Comparative transcriptome analysis suggests convergent evolution of desiccation tolerance in Selaginella species

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RESEARCH ARTICLE

Open Access

Comparative transcriptome analysis suggests convergent evolution of desiccation tolerance in Selaginella species Gerardo Alejo-Jacuinde1,2, Sandra Isabel González-Morales3, Araceli Oropeza-Aburto1, June Simpson2 and Luis Herrera-Estrella1,4*

Abstract Background: Desiccation tolerant Selaginella species evolved to survive extreme environmental conditions. Studies to determine the mechanisms involved in the acquisition of desiccation tolerance (DT) have focused on only a few Selaginella species. Due to the large diversity in morphology and the wide range of responses to desiccation within the genus, the understanding of the molecular basis of DT in Selaginella species is still limited. Results: Here we present a reference transcriptome for the desiccation tolerant species S. sellowii and the desiccation sensitive species S. denticulata. The analysis also included transcriptome data for the well-studied S. lepidophylla (desiccation tolerant), in order to identify DT mechanisms that are independent of morphological adaptations. We used a comparative approach to discriminate between DT responses and the common water loss response in Selaginella species. Predicted proteomes show strong homology, but most of the desiccation responsive genes differ between species. Despite such differences, functional analysis revealed that tolerant species with different morphologies employ similar mechanisms to survive desiccation. Significant functions involved in DT and shared by both tolerant species included induction of antioxidant systems, amino acid and secondary metabolism, whereas species-specific responses included cell wall modification and carbohydrate metabolism. Conclusions: Reference transcriptomes generated in this work represent a valuable resource to study Selaginella biology and plant evolution in relation to DT. Our results provide evidence of convergent evolution of S. sellowii and S. lepidophylla due to the different gene sets that underwent selection to acquire DT Keywords: Selaginella, Desiccation tolerance, Convergent evolution

Background The origin of the Selaginella genus has been estimated at around 383 million years ago [1]. This group of plants represents one of the oldest lineages of vascular plants (Fig. 1) and includes over 700 species [2, 7, 8]. The * Correspondence: [email protected] 1 National Laboratory of Genomics for Biodiversity (Langebio), Unit of Advanced Genomics, CINVESTAV, 36824 Irapuato, Guanajuato, Mexico 4 Institute of Genomics for Crop Abiotic Stress Tolerance, Texas Tech University, Lubbock, TX 79409, USA Full list of author information is available at the end of the article

Selaginella genus occupies a broad diversity of habitats, mainly in humid environments, however some species are adapted to extremely arid conditions [1, 3]. Some of these latter species have evolved desiccation tolerance (DT), a particular trait that allows them to withstand very long periods in the desiccated state. Tolerance to desiccation, considered as the ability to recover