Cross-stress gene expression atlas of Marchantia polymorpha reveals the hierarchy and regulatory principles of abiotic stress responses

Abstract

Abiotic stresses negatively impact ecosystems and the yield of crops, and climate change will increase their frequency and intensity. Despite progress in understanding how plants respond to individual stresses, our knowledge of plant acclimatization to combined stresses-typically occurring in nature is still lacking. Here, we used a plant with minimal regulatory network redundancy, Marchantia polymorpha, to study how seven abiotic stresses, alone and in 19 pairwise combinations, affect the phenotype, gene expression, and activity of cellular pathways. We found a high divergence of transcriptomic stress responses between Arabidopsis and Marchantia, suggesting that the stress-specific gene regulatory networks (GRNs) between bryophytes and angiosperms are not strongly conserved. The reconstructed high-confidence GRNs demonstrated that the response to specific stresses dominates those of others by relying on a large ensemble of transcription factors. We also showed that a regression model could accurately predict the gene expression under combined stresses, indicating that Marchantia performs arithmetic addition to respond to multiple stresses. Finally, we provide two online resources (https://conekt.plant.tools and http://bar.utoronto.ca/efp_marchantia/cgi-bin/efpWeb.cgi) to facilitate the study of gene expression in Marchantia exposed to abiotic stresses.