Characterization of a New Multigene Family Encoding Isomaltases in the Yeast Saccharomyces cerevisiae, the IMA Family

Abstract

It has been known for a long time that the yeast Saccharomyces cerevisiae can assimilate ␣-methylglucopyranoside and isomaltose. We here report the identification of 5 genes (YGR287c, YIL172c, YJL216c, YJL221c and YOL157c), which, similar to the SUCx, MALx, or HXTx multigene families, are located in the subtelomeric regions of different chromosomes. They share high nucleotide sequence identities between themselves (66 -100%) and with the MALx2 genes (63-74%). Comparison of their amino acid sequences underlined a substitution of threonine by valine in region II, one of the four highly conserved regions of the ␣-glucosidase family. This change was previously shown to be sufficient to discriminate ␣-1,4-to ␣-1,6-glucosidase activity in YGR287c (Yamamoto, K., Nakayama, A., Yamamoto, Y., and Tabata, S. (2004) Eur. J. Biochem. 271, 3414 -3420). We showed that each of these five genes encodes a protein with ␣-glucosidase activity on isomaltose, and we therefore renamed these genes IMA1 to IMA5 for IsoMAltase. Our results also illustrated that sequence polymorphisms among this family led to interesting variability of gene expression patterns and of catalytic efficiencies on different substrates, which altogether should account for the absence of functional redundancy for growth on isomaltose. Indeed, deletion studies revealed that IMA1/YGR287c encodes the major isomaltase and that growth on isomaltose required the presence of AGT1, which encodes an ␣-glucoside transporter. Expressions of IMA1 and IMA5/ YJL216c were strongly induced by maltose, isomaltose, and ␣-methylglucopyranoside, in accordance with their regulation by the Malx3p-transcription system. The physiological relevance of this IMAx multigene family in S. cerevisiae is discussed.Gene duplication, one of the main driving forces in genome evolution, generates paralogous genes that can acquire specificities by sequence divergence. These redundant genes are defined as multigene families, the most often located within subtelomere sequences. Very recently, Brown and coworkers demonstrated that the extraordinary instability of these regions supports rapid adaptation to novel niches.

Elimination of sucrose transport and hydrolysis in Saccharomyces cerevisiae: a platform strain for engineering sucrose metabolism

“…This confirmation does not exclude the possibility that the data of Pougach et al. (2014) are correct, since they used a different S. cerevisiae strain (KV5000, which originates from BY4741, an S288c-derived strain) whilst Teste, François and Parrou (2010) used the CEN.PK113-7D strain.…”

Reconstruction of Ancestral Metabolic Enzymes Reveals Molecular Mechanisms Underlying Evolutionary Innovation through Gene Duplication

“…The MALS genes encode α-glucosidases that allow yeast to metabolize complex carbohydrates like maltose, isomaltose, and other α-glucosides [32],[33]. Several key features make this family ideal to study duplicate gene evolution.…”

Molecular genetic differentiation of yeast α-glucosidases: Maltase and isomaltase

“…It was found that for expression of the IMA genes, the presence of the AGT1 gene responsible for isomaltose and α methylglucoside transport into the cell was required [39]. Growth on isomaltose may depend on the maltose activator gene MAL23p [38]. The expression of IMA1 and IMA5 genes is induced by maltose, isomaltose, and α methylglucoside.…”

“…The function of the IMA genes was studied thor oughly by Teste et al [38]. The cloning and expression of the IMA genes on the yeast plasmid made it possible to determine the activity of the corresponding enzymes on different substrates: p nitrophenyl α D glucopyranoside, maltose, maltotriose, α methylglu coside, and isomaltose.…”

“…The nomenclature of the IMA1-IMA4 genes is adopted in the International Saccharomyces Genome Database [36]. After our article [28] was submitted for publica tion in 2009, two more papers [37,38], in which the IMA genes were revealed, were submitted in 2010. In the study [37], the IMA genes were treated as divergent MAL genes, whereas in [38], our nomenclature of IMA1-IMA4 genes was used, with our fifth IMA?…”