Phylogenetic and specificity studies of two-domain GNA-related lectins: generation of multispecificity through domain duplication and divergent evolution

Els Jm van Damme (1) , Sachiko Nakamura-Tsurata , David F Smith , Maté Ongenaert , Harry C Winter , Pierre Rougé , Irwin J Goldstein , Hanqing Mo , Junko Kominami , Raphael Culerrier , Annick Barre , Jun Hirabayashi , Willy J Peumans

1 Molecular Biotechnology

A reinvestigation of the occurrence and taxonomic distribution revealed that proteins built up of protomers consisting of two in tandem arrayed domains equivalent to the Galanthus nivalis agglutinin (GNA) are widespread among monotyledonous plants. Phylogenetic analysis of the available sequences indicated that these proteins do not represent a monophylogenetic group but most probably result from multiple independent domain duplication/in tandem insertion events. To corroborate the relationship between inter-domain sequence divergence and widening of specificity range a detailed comparative analysis was made of the sequences and specificity of a set of two-domain GNA-related lectins. Glycan microarray analyses, frontal affinity chromatography and surface plasmon resonance measurements demonstrated that the two-domain GNA-related lectins acquired a marked diversity in carbohydrate-binding specificity that strikingly contrasts the canonical exclusive specificity of their single domain counterparts towards mannose. Moreover, it appears that most two-domain GNA-related lectins interact with both high mannose and complex N-glycans and that this dual specificity relies on the simultaneous presence of at least two different independently acting binding sites. The combined phylogenetic, specificity and structural data strongly suggest that plants used domain duplication followed by divergent evolution as a mechanism to generate multispecific plant lectins from a single mannose-binding domain. Taking into account that the shift in specificity of some binding sites from high mannose to complex type N-glycans implies that the two-domain GNA-related lectins are primarily directed against typical animal glycans, it is tempting to speculate that plants developed two-domain GNA-related lectins for defense purposes.

Mots clés: Life Sciences

Els Jm van Damme, Sachiko Nakamura-Tsurata, David F Smith, Maté Ongenaert, Harry C Winter, et al.. Phylogenetic and specificity studies of two-domain GNA-related lectins: generation of multispecificity through domain duplication and divergent evolution. Biochemical Journal, 2007, 404 (1), pp.51-61. ⟨10.1042/BJ20061819⟩. ⟨hal-00478712⟩