Insights on the evolution of trehalose biosynthesis

Abstract

Background: The compatible solute trehalose is a non-reducing disaccharide, which accumulates upon heat, cold or osmotic stress. It was commonly accepted that trehalose is only present in extremophiles or cryptobiotic organisms. However, in recent years it has been shown that although higher plants do not accumulate trehalose at significant levels they have actively transcribed genes encoding the corresponding biosynthetic enzymes.

Results: In this study we show that trehalose biosynthesis ability is present in eubacteria, archaea, plants, fungi and animals. In bacteria there are five different biosynthetic routes, whereas in fungi, plants and animals there is only one. We present phylogenetic analyses of the trehalose-6-phosphate synthase (TPS) and trehalose-phosphatase (TPP) domains and show that there is a close evolutionary relationship between these domains in proteins from diverse organisms. In bacteria TPS and TPP genes are clustered, whereas in eukaryotes these domains are fused in a single protein.

Conclusion: We have demonstrated that trehalose biosynthesis pathways are widely distributed in nature. Interestingly, several eubacterial species have multiple pathways, while eukaryotes have only the TPS/TPP pathway. Vertebrates lack trehalose biosynthetic capacity but can catabolise it. TPS and TPP domains have evolved mainly in parallel and it is likely that they have experienced several instances of gene duplication and lateral gene transfer.

Figure 1

The trehalose biosynthetic pathways. The enzymes are indicated in blue.

Figure 2

The distribution of trehalose biosynthetic proteins in nature. (A) The phyla with al least one synthesis pathway. (B) Comparative analysis between the percentage of completely sequenced genomes with at least one biosynthetic pathway.

Figure 3

The phylogeny of the TPS domain. The tree was generated with the PHYML maximum likelihood software [69]. The proteins are shown in colours according to their taxonomic group. The subdivisions of bacteria are: *Actinobacteria, **Cyanobacteria, ^α alpha-proteobacteria, ^β beta-proteobacteria, ^γ gamma-proteobacteria, ^δ delta-proteobacteria. The archaeal groups are: °Crenarchaeota, °°Euryarchaeota. The Bootstrap values (1000×) are shown in percentage.

Figure 4

The phylogeny of the TPP domain. The tree was generated with the PHYML maximum likelihood software [69]. The proteins and taxonomic subdivisions are shown as in Fig. 3. The Bootstrap values (1000×) are shown in percentage.

Figure 5

Expression levels of Arabidopsis TPS multigene family. The figure shows the transcripts level detected in microarrays experiments. (A) Detection along the Arabidopsis life cycle. (B) Organ-specific expression [1 Callus; 2. Cell suspension; 3. Seedlings; 4. Cotyledons; 5. Hypocotyl; 6. Radicle; 7. Inflorescence; 8. Flower; 9. Carpel; 10. Petal; 11. Sepal; 12. Stamen; 13. Pedicel; 14. Silique; 15. Seed; 16. Embryo; 17. Stem; 18. Node; 19. Shoot apex; 20. Cauline leaf; 21. Rosette; 22. Juvenile leaf; 23. Adult leaf, 24. Petiole; 25. Senescent leaf; 26. Roots; 27. Lateral leaf; 28. Elongation zone]. The intensity of the blue colour indicates the level of expression as percentage for each gene, as displayed in the Genevestigator server [61].