyploid species Byrne, K. P. Genome Research, Vol. 15, Issue 10 https://doi.org/10.1101/gr.3672305	journal	September 2005
Genome-scale comparative analysis of gene fusions, gene fissions, and the fungal tree of life Leonard, G.; Richards, T. A. Proceedings of the National Academy of Sciences, Vol. 109, Issue 52 https://doi.org/10.1073/pnas.1210909110	journal	December 2012
Functional Characterization of fst1 in Fusarium verticillioides During Colonization of Maize Kernels Kim, Hun; Woloshuk, Charles P. Molecular Plant-Microbe Interactions®, Vol. 24, Issue 1 https://doi.org/10.1094/MPMI-03-10-0074	journal	January 2011
Neighbor-Net: An Agglomerative Method for the Construction of Phylogenetic Networks Bryant, D. Molecular Biology and Evolution, Vol. 21, Issue 2 https://doi.org/10.1093/molbev/msh018	journal	August 2003
Discussion of Teleomorphic and Anamorphic Ascomycetous Yeasts and Yeast-like Taxa Kurtzman, Cletus P. The Yeasts https://doi.org/10.1016/B978-0-444-52149-1.00013-6	book	January 2011
Finding Functional Features in Saccharomyces Genomes by Phylogenetic Footprinting Cliften, P. Science, Vol. 301, Issue 5629 https://doi.org/10.1126/science.1084337	journal	July 2003
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models Stamatakis, Alexandros Bioinformatics, Vol. 22, Issue 21 https://doi.org/10.1093/bioinformatics/btl446	journal	August 2006
Horizontal Gene Transfer and the Evolution of Secondary Metabolite Gene Clusters in Fungi: An Hypothesis Walton, Jonathan D. Fungal Genetics and Biology, Vol. 30, Issue 3, p. 167-171 https://doi.org/10.1006/fgbi.2000.1224	journal	August 2000
Genetic and Epigenetic Regulation of the FLO Gene Family Generates Cell-Surface Variation in Yeast Halme, Adrian; Bumgarner, Stacie; Styles, Cora Cell, Vol. 116, Issue 3 https://doi.org/10.1016/S0092-8674(04)00118-7	journal	February 2004
Horizontal Gene Transfer Between Microbial Eukaryotes Andersson, Jan O. Horizontal Gene Transfer https://doi.org/10.1007/978-1-60327-853-9_27	book	January 2009
Hexose and pentose transport in ascomycetous yeasts: an overview Leandro, Maria José; Fonseca, César; Gonçalves, Paula FEMS Yeast Research, Vol. 9, Issue 4, p. 511-525 https://doi.org/10.1111/j.1567-1364.2009.00509.x	journal	June 2009
Concurrent knock-out of at least 20 transporter genes is required to block uptake of hexoses in Saccharomyces cerevisiae Wieczorke, Roman; Krampe, Stefanie; Weierstall, Thomas FEBS Letters, Vol. 464, Issue 3 https://doi.org/10.1016/S0014-5793(99)01698-1	journal	December 1999
Contribution of Horizontal Gene Transfer to the Evolution of Saccharomyces cerevisiae Hall, Charles; Brachat, Sophie; Dietrich, Fred S. Eukaryotic Cell, Vol. 4, Issue 6 https://doi.org/10.1128/EC.4.6.1102-1115.2005	journal	June 2005
The Aspergillus Genome Database, a curated comparative genomics resource for gene, protein and sequence information for the Aspergillus research community Arnaud, Martha B.; Chibucos, Marcus C.; Costanzo, Maria C. Nucleic Acids Research, Vol. 38, Issue suppl_1 https://doi.org/10.1093/nar/gkp751	journal	September 2009
Regulation of Sugar Transport Systems in Fusarium oxysporum var. lini Brandão, Rogélio L.; Loureiro-Dias, Maria C. Applied and Environmental Microbiology, Vol. 56, Issue 8 https://doi.org/10.1128/AEM.56.8.2417-2420.1990	journal	January 1990
Acquisition of prokaryotic genes by fungal genomes Marcet-Houben, Marina; Gabaldón, Toni Trends in Genetics, Vol. 26, Issue 1 https://doi.org/10.1016/j.tig.2009.11.007	journal	January 2010
