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Divergence in a stress-associated gene regulatory network underlies differential growth control in the Brassicaceae family

The use of marginal lands in agriculture is increasingly necessary to support the global human population. Elevated salinity frequently occurs in degraded soils and hinders their use due to the negative impact salt stress has on plant growth. While the hormonal networks controlling growth have been extensively characterized in stress-sensitive plants, it is unclear how these pathways are rewired in plants that maintain growth in extreme environments. We have compared the physiological and molecular responses of four closely related members of the Brassicaceae family including two salt-tolerant species (Shrenkiella parvula and Eutrema salsugineum) and two salt-sensitive species (Sisymbrium irio and Arabidopsis thaliana) to the salt stress-induced hormone, abscisic acid (ABA). While ABA inhibits root growth in most species, we uncovered substantial growth-promoting effects in Shrenkiella parvula, due to an enhancement in cell elongation. Comparative transcriptomics informed by phylogenetic relationships uncovered lineage and extremophile-specific differences in ABA response. DNA Affinity Purification followed by sequencing (DAP-Seq) was utilized to establish gene regulatory networks (GRNs) in each species for the entire ABA-RESPONSIVE ELEMENT BINDING FACTORS (AREB/ABF) clade. Comparative GRN analysis identified relative conservation in the core ABA signaling GRN, while the auxin growth-hormone GRN was highly divergent, revealing how patterns of gain and loss of cis-regulatory elements mediate novel physiological outcomes. Our findings demonstrate that the targets of hormone signaling pathways are highly divergent between species and that diametric inversion of growth regulation is possible, even between closely related species of the same plant family.