Algal origins of core land plant stress response subnetworks

Abstract

We computed co-expression networks from more than 2200 samples of nine species across 600 million years of divergent streptophyte evolution and infer that the streptophyte algal ancestors of land plants already had a remarkable fraction of the embryophytic stress response system. Despite its phytohormone-independent origin, homologs of all core components of the drought hormone abscisic acid (ABA) subnetwork are present, and we find that most are co-expressed in streptophyte algae and land plants; this subnetwork was thus co-opted in embryophytes by bringing it under the regime of ABA. The last common ancestor of embryophytes and Zygnematophyceae algae had ancient stress-responsive pathways, enabling it to face the stresses typical of the land environment - even before the origin of land plants - while evolution on land led to the adaptive refinement of these responses.

Keywords: co‐expression networks; plant evolution; plant terrestrialization; streptophyte algae; stress physiology.

Figure 1

Setup of the study. (a) The schematic bioinformatic workflow and (b) cladogram of species under study and the groups they represent.

Figure 2

Aggregated networks of conserved connections among land plants and streptophyte algae. (a) Complete network; (b) subnetwork filtered for cell wall orthogroups (based on GO terms). Names were assigned to each orthogroup based on the Arabidopsis thaliana genes that were present in that orthogroup in all subnetworks.

Figure 3

Aggregated subnetwork of conserved connections among land plants and streptophyte algae salient to abscisic acid signaling. (a) Subnetwork filtered for orthogroups related to abscisic acid (based on GO terms). The associations that were present with at least one tracheophyte, one bryophyte, and one zygnematophyceae algae were depicted as conserved among the last common ancestor of land plants and streptophyte algae via orange. (b) Similar to (a) but with the edges that were present only in land plants (i.e., at least one tracheophyte and one bryophyte) shown in green. The names of the top 20 most connected gene hubs that were not present in (a) (i.e., emerging hubs) were labeled.

Figure 4

Scenario for the evolution of abiotic stress perception and signaling. A schematic model that summarizes the emergence of stress response actors in the last common ancestor of land plants and zygnematophyceaen, as well as novel connections and recruitment that occurred after the divergence of land plants and zygnematophyceaen algae.