The Transporter Classification Database: recent advances Saier, M. H.; Yen, M. R.; Noto, K. Nucleic Acids Research, Vol. 37, Issue Database https://doi.org/10.1093/nar/gkn862	journal	January 2009
Insertion of Horizontally Transferred Genes within Conserved Syntenic Regions of Yeast Genomes Rolland, Thomas; Neuvéglise, Cécile; Sacerdot, Christine PLoS ONE, Vol. 4, Issue 8 https://doi.org/10.1371/journal.pone.0006515	journal	August 2009
Microevolution of Cryptococcus neoformans Driven by Massive Tandem Gene Amplification Chow, E. W. L.; Morrow, C. A.; Djordjevic, J. T. Molecular Biology and Evolution, Vol. 29, Issue 8 https://doi.org/10.1093/molbev/mss066	journal	February 2012
Gene transfer into the fungi Richards, Thomas A.; Leonard, Guy; Soanes, Darren M. Fungal Biology Reviews, Vol. 25, Issue 2 https://doi.org/10.1016/j.fbr.2011.04.003	journal	July 2011
Fsy1, the sole hexose-proton transporter characterized in Saccharomyces yeasts, exhibits a variable fructose:H+ stoichiometry Anjos, Jorge; Rodrigues de Sousa, Helena; Roca, Christophe Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1828, Issue 2 https://doi.org/10.1016/j.bbamem.2012.08.011	journal	February 2013
Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae Kellis, Manolis; Birren, Bruce W.; Lander, Eric S. Nature, Vol. 428, Issue 6983 https://doi.org/10.1038/nature02424	journal	March 2004
Orthologs, Paralogs, and Evolutionary Genomics Koonin, Eugene V. Annual Review of Genetics, Vol. 39, Issue 1 https://doi.org/10.1146/annurev.genet.39.073003.114725	journal	December 2005
Emergence of a new disease as a result of interspecific virulence gene transfer Friesen, Timothy L.; Stukenbrock, Eva H.; Liu, Zhaohui Nature Genetics, Vol. 38, Issue 8 https://doi.org/10.1038/ng1839	journal	July 2006
Multiple GAL pathway gene clusters evolved independently and by different mechanisms in fungi Slot, J. C.; Rokas, A. Proceedings of the National Academy of Sciences, Vol. 107, Issue 22 https://doi.org/10.1073/pnas.0914418107	journal	May 2010
Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis Castresana, J. Molecular Biology and Evolution, Vol. 17, Issue 4 https://doi.org/10.1093/oxfordjournals.molbev.a026334	journal	April 2000
Horizontal Transfer of a Nitrate Assimilation Gene Cluster and Ecological Transitions in Fungi: A Phylogenetic Study Slot, Jason C.; Hibbett, David S. PLoS ONE, Vol. 2, Issue 10 https://doi.org/10.1371/journal.pone.0001097	journal	October 2007
High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method Gietz, R. Daniel; Schiestl, Robert H. Nature Protocols, Vol. 2, Issue 1 https://doi.org/10.1038/nprot.2007.13	journal	January 2007
Phylogenetic analyses do not support horizontal gene transfers from bacteria to vertebrates Stanhope, Michael J.; Lupas, Andrei; Italia, Michael J. Nature, Vol. 411, Issue 6840 https://doi.org/10.1038/35082058	journal	June 2001
The Puzzle of Plastid Evolution Archibald, John M. Current Biology, Vol. 19, Issue 2 https://doi.org/10.1016/j.cub.2008.11.067	journal	January 2009
Evolutionary Implications of Horizontal Gene Transfer Syvanen, Michael Annual Review of Genetics, Vol. 46, Issue 1 https://doi.org/10.1146/annurev-genet-110711-155529	journal	December 2012
Horizontal Gene Transfer in Prokaryotes: Quantification and Classification Koonin, Eugene V.; Makarova, Kira S.; Aravind, L. Annual Review of Microbiology, Vol. 55, Issue 1 https://doi.org/10.1146/annurev.micro.55.1.709	journal	October 2001
