Tracking alternative versions of the galactose gene network in the genus Saccharomyces and their expansion after domestication
Ana Pontes,
Francisca Paraíso,
Yu-Ching Liu,
Savitree Limtong,
Sasitorn Jindamorakot,
Lene Jespersen,
Carla Gonçalves,
Carlos A. Rosa,
Isheng Jason Tsai,
Antonis Rokas,
Chris Todd Hittinger,
Paula Gonçalves,
José Paulo Sampaio
Affiliations
Ana Pontes
UCIBIO, Department of Life Sciences, Nova School of Science and Technology, Caparica 2829-516, Portugal; Associate Laboratory i4HB, Nova School of Science and Technology, Caparica 2829-516, Portugal; Corresponding author
Francisca Paraíso
UCIBIO, Department of Life Sciences, Nova School of Science and Technology, Caparica 2829-516, Portugal; Associate Laboratory i4HB, Nova School of Science and Technology, Caparica 2829-516, Portugal
Yu-Ching Liu
Biodiversity Research Center, Academia Sinica, Taipei 11529, Taiwan
Savitree Limtong
Department of Microbiology Faculty of Science, Kasetsart University, Bangkok 10900, Thailand; Biodiversity Center Kasetsart University, Bangkok 10900, Thailand
Sasitorn Jindamorakot
Microbial Diversity and Utilization Research Team, Thailand Bioresource Research Center, National Centre for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology, Development Agency (NSTDA), Pathum Thani 12120, Thailand
Lene Jespersen
Department of Food Science, University of Copenhagen, 1958 Frederiksberg C, Denmark
Carla Gonçalves
UCIBIO, Department of Life Sciences, Nova School of Science and Technology, Caparica 2829-516, Portugal; Associate Laboratory i4HB, Nova School of Science and Technology, Caparica 2829-516, Portugal
Carlos A. Rosa
Departamento de Microbiologia, ICB, C.P. 486, Universidade Federal de Minas Gerais, Belo Horizonte, MG 31270-901, Brazil
Isheng Jason Tsai
Biodiversity Research Center, Academia Sinica, Taipei 11529, Taiwan
Antonis Rokas
Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA; Evolutionary Studies Initiative, Vanderbilt University, Nashville, TN 37235, USA
Chris Todd Hittinger
Laboratory of Genetics, DOE Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, Center for Genomic Science Innovation, J.F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, WI 53726, USA
Paula Gonçalves
UCIBIO, Department of Life Sciences, Nova School of Science and Technology, Caparica 2829-516, Portugal; Associate Laboratory i4HB, Nova School of Science and Technology, Caparica 2829-516, Portugal; Corresponding author
José Paulo Sampaio
UCIBIO, Department of Life Sciences, Nova School of Science and Technology, Caparica 2829-516, Portugal; Associate Laboratory i4HB, Nova School of Science and Technology, Caparica 2829-516, Portugal; Corresponding author
Summary: When Saccharomyces cerevisiae grows on mixtures of glucose and galactose, galactose utilization is repressed by glucose, and induction of the GAL gene network only occurs when glucose is exhausted. Contrary to reference GAL alleles, alternative alleles support faster growth on galactose, thus enabling distinct galactose utilization strategies maintained by balancing selection. Here, we report on new wild populations of Saccharomyces cerevisiae harboring alternative GAL versions and, for the first time, of Saccharomyces paradoxus alternative alleles. We also show that the non-functional GAL version found earlier in Saccharomyces kudriavzevii is phylogenetically related to the alternative versions, which constitutes a case of trans-specific maintenance of highly divergent alleles. Strains harboring the different GAL network variants show different levels of alleviation of glucose repression and growth proficiency on galactose. We propose that domestication involved specialization toward thriving in milk from a generalist ancestor partially adapted to galactose consumption in the plant niche.
