Evolutionary diversification of type-2 HDAC structure, function and regulation in Nicotiana tabacum

•We analyzed HD2 phylogeny in Solanaceaes and identified a unique deletion of the zinc finger sequence generating Group 2 HD2s from a Group 1 precursor.•We showed in tobacco that polyploïdization led to an increase of Group 2 HD2 expression at the expense of Gr1 HD2s, suggesting that the deletion of the zinc finger sequence confers new functions to Gr2 HD2s.•A functional complementation approach with an Arabidopsis Gr1 HD2 mutant together with a side-directed mutagenesis approach allowed us to prove the functional relevance of the zing finger in Gr1 HD2s in response to salt stress. Type-2 HDACs (HD2s) are plant-specific histone deacetylases that play diverse roles during development and in responses to biotic and abiotic stresses. In this study we characterized the six tobacco genes encoding HD2s that mainly differ by the presence or the absence of a typical zinc finger in their C-terminal part. Of particular interest, these HD2 genes exhibit a highly conserved intron/exon structure. We then further investigated the phylogenetic relationships among the HD2 gene family, and proposed a model of the genetic events that led to the organization of the HD2 family in Solanaceae. Absolute quantification of HD2 mRNAs in N. tabacum and in its precursors, N. tomentosiformis and N. sylvestris, did not reveal any pseudogenization of any of the HD2 genes, but rather specific regulation of HD2 expression in these three species. Functional complementation approaches in Arabidopsis thaliana demonstrated that the four zinc finger-containing HD2 proteins exhibit the same biological function in response to salt stress, whereas the two HD2 proteins without zinc finger have different biological function.