Comparative genomic analyses of the human fungal pathogens Coccidioides and their relatives Sharpton, T. J.; Stajich, J. E.; Rounsley, S. D. Genome Research, Vol. 19, Issue 10 https://doi.org/10.1101/gr.087551.108	journal	August 2009
Evolution of pathogenicity and sexual reproduction in eight Candida genomes Butler, Geraldine; Rasmussen, Matthew D.; Lin, Michael F. Nature, Vol. 459, Issue 7247 https://doi.org/10.1038/nature08064	journal	May 2009
A fungal phylogeny based on 82 complete genomes using the composition vector method Wang, Hao; Xu, Zhao; Gao, Lei BMC Evolutionary Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2148-9-195	journal	January 2009
Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi Khaldi, Nora; Collemare, Jérôme; Lebrun, Marc-Henri Genome Biology, Vol. 9, Issue 1 https://doi.org/10.1186/gb-2008-9-1-r18	journal	January 2008
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
Rapid Expansion and Functional Divergence of Subtelomeric Gene Families in Yeasts Brown, Chris A.; Murray, Andrew W.; Verstrepen, Kevin J. Current Biology, Vol. 20, Issue 10 https://doi.org/10.1016/j.cub.2010.04.027	journal	May 2010
Comparative Genomic Analysis of Human Fungal Pathogens Causing Paracoccidioidomycosis Desjardins, Christopher A.; Champion, Mia D.; Holder, Jason W. PLoS Genetics, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pgen.1002345	journal	October 2011
Molecular and functional characterization of a fructose specific transporter from the gray mold fungus Botrytis cinerea Doehlemann, Gunther; Molitor, Frederic; Hahn, Matthias Fungal Genetics and Biology, Vol. 42, Issue 7 https://doi.org/10.1016/j.fgb.2005.03.001	journal	July 2005
Multiple Comparisons of Log-Likelihoods with Applications to Phylogenetic Inference Shimodaira, H.; Hasegawa, M. Molecular Biology and Evolution, Vol. 16, Issue 8 https://doi.org/10.1093/oxfordjournals.molbev.a026201	journal	August 1999
Engineering of Saccharomyces cerevisiae for anthranilate and methyl anthranilate production Kuivanen, Joosu; Kannisto, Matti; Mojzita, Dominik Microbial Cell Factories, Vol. 20, Issue 1 https://doi.org/10.1186/s12934-021-01532-3	journal	February 2021
Ethanol tolerance of sugar transport, and the rectification of stuck wine fermentations Santos, Júlia; Sousa, Maria João; Cardoso, Helena Microbiology, Vol. 154, Issue 2 https://doi.org/10.1099/mic.0.2007/011445-0	journal	February 2008
Transport of fructose by a proton symport in a brewing yeast Cason, David T.; Spencer-Martins, I.; Uden, N. FEMS Microbiology Letters, Vol. 36, Issue 2-3 https://doi.org/10.1111/j.1574-6968.1986.tb01715.x	journal	September 1986
Role of Horizontal Gene Transfer in the Evolution of Fungi Rosewich, U. Liane; Kistler, H. Corby Annual Review of Phytopathology, Vol. 38, Issue 1 https://doi.org/10.1146/annurev.phyto.38.1.325	journal	September 2000
The Reacquisition of Biotin Prototrophy in Saccharomyces cerevisiae Involved Horizontal Gene Transfer, Gene Duplication and Gene Clustering Hall, Charles; Dietrich, Fred S. Genetics, Vol. 177, Issue 4 https://doi.org/10.1534/genetics.107.074963	journal	December 2007
Evolutionary Origins of the Fumonisin Secondary Metabolite Gene Cluster in Fusarium verticillioides and Aspergillus niger Khaldi, Nora; Wolfe, Kenneth H. International Journal of Evolutionary Biology, Vol. 2011 https://doi.org/10.4061/2011/423821	journal	January 2011
Analysis of gene evolution and metabolic pathways using the Candida Gene Order Browser Fitzpatrick, David A.; O'Gaora, Peadar; Byrne, Kevin P. BMC Genomics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2164-11-290	journal	January 2010
