Evolutionary Biology meeting edition:11 location:Marseille, France date:19-21 September 2007
Invited oral presentation
Trehalose is a non-reducing disaccharide consisting of two glucose molecules linked by 1α–1α. It is present in very different organisms such as bacteria, fungi, nematodes, insects and plants. Several functions have been described for trehalose in nature, such as compatible solute, storage compound and structural part of cell walls. Trehalose has at least five biosynthesis pathways mostly present in eubacteria where some species has up to four pathways. The most widely distributed and best characterized consists of two steps mediated by trehalose 6-phosphate synthase (TPS) and trehalose 6-phosphate phosphatase (TPP) enzymes, were the first is catalyzing the synthesis of trehalose 6-phosphate (T6P) and TPP dephosphorylates T6P to form trehalose and Pi. The TPS and TPP domains had evolved parallel in bacteria, where they are normally found forming operon structures. The plant TPS and TPP genes form multigene families where members are divided in class I, II and III. Class I and II consist of fused TPS and TPP domains, class III consists of a single TPP domain. In Arabidopsis, T6P synthase activity has been detected only in AtTPS1, one of four class I members whereas class III proteins have TPP activity. No TPS or TPP activity has been detected in most class I, and all class II proteins. They seem to fulfill a regulatory role as they are expressed in a tissue-specific and developmental way. In addition, there is a clear interaction between trehalose metabolism and sugar allocation as well as with the ABA response but many questions about their action mechanisms still need further investigation. Here we show the genetic and phylogenetic characterization of a novel TPS-TPP fused bacterial gene, likely member of the ancestor group of eukaryan class I and II genes. The genetic and enzymatic analysis shows that this protein conserves both TPS and TPP activities, being able to complement a yeast tps1∆ tps2∆ mutant and to synthesize trehalose. The phylogenetic analysis shows that the TPS-TPP bacterial gene is situated between prokaryotic and eukaryotic TPS and TPP sequences, supporting the hypothesis of the eukaryotic ancestor sequence. All together these data suggest that fusion of TPS and TPP domains occurred in bacteria before the first plant organisms were evolved. This ancestral protein probably conserved both TPS and TPP activities but during plant evolution one or both of them were lost. Is likely that TPS and TPP multigene families were generated in parallel to plant complexity development, generating new roles for TPS proteins. This is supported by the fact that trehalose synthesis and accumulation is almost undetectable in most plants.