Embryophyte stress signaling evolved in the algal progenitors of land plants

Significance

The evolution of land plants from algae is an age-old question in biology. The entire terrestrial flora stems from a grade of algae, the streptophyte algae. Recent phylogenomic studies have pinpointed the Zygnematophyceae as the modern-day streptophyte algal lineage that is most closely related to the algal land plant ancestor. Here, we provide insight into the biology of this ancestor that might have aided in its conquest of land. Specifically, we uncover the existence of stress-signaling pathways and the potential for intimate plastid-nucleus communication. Plastids act as environmental sensors in land plants; our data suggest that this feature was present in a common ancestor they shared with streptophyte algae.

Abstract

Streptophytes are unique among photosynthetic eukaryotes in having conquered land. As the ancestors of land plants, streptophyte algae are hypothesized to have possessed exaptations to the environmental stressors encountered during the transition to terrestrial life. Many of these stressors, including high irradiance and drought, are linked to plastid biology. We have investigated global gene expression patterns across all six major streptophyte algal lineages, analyzing a total of around 46,000 genes assembled from a little more than 1.64 billion sequence reads from six organisms under three growth conditions. Our results show that streptophyte algae respond to cold and high light stress via expression of hallmark genes used by land plants (embryophytes) during stress–response signaling and downstream responses. Among the strongest differentially regulated genes were those associated with plastid biology. We observed that among streptophyte algae, those most closely related to land plants, especially Zygnema, invest the largest fraction of their transcriptional budget in plastid-targeted proteins and possess an array of land plant-type plastid-nucleus communication genes. Streptophyte algae more closely related to land plants also appear most similar to land plants in their capacity to respond to plastid stressors. Support for this notion comes from the detection of a canonical abscisic acid receptor of the PYRABACTIN RESISTANCE (PYR/PYL/RCAR) family in Zygnema, the first found outside the land plant lineage. We conclude that a fine-tuned response toward terrestrial plastid stressors was among the exaptations that allowed streptophytes to colonize the terrestrial habitat on a global scale.