Reconstructing the early evolution of Fungi using a six-gene phylogeny James, Timothy Y.; Kauff, Frank; Schoch, Conrad L. Nature, Vol. 443, Issue 7113 https://doi.org/10.1038/nature05110	journal	October 2006
Evidence for Divergent Evolution of Growth Temperature Preference in Sympatric Saccharomyces Species Gonçalves, Paula; Valério, Elisabete; Correia, Cláudia PLoS ONE, Vol. 6, Issue 6 https://doi.org/10.1371/journal.pone.0020739	journal	June 2011
Horizontal gene transfer in fungi Fitzpatrick, David A. FEMS Microbiology Letters, Vol. 329, Issue 1 https://doi.org/10.1111/j.1574-6968.2011.02465.x	journal	December 2011
The ASP3 locus in Saccharomyces cerevisiae originated by horizontal gene transfer from Wickerhamomyces League, Garrett P.; Slot, Jason C.; Rokas, Antonis FEMS Yeast Research, Vol. 12, Issue 7 https://doi.org/10.1111/j.1567-1364.2012.00828.x	journal	July 2012
Evidence of recent interkingdom horizontal gene transfer between bacteria and Candida parapsilosis Fitzpatrick, David A.; Logue, Mary E.; Butler, Geraldine BMC Evolutionary Biology, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2148-8-181	journal	January 2008
The Tree and Net Components of Prokaryote Evolution Puigbò, Pere; Wolf, Yuri I.; Koonin, Eugene V. Genome Biology and Evolution, Vol. 2 https://doi.org/10.1093/gbe/evq062	journal	January 2010
Movements of protons coupled to glucose transport in yeasts. A comparative study among 248 yeast strains Loureiro-Dias, Maria C. Antonie van Leeuwenhoek, Vol. 54, Issue 4 https://doi.org/10.1007/BF00393524	journal	January 1988
Pichia sorbitophila , an Interspecies Yeast Hybrid, Reveals Early Steps of Genome Resolution After Polyploidization Louis, Véronique Leh; Despons, Laurence; Friedrich, Anne G3: Genes\|Genomes\|Genetics, Vol. 2, Issue 2 https://doi.org/10.1534/g3.111.000745	journal	February 2012
Additions, Losses, and Rearrangements on the Evolutionary Route from a Reconstructed Ancestor to the Modern Saccharomyces cerevisiae Genome Gordon, Jonathan L.; Byrne, Kevin P.; Wolfe, Kenneth H. PLoS Genetics, Vol. 5, Issue 5 https://doi.org/10.1371/journal.pgen.1000485	journal	May 2009
The genetic code of the fungal CTG clade Santos, Manuel A. S.; Gomes, Ana C.; Santos, Maria C. Comptes Rendus Biologies, Vol. 334, Issue 8-9 https://doi.org/10.1016/j.crvi.2011.05.008	journal	August 2011
Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118 Novo, M.; Bigey, F.; Beyne, E. Proceedings of the National Academy of Sciences, Vol. 106, Issue 38 https://doi.org/10.1073/pnas.0904673106	journal	September 2009
Sequencing and comparison of yeast species to identify genes and regulatory elements Kellis, Manolis; Patterson, Nick; Endrizzi, Matthew Nature, Vol. 423, Issue 6937 https://doi.org/10.1038/nature01644	journal	May 2003
Expansion of Hexose Transporter Genes Was Associated with the Evolution of Aerobic Fermentation in Yeasts Lin, Z.; Li, W. -H. Molecular Biology and Evolution, Vol. 28, Issue 1 https://doi.org/10.1093/molbev/msq184	journal	July 2010
Non-universal Usage of the Leucine CUG Codon and the Molecular Phylogeny of the Genus Candida Sugita, Takashi; Nakase, Takashi Systematic and Applied Microbiology, Vol. 22, Issue 1 https://doi.org/10.1016/S0723-2020(99)80030-7	journal	February 1999
Altered patterns of gene duplication and differential gene gain and loss in fungal pathogens Powell, Amy J.; Conant, Gavin C.; Brown, Douglas E. BMC Genomics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2164-9-147	journal	January 2008

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