Taxonomically restricted genes are known to contribute to the evolution of new traits. In Craterostigma plantagineum two of such genes are modulated during dehydration and rehydration and seem to contribute to a successful recovery after desiccation. The resurrection plant Craterostigma plantagineum can tolerate extreme water loss. Protective molecules linked to desiccation tolerance were identified in C. plantagineum but underlying mechanisms are far from being completely understood. A transcriptome analysis revealed several genes which could not be annotated and are, therefore, interesting candidates for understanding desiccation tolerance. Genes which occur only in some species are defined as orphan or taxonomically restricted genes (TRGs) and may be important for the evolution of new traits. Several of these TRGs are modulated in expression during dehydration/rehydration in C. plantagineum. Here we report the characterisation of two of these TRGs encoding a cysteine-rich rehydration-responsive protein 1 (CpCRP1) and an early dehydration-responsive protein 1 (CpEDR1). The involvement of CpCRP1 and CpEDR1 in different phases of the dehydration/rehydration cycle is shown by transcript and protein expression analysis. In silico sequence analyses predicted that both genes are likely to interact with other cellular components and are localised in two different cellular compartments. GFP fusion proteins demonstrated that CpCRP1 is secreted into the apoplasm, whereas CpEDR1 is imported into chloroplasts. Putative homologs of CpCRP1 and CpEDR1 were identified in Lindernia brevidens and Lindernia subracemosa which belong to the same family as C. plantagineum thus suggesting a recent evolution of the genes in this family. According to expression profiles, CpCRP1 may play a role in normal conditions and during rehydration, whereas CpEDR1 may be required for the acquisition of desiccation tolerance and protect photosynthetic structures during dehydration and rehydration.