Desiccation tolerance in the vegetative state is an essential trait for colonization of land by green plants. Though lost in vegetative tissue (leaves) of most seed plants, desiccation tolerance is more common in non-vascular plants and is found among terrestrial green algae.
The green algal genus Scenedesmus is particularly well suited for exploration of desiccation tolerance because it includes multiple independently-evolved desert-dwelling species along with closely-related aquatic taxa. The shared genetic background among these algae inhabiting such drastically different habitats provided a unique system to pinpoint the genetic basis of desiccation tolerance that necessarily emerged during terrestrialization.
We selected two desiccation-tolerant desert and one desiccation-sensitive aquatic Scenedesmus species with >98% identity in their 18S gene sequence and very different habitat-adapted physiologies. We conducted a temporal analysis of the gene expression changes (RNA-seq, 5 timepoints) during slow desiccation (>12 h) and rehydration (1h). Desiccation was conducted in a controlled environment, using algae grown in liquid culture and deposited in drops on glass. RNA-Seq data were gathered from the nuclear, plastid, and mitochondrial genes and analyzed using standard pipelines and statistics in R.
Results/Conclusions
Desiccation significantly alters the expression of more than 1,300 genes. Despite the broad evolutionary distance, unicellular desert green algae respond to water loss using very similar strategies to those described in mosses and resurrection plants. In the two desert species, photosynthesis-related and energetic metabolism genes were downregulated. There was a steep increase of expression of genes associated with water-management and stress such as aquaporins, lipid and pigment synthesis, oxidoreductases, and DNA repair. Genes traditionally associated with seed maturation and desiccation in seed plants (e.g. Late Embryogenesis Abundant proteins) were highly upregulated. Though desiccation was conducted in total darkness, expression of genes usually associated with protection from photo-oxidation, such as Early Light Induced Proteins, was enhanced. In the aquatic species, though there were some similarities with desert species in shifting gene expression patterns during desiccation, overall the shifts appeared less ordered by metabolic or protective pathway and suggested cellular emergency during desiccation and death upon rehydration.
Comparisons of desert taxon gene expression with patterns in the literature revealed parallels to shifts in gene expression during seed maturation, and to shifts in gene expression during desiccation of vegetative tissues in angiosperm resurrection plants. Taken together, these data suggest that gene pathways of ancient origin have been co-opted and rewired multiple times in the green plant clade to tolerate desiccation in terrestrial environments.